The reverse Warburg Effect: Glycolysis inhibitors prevent the tumor promoting effects of caveolin-1 deficient cancer associated fibroblasts

We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent predictor of breast cancer patient tumor recurrence, metastasis, tamoxifen-resistance, and poor clinical outcome. However, it remains unknown how los...

Celý popis

Uloženo v:

Podrobná bibliografie
Vydáno v:	Cell cycle (Georgetown, Tex.) Ročník 9; číslo 10; s. 1960 - 1971
Hlavní autoři:	Bonuccelli, Gloria, Whitaker-Menezes, Diana, Castello-Cros, Remedios, Pavlides, Stephanos, Pestell, Richard G., Fatatis, Alessandro, Witkiewicz, Agnieszka K., Vander Heiden, Matthew G., Migneco, Gemma, Chiavarina, Barbara, Frank, Philippe G., Capozza, Franco, Flomenberg, Neal, Martinez-Outschoorn, Ubaldo E., Sotgia, Federica, Lisanti, Michael P.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Taylor & Francis 15.05.2010
Témata:	Animals Binding Biology Bioscience Blotting, Western Calcium Cancer Caveolin 1 - deficiency Caveolin 1 - genetics Cell Cell Line, Tumor Culture Media, Conditioned Cycle Deoxyglucose - pharmacology Dichloroacetic Acid - pharmacology Electrophoresis, Gel, Two-Dimensional Electrophoresis, Polyacrylamide Gel Fibroblasts - cytology Fibroblasts - metabolism Glycolysis - drug effects Humans Immunohistochemistry Lactate Dehydrogenases - genetics Lactate Dehydrogenases - metabolism Landes Mice Mice, Nude Microscopy, Fluorescence Organogenesis Proteins Proteomics Pyruvate Kinase - genetics Pyruvate Kinase - metabolism Xenograft Model Antitumor Assays
ISSN:	1538-4101, 1551-4005, 1551-4005
On-line přístup:	Získat plný text
Tagy:	Přidat tag Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!

Abstract	We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent predictor of breast cancer patient tumor recurrence, metastasis, tamoxifen-resistance, and poor clinical outcome. However, it remains unknown how loss of stromal Cav-1 mediates these effects clinically. To mechanistically address this issue, we have now generated a novel human tumor xenograft model. In this two-component system, nude mice are co-injected with i) human breast cancer cells (MDA-MB-231), and ii) stromal fibroblasts (wild-type (WT) versus Cav-1 (-/-) deficient). This allowed us to directly evaluate the effects of a Cav-1 deficiency solely in the tumor stromal compartment. Here, we show that Cav-1-deficient stromal fibroblasts are sufficient to promote both tumor growth and angiogenesis, and to recruit Cav-1 (+) micro-vascular cells. Proteomic analysis of Cav-1-deficient stromal fibroblasts indicates that these cells upregulate the expression of glycolytic enzymes, a hallmark of aerobic glycolysis (the Warburg effect). Thus, Cav-1-deficient stromal fibroblasts may contribute towards tumor growth and angiogenesis, by providing energy-rich metabolites in a paracrine fashion. We have previously termed this new idea the "Reverse Warburg Effect". In direct support of this notion, treatment of this xenograft model with glycolysis inhibitors functionally blocks the positive effects of Cav-1-deficient stromal fibroblasts on breast cancer tumor growth. Thus, pharmacologically-induced metabolic restriction (via treatment with glycolysis inhibitors) may be a promising new therapeutic strategy for breast cancer patients that lack stromal Cav-1 expression. We also identify the stromal expression of PKM2 and LDH-B as new candidate biomarkers for the "Reverse Warburg Effect" or "Stromal-Epithelial Metabolic Coupling" in human breast cancers.
