Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer

Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been de...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:The Journal of pathology Jg. 200; H. 2; S. 195 - 206
Hauptverfasser: Williams, Cory SM, Leek, Russell D, Robson, Alistair M, Banerji, Suneale, Prevo, Remko, Harris, Adrian L, Jackson, David G
Format: Journal Article
Sprache:Englisch
Veröffentlicht: Chichester, UK John Wiley & Sons, Ltd 01.06.2003
Wiley
Schlagworte:
ISSN:0022-3417, 1096-9896
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
Abstract Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been demonstrated in experimental breast tumours overexpressing VEGF‐C, it has yet to be determined whether the same phenomena occur in spontaneous human breast cancers. To address this important issue, the present study investigated the lymphatics in primary human breast carcinoma (75 cases of invasive ductal and lobular breast cancer) by quantitative immunohistochemical staining for the lymphatic endothelial hyaluronan receptor LYVE‐1, the blood vascular marker CD34, and the nuclear proliferation marker pKi67. None of the breast carcinomas was found to contain dividing lymph vessels, even in areas of active haemangiogenesis. Furthermore, the majority of non‐dividing lymph vessels were confined to the tumour periphery where their incidence was low and unrelated to tumour size, grade or nodal status; rather, their density was inversely correlated with tumour aggressiveness as assessed by macrophage density (p = 0.009), and blood microvessel density (p = 0.05, Spearman Rank), as well as with distance from the tumour edge. Finally, a proportion of the peritumoural lymphatics contained tumour emboli associated with hyaluronan, indicating a possible role for LYVE‐1/hyaluronan interactions in lymphatic invasion or metastasis. These results suggest that naturally occurring breast carcinomas invade and destroy lymph vessels rather than promoting their proliferation; that breast tumour lymphangiogenesis may not always occur at physiological VEGF‐C levels; and that nodal metastasis can proceed via pre‐existing lymphatics. Copyright © 2003 John Wiley & Sons, Ltd.
AbstractList Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been demonstrated in experimental breast tumours overexpressing VEGF-C, it has yet to be determined whether the same phenomena occur in spontaneous human breast cancers. To address this important issue, the present study investigated the lymphatics in primary human breast carcinoma (75 cases of invasive ductal and lobular breast cancer) by quantitative immunohistochemical staining for the lymphatic endothelial hyaluronan receptor LYVE-1, the blood vascular marker CD34, and the nuclear proliferation marker pKi67. None of the breast carcinomas was found to contain dividing lymph vessels, even in areas of active haemangiogenesis. Furthermore, the majority of non-dividing lymph vessels were confined to the tumour periphery where their incidence was low and unrelated to tumour size, grade or nodal status; rather, their density was inversely correlated with tumour aggressiveness as assessed by macrophage density (p = 0.009), and blood microvessel density (p = 0.05, Spearman Rank), as well as with distance from the tumour edge. Finally, a proportion of the peritumoural lymphatics contained tumour emboli associated with hyaluronan, indicating a possible role for LYVE-1/hyaluronan interactions in lymphatic invasion or metastasis. These results suggest that naturally occurring breast carcinomas invade and destroy lymph vessels rather than promoting their proliferation; that breast tumour lymphangiogenesis may not always occur at physiological VEGF-C levels; and that nodal metastasis can proceed via pre-existing lymphatics.Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been demonstrated in experimental breast tumours overexpressing VEGF-C, it has yet to be determined whether the same phenomena occur in spontaneous human breast cancers. To address this important issue, the present study investigated the lymphatics in primary human breast carcinoma (75 cases of invasive ductal and lobular breast cancer) by quantitative immunohistochemical staining for the lymphatic endothelial hyaluronan receptor LYVE-1, the blood vascular marker CD34, and the nuclear proliferation marker pKi67. None of the breast carcinomas was found to contain dividing lymph vessels, even in areas of active haemangiogenesis. Furthermore, the majority of non-dividing lymph vessels were confined to the tumour periphery where their incidence was low and unrelated to tumour size, grade or nodal status; rather, their density was inversely correlated with tumour aggressiveness as assessed by macrophage density (p = 0.009), and blood microvessel density (p = 0.05, Spearman Rank), as well as with distance from the tumour edge. Finally, a proportion of the peritumoural lymphatics contained tumour emboli associated with hyaluronan, indicating a possible role for LYVE-1/hyaluronan interactions in lymphatic invasion or metastasis. These results suggest that naturally occurring breast carcinomas invade and destroy lymph vessels rather than promoting their proliferation; that breast tumour lymphangiogenesis may not always occur at physiological VEGF-C levels; and that nodal metastasis can proceed via pre-existing lymphatics.
Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been demonstrated in experimental breast tumours overexpressing VEGF‐C, it has yet to be determined whether the same phenomena occur in spontaneous human breast cancers. To address this important issue, the present study investigated the lymphatics in primary human breast carcinoma (75 cases of invasive ductal and lobular breast cancer) by quantitative immunohistochemical staining for the lymphatic endothelial hyaluronan receptor LYVE‐1, the blood vascular marker CD34, and the nuclear proliferation marker pKi67. None of the breast carcinomas was found to contain dividing lymph vessels, even in areas of active haemangiogenesis. Furthermore, the majority of non‐dividing lymph vessels were confined to the tumour periphery where their incidence was low and unrelated to tumour size, grade or nodal status; rather, their density was inversely correlated with tumour aggressiveness as assessed by macrophage density (p = 0.009), and blood microvessel density (p = 0.05, Spearman Rank), as well as with distance from the tumour edge. Finally, a proportion of the peritumoural lymphatics contained tumour emboli associated with hyaluronan, indicating a possible role for LYVE‐1/hyaluronan interactions in lymphatic invasion or metastasis. These results suggest that naturally occurring breast carcinomas invade and destroy lymph vessels rather than promoting their proliferation; that breast tumour lymphangiogenesis may not always occur at physiological VEGF‐C levels; and that nodal metastasis can proceed via pre‐existing lymphatics. Copyright © 2003 John Wiley & Sons, Ltd.
Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on invasion of existing lymph vessels remains controversial. Although proliferating intratumoural lymphatics that promote nodal metastasis have been demonstrated in experimental breast tumours overexpressing VEGF-C, it has yet to be determined whether the same phenomena occur in spontaneous human breast cancers. To address this important issue, the present study investigated the lymphatics in primary human breast carcinoma (75 cases of invasive ductal and lobular breast cancer) by quantitative immunohistochemical staining for the lymphatic endothelial hyaluronan receptor LYVE-1, the blood vascular marker CD34, and the nuclear proliferation marker pKi67. None of the breast carcinomas was found to contain dividing lymph vessels, even in areas of active haemangiogenesis. Furthermore, the majority of non-dividing lymph vessels were confined to the tumour periphery where their incidence was low and unrelated to tumour size, grade or nodal status; rather, their density was inversely correlated with tumour aggressiveness as assessed by macrophage density (p = 0.009), and blood microvessel density (p = 0.05, Spearman Rank), as well as with distance from the tumour edge. Finally, a proportion of the peritumoural lymphatics contained tumour emboli associated with hyaluronan, indicating a possible role for LYVE-1/hyaluronan interactions in lymphatic invasion or metastasis. These results suggest that naturally occurring breast carcinomas invade and destroy lymph vessels rather than promoting their proliferation; that breast tumour lymphangiogenesis may not always occur at physiological VEGF-C levels; and that nodal metastasis can proceed via pre-existing lymphatics.
