Colon cancer growth and dissemination relies upon thrombin, Stromal PAR-1, and fibrinogen

Cancer Research

Volumn 75, Issue 19, 2015, Pages 4235-4243

  Adams, Gregory N ^a   Rosenfeldt, Leah ^a   Frederick, Malinda ^a   Miller, Whitney ^a   Waltz, Dusty ^a   Kombrinck, Keith ^a   McElhinney, Kathryn E ^a   Flick, Matthew J ^a   Monia, Brett P ^b   Revenko, Alexey S ^b   Palumbo, Joseph S ^a  

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

^b ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; PROTHROMBIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MALE; METASTASIS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR INVASION; TUMOR NECROSIS; TUMOR VASCULARIZATION; ADENOCARCINOMA; AFIBRINOGENEMIA; ANIMAL; C57BL MOUSE; CELL DIVISION; COLON TUMOR; COMPARATIVE STUDY; COMPLICATION; DEFICIENCY; DISEASE COURSE; EXPERIMENTAL MELANOMA; GENETICS; HCT 116 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; STROMA CELL; TRANSPLANTATION; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; TUMOR VOLUME; VASCULARIZATION; XENOGRAFT;

ADENOCARCINOMA; AFIBRINOGENEMIA; ANIMALS; CELL DIVISION; CELL LINE, TUMOR; COLONIC NEOPLASMS; DISEASE PROGRESSION; FEMALE; FIBRINOGEN; HCT116 CELLS; HETEROGRAFTS; HUMANS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; PROTHROMBIN; RECEPTOR, PAR-1; STROMAL CELLS; THROMBIN; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84945561052     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0964     Document Type: Article

References (55)

