Vascular endothelial growth factor C disrupts the endothelial lymphatic barrier to promote colorectal cancer invasion

Gastroenterology

Volumn 148, Issue 7, 2015, Pages 1438-1451.e8

  Tacconi, Carlotta ^a   Correale, Carmen ^a   Gandelli, Alessandro ^a   Spinelli, Antonino ^a   Dejana, Elisabetta ^b,c   D'Alessio, Silvia ^a,c   Danese, Silvio ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Colon Cancer; Mouse Model; Tumor Progression; VEGFC

Indexed keywords

ADENOVIRUS VECTOR; BETA CATENIN; PODOPLANIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; CADHERIN; LEUKOCYTE ANTIGEN; VEGFC PROTEIN, HUMAN; VEGFR3 PROTEIN, HUMAN;

ADENOVIRIDAE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; CYTOPLASM; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERNALIZATION; LIVER; LUNG PARENCHYMA; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR INVASION; TUMOR MICROENVIRONMENT; UPREGULATION; XENOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; CASE CONTROL STUDY; COLORECTAL TUMOR; ENDOTHELIUM CELL; GENETIC TRANSFECTION; GENETICS; LIVER TUMOR; LUNG TUMOR; LYMPH NODE METASTASIS; METABOLISM; NUDE MOUSE; PATHOLOGY; SECONDARY; TIME; TUMOR CELL LINE; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD; CADHERINS; CASE-CONTROL STUDIES; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; ENDOTHELIAL CELLS; ENDOTHELIUM, LYMPHATIC; ENDOTHELIUM, VASCULAR; HUMANS; LIVER NEOPLASMS; LUNG NEOPLASMS; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84930021607     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.03.005     Document Type: Article

References (50)

