The interplay between hemostasis and malignancy: The oral cancer paradigm

Anticancer Research

Volumn 32, Issue 5, 2012, Pages 1791-1800

  Yapijakis, Christos ^a   Bramos, Athanasios ^a   Nixon, Alexander Michael ^a   Ragos, Vassilis ^a   Vairaktaris, Eleftherios ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Angiogenesis; Carcinogenesis; Fibrin; Fibrinolysis; Review; Thrombin; Thrombosis; Tissue factor pathway

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 7A; FIBRIN; FIBRINOGEN; GELATINASE A; INTERLEUKIN 6; INTERLEUKIN 8; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLASMINOGEN ACTIVATOR INHIBITOR 2; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE C; THROMBIN; THROMBOMODULIN; THROMBOPLASTIN; THROMBOSPONDIN; TISSUE FACTOR PATHWAY INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UROKINASE RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; BINDING SITE; CANCER CELL; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; DNA POLYMORPHISM; FIBRINOLYSIS; GENE EXPRESSION; HEMOSTASIS; HUMAN; MOUTH SQUAMOUS CELL CARCINOMA; PRIORITY JOURNAL; REVIEW; THROMBOCYTE; THROMBOCYTE ACTIVATION;

BLOOD COAGULATION; BLOOD PLATELETS; HEMOSTASIS; HUMANS; LIPOPROTEINS; MOUTH NEOPLASMS; NEOVASCULARIZATION, PHYSIOLOGIC; THROMBIN; THROMBOMODULIN; THROMBOPLASTIN;

EID: 84861523367     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (108)

1. Elice F, Jacoub J, Rickles FR, Falanga A and Rodeghiero F: Hemostatic complications of angiogenesis inhibitors in cancer patients. Am J Hematol 83: 862-870, 2008.
2. Sutherland DE, Weitz IC and Liebman HA: Thromboembolic complications of cancer: Epidemiology, pathogenesis, diagnosis, and treatment. Am J Hematol 72: 43-52, 2003. (Pubitemid 36043750)
3. Monreal M and Trujillo-Santos J: Screening for occult cancer in patients with acute venous thromboembolism. Curr Opin Pulm Med 13: 368-671, 2007.
4. De Cicco M: The prothrombotic state in cancer: pathogenic mechanisms. Crit Rev Oncol Hematol 50: 187-196, 2004.
5. Falanga A, Panova-Noeva M and Russo L: Procoagulant mechanisms in tumour cells. Best Pract Res Clin Haematol 22: 49-60, 2009.
6. Franchini M, Montagnana M, Targher G, Manzato F and Lippi G: Pathogenesis, clinical and laboratory aspects of thrombosis in cancer. J Thromb Thrombolysis 24: 29-38, 2007. (Pubitemid 46831561)
7. Nash GF, Walsh DC and Kakkar AK: The role of the coagulation system in tumour angiogenesis. Lancet Oncol 2: 608-613, 2001. (Pubitemid 33009256)
8. Dvorak HF: Rous-Whipple Award Lecture. How tumors make bad blood vessels and stroma. Am J Pathol 162: 1747-1757, 2003.
9. Carmeliet P: Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
10. Dvorak HF: Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315: 1650-1659, 1986.
11. Wojtukiewicz MZ, Sierko E and Rak J: Contribution of the hemostatic system to angiogenesis in cancer. Semin Thromb Hemost 30: 5-20, 2004. (Pubitemid 38457297)
12. Coughlin SR: Thrombin signalling and protease-activated receptors. Nature 407: 258-264, 2000.
13. Vairaktaris E, Yapijakis C, Serefoglou Z, Avgoustidis D, Critselis E, Spyridonidou S, Vylliotis A, Derka S, Vassiliou S, Nkenke E and Patsouris E: Gene expression polymorphisms of interleukins-1beta, -4, -6, -8, -10, and tumor necrosis factors-alpha, -beta: regression analysis of their effect upon oral squamous cell carcinoma. J Cancer Res Clin Oncol 134: 821-832, 2008.
14. Yapijakis C, Serefoglou Z, Vylliotis A, Nkenke E, Derka S, Vassiliou S, Avgoustidis D, Neukam FW, Patsouris E and Vairaktaris E: Association of polymorphisms in tumor necrosis factor alpha and beta genes with increased risk for oral cancer. Anticancer Res 29(6): 2379-2386, 2009.