1. Palumbo JS. Mechanisms linking tumor cell-associated procoagulant function to tumor dissemination. Semin Thromb Hemost 2008;34: 154-60.
2. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and -independent mechanisms. Blood 2007;19:19.
3. Ruf W. Tissue factor and cancer. Thromb Res 2012;130 Suppl 1:S84-7.
4. Kasthuri RS, Taubman MB, Mackman N. Role of tissue factor in cancer. J Clin Oncol 2009;27:4834-8.
5. Horowitz NA, Blevins EA, Miller WM, Perry AR, Talmage KE, Mullins ES, et al. Thrombomodulin is a determinant of metastasis through a mechanism linked to the thrombin binding domain but not the lectin-like domain. Blood 2011;118:2889-95.
6. Yokota N, Zarpellon A, Chakrabarty S, Bogdanov VY, Gruber A, Castellino FJ, et al. Contributions of thrombin targets to tissue factor-dependent metastasis in hyperthrombotic mice. J Thromb Haemost 2014;12:71-81.
7. Palumbo JS, Barney KA, Blevins EA, Shaw MA, Mishra A, Flick MJ, et al. Factor XIII transglutaminase supports hematogenous tumor cell metastasis through a mechanism dependent on natural killer cell function. J Thromb Haemost 2008;6:812-9.
8. 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 fibrinogen-deficient mice. Cancer Res 2002;62:6966-72.
9. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 2005;105:178-85.
10. Camerer E, Qazi AA, Duong DN, Cornelissen I, Advincula R, Coughlin SR. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 2004;104:397-401.
11. Schulze EB, Hedley BD, Goodale D, Postenka CO, Al-Katib W, Tuck AB, et al. The thrombin inhibitor Argatroban reduces breast cancer malignancy and metastasis via osteopontin-dependent and osteopontin-independent mechanisms. Breast Cancer Res Treat 2008;112:243-54.
12. De Feo K, Hayes C, Chernick M, Ryn JV, Gilmour SK. Use of dabigatran etexilate to reduce breast cancer progression. Cancer Biol Ther 2010;10: 1001-8.
13. Nieman MT, La Rusch G, Fang C, Zhou Y, Schmaier AH. Oral thrombostatin FM19 inhibits prostate cancer. Thromb Haemost 2010;104:1044-8.
14. Hu L, Lee M, Campbell W, Perez-Soler R, Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood 2004;104:2746-51.
15. Hu L, Ibrahim S, Liu C, Skaar J, Pagano M, Karpatkin S. Thrombin induces tumor cell cycle activation and spontaneous growth by down-regulation of p27Kip1, in association with the up-regulation of Skp2 and MiR-222. Cancer Res 2009;69:3374-81.
16. Versteeg HH, Schaffner F, Kerver M, Ellies LG, Andrade-Gordon P, Mueller BM, et al. Protease-activated receptor (PAR) 2, but not PAR1, signaling promotes the development of mammary adenocarcinoma in polyoma middle T mice. Cancer Res 2008;68:7219-27.
17. Wojtukiewicz MZ, Sierko E, Rak J. Contribution of the hemostatic system to angiogenesis in cancer. Semin Thromb Hemost 2004;30:5-20.
18. Popovic M, Smiljanic K, Dobutovic B, Syrovets T, Simmet T, Isenovic ER. Thrombin and vascular inflammation. Mol Cell Biochem 2012;359: 301-13.
19. Meoli DF, White RJ. Thrombin induces fibronectin-specific migration of pulmonary microvascular endothelial cells: requirement of calcium/calmodulin-dependent protein kinase II. Am J Physiol Lung Cell Mol Physiol 2009;297:L706-14.
20. Davalos D, Akassoglou K. Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol 2012;34:43-62.
21. Rondina MT, Weyrich AS, Zimmerman GA. Platelets as cellular effectors of inflammation in vascular diseases. Circ Res 2013;112:1506-19.
22. Gawaz M, Vogel S. Platelets in tissue repair: control of apoptosis and interactions with regenerative cells. Blood 2013;122:2550-4.
23. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986;315:1650-9.
24. Vossen CY, Hoffmeister M, Chang-Claude JC, Rosendaal FR, Brenner H. Clotting factor gene polymorphisms and colorectal cancer risk. J Clin Oncol 2011;29:1722-7.
25. Turpin B, Miller W, Rosenfeldt L, Kombrinck K, Flick MJ, Steinbrecher KA, et al. Thrombin drives tumorigenesis in colitis-associated colon cancer. Cancer Res 2014;74:3020-30.
26. Steinbrecher KA, Horowitz NA, Blevins EA, Barney KA, Shaw MA, Harmel-Laws E, et al. Colitis-associated cancer is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin alpha (M)beta(2) engagement of fibrinogen. Cancer Res 2010;70:2634-43.
27. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet 2014;383:1490-502.