Author Leek, Russell D
Jackson, David G
Prevo, Remko
Harris, Adrian L
Williams, Cory SM
Banerji, Suneale
Robson, Alistair M
Author_xml – sequence: 1
  givenname: Cory SM
  surname: Williams
  fullname: Williams, Cory SM
  organization: Nuffield Department of Clinical Laboratory Sciences, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 2
  givenname: Russell D
  surname: Leek
  fullname: Leek, Russell D
  organization: ICRF Molecular Oncology Laboratory, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 3
  givenname: Alistair M
  surname: Robson
  fullname: Robson, Alistair M
  organization: Nuffield Department of Clinical Laboratory Sciences, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 4
  givenname: Suneale
  surname: Banerji
  fullname: Banerji, Suneale
  organization: MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 5
  givenname: Remko
  surname: Prevo
  fullname: Prevo, Remko
  organization: MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 6
  givenname: Adrian L
  surname: Harris
  fullname: Harris, Adrian L
  organization: ICRF Molecular Oncology Laboratory, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
– sequence: 7
  givenname: David G
  surname: Jackson
  fullname: Jackson, David G
  email: djackson@enterprise.molbiol.ox.ac.uk
  organization: MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK
BackLink http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14802366$$DView record in Pascal Francis
https://www.ncbi.nlm.nih.gov/pubmed/12754740$$D View this record in MEDLINE/PubMed
BookMark eNp9kd1rFDEUxYNU7Lb64D8geVHwYdpk8jXzuCy6K5Ra6oLgg-FO9k43Oh9rMqPuf2-G3VoQ6tMN3N85l5xzRk66vkNCXnJ2wRnLL3cwbC-4kOIJmXFW6qwsSn1CZmmXZ0Jyc0rOYvzGGCtLpZ6RU54bJY1kM_J1XkXsHNK-ps2-3W2hu_P9HXYYfaTQbajvhgDD2PZjgObA0J8YIzYx7eh2bKGjLQ4QBxi8o1XA9KQOkmt4Tp7W0ER8cZznZP3-3Xqxyq4-Lj8s5leZk0qJTMOm3EBeOlFVRaWUApCGaalYXjjOcg4AhXbcCYlgNDO5rISTBVYSGNbinLw52O5C_2PEONjWR4dNAx32Y7RGCFakQwl8dQTHqsWN3QXfQtjb-0AS8PoIQHTQ1CF9w8cHThYsF1on7u2Bc6GPMWD9gDA7lWKnUuxUSmIv_2Gdn7Lqp2R98z_FL9_g_nFrezNfr46K7KDwccDffxUQvltthFH28_XS3orbJV98-mJX4g8nFK4h
CODEN JPTLAS
CitedBy_id crossref_primary_10_1007_s10555_006_8500_x
crossref_primary_10_1136_jcp_2004_019174
crossref_primary_10_1111_j_1600_0463_2004_apm11207_0811_x
crossref_primary_10_1245_s10434_009_0707_y
crossref_primary_10_2353_ajpath_2010_090908
crossref_primary_10_1038_sj_bjc_6602844
crossref_primary_10_4137_CPath_S23035
crossref_primary_10_1007_s00428_008_0660_3
crossref_primary_10_1111_j_1447_073X_2006_00142_x
crossref_primary_10_1007_s10585_023_10229_3
crossref_primary_10_1016_j_humpath_2006_07_017
crossref_primary_10_3892_ijo_2017_4003
crossref_primary_10_1038_modpathol_3800546
crossref_primary_10_1038_modpathol_3800786
crossref_primary_10_1097_MPH_0b013e31816e2358
crossref_primary_10_1089_153968503768330274
crossref_primary_10_1111_j_1600_0463_2004_apm11207_0803_x
crossref_primary_10_1016_j_mvr_2006_03_005
crossref_primary_10_1002_path_1776
crossref_primary_10_1038_modpathol_3800651
crossref_primary_10_1038_nrc3677
crossref_primary_10_1172_JCI59858
crossref_primary_10_1038_modpathol_3800253
crossref_primary_10_1136_jcp_2006_042523
crossref_primary_10_1111_j_1365_2559_2005_02220_x
crossref_primary_10_1158_0008_5472_CAN_06_4676
crossref_primary_10_1089_lrb_2012_0008
crossref_primary_10_1136_jcp_2009_074062
crossref_primary_10_1186_1471_2407_10_416
crossref_primary_10_1158_1078_0432_CCR_04_0742
crossref_primary_10_3109_00313025_2010_522174
crossref_primary_10_1038_sj_bjc_6602794
crossref_primary_10_1111_j_1365_2613_2007_00532_x
crossref_primary_10_1371_journal_pone_0063463
crossref_primary_10_1111_j_1472_8206_2008_00614_x
crossref_primary_10_1158_1078_0432_CCR_04_0063
crossref_primary_10_1007_s12253_011_9436_1
crossref_primary_10_1016_S0002_9440_10_63379_2
crossref_primary_10_1016_j_jcpa_2013_09_006
crossref_primary_10_1016_j_prp_2015_07_001
crossref_primary_10_1007_s10555_006_9026_y
crossref_primary_10_1002_path_2517
crossref_primary_10_1097_00000478_200608000_00021
crossref_primary_10_1038_sj_bjc_6605219
crossref_primary_10_1002_ar_21217
crossref_primary_10_1016_j_mpdhp_2010_03_011
crossref_primary_10_1034_j_1399_0004_2003_00152_x
crossref_primary_10_1089_153968503768330247
crossref_primary_10_1038_modpathol_3800728
crossref_primary_10_1016_j_humpath_2007_09_006
crossref_primary_10_1136_ard_2003_005876
crossref_primary_10_3390_cells9030762
crossref_primary_10_1016_j_ajpath_2021_08_011
crossref_primary_10_1155_2017_7285656
crossref_primary_10_1002_j_2040_4603_2018_tb00006_x
crossref_primary_10_1007_s10549_008_9936_1
crossref_primary_10_1158_1078_0432_CCR_05_1238
crossref_primary_10_1038_sj_bjc_6603144
crossref_primary_10_1111_j_1600_0714_2012_01153_x
crossref_primary_10_1158_0008_5472_CAN_05_0885
crossref_primary_10_1684_bdc_2013_1719
crossref_primary_10_1136_jcp_2004_021626
crossref_primary_10_1002_path_2523
crossref_primary_10_1080_00498254_2022_2133649
crossref_primary_10_1080_2162402X_2015_1073882
crossref_primary_10_1007_s10585_007_9123_5
crossref_primary_10_1038_modpathol_2011_138
crossref_primary_10_1002_path_2760
crossref_primary_10_1038_nrc1391
crossref_primary_10_4103_ijpm_ijpm_189_24
crossref_primary_10_1038_bjc_2015_282
crossref_primary_10_1053_j_gastro_2006_09_014
crossref_primary_10_1186_1756_9966_30_14
crossref_primary_10_1177_1066896909337505
crossref_primary_10_1016_j_canlet_2007_07_005
crossref_primary_10_1016_S0022_5347_06_00520_9
crossref_primary_10_1007_s12253_016_0147_5
crossref_primary_10_1016_j_breast_2006_06_007
crossref_primary_10_1016_j_canlet_2007_07_004
crossref_primary_10_1016_j_semcancer_2009_05_005
crossref_primary_10_1593_neo_12956
crossref_primary_10_1136_jcp_2004_020123
crossref_primary_10_2353_ajpath_2008_070360
crossref_primary_10_1080_19420862_2025_2492236
crossref_primary_10_1002_path_1840
crossref_primary_10_1016_j_ccr_2004_08_034
crossref_primary_10_4103_IJPM_IJPM_774_16
crossref_primary_10_1136_jcp_2003_014480
crossref_primary_10_1016_j_ccr_2007_04_020
crossref_primary_10_1186_s12885_017_3769_4
crossref_primary_10_2353_ajpath_2007_060447
crossref_primary_10_1158_1078_0432_CCR_04_0397
crossref_primary_10_1038_modpathol_3800985
crossref_primary_10_1097_01_pas_0000149706_74216_b6
crossref_primary_10_1007_s00428_013_1502_5
crossref_primary_10_1096_fj_202500024R
crossref_primary_10_1111_cas_13738
crossref_primary_10_1111_j_1464_410X_2006_06403_x
crossref_primary_10_1073_pnas_1115542109
crossref_primary_10_1016_j_addr_2015_12_011
crossref_primary_10_1038_sj_bjc_6603445
crossref_primary_10_1097_MPA_0b013e318068fcba
crossref_primary_10_1016_j_humpath_2008_06_031
crossref_primary_10_1309_7FXVRMXF58PVRJUH
crossref_primary_10_1371_journal_pone_0144376
crossref_primary_10_1089_1539685041690427
crossref_primary_10_1016_j_canlet_2007_03_001
crossref_primary_10_1111_j_1463_1318_2006_01199_x
crossref_primary_10_1002_jso_21607
crossref_primary_10_1038_srep40364
crossref_primary_10_1016_j_pathophys_2009_11_003
crossref_primary_10_1016_j_jss_2010_09_012
crossref_primary_10_1016_j_yexmp_2020_104385
crossref_primary_10_1007_s10585_023_10230_w
crossref_primary_10_1002_ar_20845
crossref_primary_10_1200_JCO_2006_07_1092
crossref_primary_10_1111_j_1464_410X_2008_08135_x
crossref_primary_10_1152_ajprenal_00077_2019
crossref_primary_10_1016_j_eururo_2007_08_030
crossref_primary_10_4061_2011_867152
crossref_primary_10_1111_j_1600_0463_2004_apm11207_0804_x
crossref_primary_10_1007_s10555_006_8496_2
crossref_primary_10_1186_s12885_015_1501_9
crossref_primary_10_1038_sj_bjc_6603067
crossref_primary_10_1158_1078_0432_CCR_05_1142
crossref_primary_10_3390_biomedicines11030968
crossref_primary_10_1016_j_canlet_2008_01_017
crossref_primary_10_1016_j_jss_2009_03_081
crossref_primary_10_1016_j_urolonc_2011_08_006
crossref_primary_10_1038_sj_bjc_6601727
crossref_primary_10_1007_s13402_013_0151_7
crossref_primary_10_1097_01_pas_0000174269_99459_9d
crossref_primary_10_1016_j_jcpa_2012_09_007
crossref_primary_10_1111_j_1349_7006_2008_00885_x
crossref_primary_10_1111_j_1600_0714_2008_00707_x
crossref_primary_10_1158_1078_0432_CCR_03_0826
Cites_doi 10.1083/jcb.144.4.789
10.1093/oso/9780198549376.003.0008
10.1016/0092-8674(91)90033-U
10.1016/S1471-4906(01)01936-6
10.1038/84651
10.1054/bjoc.2001.1846
10.1016/S0022-5223(00)70017-1
10.1002/ijc.10283
10.1016/S0002-9440(10)65550-2
10.1016/S0092-8674(00)00139-2
10.1002/path.808
10.1093/emboj/20.6.1223
10.1006/dbio.1997.8639
10.1084/jem.194.6.797
10.1097/00006676-200104000-00010
10.1093/emboj/20.17.4762
10.1074/jbc.M011004200
10.1016/S1471-4914(00)01864-5
10.1054/bjoc.2000.1396
10.1023/A:1006308619659
10.1038/sj.bjc.6690356
10.1001/archsurg.135.5.586
10.1111/j.1365-2559.1993.tb00135.x
10.1016/S0002-9440(10)65392-8
10.1161/01.RES.88.6.623
10.1038/84635
10.1054/bjoc.2001.1882
10.1002/path.1711770310
10.1002/(SICI)1097-0215(20000120)89:1<69::AID-IJC11>3.0.CO;2-M
10.1093/humrep/17.4.1086
10.1038/84643
10.1006/gyno.2001.6292
10.1093/emboj/20.4.672
10.1023/A:1010692132669
10.1016/S1050-1738(02)00189-5
10.1016/S0959-8049(01)00015-6
10.1002/ijc.1379
10.1016/S0092-8674(00)81683-9
10.1002/1097-0029(20010115)52:2<182::AID-JEMT1004>3.0.CO;2-M
10.1056/NEJM199101033240101
10.1111/j.1349-7006.1999.tb00844.x
10.1016/S0002-9440(10)64757-8
10.1101/gad.975002
10.1073/pnas.95.24.14389
10.1038/35036374
ContentType Journal Article
Copyright Copyright © 2003 John Wiley & Sons, Ltd.