15. Gomez K and McVey JH: Tissue factor initiated blood coagulation. Front Biosci 11: 1349-1359, 2006. (Pubitemid 43253427)
16. Peppelenbosch MP and Versteeg HH: Cell biology of tissue factor, an unusual member of the cytokine receptor family. Trends Cardiovasc Med 11: 335-339, 2001. (Pubitemid 33116307)
17. Nemerson Y and Repke D: Tissue factor accelerates the activation of coagulation factor VII: the role of a bifunctional coagulation cofactor. Thromb Res 40: 351-358, 1985. (Pubitemid 16181507)
18. Carmeliet P, Mackman N, Moons L, Luther T, Gressens P, Van Vlaenderen I, Demunck H, Kasper M, Breier G, Evrard P, Müller M, Risau W, Edgington T and Collen D: Role of tissue factor in embryonic blood vessel development. Nature 383: 73-75, 1996. (Pubitemid 26296462)
19. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W and Nagy A: Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439, 1996b. (Pubitemid 26102719)
20. Fernandez PM, Patierno SR and Rickles FR: Tissue factor and fibrin in tumor angiogenesis. Semin Thromb Hemost 30: 31-44, 2004. (Pubitemid 38457299)
21. Arora P, Ricks TK and Trejo J: Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci 120: 921-928, 2007. (Pubitemid 46638507)
22. Yin YJ, Salah Z, Grisaru-Granovsky S, Cohen I, Even-Ram SC, Maoz M, Uziely B, Peretz T and Bar-Shavit R: Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol 23: 940-944, 2003. (Pubitemid 36713545)
23. Rao LV and Pendurthi UR: Tissue factor-factor VIIa signaling. Arterioscler Thromb Vasc Biol 25: 47-56, 2005. (Pubitemid 40054253)
24. Ruf W and Mueller BM: Thrombin generation and the pathogenesis of cancer. Semin Thromb Hemost 32(S1): 61-68, 2006.
25. Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A, Carmeliet P, Mueller BM, Friedlander M and Ruf W: Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med 10: 502-509, 2004. (Pubitemid 38667909)
26. Belting M, Ahamed J and Ruf W: Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol 25: 1545-1550, 2005. (Pubitemid 41098920)
27. Zhang Y, Deng Y, Luther T, Müller M, Ziegler R, Waldherr R, Stern DM and Nawroth PP: Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest 94: 1320-1327, 1994. (Pubitemid 24286478)
28. Abe K, Shoji M, Chen J, Bierhaus A, Danave I, Micko C, Casper K, Dillehay DL, Nawroth PP and Rickles FR: Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc Natl Acad Sci USA 96: 8663-8668, 1999. (Pubitemid 29354848)
29. Bromberg ME, Sundaram R, Homer RJ, Garen A and Konigsberg WH: Role of tissue factor in metastasis: functions of the cytoplasmic and extracellular domains of the molecule. Thromb Haemost 82: 88-92, 1999. (Pubitemid 29368778)
30. Ueno T, Toi M, Koike M, Nakamura S and Tominaga T: Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer 83: 164-170, 2000. (Pubitemid 30411712)
31. Minamiya Y, Matsuzaki I, Sageshima, Saito H, Taguchi K, Nakagawa T and Ogawa J: Expression of tissue factor mRNA and invasion of blood vessels by tumor cells in non-small cell lung cancer. Surg Today 34: 1-5, 2004. (Pubitemid 38067885)
32. Buchs AE, Zehavi S, Sher O, Yeheskely E, Muggia-Sulam M, Sherman Y and Rapoport MJ: Heparanase, galectin-3, and tissue factor mRNA are expressed in benign neoplasms of the thyroid. Endocrine 22: 81-84, 2003.
33. Wojtukiewicz MZ, Zacharski LR, Rucinska M, Zimnoch L, Jaromin J, Rózañska-Kudelska M, Kisiel W and Kudryk BJ: Expression of tissue factor and tissue factor pathway inhibitor in situ in laryngeal carcinoma. Thromb Haemost 82: 1659-1662, 1999.