AbstractList	We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent predictor of breast cancer patient tumor recurrence, metastasis, tamoxifen-resistance, and poor clinical outcome. However, it remains unknown how loss of stromal Cav-1 mediates these effects clinically. To mechanistically address this issue, we have now generated a novel human tumor xenograft model. In this two-component system, nude mice are co-injected with i) human breast cancer cells (MDA-MB-231), and ii) stromal fibroblasts (wild-type (WT) versus Cav-1 (-/-) deficient). This allowed us to directly evaluate the effects of a Cav-1 deficiency solely in the tumor stromal compartment. Here, we show that Cav-1-deficient stromal fibroblasts are sufficient to promote both tumor growth and angiogenesis, and to recruit Cav-1 (+) micro-vascular cells. Proteomic analysis of Cav-1-deficient stromal fibroblasts indicates that these cells upregulate the expression of glycolytic enzymes, a hallmark of aerobic glycolysis (the Warburg effect). Thus, Cav-1-deficient stromal fibroblasts may contribute towards tumor growth and angiogenesis, by providing energy-rich metabolites in a paracrine fashion. We have previously termed this new idea the "Reverse Warburg Effect". In direct support of this notion, treatment of this xenograft model with glycolysis inhibitors functionally blocks the positive effects of Cav-1-deficient stromal fibroblasts on breast cancer tumor growth. Thus, pharmacologically-induced metabolic restriction (via treatment with glycolysis inhibitors) may be a promising new therapeutic strategy for breast cancer patients that lack stromal Cav-1 expression. We also identify the stromal expression of PKM2 and LDH-B as new candidate biomarkers for the "Reverse Warburg Effect" or "Stromal-Epithelial Metabolic Coupling" in human breast cancers.We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent predictor of breast cancer patient tumor recurrence, metastasis, tamoxifen-resistance, and poor clinical outcome. However, it remains unknown how loss of stromal Cav-1 mediates these effects clinically. To mechanistically address this issue, we have now generated a novel human tumor xenograft model. In this two-component system, nude mice are co-injected with i) human breast cancer cells (MDA-MB-231), and ii) stromal fibroblasts (wild-type (WT) versus Cav-1 (-/-) deficient). This allowed us to directly evaluate the effects of a Cav-1 deficiency solely in the tumor stromal compartment. Here, we show that Cav-1-deficient stromal fibroblasts are sufficient to promote both tumor growth and angiogenesis, and to recruit Cav-1 (+) micro-vascular cells. Proteomic analysis of Cav-1-deficient stromal fibroblasts indicates that these cells upregulate the expression of glycolytic enzymes, a hallmark of aerobic glycolysis (the Warburg effect). Thus, Cav-1-deficient stromal fibroblasts may contribute towards tumor growth and angiogenesis, by providing energy-rich metabolites in a paracrine fashion. We have previously termed this new idea the "Reverse Warburg Effect". In direct support of this notion, treatment of this xenograft model with glycolysis inhibitors functionally blocks the positive effects of Cav-1-deficient stromal fibroblasts on breast cancer tumor growth. Thus, pharmacologically-induced metabolic restriction (via treatment with glycolysis inhibitors) may be a promising new therapeutic strategy for breast cancer patients that lack stromal Cav-1 expression. We also identify the stromal expression of PKM2 and LDH-B as new candidate biomarkers for the "Reverse Warburg Effect" or "Stromal-Epithelial Metabolic Coupling" in human breast cancers. We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent predictor of breast cancer patient tumor recurrence, metastasis, tamoxifen-resistance, and poor clinical outcome. However, it remains unknown how loss of stromal Cav-1 mediates these effects clinically. To mechanistically address this issue, we have now generated a novel human tumor xenograft model. In this two-component system, nude mice are co-injected with i) human breast cancer cells (MDA-MB-231), and ii) stromal fibroblasts (wild-type (WT) versus Cav-1 (-/-) deficient). This allowed us to directly evaluate the effects of a Cav-1 deficiency solely in the tumor stromal compartment. Here, we show that Cav-1-deficient stromal fibroblasts are sufficient to promote both tumor growth and angiogenesis, and to recruit Cav-1 (+) micro-vascular cells. Proteomic analysis of Cav-1-deficient stromal fibroblasts indicates that these cells upregulate the expression of glycolytic enzymes, a hallmark of aerobic glycolysis (the Warburg effect). Thus, Cav-1-deficient stromal fibroblasts may contribute towards tumor growth and angiogenesis, by providing energy-rich metabolites in a paracrine fashion. We have previously termed this new idea the "Reverse Warburg Effect". In direct support of this notion, treatment of this xenograft model with glycolysis inhibitors functionally blocks the positive effects of Cav-1-deficient stromal fibroblasts on breast cancer tumor growth. Thus, pharmacologically-induced metabolic restriction (via treatment with glycolysis inhibitors) may be a promising new therapeutic strategy for breast cancer patients that lack stromal Cav-1 expression. We also identify the stromal expression of PKM2 and LDH-B as new candidate biomarkers for the "Reverse Warburg Effect" or "Stromal-Epithelial Metabolic Coupling" in human breast cancers.