2003 INIST-CNRS
Copyright 2003 John Wiley & Sons, Ltd.
Copyright_xml – notice: Copyright © 2003 John Wiley & Sons, Ltd.
– notice: 2003 INIST-CNRS
– notice: Copyright 2003 John Wiley & Sons, Ltd.
DBID BSCLL
AAYXX
CITATION
IQODW
CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1002/path.1343
DatabaseName Istex
CrossRef
Pascal-Francis
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic

MEDLINE
CrossRef
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
EISSN 1096-9896
EndPage 206
ExternalDocumentID 12754740
14802366
10_1002_path_1343
PATH1343
ark_67375_WNG_R3RG1CSZ_H
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: Imperial Cancer Research Fund
– fundername: UK Medical Research Council
– fundername: Association for International Cancer Research
  funderid: 00–311
GroupedDBID ---
-~X
.3N
.55
.GA
.GJ
.Y3
05W
0R~
10A
123
1KJ
1L6
1OB
1OC
1ZS
29L
31~
33P
3O-
3SF
3UE
3WU
4.4
4ZD
50Y
50Z
51W
51X
52M
52N
52O
52P
52R
52S
52T
52U
52V
52W
52X
53G
5RE
5VS
66C
702
7PT
8-0
8-1
8-3
8-4
8-5
8UM
930
A01
A03
AAESR
AAEVG
AAHQN
AAIPD
AAMMB
AAMNL
AANHP
AANLZ
AAONW
AASGY
AAXRX
AAYCA
AAZKR
ABCQN
ABCUV
ABEML
ABIJN
ABJNI
ABLJU
ABQWH
ABXGK
ACAHQ
ACBWZ
ACCZN
ACFBH
ACGFS
ACGOF
ACIWK
ACMXC
ACPOU
ACPRK
ACRPL
ACSCC
ACXBN
ACXQS
ACYXJ
ADBBV
ADBTR
ADEOM
ADIZJ
ADKYN
ADMGS
ADNMO
ADOZA
ADXAS
ADZMN
AEFGJ
AEIGN
AEIMD
AENEX
AEUYR
AEYWJ
AFBPY
AFFNX
AFFPM
AFGKR
AFRAH
AFWVQ
AFZJQ
AGHNM
AGQPQ
AGXDD
AGYGG
AHBTC
AHMBA
AI.
AIACR
AIDQK
AIDYY
AIQQE
AITYG
AIURR
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
ALVPJ
AMBMR
AMYDB
ASPBG
ATUGU
AVWKF
AZBYB
AZFZN
AZVAB
BAFTC
BDRZF
BFHJK
BHBCM
BMXJE
BROTX
BRXPI
BSCLL
BY8
C45
CS3
D-6
D-7
D-E
D-F
DCZOG
DPXWK
DR2
DRFUL
DRMAN
DRSTM
DU5
EBS
EJD
EMOBN
F00
F01
F04
F5P
FEDTE
FUBAC
G-S
G.N
GNP
GODZA
GSXLS
H.X
HBH
HF~
HGLYW
HHY
HHZ
HVGLF
HZ~
IX1
J0M
J5H
JPC
KBYEO
KQQ
L7B
LATKE
LAW
LC2
LC3
LEEKS
LH4
LITHE
LOXES
LP6
LP7
LUTES
LW6
LYRES
M68
MEWTI
MK4
MRFUL
MRMAN
MRSTM
MSFUL
MSMAN
MSSTM
MVM
MXFUL
MXMAN
MXSTM
N04
N05
N9A
NF~
NNB
O66
O9-
OHT
OIG
OVD
P2P
P2W
P2X
P2Z
P4B
P4D
PALCI
PQQKQ
Q.N
Q11
QB0
QRW
R.K
RIWAO
RJQFR
ROL
RX1
SAMSI
SUPJJ
SV3
TEORI
UB1
V2E
VH1
W8V
W99
WBKPD
WH7
WHWMO
WIB
WIH
WIJ
WIK
WJL
WOHZO
WQJ
WVDHM
WXI
WXSBR
X7M
XG1
XPP
XV2
YQI
YQJ
ZGI
ZXP
ZZTAW
~IA
~KM
~WT
AAHHS
ACCFJ
AEEZP
AEQDE
AEUQT
AFPWT
AIWBW
AJBDE
RWI
WRC
WUP
AAYXX
CITATION
O8X
IQODW
CGR
CUY
CVF
ECM
EIF
NPM
VXZ
7X8
ID FETCH-LOGICAL-c4553-6ad9da29c3bb8b555aa470645028c1021aaa86c1c34ea760724b3c48eb4a0ef3
IEDL.DBID DRFUL
ISICitedReferencesCount 183
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000183485900007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 0022-3417
IngestDate Thu Oct 02 05:25:42 EDT 2025
Wed Feb 19 01:32:18 EST 2025
Wed Apr 02 07:29:32 EDT 2025
Tue Nov 18 22:09:48 EST 2025
Sat Nov 29 07:08:51 EST 2025
Wed Jan 22 16:23:10 EST 2025
Sun Sep 21 06:18:52 EDT 2025
IsPeerReviewed true
IsScholarly true
Issue 2
Keywords Human
Immunohistochemistry
Carcinoma
Lymph node
Cytokine
Malignant lymphadenopathy
Lymphatic
breast cancer
VEGF-C
Malignant tumor
Pathology
Mammary gland diseases
Angiogenesis
Vascular endothelium growth factor
metastasis
Tumor progression
lymphangiogenesis
Metastatic
Mammary gland
Molecular biology
Immunofluorescence
LYVE-1
Growth factor
Language English
License CC BY 4.0
Copyright 2003 John Wiley & Sons, Ltd.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4553-6ad9da29c3bb8b555aa470645028c1021aaa86c1c34ea760724b3c48eb4a0ef3
Notes UK Medical Research Council
Association for International Cancer Research - No. 00-311
ark:/67375/WNG-R3RG1CSZ-H
Imperial Cancer Research Fund
ArticleID:PATH1343
istex:871692DCD552D4AE632C8053410B17E98C9397F2
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
PMID 12754740
PQID 73308553
PQPubID 23479
PageCount 12
ParticipantIDs proquest_miscellaneous_73308553
pubmed_primary_12754740
pascalfrancis_primary_14802366
crossref_primary_10_1002_path_1343
crossref_citationtrail_10_1002_path_1343
wiley_primary_10_1002_path_1343_PATH1343
istex_primary_ark_67375_WNG_R3RG1CSZ_H
PublicationCentury 2000
PublicationDate June 2003
PublicationDateYYYYMMDD 2003-06-01
PublicationDate_xml – month: 06
  year: 2003
  text: June 2003
PublicationDecade 2000
PublicationPlace Chichester, UK
PublicationPlace_xml – name: Chichester, UK
– name: Chichester
– name: England
PublicationTitle The Journal of pathology
PublicationTitleAlternate J. Pathol
PublicationYear 2003
Publisher John Wiley & Sons, Ltd
Wiley
Publisher_xml – name: John Wiley & Sons, Ltd
– name: Wiley
References Oliver G, Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev 2002; 16: 773-783.