34. Abdulkadir SA, Carvalhal GF, Kaleem Z, Kisiel W, Humphrey PA, Catalona WJ and Milbrandt J: Tissue factor expression and angiogenesis in human prostate carcinoma. Hum Pathol 31: 443-447, 2000. (Pubitemid 30262866)
35. Rong Y, Hu F, Huang R, Mackman N, Horowitz JM, Jensen RL, Durden DL, Van Meir EG and Brat DJ: Early growth response gene-1 regulates hypoxia-induced expression of tissue factor in glioblastoma multiforme through hypoxia-inducible factor-1-independent mechanisms. Cancer Res 66: 7067-7074, 2006. (Pubitemid 44197683)
36. Nakasaki T, Wada H, Shigemori C, Miki C, Gabazza EC, Nobori T, Nakamura S and Shiku H: Expression of tissue factor and vascular endothelial growth factor is associated with angiogenesis in colorectal cancer. Am J Hematol 69: 247-254, 2002. (Pubitemid 34259846)
37. Khorana AA, Ahrendt SA, Ryan CK, Francis CW, Hruban RH, Hu YC, Hostetter G, Harvey J and Taubman MB: Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin Cancer Res 13: 2870-2875, 2007. (Pubitemid 46849560)
38. Rak J, Milsom C, May L, Klement P and Yu J: Tissue factor in cancer and angiogenesis: the molecular link between genetic tumor progression, tumor neovascularization, and cancer coagulopathy. Semin Thromb Hemost 32: 54-70, 2006.
39. Altomare DF, Rotelli MT, Pentimone A, Rossiello MR, Martinelli E, Guglielmi A, De Fazio M, Marino F, Memeo V, Colucci M and Semeraro N: Tissue factor and vascular endothelial growth factor expression in colorectal cancer: relation with cancer recurrence. Colorectal Dis 9: 133-138, 2007. (Pubitemid 46111596)
40. Ollivier V, Bentolila S, Chabbat J, Hakim J and de Prost D: Tissue factor-dependent vascular endothelial growth factor production by human fibroblasts in response to activated factor VII. Blood 91: 2698-2703, 1998. (Pubitemid 28227518)
41. Taniguchi T, Kakkar AK, Tuddenham EG, Williamson RC and Lemoine NR: Enhanced expression of urokinase receptor induced through the tissue factor-factor VIIa pathway in human pancreatic cancer. Cancer Res 58: 4461-4467, 1998. (Pubitemid 28450052)
42. Vairaktaris E, Yapijakis C, Serefoglou Z, Vylliotis A, Ries J, Nkenke E, Wiltfang J, Derka S, Vassiliou S, Springer I, Kessler P and Neukam FW: Plasminogen activator inhibitor-1 polymorphism is associated with increased risk for oral cancer. Oral Oncol 42: 888-892, 2006. (Pubitemid 44467859)
43. Yapijakis C, Vairaktaris E, Vassiliou S, Vylliotis A, Nkenke E, Nixon AM, Derka S, Spyridonidou S, Vorris E, Neukam F and Patsouris E: The low VEGF production allele of the +936C/T polymorphism is strongly associated with increased risk for oral cancer. J Cancer Res Clin Oncol 133: 787-791, 2007. (Pubitemid 47319247)
44. Mechtcheriakova D, Wlachos A, Holzmuller, Binder BR and Hofer E: Vascular endothelial cell growth factor-induced tissue factor expression in endothelial cells is mediated by EGR-1. Blood 93: 3811-3823, 1999. (Pubitemid 29249828)
45. Shoji M, Hancock WW, Abe K, Micko C, Casper KA, Baine RM, Wilcox JN, Danave I, Dillehay DL, Matthews E, Contrino J, Morrissey JH, Gordon S, Edgington TS, Kudryk B, Kreutzer DL and Rickles FR: Activation of coagulation and angiogenesis in cancer: immunohistochemical localization in situ of clotting proteins and vascular endothelial growth factor in human cancer. Am J Pathol 152: 399-411, 1998. (Pubitemid 28106386)
46. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Jirousková M and Degen JL: Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 105: 178-185, 2005. (Pubitemid 40053080)
47. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, Hu Z, Barney KA and Degen JL: Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and -independent mechanisms. Blood 110: 133-141, 2007. (Pubitemid 47026828)