Author	Capozza, Franco Pavlides, Stephanos Castello-Cros, Remedios Martinez-Outschoorn, Ubaldo E. Migneco, Gemma Frank, Philippe G. Fatatis, Alessandro Lisanti, Michael P. Whitaker-Menezes, Diana Witkiewicz, Agnieszka K. Sotgia, Federica Pestell, Richard G. Vander Heiden, Matthew G. Bonuccelli, Gloria Chiavarina, Barbara Flomenberg, Neal
Author_xml	– sequence: 1 givenname: Gloria surname: Bonuccelli fullname: Bonuccelli, Gloria – sequence: 2 givenname: Diana surname: Whitaker-Menezes fullname: Whitaker-Menezes, Diana – sequence: 3 givenname: Remedios surname: Castello-Cros fullname: Castello-Cros, Remedios – sequence: 4 givenname: Stephanos surname: Pavlides fullname: Pavlides, Stephanos – sequence: 5 givenname: Richard G. surname: Pestell fullname: Pestell, Richard G. – sequence: 6 givenname: Alessandro surname: Fatatis fullname: Fatatis, Alessandro – sequence: 7 givenname: Agnieszka K. surname: Witkiewicz fullname: Witkiewicz, Agnieszka K. – sequence: 8 givenname: Matthew G. surname: Vander Heiden fullname: Vander Heiden, Matthew G. – sequence: 9 givenname: Gemma surname: Migneco fullname: Migneco, Gemma – sequence: 10 givenname: Barbara surname: Chiavarina fullname: Chiavarina, Barbara – sequence: 11 givenname: Philippe G. surname: Frank fullname: Frank, Philippe G. – sequence: 12 givenname: Franco surname: Capozza fullname: Capozza, Franco – sequence: 13 givenname: Neal surname: Flomenberg fullname: Flomenberg, Neal – sequence: 14 givenname: Ubaldo E. surname: Martinez-Outschoorn fullname: Martinez-Outschoorn, Ubaldo E. – sequence: 15 givenname: Federica surname: Sotgia fullname: Sotgia, Federica email: federica.sotgia@jefferson.edu – sequence: 16 givenname: Michael P. surname: Lisanti fullname: Lisanti, Michael P. email: mlisanti@KimmelCancerCenter.org
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/20495363$$D View this record in MEDLINE/PubMed
BookMark	eNqFkT1vFDEQhlcoiHxASYvcUe1hr9f7QQenEJAi0QRRWt7xODHy2oftS3S_gT-N9-6SAoGo7LHeZ97xvOfViQ8eq-o1o6uWdewdwGpclYKxjrJn1RkTgtUtpeJkufOhbhllp9V5Sj8obYZ-ZC-q04a2o-AdP6t-3dwhiXiPMSH5ruK0jbfk0hiE_J5cuR0Et0s2Eevv7GRziIlsFrnPJBcyb-cQy0uYQ7b-luCeTCQYAuoeg7O-ZkSjsWAXBpQHjESlFMCqjJoYO8UwOZVyelk9N8olfHU8L6pvny5v1p_r669XX9YfrmsQnOW6a9SojJhGIbRuoJu6tunUNPTAjWlGDWCapmNTL_qmLTsCGJFT0w8D7bXgml9Ubw99y9w_t5iynG0CdE55DNskB963gnPRF-Wbo3I7zajlJtpZxZ183F8R8IMAYkgpopFgs8o2-ByVdZJRuaQkAeS4FPuUClX_QT02_pf-6FIm1JgmG9KyTsAn7mPw2-UHdr3ecxttCkX_QxUXFbMFh09GwwGx3oQ4q4cQnZZZ7VyIJpbsbJL87zP-Bn2Pzco
CitedBy_id	crossref_primary_10_3389_fphar_2021_747001 crossref_primary_10_3390_ijms21249721 crossref_primary_10_17656_jzs_10638 crossref_primary_10_1016_j_prp_2024_155597 crossref_primary_10_3390_ph8040675 crossref_primary_10_4161_cc_9_17_12908 crossref_primary_10_3892_or_2021_8179 crossref_primary_10_1016_j_bbagen_2013_10_016 crossref_primary_10_1002_wsbm_1474 crossref_primary_10_1016_j_biocel_2014_09_004 crossref_primary_10_1371_journal_pone_0097239 crossref_primary_10_1146_annurev_pathol_011811_120856 crossref_primary_10_3389_fonc_2021_641428 crossref_primary_10_1002_jcp_25349 crossref_primary_10_1111_j_1349_7006_2011_01985_x