Oh S-J, Jeltsch MM, Birkenhager R, et al. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol 1997; 188: 96-109.
Fox SB, Leek RD, Weekes MP, Whitehouse RM, Gatter KC, Harris AL. Quantitation and prognostic value of breast cancer angiogenesis: comparison of microvessel density, Chalkley count, and computer image analysis. J Pathol 1995; 177: 275-283.
Salven P, Lymboussaki A, Heikkila P, et al. Vascular endothelial growth factors VEGF-B and VEGF-C are expressed in human tumours. Am J Pathol 1998; 153: 103-108.
Kajita T, Ohta Y, Kimura K, et al. The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 2001; 85: 255-260.
Veikkola T, Jussila L, Makinen T, et al. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 2001; 20: 1223-1231.
Akagi K, Ikeda Y, Miyazaki M, et al. Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer 2000; 83: 887-891.
Stacker SA, Caesar C, Baldwin ME, et al. Vascular endothelial growth factor-D promotes tumour growth and spread via the lumphatics. Nature Med 2001; 7: 186-191.
Hashimoto I, Kodama J, Seki N, et al. Vascular endothelial growth factor-c expression and its relationship to pelvic lymph node status in invasive cervical cancer. Br J Cancer 2001; 85: 93-97.
Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
Jackson DG. The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1. Trends Cardiovascular Med 2003; 13: 1-7.
Skobe M, Hawighorst T, Jackson DG, et al. Induction of tumor lymphangiogenesis by vascular endothelial growth factor-C promotes breast cancer metastasis. Nature Med 2001; 7: 192-198.
Kriehuber E, Breiteneder-Geleff S, Groeger M, et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 2001; 194: 797-808.
Valtola R, Salven P, Heikkila P, et al. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 1999; 154: 1381-1390.
Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 2001; 61: 1786-1790.
McCormick D, Chong H, Hobbs C, Datta C, Hall PA. Detection of the Ki-67 antigen in fixed and wax-embedded sections with the monoclonol antibody MIB1. Histopathology 1993; 22: 355-360.
Cursiefen C, Schlotzer-Schrehardt U, Kuchle M, et al. Lymphatic vessels in vascularized human corneas: Immunohistochemical evidence using LYVE-1 and podoplanin. Invest Ophthalmol Vis Sci 2002; 43: 2127-2135.
Relf M, LeJeune S, Scott PAE, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumour growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 1997; 57: 963-969.
Haak MC, Bartelings MM, Jackson DG, Webb S, van Vogt JM, Groot AC. Increased nuchal translucency is associated wtih jugular lymphatic distension. Hum Reprod 2002; 17: 1086-1092.
Makinen T, Jussila L, Veikkola T, et al. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nature Med 2001; 7: 199-205.
Djonov V, Andres A-C, Ziemiecki A. Vascular re-modellng during the normal and malignant life cycle of the mammary gland. Microsc Res Tech 2001; 52: 182-189.
Beasley NJP, Prevo R, Banerji S, et al. Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res 2002; 62: 1315-1320.
Jacquemier J, Mathoulin-Portier M-P, Valtola R, et al. Prognosis of breast carcinoma lymphagenesis evaluated by immunohistochemical investigation of vascular endothelial growth factor receptor-3. Int J Cancer 2000; 89: 69-73.
Mattila M-T, Ruohola JK, Karpanen T, et al. VEGF-C induced lymphangiogenesis and lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 2002; 98: 946-951.
Mandriota S, Jussila L, Jeltsch M, et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 2001; 20: 672-682.
Straume O, Jackson DG, Akslen LA. Independent prognostic impact of lymphatic vessel density and presence of low-grade lymphangiogenesis in cutaneous melanoma. Clin Cancer Res 2003; 9: 250-256.
Prevo R, Banerji S, Ferguson D, Jackson DG. Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J Biol Chem 2001; 276: 19 420-19 430.
Jackson DG. New molecular markers for the study of tumour lymphangiogenesis. Anticancer Res 2001; 7: 1-5.
Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med 1991; 324: 1-8.
Tang RF, Itakura J, Aikawa T, et al. Overexpression of lymphangiogenesis growth factor VEGF-C in human pancreatic cancer. Pancreas 2001; 3: 285-292.
Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996; 56: 4625-4629.
Nathanson SD, Zarbo RJ, Wachna DL, Spence CA, Andrzejewski TA, Abrams J. Microvessels that predict axillary lymph node metastases in patients with breast cancer. Arch Surg 2000; 135: 586-593.
van Trappen PO, Pepper MS. Lymphangiogenesis and lymph node microdissemination. Gynecol Oncol 2001; 82: 1-3.
Pepper MS. Lymphangiogenesis and tumor metastasis: myth or reality? Clin Cancer Res 2001; 7: 462-468.
Karkkainen MJ, Jussila L, Ferrell RE, Finegold DN, Alitalo K. Molecular regulation of lymphangiogenesis and targets for tissue oedema. Trends Mol Med 2001; 7: 18-22.
Kitadai Y, Amioka T, Haruma K, et al. Clinicopathological significance of vascular endothelial growth factor (VEGF)-C in human esophageal squamous cell carcinomas. Int J Cancer 2001; 93: 662-666.
Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000; 103: 481-490.
Makinen T, Veikkola T, Mustjoki S, et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 2001; 20: 4726-4773.
Cao Y, Linden P, Farnebo J, et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A 1998; 95: 14 389-14 394.
Yonemura Y, Fushida S, Bando E, et al. Lymphangiogenesis and the vascular endothelial growth factor receptor (VEGFR)-3 in gastric cancer. Eur J Cancer 2001; 37: 918-923.
Fox S, Fawcett J, Jackson DG, et al. Normal human tissues in addition to some tumours express multiple different CD44 isoforms. Cancer Res 1994; 54: 4539-4546.
Kandel J, Bossy-Wetzel E, Radvanyi F, Klagsbrun M, Folkman J, Hanahan D. Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosrcoma. Cell 1991; 66: 1095-1104.
Tsurusaki T, Kanda S, Sakai H, et al. Vascular endothelial growth factor-c expression in human prostatic carcinoma and its relationship to lymph node metastasis. Br J Cancer 1999; 80: 309-313.
Kurebayashi J, Otsuki T, Kunisue H, et al. Expression of vascular endothelial growth factor (VEGF) family members in breast cancer. Jpn J Cancer Res 1999; 90: 977-981.
Gunningham SP, Currie MJ, Han C, et al. The short form of the alternatively spliced flt-4 but not its ligand vascular endothelial growth factor C is related to lymph node metastasis in human breast cancers. Clin Cancer Res 2000; 6: 4278-4286.
Clarijs R, Ruiter DJ, de Waal RM. Lymphangiogenesis in malignant tumours: Does it occur? J Pathol 2001; 193: 143-146.
Niki T, Iba S, Tokunou M, et al. Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Clin Cancer Res 2000; 6: 2431-2439.
Enholm B, Karpanen T, Jeltsch M, et al. Adenoviral expression of vascular endothelial growth factor-c induces lymphangiogenesis in the skin. Circ Res 2001; 88: 623-629.
Auvinen P, Tammi R, Parkkinen J, et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol 2000; 156: 529-536.
Solomayer EF, Diel IJ, Meyberg GC, Gollan C, Bastert G. Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res Treat 2000; 59: 271-278.
Ohta Y, Nozawa H, Tanaka Y, Oda M, Watanabe Y. Increased vascular endothelial growth factor and vascular endothelial growth factor-c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. J Thorac Cardiovasc Surg 2000; 119: 804-813.
Kinoshita J, Kitamura K, Kabashima A, Saeki H, Tanaka S, Sugimachi K. Clinical significance of vascular endothelial growth factor-C (VEGF-C) in breast cancer. Breast Cancer Res Treat 2001; 66: 159-164.
Banerji S, Ni J, Wang S-X, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999; 144: 789-801.
Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biol 2000; 2: 737-744.
Jackson DG, Prevo R, Clasper S, Banerji S. LYVE-1, the lymphatics and tumor lymphangiogenesis. Trends Immunol 2001; 22: 317-321.