48. Crawley JT and Lane DA: The haemostatic role of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol 28(2): 233-242, 2008. (Pubitemid 351161194)
49. Amirkhosravi A, Meyer T, Chang JY, Amaya M, Siddiqui F, Desai H and Francis JL: Tissue factor pathway inhibitor reduces experimental lung metastasis of B16 melanoma. Thromb Haemost 87: 930-936, 2002. (Pubitemid 34624872)
50. Sprecher CA, Kisiel W, Mathewes S and Foster DC: Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor. Proc Natl Acad Sci USA 91: 3353-3357, 1994. (Pubitemid 24130235)
51. Chand HS, Foster DC and Kisiel W: Structure, function and biology of tissue factor pathway inhibitor-2. Thromb Haemost 94: 1122-1130, 2005. (Pubitemid 41819605)
52. Vairaktaris E, Serefoglou Z, Yapijakis C, Vylliotis A, Nkenke E, Derka S, Vassiliou S, Avgoustidis D, Neukam FW and Patsouris E: High gene expression of matrix metalloproteinase-7 is associated with early stages of oral cancer. Anticancer Res 27(4B): 2493-2498, 2007. (Pubitemid 47228094)
53. Vairaktaris E, Yapijakis C, Derka S, Serefoglou Z, Vassiliou S, Nkenke E, Ragos V, Vylliotis A, Spyridonidou S, Tsigris C, Yannopoulos A, Tesseromatis C, Neukam FW and Patsouris E : Association of matrix metalloproteinase-1 (-1607 1G/2G) polymorphism with increased risk for oral squamous cell carcinoma. Anticancer Res 27(1A): 459-464, 2007. (Pubitemid 46363366)
54. Vairaktaris E, Yapijakis C, Nkenke E, Serefoglou ZC, Chatzitheofylaktou A, Vassiliou S, Derka S, Vylliotis A, Perrea D, Neukam FW and Patsouris E: A metalloproteinase-13 polymorphism affecting its gene expression is associated with advanced stages of oral cancer. Anticancer Res 27(6B): 4027-4030, 2007.
55. Vairaktaris E, Yapijakis C, Vasiliou S, Derka S, Nkenke E, Serefoglou Z, Vorris E, Vylliotis A, Ragos V, Neukam FW and Patsouris E: Association of -1171 promoter polymorphism of matrix metalloproteinase-3 with increased risk for oral cancer. Anticancer Res 27(6B): 4095-4100, 2007.
56. Vairaktaris E, Vassiliou S, Nkenke E, Serefoglou Z, Derka S, Tsigris C, Vylliotis A, Yapijakis C, Neukam FW and Patsouris E: A metalloproteinase-9 polymorphism which affects its expression is associated with increased risk for oral squamous cell carcinoma. Eur J Surg Oncol 34: 450-455, 2008. (Pubitemid 351391904)
57. Wojtukiewicz MZ, Sierko E, Zimnoch L, Kozlowski L and Kisiel W: Immunohistochemical localization of tissue factor pathway inhibitor-2 in human tumor tissue. Thromb Haemost 90: 140-146, 2003. (Pubitemid 36873870)
58. Iino M, Foster DC and Kisiel W: Quantification and characterization of human endothelial cell-derived tissue factor pathway inhibitor-2. Arterioscler Thromb Vasc Biol 18: 40-46, 1998. (Pubitemid 28047597)
59. Tasiou A, Konduri SD, Yanamandra N, Dinh DH, Olivero WC, Gujrati M, Obeyesekere M and Rao JS: A novel role of tissue factor pathway inhibitor-2 in apoptosis of malignant human gliomas. Int J Oncol 19: 591-597, 2001.
60. Nobeyama Y, Okochi-Takada E, Furuta J, Miyagi Y, Kikuchi K, Yamamoto A, Nakanishi Y, Nakagawa H and Ushijima T: Silencing of tissue factor pathway inhibitor-2 gene in malignant melanomas. Int J Cancer 121: 301-307, 2007. (Pubitemid 46917698)
61. Crawley JT, Zanardelli S, Chion CK and Lane DA: The central role of thrombin in hemostasis. J Thromb Haemost 5(S1): 95-101, 2007. (Pubitemid 46958822)
62. Zacharski LR, Memoli VA, Morain WD, Schlaeppi JM and Rousseau SM: Cellular localization of enzymatically active thrombin in intact human tissues by hirudin binding. Thromb Haemost 73: 793-797, 1995.
