Tumor-derived GM-CSF promotes inflammatory colon carcinogenesis via stimulating epithelial release of VEGF

Cancer Research

Volumn 74, Issue 3, 2014, Pages 716-726

  Wang, Yi ^a   Han, Gencheng ^a   Wang, Ke ^a,b   Liu, Guijun ^c   Wang, Renxi ^a   Xiao, He ^a   Li, Xinying ^a   Hou, Chunmei ^a   Shen, Beifen ^a   Guo, Renfeng ^d   Li, Yan ^a   Chen, Guojiang ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c INNER MONGOLIA MEDICAL COLLEGE   (China)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHRONIC DISEASE; COLITIS; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MALE; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; TOLL-LIKE RECEPTOR 4; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84893837713     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1459     Document Type: Article

References (37)

1. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
2. Itzkowitz SH, Yio X. Inflammation and cancer. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-17.
3. Seril DN, Liao J, Yang GY, Yang CS. Oxidative stress and ulcerative colitis-associated carcinogenesis: studies in humans and animal models. Carcinogenesis 2003;24:353-62.
4. Rutter M, Saunders B, Wilkinson K, Rumbles S, Schofield G, Kamm M, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004;126:451-9.
5. Fantini MC, Pallone F. Cytokines: from gut inflammation to colorectal cancer. Curr Drug Targets 2008;9:375-80.
6. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6.
7. Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 2006;312:549-60.
8. Costa C, Incio J, Soares R. Angiogenesis and chronic inflammation: cause or consequence? Angiogenesis 2007;10:149-66.
9. Waldner MJ,Wirtz S, Jefremow A, Warntjen M, Neufert C, Atreya R, et al. VEGF receptor signaling links inflammation and tumorigenesis in colitis-associated cancer. J Exp Med 2010;207:2855-68.
10. Noguchi M, Hiwatashi N, Liu ZX, Toyota T. Increased secretion of granulocyte-macrophage colony-stimulating factor in mucosal lesions of inflammatory bowel disease. Digestion 2001;63:32-36.
11. Ina K, Kusugami K, Hosokawa T, Imada A, Shimizu T, Yama guchi T, et al. Increased mucosal production of granulocyte colony-stimulating factor is related to a delay in neutrophil apoptosis in inflammatory bowel disease. J Gastroenterol Hepatol 1999;14:46-53.
12. Xu Y, Hunt NH, Bao S. The role of granulocyte macrophage- colonystimulating factor in acute intestinal inflammation. Cell Res 2008;18: 1220-9.
13. Bernasconi E, Favre L, Maillard MH, Bachmann D, Pythoud C, Bouzourene H, et al. Granulocyte-macrophage colony-stimulating factor elicits bone marrow-derived cells that promote efficient colonic mucosal healing. Inflamm Bowel Dis 2010;16:428-41.
14. Wirtz S, Neufert C, Weigmann B, Neurath MF. Chemically induced mouse models of intestinal inflammation. Nat Protoc 2007;2: 541-6.
15. Wang K, Han G, Dou Y, Wang Y, Liu G, Wang R, et al. Opposite role of tumor necrosis factor receptors in dextran sulfate sodium-induced colitis in mice. PLoS ONE 2012;7:e52924.
16. Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, et al. The Toll-Interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 2007;26: 461-75.
17. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, et al. IL-6 and stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009;15: 103-113.
18. Martinez-Moczygemba M, Huston DP. Biology of common b receptorsignaling cytokines: IL-3, IL-5, and GM-CSF. J Allergy Clin Immunol 2003;112:653-65.