crossref_primary_10_3389_fcell_2023_1274682 crossref_primary_10_3390_ijms231710172 crossref_primary_10_1053_j_seminoncol_2017_10_004 crossref_primary_10_1007_s10555_020_09890_x crossref_primary_10_1089_ars_2011_4243 crossref_primary_10_1016_j_tranon_2023_101845 crossref_primary_10_1002_pmic_201700167 crossref_primary_10_1007_s10555_021_09960_8 crossref_primary_10_3390_cells13201721 crossref_primary_10_1007_s13577_021_00622_z crossref_primary_10_1111_j_1349_7006_2011_02183_x crossref_primary_10_3390_biomedicines11010197 crossref_primary_10_1016_j_cmet_2019_08_013 crossref_primary_10_1016_j_csbj_2023_04_003 crossref_primary_10_1016_j_ctrv_2013_07_006 crossref_primary_10_1186_s13045_024_01600_2 crossref_primary_10_1007_s11427_021_1999_2 crossref_primary_10_3390_ijms26125583 crossref_primary_10_1016_j_bbcan_2014_07_008 crossref_primary_10_1038_aps_2016_47 crossref_primary_10_1186_2193_1801_3_470 crossref_primary_10_4251_wjgo_v13_i11_1561 crossref_primary_10_4161_cc_26182 crossref_primary_10_1016_j_ejps_2012_08_012 crossref_primary_10_1371_journal_pcbi_1006584 crossref_primary_10_3390_antiox10020169 crossref_primary_10_3748_wjg_v21_i4_1140 crossref_primary_10_1093_neuonc_nou035 crossref_primary_10_1186_s10020_024_01051_y crossref_primary_10_1016_j_jhep_2014_04_040 crossref_primary_10_3390_ijms161024574 crossref_primary_10_1111_jog_13867 crossref_primary_10_1016_j_canlet_2019_07_010 crossref_primary_10_18632_oncotarget_3838 crossref_primary_10_4161_cc_10_12_16002 crossref_primary_10_1016_j_prp_2022_154177 crossref_primary_10_1016_j_semcancer_2015_08_008 crossref_primary_10_1186_1475_2867_12_6 crossref_primary_10_1051_epjconf_202532501011 crossref_primary_10_1155_2018_8651790 crossref_primary_10_3390_cells7030021 crossref_primary_10_1093_bib_bbae258 crossref_primary_10_1155_2012_574025 crossref_primary_10_1158_1940_6207_CAPR_11_0028 crossref_primary_10_4161_cc_10_24_18487 crossref_primary_10_1182_blood_2015_12_688051 crossref_primary_10_1371_journal_pone_0256615 crossref_primary_10_5604_01_3001_0014_1528 crossref_primary_10_3389_fnut_2021_588466 crossref_primary_10_3892_mmr_2023_13135 crossref_primary_10_1155_2013_242513 crossref_primary_10_1155_2017_9634172 crossref_primary_10_1016_j_molmed_2011_11_003 crossref_primary_10_1007_s43440_023_00504_1 crossref_primary_10_1016_j_ejca_2019_09_002 crossref_primary_10_4161_cc_10_11_15675 crossref_primary_10_1155_2016_8549635 crossref_primary_10_1007_s10555_020_09900_y crossref_primary_10_1155_2013_195028 crossref_primary_10_1038_nrc3365 crossref_primary_10_1016_j_drup_2020_100715 crossref_primary_10_1177_1758834014521111 crossref_primary_10_1016_j_neo_2016_11_003 crossref_primary_10_3390_cells8040293 crossref_primary_10_1155_2017_7454031 crossref_primary_10_3389_fonc_2022_942064 crossref_primary_10_1016_j_omtn_2023_03_003 crossref_primary_10_3389_fonc_2018_00341 crossref_primary_10_3389_fonc_2019_01248 crossref_primary_10_3389_fimmu_2025_1561577 crossref_primary_10_3390_cancers15041070 crossref_primary_10_3390_cancers14020322 crossref_primary_10_3390_antiox10111838 crossref_primary_10_3390_ijms20020306 