63. Tsopanoglou NE and Maragoudakis ME: On the mechanism of thrombin-induced angiogenesis. Potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors. J Biol Chem 274: 23969-23976, 1999.
64. Maragoudakis ME, Kraniti N, Giannopoulou E, Alexopoulos K and Matsoukas J: Modulation of angiogenesis and progelatinase a by thrombin receptor mimetics and antagonists. Endothelium 8: 195-205, 2001. (Pubitemid 34056069)
65. Mohle R, Green D, Moore MA, Nachman RL and Rafii S: Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci USA 94: 663-668, 1997. (Pubitemid 27053690)
66. Ferrara N, Gerber HP and LeCouter J: The biology of VEGF and its receptors. Nat Med 9: 669-676, 2003. (Pubitemid 36749215)
67. Tsopanoglou NE, Andriopoulou P and Maragoudakis ME: On the mechanism of thrombin-induced angiogenesis: involvement of αvβ3-integrin. Am J Physiol Cell Physiol 283: C1501-1510, 2002. (Pubitemid 35178442)
68. Tsopanoglou NE and Maragoudakis ME: Role of thrombin in angiogenesis and tumor progression. Semin Thromb Hemost 30: 63-69, 2004. (Pubitemid 38457301)
69. Vairaktaris E, Yapijakis C, Wiltfang J, Ries J, Vylliotis A, Derka S, Vasiliou S and Neukam FW: Are factor V and prothrombin mutations associated with increased risk of oral cancer? Anticancer Res 25(3C): 2561-2565, 2005. (Pubitemid 41044749)
70. Vairaktaris E, Vassiliou S, Yapijakis C, Spyridonidou S, Vylliotis A, Derka S, Nkenke E, Fourtounis G, Neukam FW and Patsouris E: Increased risk for oral cancer is associated with coagulation factor XIII but not with factor XII. Oncol Rep 18: 1537-1543, 2007.
71. Vairaktaris E, Yapijakis C, Nkenke E, Vassiliou S, Vylliotis A, Nixon AM, Derka S, Ragos V, Spyridonidou S, Tsigris C, Neukam FW and Patsouris E: The 1040C/T polymorphism influencing thermal stability and activity of thrombin activatable fibrinolysis inhibitor is associated with risk for oral cancer. Am J Hematol 82: 1010-1012, 2007. (Pubitemid 350004393)
72. Nierodzik ML and Karpatkin S: Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 10: 355-362, 2006. (Pubitemid 44693468)
73. Lee TH, Rhim T and Kim SS: Prothrombin kringle-2 domain has a growth inhibitory activity against basic fibroblast growth factor-stimulated capillary endothelial cells. J Biol Chem 273: 28805-28812, 1998. (Pubitemid 28507571)
74. Rhim TY, Park CS, Kim E and Kim SS: Human prothrombin fragment 1 and 2 inhibit bFGF-induced BCE cell growth. Biochem Biophys Res Commun 252: 513-516, 1998. (Pubitemid 28542919)
75. Bouma BN and Mosnier LO: Thrombin activatable fibrinolysis inhibitor (TAFI) - How does thrombin regulate fibrinolysis? Ann Med 38: 378-388, 2006. (Pubitemid 44484876)
76. Hataji O, Taguchi O, Gabazza EC, Yuda H, D'Alessandro-Gabazza CN, Fujimoto H, Nishii Y, Hayashi T, Suzuki K and Adachi Y: Increased circulating levels of thrombin-activatable fibrinolysis inhibitor in lung cancer patients. Am J Hematol 76: 214-219, 2004. (Pubitemid 38828838)
77. Meijers JC, Oudijk EJ, Mosnier LO, Bos R, Bouma BN, Nieuwenhuis HK and Fijnheer R: Reduced activity of TAFI (thrombin-activatable fibrinolysis inhibitor) in acute promyelocytic leukaemia. Br J Haematol 108: 518-523, 2000. (Pubitemid 30196247)