2002; 16
2002; 17
2001; 93
2000; 135
2000; 6
2000; 89
1993; 22
2000; 119
2002; 98
2003; 13
1997
2000; 2
1999; 144
1995; 177
2000; 156
2001; 88
2001; 66
2001; 22
1999; 80
2001; 85
1998; 153
1996; 56
2001; 20
2001; 276
2001; 82
2001; 61
2001; 194
2001; 7
2000; 59
2000; 103
2001; 193
1991; 66
2002; 62
1997; 188
2002; 43
1997; 57
2003; 9
2000; 83
1999; 154
2001; 37
2001; 3
2000; 100
1998; 95
1991; 324
1999; 90
2001; 52
1994; 54
Pepper MS (e_1_2_6_6_2) 2001; 7
e_1_2_6_51_2
Relf M (e_1_2_6_53_2) 1997; 57
e_1_2_6_30_2
Cursiefen C (e_1_2_6_47_2) 2002; 43
Jackson DG (e_1_2_6_24_2) 2001; 7
e_1_2_6_19_2
e_1_2_6_13_2
e_1_2_6_34_2
e_1_2_6_11_2
e_1_2_6_32_2
e_1_2_6_17_2
e_1_2_6_38_2
e_1_2_6_55_2
e_1_2_6_15_2
e_1_2_6_36_2
e_1_2_6_57_2
e_1_2_6_20_2
Niki T (e_1_2_6_23_2) 2000; 6
e_1_2_6_41_2
e_1_2_6_7_2
e_1_2_6_9_2
e_1_2_6_3_2
e_1_2_6_5_2
Leek RD (e_1_2_6_31_2) 1996; 56
Beasley NJP (e_1_2_6_44_2) 2002; 62
e_1_2_6_28_2
e_1_2_6_43_2
e_1_2_6_45_2
Karpanen T (e_1_2_6_26_2) 2001; 61
e_1_2_6_52_2
Leek RD (e_1_2_6_50_2) 1997
Fox S (e_1_2_6_29_2) 1994; 54
e_1_2_6_18_2
e_1_2_6_12_2
e_1_2_6_35_2
e_1_2_6_10_2
e_1_2_6_33_2
e_1_2_6_16_2
e_1_2_6_39_2
e_1_2_6_54_2
e_1_2_6_14_2
e_1_2_6_37_2
e_1_2_6_56_2
e_1_2_6_42_2
Straume O (e_1_2_6_49_2) 2003; 9
e_1_2_6_40_2
e_1_2_6_8_2
e_1_2_6_4_2
Gunningham SP (e_1_2_6_22_2) 2000; 6
e_1_2_6_48_2
e_1_2_6_2_2
e_1_2_6_21_2
e_1_2_6_27_2
e_1_2_6_25_2
e_1_2_6_46_2
References_xml – reference: Skobe M, Hawighorst T, Jackson DG, et al. Induction of tumor lymphangiogenesis by vascular endothelial growth factor-C promotes breast cancer metastasis. Nature Med 2001; 7: 192-198.
– reference: Ohta Y, Nozawa H, Tanaka Y, Oda M, Watanabe Y. Increased vascular endothelial growth factor and vascular endothelial growth factor-c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. J Thorac Cardiovasc Surg 2000; 119: 804-813.
– reference: Jackson DG. The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1. Trends Cardiovascular Med 2003; 13: 1-7.
– reference: Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biol 2000; 2: 737-744.
– reference: Kandel J, Bossy-Wetzel E, Radvanyi F, Klagsbrun M, Folkman J, Hanahan D. Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosrcoma. Cell 1991; 66: 1095-1104.
– reference: Haak MC, Bartelings MM, Jackson DG, Webb S, van Vogt JM, Groot AC. Increased nuchal translucency is associated wtih jugular lymphatic distension. Hum Reprod 2002; 17: 1086-1092.
– reference: Oliver G, Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev 2002; 16: 773-783.
– reference: Tsurusaki T, Kanda S, Sakai H, et al. Vascular endothelial growth factor-c expression in human prostatic carcinoma and its relationship to lymph node metastasis. Br J Cancer 1999; 80: 309-313.
– reference: Makinen T, Veikkola T, Mustjoki S, et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 2001; 20: 4726-4773.
– reference: Fox SB, Leek RD, Weekes MP, Whitehouse RM, Gatter KC, Harris AL. Quantitation and prognostic value of breast cancer angiogenesis: comparison of microvessel density, Chalkley count, and computer image analysis. J Pathol 1995; 177: 275-283.
– reference: van Trappen PO, Pepper MS. Lymphangiogenesis and lymph node microdissemination. Gynecol Oncol 2001; 82: 1-3.
– reference: Yonemura Y, Fushida S, Bando E, et al. Lymphangiogenesis and the vascular endothelial growth factor receptor (VEGFR)-3 in gastric cancer. Eur J Cancer 2001; 37: 918-923.
– reference: Cursiefen C, Schlotzer-Schrehardt U, Kuchle M, et al. Lymphatic vessels in vascularized human corneas: Immunohistochemical evidence using LYVE-1 and podoplanin. Invest Ophthalmol Vis Sci 2002; 43: 2127-2135.
– reference: Gunningham SP, Currie MJ, Han C, et al. The short form of the alternatively spliced flt-4 but not its ligand vascular endothelial growth factor C is related to lymph node metastasis in human breast cancers. Clin Cancer Res 2000; 6: 4278-4286.
– reference: Mattila M-T, Ruohola JK, Karpanen T, et al. VEGF-C induced lymphangiogenesis and lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 2002; 98: 946-951.
– reference: Relf M, LeJeune S, Scott PAE, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumour growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 1997; 57: 963-969.
– reference: Akagi K, Ikeda Y, Miyazaki M, et al. Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer 2000; 83: 887-891.
– reference: Beasley NJP, Prevo R, Banerji S, et al. Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res 2002; 62: 1315-1320.
– reference: Valtola R, Salven P, Heikkila P, et al. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 1999; 154: 1381-1390.
– reference: Tang RF, Itakura J, Aikawa T, et al. Overexpression of lymphangiogenesis growth factor VEGF-C in human pancreatic cancer. Pancreas 2001; 3: 285-292.
– reference: Straume O, Jackson DG, Akslen LA. Independent prognostic impact of lymphatic vessel density and presence of low-grade lymphangiogenesis in cutaneous melanoma. Clin Cancer Res 2003; 9: 250-256.
– reference: Jackson DG. New molecular markers for the study of tumour lymphangiogenesis. Anticancer Res 2001; 7: 1-5.
– reference: Pepper MS. Lymphangiogenesis and tumor metastasis: myth or reality? Clin Cancer Res 2001; 7: 462-468.
– reference: Djonov V, Andres A-C, Ziemiecki A. Vascular re-modellng during the normal and malignant life cycle of the mammary gland. Microsc Res Tech 2001; 52: 182-189.
– reference: Kurebayashi J, Otsuki T, Kunisue H, et al. Expression of vascular endothelial growth factor (VEGF) family members in breast cancer. Jpn J Cancer Res 1999; 90: 977-981.
– reference: Nathanson SD, Zarbo RJ, Wachna DL, Spence CA, Andrzejewski TA, Abrams J. Microvessels that predict axillary lymph node metastases in patients with breast cancer. Arch Surg 2000; 135: 586-593.
– reference: Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med 1991; 324: 1-8.
– reference: McCormick D, Chong H, Hobbs C, Datta C, Hall PA. Detection of the Ki-67 antigen in fixed and wax-embedded sections with the monoclonol antibody MIB1. Histopathology 1993; 22: 355-360.
– reference: Prevo R, Banerji S, Ferguson D, Jackson DG. Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J Biol Chem 2001; 276: 19 420-19 430.
– reference: Niki T, Iba S, Tokunou M, et al. Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Clin Cancer Res 2000; 6: 2431-2439.
– reference: Clarijs R, Ruiter DJ, de Waal RM. Lymphangiogenesis in malignant tumours: Does it occur? J Pathol 2001; 193: 143-146.
– reference: Jacquemier J, Mathoulin-Portier M-P, Valtola R, et al. Prognosis of breast carcinoma lymphagenesis evaluated by immunohistochemical investigation of vascular endothelial growth factor receptor-3. Int J Cancer 2000; 89: 69-73.
– reference: Kriehuber E, Breiteneder-Geleff S, Groeger M, et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 2001; 194: 797-808.
– reference: Kitadai Y, Amioka T, Haruma K, et al. Clinicopathological significance of vascular endothelial growth factor (VEGF)-C in human esophageal squamous cell carcinomas. Int J Cancer 2001; 93: 662-666.
– reference: Veikkola T, Jussila L, Makinen T, et al. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 2001; 20: 1223-1231.
– reference: Salven P, Lymboussaki A, Heikkila P, et al. Vascular endothelial growth factors VEGF-B and VEGF-C are expressed in human tumours. Am J Pathol 1998; 153: 103-108.
– reference: Solomayer EF, Diel IJ, Meyberg GC, Gollan C, Bastert G. Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res Treat 2000; 59: 271-278.
– reference: Enholm B, Karpanen T, Jeltsch M, et al. Adenoviral expression of vascular endothelial growth factor-c induces lymphangiogenesis in the skin. Circ Res 2001; 88: 623-629.
– reference: Fox S, Fawcett J, Jackson DG, et al. Normal human tissues in addition to some tumours express multiple different CD44 isoforms. Cancer Res 1994; 54: 4539-4546.