crossref_primary_10_1002_ijc_30540 crossref_primary_10_1016_j_molcel_2020_05_034 crossref_primary_10_1007_s10555_021_10013_3 crossref_primary_10_1007_s11306_016_1065_y crossref_primary_10_4161_cc_25794 crossref_primary_10_1016_j_devcel_2024_06_022 crossref_primary_10_1016_j_bbcan_2012_04_005 crossref_primary_10_1007_s13277_014_2482_z crossref_primary_10_1158_1078_0432_CCR_12_2123 crossref_primary_10_3389_fcell_2020_00651 crossref_primary_10_4161_cc_11_6_19530 crossref_primary_10_4161_cc_9_21_13817 crossref_primary_10_3389_fonc_2021_697894 crossref_primary_10_4161_cc_19841 crossref_primary_10_1242_dmm_016287 crossref_primary_10_3389_fonc_2021_700629 crossref_primary_10_1371_journal_pone_0075154 crossref_primary_10_1186_s12935_018_0715_8 crossref_primary_10_1038_onc_2016_370 crossref_primary_10_3389_fonc_2020_604143 crossref_primary_10_3389_fcell_2017_00027 crossref_primary_10_1186_s12943_016_0577_4 crossref_primary_10_1186_s12943_025_02297_8 crossref_primary_10_3892_ijmm_2017_3267 crossref_primary_10_1111_vco_12551 crossref_primary_10_1186_s12967_023_04498_5 crossref_primary_10_1016_j_jgo_2018_07_010 crossref_primary_10_3390_ijms251910486 crossref_primary_10_1172_JCI69741 crossref_primary_10_3389_fimmu_2018_00353 crossref_primary_10_3390_cancers6031570 crossref_primary_10_1093_neuonc_now258 crossref_primary_10_3892_or_2017_5479 crossref_primary_10_1002_cac2_12291 crossref_primary_10_1016_j_yexcr_2017_11_020 crossref_primary_10_1016_j_plipres_2013_06_002 crossref_primary_10_1146_annurev_cancerbio_030419_033333 crossref_primary_10_1016_j_bbcan_2019_07_004 crossref_primary_10_1007_s10549_011_1751_4 crossref_primary_10_1007_s10555_018_9772_7 crossref_primary_10_1002_ijc_32987 crossref_primary_10_1186_s12967_019_1936_x crossref_primary_10_4161_cc_11_2_19006 crossref_primary_10_1007_s11060_021_03903_7 crossref_primary_10_1038_s41598_017_02251_9 crossref_primary_10_3892_ijo_2025_5796 crossref_primary_10_3390_cancers14071621 crossref_primary_10_1155_2020_4027627 crossref_primary_10_7554_eLife_09943 crossref_primary_10_1016_j_ejso_2014_04_005 crossref_primary_10_4161_cc_10_15_16870 crossref_primary_10_3390_ijms24087208 crossref_primary_10_3390_ijms22126262 crossref_primary_10_4103_0973_1482_193113 crossref_primary_10_1038_s41392_020_00359_5 crossref_primary_10_31083_j_fbl2912402 crossref_primary_10_3892_ijo_2018_4640 crossref_primary_10_4103_1673_5374_361536 crossref_primary_10_3892_ijo_2013_1985 crossref_primary_10_1089_cell_2023_0010 crossref_primary_10_4161_cc_9_17_12731
ContentType	Journal Article
Copyright	Copyright © 2010 Landes Bioscience 2010
Copyright_xml	– notice: Copyright © 2010 Landes Bioscience 2010
DBID	0YH AAYXX CITATION CGR CUY CVF ECM EIF NPM 7X8
DOI	10.4161/cc.9.10.11601
DatabaseName	Taylor & Francis Open Access CrossRef 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
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: 0YH name: Taylor & Francis Open Access url: https://www.tandfonline.com sourceTypes: Publisher – sequence: 3 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database
DeliveryMethod	fulltext_linktorsrc