28. Mullins ES, Kombrinck KW, Talmage KE, Shaw MA, Witte DP, Ullman JM, et al. Genetic elimination of prothrombin in adult mice is not compatible with survival and results in spontaneous hemorrhagic events in both heart and brain. Blood 2009;113:696-704.
29. Suh TT, Holmback K, Jensen NJ, Daugherty CC, Small K, Simon DI, et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 1995;9:2020-33.
30. Darrow AL, Fung-Leung WP, Ye RD, Santulli RJ, Cheung WM, Derian CK, et al. Biological consequences of thrombin receptor deficiency in mice. Thromb Haemost 1996;76:860-6.
31. Laubli H, Pearce OM, Schwarz F, Siddiqui SS, Deng L, Stanczak MA, et al. Engagement of myelomonocytic Siglecs by tumor-associated ligands modulates the innate immune response to cancer. Proc Natl Acad Sci U S A 2014;111:14211-6.
32. Rak J, Mitsuhashi Y, Bayko L, Filmus J, Shirasawa S, Sasazuki T, et al. Mutant ras oncogenes upregulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res 1995;55:4575-80.
33. Palumbo JS, Kombrinck KW, Drew AF, Grimes TS, Kiser JH, Degen JL, et al. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 2000;96:3302-9.
34. Drew AF, Kaufman AH, Kombrinck KW, Danton MJ, Daugherty CC, Degen JL, et al. Ligneous conjunctivitis in plasminogen-deficient mice. Blood 1998;91:1616-24.
35. Tan MH, Holyoke ED, Goldrosen MH. Murine colon adenocarcinomas: methods for selective culture in vitro. J Natl Cancer Inst 1976;56:871-3.
36. Milsom C, Magnus N, Meehan B, Al-Nedawi K, Garnier D, Rak J. Tissue factor and cancer stem cells: is there a linkage? Arterioscler Thromb Vasc Biol 2009;29:2005-14.
37. Yu JL, May L, Lhotak V, Shahrzad S, Shirasawa S, Weitz JI, et al. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 2005;105:1734-41.
38. Zhao J, Aguilar G, Palencia S, Newton E, Abo A. rNAPc2 inhibits colorectal cancer in mice through tissue factor. Clin Cancer Res 2009;15:208-16.
39. Schaffner F, Versteeg HH, Schillert A, Yokota N, Petersen LC, Mueller BM, et al. Cooperation of tissue factor cytoplasmic domain and PAR2 signaling in breast cancer development. Blood 2010;116:6106-13.
40. Kocaturk B, Van den Berg YW, Tieken C, Mieog JS, de Kruijf EM, Engels CC, et al. Alternatively spliced tissue factor promotes breast cancer growth in a beta1 integrin-dependent manner. Proc Natl Acad Sci U S A 2013;110: 11517-22.
41. Siller-Matula JM, Schwameis M, Blann A, Mannhalter C, Jilma B. Thrombin as a multi-functional enzyme. Focus on in vitro and in vivo effects. Thromb Haemost 2011;106:1020-33.
42. Darmoul D, Gratio V, Devaud H, Peiretti F, Laburthe M. Activation of proteinase-activated receptor 1 promotes human colon cancer cell proliferation through epidermal growth factor receptor transactivation. Mol Cancer Res 2004;2:514-22.
43. Green D, Karpatkin S. Role of thrombin as a tumor growth factor. Cell Cycle 2010;9:656-61.
44. Coughlin SR, Camerer E. PARticipation in inflammation. J Clin Invest 2003;111:25-7.
45. Vergnolle N. Review article: proteinase-activated receptors - novel signals for gastrointestinal pathophysiology. Aliment Pharmacol Ther 2000;14: 257-66.
46. Sahni A, Francis CW. Vascular endothelial growth factor binds to fibrinogen and fibrin and stimulates endothelial cell proliferation. Blood 2000;96:3772-8.
47. Dvorak HF, Nagy JA, Berse B, Brown LF, Yeo KT, Yeo TK, et al. Vascular permeability factor, fibrin, and the pathogenesis of tumor stroma formation. Ann N Y Acad Sci 1992;667:101-11.
48. Drew AF, Liu H, Davidson JM, Daugherty CC, Degen JL. Wound-healing defects in mice lacking fibrinogen. Blood 2001;97:3691-8.
49. Mosesson MW. Fibrinogen and fibrin structure and functions. J Thromb Haemost 2005;3:1894-904.
50. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, et al. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J Neurosci 2010;30: 5843-54.
51. Flick MJ, Du X, Witte DP, Jirouskova M, Soloviev DA, Busuttil SJ, et al. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004;113:1596-606.
52. Martinez J, Ferber A, Bach TL, Yaen CH. Interaction of fibrin with VEcadherin. Ann N Y Acad Sci 2001;936:386-405.
53. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through Toll-like receptor 4. J Immunol 2001;167: 2887-94.
54. Irrazabal T, Belcheva A, Girardin SE, Martin A, Philpott DJ. The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell 2014;54:309-20.
55. Yeh CH, Gross PL, Weitz JI. Evolving use of new oral anticoagulants for treatment of venous thromboembolism. Blood 2014;124:1020-8.