78. Reijerkerk A, Meijers JC, Havik SR, Bouma BN, Voest EE and Gebbink MF: Tumor growth and metastasis are not affected in thrombin-activatable fibrinolysis inhibitor-deficient mice. J Thromb Haemost 2: 769-779, 2004. (Pubitemid 40185716)
79. Guimaraes AH, Laurens N, Weijers EM, Koolwijk P, van Hinsbergh VW and Rijken DC: TAFI and pancreatic carboxypeptidase B modulate in vitro capillary tube formation by human microvascular endothelial cells. Arterioscler Thromb Vasc Biol 27: 2157-2162, 2007. (Pubitemid 350287244)
80. Zhang W, Chuang YJ, Swanson R, Li J, Seo K, Leung L, Lau LF and Olson ST: Antiangiogenic antithrombin down-regulates the expression of the proangiogenic heparan sulfate proteoglycan, perlecan, in endothelial cells. Blood 103: 1185-1191, 2004. (Pubitemid 38168626)
81. Zhang W, Chuang YJ, Jin T, Swanson R, Xiong Y, Leung L and Olson ST: Antiangiogenic antithrombin induces global changes in the gene expression profile of endothelial cells. Cancer Res 66: 5047-5055, 2006. (Pubitemid 43844925)
82. Zhang W, Swanson R, Xiong Y, Richard B and Olson ST: Antiangiogenic antithrombin blocks the heparan sulfate-dependent binding of proangiogenic growth factors to their endothelial cell receptors: evidence for differential binding of antiangiogenic and anticoagulant forms of antithrombin to proangiogenic heparan sulfate domains. J Biol Chem 281: 37302-37310, 2006. (Pubitemid 46042034)
83. Larsson H, Akerud P, Nordling K, Raub-Segall E, Claesson-Welsh L and Björk I: A novel anti-angiogenic form of antithrombin with retained proteinase binding ability and heparin affinity. J Biol Chem 276: 11996-20002, 2001.
84. Zhang W, Swanson R, Izaguirre G, Xiong Y, Lau LF and Olson ST: The heparin-binding site of antithrombin is crucial for antiangiogenic activity. Blood 106: 1621-1628, 2005. (Pubitemid 41208574)
85. Koutsi A, Papapanagiotou A and Papavassiliou AG: Thrombomodulin: From haemostasis to inflammation and tumourigenesis. Int J Biochem Cell Biol 40: 1669-1673, 2008. (Pubitemid 351815187)
86. Hanly AM, Hayanga A, Winter DC and Bouchier-Hayes DJ: Thrombomodulin: tumour biology and prognostic implications. Eur J Surg Oncol 31: 217-220, 2005. (Pubitemid 40361508)
87. Hanly AM, Redmond M, Winter DC, Brophy S, Deasy JM, Bouchier-Hayes DJ and Kay EW: Thrombomodulin expression in colorectal carcinoma is protective and correlates with survival. Br J Cancer 94: 1320-1325, 2006.
88. Hosaka Y, Higuchi T, Tsumagari M and Ishii H: Inhibition of invasion and experimental metastasis of murine melanoma cells by human soluble thrombomodulin. Cancer Lett 161: 231-240, 2000.
89. Zhang Y, Weiler-Guettler H, Chen J, Wilhelm O, Deng Y, Qiu F, Nakagawa K, Klevesath M, Wilhelm S, Böhrer H, Nakagawa M, Graeff H, Martin E, Stern DM, Rosenberg RD, Ziegler R and Nawroth PP: Thrombomodulin modulates growth of tumor cells independent of its anticoagulant activity. J Clin Invest 101: 1301-1309, 1998. (Pubitemid 28166827)
90. Calnek DS and Grinnell BW: Thrombomodulin-dependent anticoagulant activity is regulated by vascular endothelial growth factor. Exp Cell Res 238: 294-298, 1998. (Pubitemid 28366153)
91. Huang HC, Shi GY, Jiang SJ, Shi CS, Wu CM, Yang HY and Wu HL: Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J Biol Chem 278: 46750-46759, 2003.