Discipline	Biology
EISSN	1551-4005
EndPage	1971
ExternalDocumentID	20495363 10_4161_cc_9_10_11601 10911601
Genre	Research Article Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural
GrantInformation_xml	– fundername: NCI NIH HHS grantid: R01-CA-120876 – fundername: NCI NIH HHS grantid: R01-CA-080250 – fundername: NIAMS NIH HHS grantid: R01-AR-055660 – fundername: NCI NIH HHS grantid: R01-CA-75503 – fundername: NCI NIH HHS grantid: R01-CA-86072 – fundername: NCI NIH HHS grantid: R01-CA-098779 – fundername: NCI NIH HHS grantid: R01-CA-107382 – fundername: NCI NIH HHS grantid: P30-CA-56036 – fundername: NCI NIH HHS grantid: R01-CA-70896
GroupedDBID	--- 0BK 0R~ 0YH 29B 30N 4.4 53G 5GY AAGDL AAHBH AAHIA AAJMT AALDU AAMIU AAPUL AAQRR ABCCY ABFIM ABFMO ABJNI ABLIJ ABPAQ ABPEM ABTAI ABXUL ABXYU ACFTK ACGFS ACTIO ADBBV ADCVX ADGTB AEISY AENEX AEXWM AEYOC AFRVT AGDLA AHDZW AIJEM AIYEW AKBVH AKOOK ALMA_UNASSIGNED_HOLDINGS ALQZU AOIJS AQRUH AQTUD AVBZW AWYRJ BAWUL BLEHA CCCUG DGEBU DIK DKSSO E3Z EBS EJD F5P GTTXZ H13 HYE KRBQP KWAYT KYCEM M4Z O9- OK1 P2P RNANH ROSJB RPM RTWRZ SJN SNACF TASJS TBQAZ TDBHL TEI TFL TFT TFW TQWBC TR2 TTHFI TUROJ ZGOLN - 0R AAAVI ABJVF ABQHQ ADACO AEGYZ AFOLD AHDLD AIRXU FUNRP FVPDL UNR V1K ZA5 AAYXX CITATION ADYSH CGR CUY CVF ECM EIF NPM 7X8
ID	FETCH-LOGICAL-c531t-62a9af5b955dd2c6b6426ab87c3ff29dccf2261b75724416cc9e30f78807d53d3
IEDL.DBID	0YH
ISICitedReferencesCount	196
ISICitedReferencesURI	http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000278015900024&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN	1538-4101 1551-4005
IngestDate	Sun Aug 24 03:58:49 EDT 2025 Mon Jul 21 05:52:48 EDT 2025 Tue Nov 18 21:51:56 EST 2025 Sat Nov 29 03:33:02 EST 2025 Tue May 21 11:32:56 EDT 2019 Fri Jan 15 03:37:37 EST 2021 Mon Oct 20 23:45:40 EDT 2025
IsDoiOpenAccess	true
IsOpenAccess	true
IsPeerReviewed	true
IsScholarly	true
Issue	10
Language	English
License	open-access: http://creativecommons.org/licenses/by-nc/3.0/: This is an open-access article licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License. The article may be redistributed, reproduced, and reused for non-commercial purposes, provided the original source is properly cited.
LinkModel	DirectLink
MergedId	FETCHMERGED-LOGICAL-c531t-62a9af5b955dd2c6b6426ab87c3ff29dccf2261b75724416cc9e30f78807d53d3
Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
OpenAccessLink	https://www.tandfonline.com/doi/abs/10.4161/cc.9.10.11601
PMID	20495363
PQID	837453357
PQPubID	23479
PageCount	12
ParticipantIDs	pubmed_primary_20495363 informaworld_taylorfrancis_310_4161_cc_9_10_11601 landesbioscience_primary_cc_article_11601 crossref_citationtrail_10_4161_cc_9_10_11601 proquest_miscellaneous_837453357 crossref_primary_10_4161_cc_9_10_11601
PublicationCentury	2000
PublicationDate	5/15/2010 2010/05/15 2010-05-15 2010-May-15 20100515
PublicationDateYYYYMMDD	2010-05-15
PublicationDate_xml	– month: 05 year: 2010 text: 5/15/2010 day: 15
PublicationDecade	2010
PublicationPlace	United States
PublicationPlace_xml	– name: United States
PublicationTitle	Cell cycle (Georgetown, Tex.)
