Colitis-associated cancer Is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin αMβ2 engagement of fibrinogen

Cancer Research

Volumn 70, Issue 7, 2010, Pages 2634-2643

  Steinbrecher, Kris A ^a   Horowitz, Netanel A ^b   Blevins, Elizabeth A ^b   Barney, Kelley A ^b   Shaw, Maureen A ^b   Harmel Laws, Eleana ^a   Finkelman, Fred D ^a   Flick, Matthew J ^a   Pinkerton, Malinda D ^a   Talmage, Kathryn E ^a   Kombrinck, Keith W ^a   Witte, David P ^a   Palumbo, Joseph S ^b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAMBETA2 INTEGRIN; AZOXYMETHANE; DEXTRAN SULFATE; FIBRIN; FIBRINOGEN; INTEGRIN; INTEGRIN RECEPTOR; INTERLEUKIN 6; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; COLITIS; COLON ADENOMA; COLON CANCER; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE PRODUCTION; HEMOSTASIS; INFLAMMATION; MALE; MITOSIS INDEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF;

ADENOMA; ANIMALS; AZOXYMETHANE; CARCINOGENS; CELL GROWTH PROCESSES; CELL TRANSFORMATION, NEOPLASTIC; COLITIS; COLONIC NEOPLASMS; CYTOKINES; DEXTRAN SULFATE; DISEASE PROGRESSION; FIBRONECTINS; HEMOSTASIS; MACROPHAGE-1 ANTIGEN; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 77950799464     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3465     Document Type: Article

References (44)

1. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-444
2. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J Gastroenterol 2008;14:378-389
3. 3. Adams RA, Bauer J, Flick M J, et al. The fibrin-derived y377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 2007; 204:571-582 (Pubitemid 46457080)
4. Drew AF, Liu H, Davidson JM, Daugherty CC, Degen JL. Woundhealing defects in mice lacking fibrinogen. Blood 2001;97:3691-3698
5. Flick MJ, Du X, Witte DP, et al. Leukocyte engagement of fibrinogen) via the integrin receptor αMβ2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004;113:1596-1606
6. Flick MJ, LaJeunesse CM, Talmage KE, et al. Fibrinogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin αMβ2 binding motif. J Clin Invest 2007;117:3224-3235
7. 7. Danese S, Papa A, Saibeni S, Repici A, Malesci A, Vecchi M. Inflammation and coagulation in inflammatory bowel disease: the clot thickens. Am J Gastroenterol 2007;102:174-186 (Pubitemid 46072059)
8. 8. Kilic M, Yoldas O, Keskek M. et al. Prognostic value of plasma D-dimer levels in patients with colorectal cancer. Colorectal Dis 2008;10: 238-241 (Pubitemid 351284674)
9. 9. Anthoni C, Russell J, Wood KC, et al. Tissue factor: a mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med 2007;204:1595-1601 (Pubitemid 47048026)
10. Palumbo JS. Mechanisms linking tumor cell-associated procoagulant function to tumor dissemination. Semin Thromb Hemost 2008; 34:154-160
11. Laurens N, Koolwijk P, de Maat MP. Fibrin structure and wound healing. J Thromb Haemost 2006;4:932-939
12. Degen JL, Palumbo JS. Mechanisms linking hemostatic factors to tumor growth in mice. Pathophysiol Haemost Thromb 2003;33:31-35
13. Staton CA, Brown NJ, Lewis CE. The role of fibrinogen and related fragments in tumour angiogenesis and metastasis. Expert Opin Biol Ther 2003;3:1105-1120
14. Suh TT, Holmback K, Jensen NJ, et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 1995;9:2020-2033
15. Neufert C, Becker C, Neurath MF. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammationdriven tumor progression. Nat Protoč 2007;2:1998-2004.
16. Steinbrecher KA, Harmel-Laws E, Sitcheran R, Baldwin AS. Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J Immunol 2008; 180:2588-2599
17. 17. Palumbo JS, Talmage KE, Liu H, La Jeunesse CM, Witte DP, Degen JL. Plasminogen supports tumor growth through a fibrinogendependent mechanism linked to vascular patency. Blood 2003;102: 2819-2827 (Pubitemid 37248852)
18. 18. Schulzke JD, Bojarski C, Zeissig S, Heller F, Gitter AH, Fromm M. Disrupted barrier function through epithelial cell apoptosis. Ann N Y Acad Sci 2006;1072:288-299 (Pubitemid 44448461)
19. Finkelman FD, Morris SC. Development of an assay to measure in vivo cytokine production in the mouse. Int Immunol 1999;11: 1811-1818
20. Siegmund B, Fantuzzi G, Rieder F, et al. Neutralization of interleukin-18 reduces severity in murine colitis and intestinal IFN-γ and TNF-α production. Am J Physiol Regul lntegr Comp Physiol 2001; 281: R1264-73.
21. 21. Kwon KH, Murakami A, Hayashi R, Ohigashi H. Interleukin-1 β targets interleukin-6 in progressing dextran sulfate sodium-induced experimental colitis. Biochem Biophys Res Commun 2005;337:647-654 (Pubitemid 41429334)
22. Naito Y, Takagi T, Uchiyama K, et al. Reduced intestinal inflammation induced by dextran sodium sulfate in interleukin-6-deficient mice. Int J Mol Med 2004;14:191-196
23. Marini M, Bamias G, Rivera-Nieves J, et al. TNF-α neutralization ameliorates the severity of murine Crohn's-like ileitis by abrogation of intestinal epithelial cell apoptosis. Proc Natl Acad Sci U S A 2003; 100:8366-8371
24. Pluskota E, Soloviev DA, Szpak D, Weber C, Plow EF. Neutrophil apoptosis: selective regulation by different ligands of integrin αMβ2. J Immunol 2008;181:3609-3619
25. 25. Rubel C, Gomez S, Fernandez GC, Isturiz MA, Caamano J, Palermo MS. Fibrinogen-CD11b/CD18 interaction activates the NF-K B pathway and delays apoptosis in human neutrophils. Eur J Immunol 2003;33:1429-1438 (Pubitemid 36609162)
26. Nagy JA, Brown LF, Senger DR, et al. Pathogenesis of tumor stroma generations critical role for leaky blood vessels and fibrin deposition. Biochim Biophys Acta 1989;948:305-326
27. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986; 315:1650-1659
28. 28. Palumbo JS, Potter JM, Kaplan LS, Talmage K, Jackson DG, Degen JL. Spontaneous hematogenous and lymphatic metastasis, but not primary tumor growth or angiogenesis, is diminished in fibrinogendeficient mice. Cancer Res 2002;62:6966-6972 (Pubitemid 35424088)
29. Allavena P, Garlanda C, Borrello MG, Sica A, Mantovani A. Pathways connecting inflammation and cancer. Curr Opin Genet Dev 2008;18: 3-10.
30. 30. Lu H, Smith CW, Perrard J, et al. LFA-1 is sufficient in mediating neutrophil emigration in Mac-1-deficient mice. J Clin Invest 1997; 99:1340-1350 (Pubitemid 27142772)
31. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001;167:2887-2894
32. Flick MJ, Du X, Degen JL. Fibrin(ogen)-α M β 2 interactions regulate leukocyte function and innate immunity in vivo. Exp Biol Med (Maywood) 2004;229:1105-1110
33. Alex P, Zachos NC, Nguyen T, et al. Distinct cytokine patterns iden-tified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis 2009;15:341-352
34. Melgar S, Karlsson A, Michaelsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol Gastrointest Liver Physiol 2005;288:G1328-38.
35. 35. Popivanova BK, Kitamura K, Wu Y, et al. Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-570 (Pubitemid 351206546)
36. Grivennikov S, Karin E, Terzic J, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitisassociated cancer. Cancer Cell 2009;15:103-113
37. 37. Bach TL, Barsigian C, Yaen CH, Martinez J. Endothelial cell VE-cadherin functions as a receptor for the β15-42 sequence of fibrin. J Biol Chem 1998;273:30719-30728 (Pubitemid 28545554)
38. Holmback K, Danton MJ, Suh TT, Daugherty CC, Degen JL. Impaired platelet aggregation and sustained bleeding in mice lacking the fibrinogen motif bound by integrin αllb(33. Embo J 1996;15:5760-71.
39. 39. Schick PK, Wojenski CM, He X, Walker J, Marcinkiewicz C, Niewiarowski S. Integrins involved in the adhesion of megakaryocytes to fibronectin and fibrinogen. Blood 1998;92:2650-2656 (Pubitemid 28469075)
40. Suehiro K, Gailit J, Plow EF. Fibrinogen is a ligand for integrin α5β1 on endothelial cells. J Biol Chem 1997;272:5360-5366
41. Ugarova TP, Yakubenko VP. Recognition of fibrinogen by leukocyte integrins. Ann N Y Acad Sci 2001;936:368-385
42. Papa A, Scaldaferri F, Danese S, et al. Vascular involvement in inflammatory bowel disease: pathogenesis and clinical aspects. Dig Dis 2008;26:149-155
43. 43. Vowinkel T, Wood KC, Stokes KY, et al. Mechanisms of platelet and leukocyte recruitment in experimental colitis. Am J Physiol Gastrointest Liver Physiol 2007;293:G1054-60. (Pubitemid 350106564)
44. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001 ;357:539-545