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...
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| Veröffentlicht in: | The Journal of pathology Jg. 200; H. 2; S. 195 - 206 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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Chichester, UK
John Wiley & Sons, Ltd
01.06.2003
Wiley |
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| ISSN: | 0022-3417, 1096-9896 |
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| 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 |
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| 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 |
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| 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 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| 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 |
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