Progastrin a new pro-angiogenic factor in colorectal cancer

Oncogene

Volumn 34, Issue 24, 2015, Pages 3120-3130

  Najib, S ^a   Kowalski Chauvel, A ^a   Do, C ^a   Roche, S ^b   Cohen Jonathan Moyal, E ^a,c   Seva, C ^a  

^a CANCER RESEARCH CENTER OF TOULOUSE   (France)

^b Centre National de la Recherche Scientifique   (France)

^c INSTITUT CLAUDIUS REGAUD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANGIOGENIC FACTOR; FOCAL ADHESION KINASE; P125 FAK PROTEIN; PAXILLIN; PROGASTRIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; BIG GASTRIN; GASTRINS; PROTEIN PRECURSORS; RNA, SMALL INTERFERING;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CELL MIGRATION; CELL PERMEABILIZATION; CELL PROLIFERATION; CHICK; CHORIOALLANTOIS; COLORECTAL CANCER; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; METASTASIS; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; TREATMENT RESPONSE; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMALS; BLOOD SUPPLY; CELLS, CULTURED; CHICK EMBRYO; COLORECTAL NEOPLASMS; GENETICS; HCT116 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, SCID; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PHYSIOLOGY;

MUS; MUS MUSCULUS;

ANIMALS; CELLS, CULTURED; CHICK EMBRYO; COLORECTAL NEOPLASMS; GASTRINS; HCT116 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, SCID; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN PRECURSORS; RNA, SMALL INTERFERING;

EID: 84930821804     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.255     Document Type: Article

References (40)