PublicationTitleAlternate	Cell Cycle
PublicationYear	2010
Publisher	Taylor & Francis
Publisher_xml	– name: Taylor & Francis
SSID	ssj0028791
Score	2.4106667
Snippet	We and others have previously identified a loss of stromal caveolin-1 (Cav-1) in cancer-associated fibroblasts (CAFs) as a powerful single independent...
SourceID	proquest pubmed crossref landesbioscience informaworld
SourceType	Aggregation Database Index Database Enrichment Source Publisher
StartPage	1960
SubjectTerms	Animals Binding Biology Bioscience Blotting, Western Calcium Cancer Caveolin 1 - deficiency Caveolin 1 - genetics Cell Cell Line, Tumor Culture Media, Conditioned Cycle Deoxyglucose - pharmacology Dichloroacetic Acid - pharmacology Electrophoresis, Gel, Two-Dimensional Electrophoresis, Polyacrylamide Gel Fibroblasts - cytology Fibroblasts - metabolism Glycolysis - drug effects Humans Immunohistochemistry Lactate Dehydrogenases - genetics Lactate Dehydrogenases - metabolism Landes Mice Mice, Nude Microscopy, Fluorescence Organogenesis Proteins Proteomics Pyruvate Kinase - genetics Pyruvate Kinase - metabolism Xenograft Model Antitumor Assays
Title	The reverse Warburg Effect: Glycolysis inhibitors prevent the tumor promoting effects of caveolin-1 deficient cancer associated fibroblasts
URI	https://www.tandfonline.com/doi/abs/10.4161/cc.9.10.11601 http://www.landesbioscience.com/journals/cc/article/11601/ https://www.ncbi.nlm.nih.gov/pubmed/20495363 https://www.proquest.com/docview/837453357
Volume	9
WOSCitedRecordID	wos000278015900024&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: PRVAWR databaseName: Taylor and Francis Online Journals customDbUrl: eissn: 1551-4005 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0028791 issn: 1538-4101 databaseCode: TFW dateStart: 20020101 isFulltext: true titleUrlDefault: https://www.tandfonline.com providerName: Taylor & Francis
link	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Nb9QwELVQAYkeKN9dvuQDQkJq2sRO4pgbrFh6QBWHoi4ny3bsEqkkq2y2Un8Df5oZO7tqQXuBiw-R7cjOG_tNPH5DyBvmgWNzx5PMeZfkpfWJyR3aFTfWMVdIGS4KfxEnJ9V8Lr9eS_WFYZXoQ_soFBHWajRubUIGEqTjR9YeysNg7SXe3LrNwCXBaK70-_HG16qEHKVSqyQH2EV5zb-b39iOboiV7pI9jC3EY5pRVtJtZ6FhN5rt_cc4HpD7IwWlHyJmHpJbrn1E7saklFePyS9ADkVhp37p6JnGWT-nUeT4Pf18cQXIQRUT2rQ_GtNgsh66iDpQFMgkHVY_ux6ehCi_9pyOASO089TqS4c5gpKM1g6VK7CNRdj1VI8wcTX14MF3Blj9sHxCvs0-nU6PkzFlQ2LBmIekZFpqXxhZFHXNbGnAvSm1qYTl3jNZW-uB72VGFAJ4RVZaKx1PPfjhqagLXvOnZKftWrdPaG6ZdHmVlpWBhSaTGrXJOCt0phFAZkIO1l9O2VHPHNNqXCjwa3B-lbVKquDkwPxOyNtN9UUU8thWMbsOAzWEPyc-pjlRfEubgz-xsnnJx65d4SFMM52GBovaT8i7rdWh33HNWHdN15hTYPnYk25dt1qqioscyHohJuRZxOKmE5Zi2HDJn__DWF6Qe-sIiax4SXaGfuVekTv2cmiW_etgZVCKeQXl6ezsN8CSL-I