– reference: Cao Y, Linden P, Farnebo J, et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A 1998; 95: 14 389-14 394.
– reference: Kajita T, Ohta Y, Kimura K, et al. The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 2001; 85: 255-260.
– reference: Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 2001; 61: 1786-1790.
– reference: Makinen T, Jussila L, Veikkola T, et al. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nature Med 2001; 7: 199-205.
– reference: Hashimoto I, Kodama J, Seki N, et al. Vascular endothelial growth factor-c expression and its relationship to pelvic lymph node status in invasive cervical cancer. Br J Cancer 2001; 85: 93-97.
– reference: Karkkainen MJ, Jussila L, Ferrell RE, Finegold DN, Alitalo K. Molecular regulation of lymphangiogenesis and targets for tissue oedema. Trends Mol Med 2001; 7: 18-22.
– reference: Jackson DG, Prevo R, Clasper S, Banerji S. LYVE-1, the lymphatics and tumor lymphangiogenesis. Trends Immunol 2001; 22: 317-321.
– reference: Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
– reference: Stacker SA, Caesar C, Baldwin ME, et al. Vascular endothelial growth factor-D promotes tumour growth and spread via the lumphatics. Nature Med 2001; 7: 186-191.
– reference: Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000; 103: 481-490.
– reference: Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996; 56: 4625-4629.
– reference: Banerji S, Ni J, Wang S-X, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999; 144: 789-801.
– reference: Oh S-J, Jeltsch MM, Birkenhager R, et al. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol 1997; 188: 96-109.
– reference: Kinoshita J, Kitamura K, Kabashima A, Saeki H, Tanaka S, Sugimachi K. Clinical significance of vascular endothelial growth factor-C (VEGF-C) in breast cancer. Breast Cancer Res Treat 2001; 66: 159-164.
– reference: Auvinen P, Tammi R, Parkkinen J, et al. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol 2000; 156: 529-536.
– reference: Mandriota S, Jussila L, Jeltsch M, et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 2001; 20: 672-682.
– volume: 193
  start-page: 143
  year: 2001
  end-page: 146
  article-title: Lymphangiogenesis in malignant tumours: Does it occur
  publication-title: J Pathol
– volume: 95
  start-page: 14 389
  year: 1998
  end-page: 14 394
  article-title: Vascular endothelial growth factor C induces angiogenesis in vivo
  publication-title: Proc Natl Acad Sci U S A
– volume: 2
  start-page: 737
  year: 2000
  end-page: 744
  article-title: Matrix metalloproteinase‐9 triggers the angiogenic switch during carcinogenesis
  publication-title: Nature Cell Biol
– volume: 7
  start-page: 186
  year: 2001
  end-page: 191
  article-title: Vascular endothelial growth factor‐D promotes tumour growth and spread via the lumphatics
  publication-title: Nature Med
– volume: 66
  start-page: 159
  year: 2001
  end-page: 164
  article-title: Clinical significance of vascular endothelial growth factor‐C (VEGF‐C) in breast cancer
  publication-title: Breast Cancer Res Treat
– volume: 54
  start-page: 4539
  year: 1994
  end-page: 4546
  article-title: Normal human tissues in addition to some tumours express multiple different CD44 isoforms
  publication-title: Cancer Res
– volume: 61
  start-page: 1786
  year: 2001
  end-page: 1790
  article-title: Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth
  publication-title: Cancer Res
– volume: 93
  start-page: 662
  year: 2001
  end-page: 666
  article-title: Clinicopathological significance of vascular endothelial growth factor (VEGF)‐C in human esophageal squamous cell carcinomas
  publication-title: Int J Cancer
– volume: 177
  start-page: 275
  year: 1995
  end-page: 283
  article-title: Quantitation and prognostic value of breast cancer angiogenesis: comparison of microvessel density, Chalkley count, and computer image analysis
  publication-title: J Pathol
– volume: 56
  start-page: 4625
  year: 1996
  end-page: 4629
  article-title: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma
  publication-title: Cancer Res
– volume: 100
  start-page: 57
  year: 2000
  end-page: 70
  article-title: The hallmarks of cancer
  publication-title: Cell
– volume: 20
  start-page: 4726
  year: 2001
  end-page: 4773
  article-title: Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF‐C/D receptor VEGFR‐3
  publication-title: EMBO J
– volume: 324
  start-page: 1
  year: 1991
  end-page: 8
  article-title: Tumor angiogenesis and metastasis—correlation in invasive breast carcinoma
  publication-title: N Engl J Med
– volume: 20
  start-page: 672
  year: 2001
  end-page: 682
  article-title: Vascular endothelial growth factor‐C‐mediated lymphangiogenesis promotes tumour metastasis
  publication-title: EMBO J
– volume: 43
  start-page: 2127
  year: 2002
  end-page: 2135
  article-title: Lymphatic vessels in vascularized human corneas: Immunohistochemical evidence using LYVE‐1 and podoplanin
  publication-title: Invest Ophthalmol Vis Sci
– volume: 17
  start-page: 1086
  year: 2002
  end-page: 1092
  article-title: Increased nuchal translucency is associated wtih jugular lymphatic distension
  publication-title: Hum Reprod
– volume: 89
  start-page: 69
  year: 2000
  end-page: 73
  article-title: Prognosis of breast carcinoma lymphagenesis evaluated by immunohistochemical investigation of vascular endothelial growth factor receptor‐3
  publication-title: Int J Cancer
– volume: 59
  start-page: 271
  year: 2000
  end-page: 278
  article-title: Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis
  publication-title: Breast Cancer Res Treat
– volume: 7
  start-page: 462
  year: 2001
  end-page: 468
  article-title: Lymphangiogenesis and tumor metastasis: myth or reality
  publication-title: Clin Cancer Res
– volume: 3
  start-page: 285
  year: 2001
  end-page: 292
  article-title: Overexpression of lymphangiogenesis growth factor VEGF‐C in human pancreatic cancer
  publication-title: Pancreas
– volume: 7
  start-page: 192
  year: 2001
  end-page: 198
  article-title: Induction of tumor lymphangiogenesis by vascular endothelial growth factor‐C promotes breast cancer metastasis
  publication-title: Nature Med
– volume: 156
  start-page: 529
  year: 2000
  end-page: 536
  article-title: Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival
  publication-title: Am J Pathol
– volume: 85
  start-page: 93
  year: 2001
  end-page: 97
  article-title: Vascular endothelial growth factor‐c expression and its relationship to pelvic lymph node status in invasive cervical cancer
  publication-title: Br J Cancer
– volume: 98
  start-page: 946
  year: 2002
  end-page: 951
  article-title: VEGF‐C induced lymphangiogenesis and lymph node metastasis in orthotopic MCF‐7 tumors
  publication-title: Int J Cancer
– volume: 7
  start-page: 18
  year: 2001
  end-page: 22
  article-title: Molecular regulation of lymphangiogenesis and targets for tissue oedema
  publication-title: Trends Mol Med
– volume: 135
  start-page: 586
  year: 2000
  end-page: 593
  article-title: Microvessels that predict axillary lymph node metastases in patients with breast cancer
  publication-title: Arch Surg
– volume: 62
  start-page: 1315
  year: 2002
  end-page: 1320
  article-title: Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer
  publication-title: Cancer Res
– volume: 57
  start-page: 963
  year: 1997
  end-page: 969
  article-title: Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumour growth factor beta‐1, platelet‐derived endothelial cell growth factor, placenta growth factor and pleiotrophin in human primary breast cancer and its relation to angiogenesis
  publication-title: Cancer Res
– start-page: 81
  year: 1997
  end-page: 100
– volume: 52
  start-page: 182
  year: 2001
  end-page: 189
  article-title: Vascular re‐modellng during the normal and malignant life cycle of the mammary gland
  publication-title: Microsc Res Tech
– volume: 154
  start-page: 1381
  year: 1999
  end-page: 1390
  article-title: VEGFR‐3 and its ligand VEGF‐C are associated with angiogenesis in breast cancer
  publication-title: Am J Pathol
– volume: 103
  start-page: 481
  year: 2000
  end-page: 490
  article-title: MMP‐9 supplied by bone marrow‐derived cells contributes to skin carcinogenesis
  publication-title: Cell
– volume: 66
  start-page: 1095
  year: 1991
  end-page: 1104
  article-title: Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosrcoma
  publication-title: Cell
– volume: 22
  start-page: 355
  year: 1993
  end-page: 360
  article-title: Detection of the Ki‐67 antigen in fixed and wax‐embedded sections with the monoclonol antibody MIB1
  publication-title: Histopathology
– volume: 90
  start-page: 977
  year: 1999
  end-page: 981
  article-title: Expression of vascular endothelial growth factor (VEGF) family members in breast cancer
  publication-title: Jpn J Cancer Res
– volume: 83
  start-page: 887
  year: 2000
  end-page: 891
  article-title: Vascular endothelial growth factor‐C (VEGF‐C) expression in human colorectal cancer tissues
  publication-title: Br J Cancer
– volume: 7
  start-page: 1