1. A. Schoppmann, D. Tamandl, and B. Herberger Comparison of lymphangiogenesis between primary colorectal cancer and corresponding liver metastases Anticancer Res 31 2011 4605 4611
2. X. Li, B. Liu, and J. Xiao Roles of VEGF-C and Smad4 in the lymphangiogenesis, lymphatic metastasis, and prognosis in colon cancer J Gastrointest Surg 15 2011 2001 2010
3. A. Broermann, M. Winderlich, and H. Block Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo J Exp Med 208 2011 2393 2401
4. A. Garouniatis, A. Zizi-Sermpetzoglou, and S. Rizos Vascular endothelial growth factor receptors 1,3 and caveolin-1 are implicated in colorectal cancer aggressiveness and prognosis - correlations with epidermal growth factor receptor, CD44v6, focal adhesion kinase, and c-Met Tumour Biol 34 2013 2109 2117
5. D. Royston, and D.G. Jackson Mechanisms of lymphatic metastasis in human colorectal adenocarcinoma J Pathol 217 2009 608 619
6. Y. Wang, and G. Oliver Current views on the function of the lymphatic vasculature in health and disease Genes Dev 24 2010 2115 2126
7. B. Pytowski, J. Goldman, and K. Persaud Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody J Natl Cancer Inst 97 2005 14 21
8. M.L. George, M.G. Tutton, and F. Janssen VEGF-A, VEGF-C, and VEGF-D in colorectal cancer progression Neoplasia 3 2001 420 427
9. M. Shibuya, and L. Claesson-Welsh Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis Exp Cell Res 312 2006 549 560
10. T. Tammela, and K. Alitalo Lymphangiogenesis: molecular mechanisms and future promise Cell 140 2010 460 476
11. P.S. Steeg Tumor metastasis: mechanistic insights and clinical challenges Nat Med 12 2006 895 904
12. S.J. Mandriota, L. Jussila, and M. Jeltsch Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis EMBO J 20 2001 672 682
13. M. Skobe, T. Hawighorst, and D.G. Jackson Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis Nat Med 7 2001 192 198
14. Y. He, I. Rajantie, and K. Pajusola Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels Cancer Res 65 2005 4739 4746
15. S.A. Stacker, S.P. Williams, and T. Karnezis Lymphangiogenesis and lymphatic vessel remodelling in cancer Nat Rev Cancer 14 2014 159 172
16. E. Dejana, F. Orsenigo, and M.G. Lampugnani The role of adherens junctions and VE-cadherin in the control of vascular permeability J Cell Sci 121 2008 2115 2122
17. D. Leckband, and S. Sivasankar Mechanism of homophilic cadherin adhesion Curr Opin Cell Biol 12 2000 587 592
18. M.G. Lampugnani, M. Corada, and L. Caveda The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin) J Cell Biol 129 1995 203 217
19. S. Weis, J. Cui, and L. Barnes Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis J Cell Biol 167 2004 223 229
20. M. Donigan, B.D. Loh, and L.S. Norcross A metastatic colon cancer model using nonoperative transanal rectal injection Surg Endosc 24 2010 642 647
21. M. Nagahashi, S. Ramachandran, and O.M. Rashid Lymphangiogenesis: a new player in cancer progression World J Gastroenterol 16 2010 4003 4012
22. S. D'Alessio, C. Correale, and C. Tacconi VEGF-C-dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease J Clin Invest 124 2014 3863 3878
23. T. Karpanen, and K. Alitalo Lymphatic vessels as targets of tumor therapy? J Exp Med 194 2001 F37 F42
24. P. Baluk, J. Fuxe, and H. Hashizume Functionally specialized junctions between endothelial cells of lymphatic vessels J Exp Med 204 2007 2349 2362
25. A. Alam, I. Blanc, and G. Gueguen-Dorbes SAR131675, a potent and selective VEGFR-3-TK inhibitor with antilymphangiogenic, antitumoral, and antimetastatic activities Mol Cancer Ther 11 2012 1637 1649
26. S.M. Weis, and D.A. Cheresh Tumor angiogenesis: molecular pathways and therapeutic targets Nat Med 17 2011 1359 1370
27. M. Matsumoto, S. Roufail, and R. Inder Signaling for lymphangiogenesis via VEGFR-3 is required for the early events of metastasis Clin Exp Metastasis 30 2013 819 832
28. M.G. Achen, and S.A. Stacker Vascular endothelial growth factor-D: signaling mechanisms, biology, and clinical relevance Growth Factors 30 2012 283 296
29. R. Liersch, S. Hirakawa, and W.E. Berdel Induced lymphatic sinus hyperplasia in sentinel lymph nodes by VEGF-C as the earliest premetastatic indicator Int J Oncol 41 2012 2073 2078
30. A. Saaristo, T. Veikkola, and B. Enholm Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes FASEB J 16 2002 1041 1049
31. C.T. Mierke Role of the endothelium during tumor cell metastasis: is the endothelium a barrier or a promoter for cell invasion and metastasis? J Biophys 2008 2008 183516
32. M. Corada, M. Mariotti, and G. Thurston Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo Proc Natl Acad Sci U S A 96 1999 9815 9820
33. D. Schulte, V. Kuppers, and N. Dartsch Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability EMBO J 30 2011 4157 4170
34. J. Folkman Angiogenesis Annu Rev Med 57 2006 1 18
35. J.W. Breslin, S.Y. Yuan, and M.H. Wu VEGF-C alters barrier function of cultured lymphatic endothelial cells through a VEGFR-3-dependent mechanism Lymphat Res Biol 5 2007 105 113
36. T. Tammela, A. Saaristo, and T. Holopainen Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation Nat Med 13 2007 1458 1466
37. S.D. Nathanson Insights into the mechanisms of lymph node metastasis Cancer 98 2003 413 423
38. J.W. Breslin ROCK and cAMP promote lymphatic endothelial cell barrier integrity and modulate histamine and thrombin-induced barrier dysfunction Lymphat Res Biol 9 2011 3 11
39. A. Alitalo, and M. Detmar Interaction of tumor cells and lymphatic vessels in cancer progression Oncogene 31 2012 4499 4508
40. A. Grothey, E. Van Cutsem, and A. Sobrero Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial Lancet 381 2013 303 312
41. V. Schacht, S.S. Dadras, and L.A. Johnson Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors Am J Pathol 166 2005 913 921
42. H.K. Schackert, and I.J. Fidler Development of an animal model to study the biology of recurrent colorectal cancer originating from mesenteric lymph system metastases Int J Cancer 44 1989 177 181
43. T. Dull, R. Zufferey, and M. Kelly A third-generation lentivirus vector with a conditional packaging system J Virol 72 1998 8463 8471
44. B. Pytowski, J. Goldman, and K. Persaud Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody J Natl Cancer Inst 97 2005 14 21
45. S. D'Alessio, C. Correale, and C. Tacconi VEGF-C-dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease J Clin Invest 124 2014 3863 3878
46. E. Vega-Avila, and M.K. Pugsley An overview of colorimetric assay methods used to assess survival or proliferation of mammalian cells Proc West Pharmacol Soc 54 2011 10 14
47. I.B. Enquist, Z. Good, and A.M. Jubb Lymph node-independent liver metastasis in a model of metastatic colorectal cancer Nat Commun 5 2014 3530
48. T. Tammela, T.V. Petrova, and K. Alitalo Molecular lymphangiogenesis: new players Trends Cell Biol 15 2005 434 441
49. F. Scaldaferri, S. Vetrano, and M. Sans VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis Gastroenterology 136 2009 585 595 e5
50. J.W. Breslin, S.Y. Yuan, and M.H. Wu VEGF-C alters barrier function of cultured lymphatic endothelial cells through a VEGFR-3-dependent mechanism Lymphat Res Biol 5 2007 105 113