1. Rmali KA, Puntis MC, Jiang WG. Tumour-associated angiogenesis in human colorectal cancer. Colorectal Dis 2007; 9: 3-14.
2. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 1995; 55: 3964-3968.
3. Tokunaga T, Oshika Y, Abe Y, Ozeki Y, Sadahiro S, Kijima H et al. Vascular endothelial growth factor (VEGF) mRNA isoform expression pattern is correlated with liver metastasis and poor prognosis in colon cancer. Br J Cancer 1998; 77: 998-1002.
4. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008; 8: 592-603.
5. Shojaei F. Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett 2012; 320: 130-137.
6. Clarke PA, Dickson JH, Harris JC, Grabowska A, Watson SA. Gastrin enhances the angiogenic potential of endothelial cells via modulation of heparin-binding epidermal-like growth factor. Cancer Res 2006; 66: 3504-3512.
7. Nemeth J, Taylor B, Pauwels S, Varro A, Dockray GJ. Identification of progastrin derived peptides in colorectal carcinoma extracts. Gut 1993; 34: 90-95.
8. Siddheshwar RK, Gray JC, Kelly SB. Plasma levels of progastrin but not amidated gastrin or glycine extended gastrin are elevated in patients with colorectal carcinoma. Gut 2001; 48: 47-52.
9. Van Solinge WW, Nielsen FC, Friis-Hansen L, Falkmer UG, Rehfeld JF. Expression but incomplete maturation of progastrin in colorectal carcinomas. Gastroenterology 1993; 104: 1099-1107.
10. Smith AM, Watson SA. Gastrin and gastrin receptor activation: an early event in the adenoma-carcinoma sequence. Gut 2000; 47: 820-824.
11. Baldwin GS, Hollande F, Yang Z, Karelina Y, Paterson A, Strang R et al. Biologically active recombinant human progastrin(6-80) contains a tightly bound calcium ion. J Biol Chem 2001; 276: 7791-7796.
12. Brown D, Yallampalli U, Owlia A, Singh P. pp60c-Src Kinase mediates growth effects of the full-length precursor progastrin1-80 peptide on rat intestinal epithelial cells, in vitro. Endocrinology 2003, Jan 144: 201-211.
13. Hollande F, Lee DJ, Choquet A, Roche S, Baldwin GS. Adherens junctions and tight junctions are regulated via different pathways by progastrin in epithelial cells. J Cell Sci 2003; 116(Pt 7): 1187-1197.
14. Singh P, Lu X, Cobb S, Miller BT, Tarasova N, Varro A et al. Progastrin1-80 stimulates growth of intestinal epithelial cells in vitro via high-affinity binding sites. Am J Physiol Gastrointest Liver Physiol 2003; 284: G328-G339.
15. Umar S, Sarkar S, Cowey S, Singh P. Activation of NF-kappaB is required for mediating proliferative and antiapoptotic effects of progastrin on proximal colonic crypts of mice, in vivo. Oncogene 2008; 27: 5599-5611.
16. Wu H, Owlia A, Singh P. Precursor peptide progastrin(1-80) reduces apoptosis of intestinal epithelial cells and upregulates cytochrome c oxidase Vb levels and synthesis of ATP. Am J Physiol Gastrointest Liver Physiol 2003; 285: G1097-G1110.
17. Singh P, Velasco M, Given R, Varro A, Wang TC. Progastrin expression predisposes mice to colon carcinomas and adenomas in response to a chemical carcinogen. Gastroenterology 2000; 119: 162-171.
18. Wang TC, Koh TJ, Varro A, Cahill RJ, Dangler CA, Fox JG et al. Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 1996; 98: 1918-1929.
19. Ferrand A, Bertrand C, Portolan G, Cui G, Carlson J, Pradayrol L et al. Signaling pathways associated with colonic mucosa hyperproliferation in mice overexpressing gastrin precursors. Cancer Res 2005; 65: 2770-2777.
20. Dimaline R, Varro A. Novel Roles of Gastrin. J Physiol 2014; 592: 2951-2958.
21. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-676.
22. Chen XL, Nam JO, Jean C, Lawson C, Walsh CT, Goka E et al. VEGF-induced vascular permeability is mediated by FAK. Dev Cell 2012; 22: 146-157.
23. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006; 8: 1223-1234.
24. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999; 98: 147-157.
25. Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M et al. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA 1999; 96: 9815-9820.
26. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 2004; 5: 261-270.
27. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 1998; 111(Pt 13): 1853-1865.
28. Abedi H, Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 1997; 272: 15442-15451.
29. Do C, Bertrand C, Palasse J, Delisle MB, Shulkes A, Cohen-Jonathan-Moyal E et al. A new biomarker that predicts colonic neoplasia outcome in patients with hyperplastic colonic polyps. Cancer Prev Res 2012; 5: 675-684.
30. Des Guetz G, Uzzan B, Nicolas P, Cucherat M, Morere JF, Benamouzig R et al. Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer 2006; 94: 1823-1832.
31. Clarke JM, Hurwitz HI. Understanding and targeting resistance to anti-angiogenic therapies. J Gastrointest Oncol 2013; 4: 253-263.
32. Duckworth CA, Clyde D, Worthley DL, Wang TC, Varro A, Pritchard DM. Progastrininduced secretion of insulin-like growth factor 2 from colonic myofibroblasts stimulates colonic epithelial proliferation in mice. Gastroenterology 2013; 145: 197-208.
33. Hollande F, Imdahl A, Mantamadiotis T, Ciccotosto GD, Shulkes A, Baldwin GS. Glycine-extended gastrin acts as an autocrine growth factor in a nontransformed colon cell line. Gastroenterology 1997; 113: 1576-1588.
34. Jin G, Westphalen CB, Hayakawa Y, Worthley DL, Asfaha S, Yang X et al. Progastrin stimulates colonic cell proliferation via CCK2R-and ?-arrestin-dependent suppression of BMP2. Gastroenterology 2013; 145: 820-830.
35. Sirvent A, Benistant C, Pannequin J, Veracini L, Simon V, Bourgaux JF et al. Src family tyrosine kinases-driven colon cancer cell invasion is induced by Csk membrane delocalization. Oncogene 2010; 29: 1303-1315.
36. Kowalski-Chauvel A, Najib S, Tikhonova IG, Huc L, Lopez F, Martinez LO et al. Identification of the F1-ATPase at the cell surface of colonic epithelial cells: role in mediating cell proliferation. J Biol Chem 2013; 287: 41458-41468.
37. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 2009; 284: 25602-25611.
38. Bertrand C, Kowalski-Chauvel A, Do C, Resa C, Najib S, Daulhac L et al. A gastrin precursor, gastrin-gly, upregulates VEGF expression in colonic epithelial cells through an HIF-1-independent mechanism. Int J Cancer 2010; 126: 2847-2857.
39. Ribatti D, Nico B, Vacca A, Presta M. The gelatin sponge-chorioallantoic membrane assay. Nat Protoc 2006; 1: 85-91.
40. Ciccotosto GD, McLeish A, Hardy KJ, Shulkes A. Expression, processing, and secretion of gastrin in patients with colorectal carcinoma. Gastroenterology 1995; 109: 1142-1153.