92. Iino S, Abeyama K, Kawahara K, Yamakuchi M, Hashiguchi T, Matsukita S, Yonezawa S, Taniguchi S, Nakata M, Takao S, Aikou T and Maruyama I: The antimetastatic role of thrombomodulin expression in islet cell-derived tumors and its diagnostic value. Clin Cancer Res 10: 6179-6188, 2004. (Pubitemid 39287524)
93. Vairaktaris E, Serefoglou Z, Yapijakis C, Nkenke E, Vassiliou S, Spyridonidou S, Vylliotis A, Nixon AM, Neukam FW and Patsouris E: Coagulation-related factors, thrombomodulin and protein Z, are not associated with risk for oral cancer. Anticancer Res 27(4B): 2449-2451, 2007. (Pubitemid 47228087)
94. Vairaktaris E, Serefoglou Z, Yapijakis C, Stathopoulos P, Vassiliou S, Derka S, Nkenke E, Vylliotis A, Ragos V, Neukam FW and Patsouris E: The interleukin-1 beta gene polymorphism +3953 C/T is not associated with risk for oral cancer. Anticancer Res 27(6B): 3981-3986, 2007.
95. Mosesson MW: Fibrinogen and fibrin structure and functions. J Thromb Haemost 3: 1894-1904, 2005.
96. Sahni A, Simpson-Haidaris PJ, Sahni SK, Vaday GG and Francis CW: Fibrinogen synthesized by cancer cells augments the proliferative effect of FGF-2. J Thromb Haemost 6: 176-183, 2008.
97. Lalla RV, Goralnick SJ, Tanzer ML and Kreutzer DL: Fibrin induces IL-8 expression from human oral squamous cell carcinoma cells. Oral Oncol 37: 234-242, 2001. (Pubitemid 32245847)
98. Dvorak HF, Nagy JA, Berse B, Brown LF, Yeo KT, Yeo TK, Dvorak AM, van de Water L, Sioussat TM and Senger DR: Vascular permeability factor, fibrin, and the pathogenesis of tumor stroma formation. Ann NY Acad Sci 667: 101-111, 1992. (Pubitemid 23061569)
99. Vairaktaris E, Yapijakis C, Serefoglou Z, Derka S, Vassiliou S, Nkenke E, Vylliotis A, Wiltfang J, Avgoustidis D, Critselis E, Neukam FW and Patsouris E: The interleukin-8 (-251A/T) polymorphism is associated with increased risk for oral squamous cell carcinoma. Eur J Surg Oncol 33(4): 504-507, 2007. (Pubitemid 46620664)
100. Henschen A: On the structure of functional sites in fibrinogen. Thromb Res S5: 27-33, 1983.
101. Bach TL, Barsigian C, Yaen CH and Martinez J: Endothelial cell VE-cadherin functions as a receptor for the beta15-42 sequence of fibrin. J Biol Chem 273: 30719-30728, 1998. (Pubitemid 28545554)
102. Cavallaro U, Liebner S and Dejana E: Endothelial cadherins and tumor angiogenesis. Exp Cell Res 312: 659-667, 2006. (Pubitemid 43290342)
103. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, Huang X, Sheppard D, Hynes RO and Hodivala-Dilke KM: Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 8: 27-34, 2002. (Pubitemid 34101725)
104. Biggerstaff JP, Seth N, Amirkhosravi A, Amaya M, Fogarty S, Meyer TV, Siddiqui F and Francis JL: Soluble fibrin augments platelet/tumor cell adherence in vitro and in vivo, and enhances experimental metastasis. Clin Exp Metastasis 17: 723-730, 1999. (Pubitemid 30450194)
105. Palumbo JS, Kombrinck KW, Drew AF, Grimes TS, Kiser JH, Degen JL and Bugge TH: Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 96: 3302-3309, 2000.
106. Palumbo JS, Potter JM, Kaplan LS, Talmage K, Jackson DG and Degen JL: Spontaneous hematogenous and lymphatic metastasis, but not primary tumor growth or angiogenesis, is diminished in fibrinogen-deficient mice. Cancer Res 62: 6966-6972, 2002. (Pubitemid 35424088)
107. Engelse MA, Hanemaaijer R, Koolwijk P and van Hinsbergh VW: The fibrinolytic system and matrix metalloproteinases in angiogenesis and tumor progression. Semin Thromb Hemost 30: 71-82, 2004. (Pubitemid 38457302)
108. Rabbani SA: Metalloproteases and urokinase in angiogenesis and tumor progression. In Vivo 12: 135-42, 1998.