  year: 2001
  end-page: 5
  article-title: New molecular markers for the study of tumour lymphangiogenesis
  publication-title: Anticancer Res
– volume: 276
  start-page: 19 420
  year: 2001
  end-page: 19 430
  article-title: Mouse LYVE‐1 is an endocytic receptor for hyaluronan in lymphatic endothelium
  publication-title: J Biol Chem
– volume: 82
  start-page: 1
  year: 2001
  end-page: 3
  article-title: Lymphangiogenesis and lymph node microdissemination
  publication-title: Gynecol Oncol
– volume: 9
  start-page: 250
  year: 2003
  end-page: 256
  article-title: Independent prognostic impact of lymphatic vessel density and presence of low‐grade lymphangiogenesis in cutaneous melanoma
  publication-title: Clin Cancer Res
– volume: 6
  start-page: 4278
  year: 2000
  end-page: 4286
  article-title: The short form of the alternatively spliced flt‐4 but not its ligand vascular endothelial growth factor C is related to lymph node metastasis in human breast cancers
  publication-title: Clin Cancer Res
– volume: 7
  start-page: 199
  year: 2001
  end-page: 205
  article-title: Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor‐3
  publication-title: Nature Med
– volume: 6
  start-page: 2431
  year: 2000
  end-page: 2439
  article-title: Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma
  publication-title: Clin Cancer Res
– volume: 153
  start-page: 103
  year: 1998
  end-page: 108
  article-title: Vascular endothelial growth factors VEGF‐B and VEGF‐C are expressed in human tumours
  publication-title: Am J Pathol
– volume: 80
  start-page: 309
  year: 1999
  end-page: 313
  article-title: Vascular endothelial growth factor‐c expression in human prostatic carcinoma and its relationship to lymph node metastasis
  publication-title: Br J Cancer
– volume: 188
  start-page: 96
  year: 1997
  end-page: 109
  article-title: VEGF and VEGF‐C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane
  publication-title: Dev Biol
– volume: 88
  start-page: 623
  year: 2001
  end-page: 629
  article-title: Adenoviral expression of vascular endothelial growth factor‐c induces lymphangiogenesis in the skin
  publication-title: Circ Res
– volume: 13
  start-page: 1
  year: 2003
  end-page: 7
  article-title: The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE‐1
  publication-title: Trends Cardiovascular Med
– volume: 22
  start-page: 317
  year: 2001
  end-page: 321
  article-title: LYVE‐1, the lymphatics and tumor lymphangiogenesis
  publication-title: Trends Immunol
– volume: 119
  start-page: 804
  year: 2000
  end-page: 813
  article-title: Increased vascular endothelial growth factor and vascular endothelial growth factor‐c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non‐small cell lung cancer
  publication-title: J Thorac Cardiovasc Surg
– volume: 144
  start-page: 789
  year: 1999
  end-page: 801
  article-title: LYVE‐1, a new homologue of the CD44 glycoprotein, is a lymph‐specific receptor for hyaluronan
  publication-title: J Cell Biol
– volume: 37
  start-page: 918
  year: 2001
  end-page: 923
  article-title: Lymphangiogenesis and the vascular endothelial growth factor receptor (VEGFR)‐3 in gastric cancer
  publication-title: Eur J Cancer
– volume: 85
  start-page: 255
  year: 2001
  end-page: 260
  article-title: The expression of vascular endothelial growth factor C and its receptors in non‐small cell lung cancer
  publication-title: Br J Cancer
– volume: 20
  start-page: 1223
  year: 2001
  end-page: 1231
  article-title: Signalling via vascular endothelial growth factor receptor‐3 is sufficient for lymphangiogenesis in transgenic mice
  publication-title: EMBO J
– volume: 16
  start-page: 773
  year: 2002
  end-page: 783
  article-title: The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature
  publication-title: Genes Dev
– volume: 194
  start-page: 797
  year: 2001
  end-page: 808
  article-title: Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages
  publication-title: J Exp Med
– ident: e_1_2_6_28_2
  doi: 10.1083/jcb.144.4.789
– volume: 6
  start-page: 4278
  year: 2000
  ident: e_1_2_6_22_2
  article-title: The short form of the alternatively spliced flt‐4 but not its ligand vascular endothelial growth factor C is related to lymph node metastasis in human breast cancers
  publication-title: Clin Cancer Res
– volume: 54
  start-page: 4539
  year: 1994
  ident: e_1_2_6_29_2
  article-title: Normal human tissues in addition to some tumours express multiple different CD44 isoforms
  publication-title: Cancer Res
– volume: 57
  start-page: 963
  year: 1997
  ident: e_1_2_6_53_2
  article-title: Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumour growth factor beta‐1, platelet‐derived endothelial cell growth factor, placenta growth factor and pleiotrophin in human primary breast cancer and its relation to angiogenesis
  publication-title: Cancer Res
– start-page: 81
  volume-title: Tumour Angiogenesis
  year: 1997
  ident: e_1_2_6_50_2
  doi: 10.1093/oso/9780198549376.003.0008
– ident: e_1_2_6_36_2
  doi: 10.1016/0092-8674(91)90033-U
– volume: 6
  start-page: 2431
  year: 2000
  ident: e_1_2_6_23_2
  article-title: Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma
  publication-title: Clin Cancer Res
– ident: e_1_2_6_32_2
  doi: 10.1016/S1471-4906(01)01936-6
– ident: e_1_2_6_42_2
  doi: 10.1038/84651
– ident: e_1_2_6_13_2
  doi: 10.1054/bjoc.2001.1846
– ident: e_1_2_6_16_2
  doi: 10.1016/S0022-5223(00)70017-1
– ident: e_1_2_6_27_2
  doi: 10.1002/ijc.10283
– volume: 9
  start-page: 250
  year: 2003
  ident: e_1_2_6_49_2
  article-title: Independent prognostic impact of lymphatic vessel density and presence of low‐grade lymphangiogenesis in cutaneous melanoma
  publication-title: Clin Cancer Res
– ident: e_1_2_6_11_2
  doi: 10.1016/S0002-9440(10)65550-2
– ident: e_1_2_6_55_2
  doi: 10.1016/S0092-8674(00)00139-2
– ident: e_1_2_6_7_2
  doi: 10.1002/path.808
– ident: e_1_2_6_43_2
  doi: 10.1093/emboj/20.6.1223
– ident: e_1_2_6_8_2
  doi: 10.1006/dbio.1997.8639
– ident: e_1_2_6_54_2
  doi: 10.1084/jem.194.6.797
– ident: e_1_2_6_18_2
  doi: 10.1097/00006676-200104000-00010
– ident: e_1_2_6_57_2
  doi: 10.1093/emboj/20.17.4762
– ident: e_1_2_6_39_2
  doi: 10.1074/jbc.M011004200
– ident: e_1_2_6_52_2
  doi: 10.1016/S1471-4914(00)01864-5
– ident: e_1_2_6_15_2
  doi: 10.1054/bjoc.2000.1396
– ident: e_1_2_6_2_2
  doi: 10.1023/A:1006308619659
– ident: e_1_2_6_19_2
  doi: 10.1038/sj.bjc.6690356
– ident: e_1_2_6_3_2
  doi: 10.1001/archsurg.135.5.586
– ident: e_1_2_6_34_2
  doi: 10.1111/j.1365-2559.1993.tb00135.x
– ident: e_1_2_6_38_2
  doi: 10.1016/S0002-9440(10)65392-8
– ident: e_1_2_6_10_2
  doi: 10.1161/01.RES.88.6.623
– ident: e_1_2_6_41_2
  doi: 10.1038/84635
– ident: e_1_2_6_20_2
  doi: 10.1054/bjoc.2001.1882
– ident: e_1_2_6_30_2
  doi: 10.1002/path.1711770310
– ident: e_1_2_6_12_2
  doi: 10.1002/(SICI)1097-0215(20000120)89:1<69::AID-IJC11>3.0.CO;2-M
– ident: e_1_2_6_46_2
  doi: 10.1093/humrep/17.4.1086
– ident: e_1_2_6_25_2
  doi: 10.1038/84643
– ident: e_1_2_6_4_2
  doi: 10.1006/gyno.2001.6292
– ident: e_1_2_6_40_2
  doi: 10.1093/emboj/20.4.672
– ident: e_1_2_6_17_2
  doi: 10.1023/A:1010692132669
– volume: 7
  start-page: 1
  year: 2001
  ident: e_1_2_6_24_2
  article-title: New molecular markers for the study of tumour lymphangiogenesis
  publication-title: Anticancer Res
– ident: e_1_2_6_33_2
  doi: 10.1016/S1050-1738(02)00189-5
– ident: e_1_2_6_14_2
  doi: 10.1016/S0959-8049(01)00015-6
– ident: e_1_2_6_21_2
  doi: 10.1002/ijc.1379
– ident: e_1_2_6_35_2
  doi: 10.1016/S0092-8674(00)81683-9
– volume: 56
  start-page: 4625
  year: 1996
  ident: e_1_2_6_31_2
  article-title: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma
  publication-title: Cancer Res
– ident: e_1_2_6_48_2
  doi: 10.1002/1097-0029(20010115)52:2<182::AID-JEMT1004>3.0.CO;2-M
– volume: 43
  start-page: 2127
  year: 2002
  ident: e_1_2_6_47_2
  article-title: Lymphatic vessels in vascularized human corneas: Immunohistochemical evidence using LYVE‐1 and podoplanin
  publication-title: Invest Ophthalmol Vis Sci
– ident: e_1_2_6_5_2
  doi: 10.1056/NEJM199101033240101
– ident: e_1_2_6_51_2
  doi: 10.1111/j.1349-7006.1999.tb00844.x
– volume: 61
  start-page: 1786
  year: 2001
  ident: e_1_2_6_26_2
  article-title: Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth
  publication-title: Cancer Res
– volume: 62
  start-page: 1315
  year: 2002
  ident: e_1_2_6_44_2
  article-title: Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer
  publication-title: Cancer Res
– ident: e_1_2_6_56_2
  doi: 10.1016/S0002-9440(10)64757-8
– ident: e_1_2_6_45_2
  doi: 10.1101/gad.975002
– ident: e_1_2_6_9_2
  doi: 10.1073/pnas.95.24.14389
– volume: 7
  start-page: 462
  year: 2001
  ident: e_1_2_6_6_2
  article-title: Lymphangiogenesis and tumor metastasis: myth or reality
  publication-title: Clin Cancer Res
– ident: e_1_2_6_37_2
  doi: 10.1038/35036374
SSID ssj0009955
Score 2.1824658
Snippet Early metastasis to lymph nodes is a frequent complication in human breast cancer. However, the extent to which this depends on lymphangiogenesis or on...