19. De Groot RP, Coffer PJ, Koenderman L. Regulation of proliferation, differentiation and survival by the IL-3/IL-5/GM-CSF receptor family. Cell Signal 1998;16:301-13.
20. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004;118:229-41.
21. Calvani M, Trisciuoglio D, Bergamaschi C, Shoemaker RH, Melillo G. Differential involvement of vascular endothelial growth factor in the survival of hypoxic colon cancer cells. Cancer Res 2008;68:285-91.
22. Nguyen QD, Rodrigues S, Rodrigue CM, Rivat C, Grijelmo C, Bruyneel E, et al. Inhibition of vascular endothelial growth factor (VEGF)-165 and semaphorin 3A-mediated cellular invasion and tumor growth by the VEGF signaling inhibitor ZD4190 in human colon cancer cells and xenografts. Mol Cancer Ther 2006;5:2070-7.
23. Sussman DA, Santaolalla R, Strobel S, Dheer R, Abreu MT. Cancer in inflammatory bowel disease: lessons from animal models. Curr Opin Gastroenterol 2012;28:327-33.
24. Fukata M, Chen A, Vamadevan AS, Cohen J, Breglio K, Krishnareddy S, et al. Toll-like receptor-4 promotes the development of colitisassociated colorectal tumors. Gastroenterology 2007;133:1869-81.
25. Egea L, McAllister CS, Lakhdari O, Minev I, Shenouda S, Kagnoff MF. GM-CSF produced by nonhematopoietic cells is required for early epithelial cell proliferation and repair of injured colonic mucosa. J Immunol 2013;190:1702-13.
26. Sainathan SK, Hanna EM, Gong Q, Bishupuri KS, Luo Q, Colonna M, et al. Granulocyte macrophage colony-stimulating factor ameliorates DSS-induced experimental colitis. Inflamm Bowel Dis 2008;14:88-99.
27. Revoltella P, Menicagli M, Campani D. Granulocyte-macrophage colony-stimulating factor as an autocrine survival-growth factor in human gliomas. Cytokine 2012;57:347-59.
28. Cianfarani F, Tommasi R, Failla CM, Viviano MT, Annessi G, Papi M, et al. Granulocyte/macrophage colony-stimulating factor treatment of human chronic ulcers promotes angiogenesis associated with de novo vascular endothelial growth factor transcription in the ulcer bed. Br J Dermatol 2006;154:34-41.
29. Hu D, Fukuhara A, Miyata Y, Yokoyama C, Otsuki M, Kihara S, et al. Adiponectin regulates vascular endothelial growth factor-C expression in macrophages via Syk-ERK pathway. PLoS ONE 2013;8: e56071.
30. Clarke DN, Al Ahmad A, Lee B, Parham C, Auckland L, Fertala A, et al. Perlecan Domain V induces VEGf secretion in brain endothelial cells through integrin a5b1 and ERK-dependent signaling pathways. PLoS ONE 2012;7:e45257.
31. Shen K, Ji L, Gong C, Ma Y, Yang L, Fan Y, et al. Notoginsenoside Ft1 promotes angiogenesis via HIF-1a mediated VEGF secretion and the regulation of PI3K/AKT and Raf/MEK/ERK signaling pathways. Biochem Pharmacol 2012;84:784-92.
32. Keith B, Johnson RS, Simon MC. HIF1a and HIF2a: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2011;12:9-22.
33. Fleetwood AJ, Cook AD, Hamilton JA. Functions of granulocytemacrophage colony-stimulating factor. Crit Rev Immunol 2005;25: 405-28.
34. Newton R, King EM, Gong W, Rider CF, Staples KJ, Holden NS, et al. Glucocorticoids inhibit IL-1beta-induced GM-CSF expression at multiple levels: roles for the ERK pathway and repression by MKP-1. Biochem J 2010;427:113-24.
35. Popivanova BK, Kitamura K,WuY, Kondo T, Kagaya T, Kaneko S, et al. Blocking TNF-a in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-70.
36. Imani Fooladi AA, Mousavi SF, Seghatoleslami S, Yazdani S, Nourani MR. Toll-like receptors: role of inflammation and commensal bacteria. Inflamm Allergy Drug Targets 2011;10:198-207.
37. Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, et al. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell 2012;21:822-35.