linkProvider	Taylor & Francis
linkToHtml	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Nb9QwELVQAUEPlI9Cl08fEBJSUzZxnMTcYMVSxLLisKi9WbZjl0glWSXZSv0N_GlmYu-KgvYC18ieyM4b-008fkPIy8QBx2aWRbF1Nkoz4yKdWvQrpo1NLBdiuCg8y-fz4vRUfA1ZlV1Iq8QY2nmhiGGtRufGn9Ho4cjH3xhzJI4Gd8_w6tZ1DnsspvMtpiebYKvIRdBKLaIUcOf1Nf_ufmU_uqJWukv2MLkQz2mCrqTdTkOH7Wi69z8DuUvuBBJK33nU3CPXbH2f3PRlKS8fkJ-AHYrSTm1n6YnCeT-jXub4Lf14fgnYQR0TWtXfK11huR669EpQFOgk7Vc_mhaeDHl-9RkNKSO0cdSoC4tVgqKYlha1K7CPQeC1VAWg2JI6iOEbDby-7_bJt-mHxeQ4CkUbIgPu3EdZooRyXAvOyzIxmYYAJ1O6yA1zLhGlMQ4YX6xzngOziDNjhGVjB5H4OC85K9lDslM3tT0gNDWJsGkxzgoNS00sFKqTsYSrWCGE9Igcrj-dNEHRHAtrnEuIbHB-pTFSyCHMgfkdkVeb5ksv5bGtYfw7DmQ__DtxvtCJZFv6HP4Jls1L3jf1Co9hqslk6LAs3Yi83toc7IZVY22arkEnwffRkqpts-pkwfIU6DrPR-SRB-PGSDLGxOGMPf6Hsbwgt44XX2Zy9mn--Qm5vc6XiPlTstO3K_uM3DAXfdW1zweX-wXdQjIS
linkToPdf	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lb9QwELZQeagcKG-Wpw8ICakpmzgvc4OFBUS16qGovVn2xC6R2mSVzVbqb-BPM2NnVy1oL3CN7InsfGN_E4-_Yex14pBjCyui2DobpTm4yKSW_EoYsInNpPQXhfeL2aw8PpYHl0p9UVolxdAuCEX4tZqce145cnCi4-8A9uSe9_acbm5d96JYCOXD6dE61ioLOUilllGKsAvymn93v7IdXRErvc12KLeQjmkGWUm7mYX63Wi68x_juMvuDBSUfwiYuceu2eY-uxmKUl48YL8QOZyEnbqF5UeaZv2EB5Hj9_zL6QUih1RMeN38rE1NxXr4POhAcSSTvF-etR0-8Vl-zQkfEkZ46zjoc0s1gqKYV5aUK6gPEOw6rgeY2Io7jOBbg6y-XzxkP6afDydfo6FkQwTozH2UJ1pqlxmZZVWVQG4wvMm1KQsQziWyAnDI92JTZAXyijgHkFaMHcbh46LKRCUesa2mbewTxlNIpE3LcV4aXGhiqUmbTCSZjjUByIzY7urLKRj0zKmsxqnCuIbmVwEoqXyQg_M7Ym_WzedByGNTw_gyDFTv_5y4UOZEiQ19dv_EyvolH9tmSYcw9WTiOyACRuztxuZod1gzVqb5CnMKPZ8s6ca2y4UqRZEiWc-KEXscsLg2kowpbTgXT_9hLK_YrYNPU7X_bfb9GdteJUvE2XO21XdL-4LdgPO-XnQvvcP9BgdGMLY
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=The+reverse+Warburg+effect%3A+glycolysis+inhibitors+prevent+the+tumor+promoting+effects+of+caveolin-1+deficient+cancer+associated+fibroblasts&rft.jtitle=Cell+cycle+%28Georgetown%2C+Tex.%29&rft.au=Bonuccelli%2C+Gloria&rft.au=Whitaker-Menezes%2C+Diana&rft.au=Castello-Cros%2C+Remedios&rft.au=Pavlides%2C+Stephanos&rft.date=2010-05-15&rft.issn=1551-4005&rft.eissn=1551-4005&rft.volume=9&rft.issue=10&rft.spage=1960&rft_id=info:doi/10.4161%2Fcc.9.10.11601&rft.externalDBID=NO_FULL_TEXT
thumbnail_l	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1538-4101&client=summon
thumbnail_m	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1538-4101&client=summon
thumbnail_s	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1538-4101&client=summon