SourceID proquest
pubmed
pascalfrancis
crossref
wiley
istex
SourceType Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 195
SubjectTerms Adult
Aged
Aged, 80 and over
Biological and medical sciences
breast cancer
Breast Neoplasms - blood supply
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Female
Glycoproteins - metabolism
Gynecology. Andrology. Obstetrics
Humans
Immunoenzyme Techniques
lymphangiogenesis
Lymphatic Metastasis
Lymphatic System - pathology
LYVE-1
Macrophages - pathology
Mammary gland diseases
Medical sciences
metastasis
Middle Aged
Neoplasm Invasiveness
Neoplasm Proteins - metabolism
Neovascularization, Pathologic - pathology
Statistics as Topic
Tumors
VEGF-C
Vesicular Transport Proteins
Title Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer
URI https://api.istex.fr/ark:/67375/WNG-R3RG1CSZ-H/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fpath.1343
https://www.ncbi.nlm.nih.gov/pubmed/12754740
https://www.proquest.com/docview/73308553
Volume 200
WOSCitedRecordID wos000183485900007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVWIB
  databaseName: Wiley Online Library Full Collection 2020
  customDbUrl:
  eissn: 1096-9896
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0009955
  issn: 0022-3417
  databaseCode: DRFUL
  dateStart: 19960101
  isFulltext: true
  titleUrlDefault: https://onlinelibrary.wiley.com
  providerName: Wiley-Blackwell
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1bi9NAFD7sbkV88X6plzqIiC_ZTTIzmQSfymq3D1qWWrH44HBmki7BbiJNuui_d06SthRWEHwL5EySOZecuZz5PoDXwmVhI4zxbBJImqAID42VXhpzP42siz_bkk2oySSez5PzA3i3OQvT4kNsF9woMpr_NQU4mupkBxpKjL3HARf8EHp0qMrNvHrvp6MvH3eYu4mUW7BwEagNsJAfnmwb76WjHmn2F5VHYuU0tGipLa4be-4PZZtcNLrzX724C7e7ISgbtj5zDw6y4j7c_NRtsj-A70NTUbyzcsGWv521sbjIywv6KeYVwyJlOa0I1-vLkjA7Whl2RSDky8rdYw3vH7vMaqTjSrllhirfa2bJw1YPYTb6MDsdex0Ng2edJbkXYZqkGCaWGxMbKSWiUARz54YmlpjBETF2JrVcZKgiX4XCcCvizAj0swV_BEdFWWRPgJkUuW8iE0cyE2kSmEXsMqdEN63ykYukD283xtC2gygnpoylbsGVQ03q0qSuPrzaiv5scTmuE3rTWHQrgasfVMimpP46OdNTPj0LTj9_0-M-DPZMvnukIIC8KOrDy40PaBd_tKmCRVauK604p1I_967HrWvs2oZKCiV816vGA_7-nfp8OBvTxdN_F30Gt8KWCdLzg-dwVK_W2Qu4Ya_qvFoN4FDN40EXEH8AhNYOXw
linkProvider Wiley-Blackwell
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1bb9MwFD4aLQJeuF_KZbMQQryEJbEdJxIv1aAroqumUsTEA5btuFNEl6AmneDf45OkqSoNCYm3SDlO4nPJ8eX4-wBeMZeFNdPaM0nAcYLCPKUN99KY-mlkXPyZhmxCTKfx2VlyugfvNmdhGnyIbsENI6P-X2OA44L04RY1FCl73waU0WvQZxEVcQ_672ejL5Mt6G7CeYcWzgKxQRbyw8Ou8U4-6qNqf2F9pCqdihYNt8VVg8_dsWydjEZ3_q8bd-F2Owglw8Zr7sGeze_DjZN2m_0BfB_qEiOeFAuy_O3srfLzrDjH32JWEpWnJMM14Wp9USBqRyNDLhGGfFm6e6Rm_iMXtlJ4YCkzRGPte0UM-tjqIcxHH-ZHY68lYvCMsyX1IpUmqQoTQ7WONedcKSYQ6M4NTgxygyulYmdUQ5lVIvJFyDQ1LLaaKd8u6CPo5UVunwDRqaK-jnQcccvSJNCL2OVOrtzEyleUJQN4s7GGNC1IOXJlLGUDrxxKVJdEdQ3gZSf6s0HmuErodW3STkKtfmApm-Dy6_RYzujsODj6_E2OB7C_Y_PtIxlC5EXRAA42TiBdBOK2isptsS6loBSL_dy7Hje-sW0bCs4E812vahf4-3fK0-F8jBdP_130AG6O5ycTOfk4_fQMboUNL6TnB8-hV63W9gVcN5dVVq7227j4A0a0EWc
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1ba9swFD50ySh76e5rdmnFGGMvXm1L8gX2EtqlGetCyDJW-jAhyXIxS-0SO2X799OxHYdAB4O9GXxkW-fio8vR9wG8YTYLK6aUo2OP4wSFOVJp7iQRdZNA2_jTDdlEOJlE5-fxdAc-rM_CNPgQ3YIbRkb9v8YAN9dJerRBDUXK3vceZfQO9BmPOetB_2Q2-na2Ad2NOe_QwpkXrpGFXP-oa7yVj_qo2l9YHylLq6K04ba4bfC5PZatk9Ho_v914wHstYNQMmy85iHsmPwR7H5pt9kfw4-hKjHiSZGSxW9rb5lfZsUl_hazksg8IRmuCVerqwJROxoZcoMw5IvS3iM18x-5MpXEA0uZJgpr3yui0ceWT2A--jg_HjstEYOjrS2pE8gkTqQfa6pUpDjnUrIQge7s4EQjN7iUMrJG1ZQZGQZu6DNFNYuMYtI1KX0KvbzIzT4QlUjqqkBFATcsiT2VRjZ3cmknVq6kLB7Au7U1hG5BypErYyEaeGVfoLoEqmsArzvR6waZ4zaht7VJOwm5_ImlbCEX3yenYkZnp97x1wsxHsDBls03j2QIkRcEAzhcO4GwEYjbKjI3xaoUIaVY7Gff9azxjU1bP-QsZK7tVe0Cf_9OMR3Ox3jx_N9FD2F3ejISZ58mn1_APb-hhXRc7yX0quXKvIK7-qbKyuVBGxZ_ALrSEOI
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Absence+of+lymphangiogenesis+and+intratumoural+lymph+vessels+in+human+metastatic+breast+cancer&rft.jtitle=The+Journal+of+pathology&rft.au=WILLIAMS%2C+Cory+S.+M&rft.au=LEEK%2C+Russell+D&rft.au=ROBSON%2C+Alistair+M&rft.au=BANERJI%2C+Suneale&rft.date=2003-06-01&rft.pub=Wiley&rft.issn=0022-3417&rft.volume=200&rft.issue=2&rft.spage=195&rft.epage=206&rft_id=info:doi/10.1002%2Fpath.1343&rft.externalDBID=n%2Fa&rft.externalDocID=14802366
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0022-3417&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0022-3417&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0022-3417&client=summon