Preview

Онкогематология

Расширенный поиск

Роль тканевого фактора в метастазировании, неоангиогенезе и гемостазе при онкологических заболеваниях

https://doi.org/10.17650/1818-8346-2019-14-2-70-85

Полный текст:

Аннотация

Тканевый фактор, являясь основным инициатором системы свертывания крови in vivo, принимает участие еще в ряде физиологических процессов, таких как ангиогенез или миграция клеток. Данные процессы не только значимы для нормальной физиологии, но и играют роль в развитии и прогрессировании онкологических заболеваний. В настоящем обзоре приведены данные о структуре тканевого фактора, его экспрессии в норме и при онкологических заболеваниях, его роли в развитии тромбоза, ассоциированного с онкологическими заболеваниями, в ангиогенезе опухолевых сосудов и метастазировании. Участие тканевого фактора в таком широком спектре физиологических процессов, важных для прогрессирования онкологического заболевания, делает его привлекательной молекулой-мишенью для терапии.

Об авторах

Т. А. Коваленко
ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова»; ФГБУН «Центр теоретических проблем физико-химической фармакологии РАН»;
Россия

Россия, 119991 Москва, ул. Ленинские горы, 1, стр. 2

Россия, 119991 Москва, ул. Косыгина, 4



М. А. Пантелеев
ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова»; ФГБУН «Центр теоретических проблем физико-химической фармакологии РАН»; ФГБУ «Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева» Минздрава России;
Россия

Россия, 119991 Москва, ул. Ленинские горы, 1, стр. 2

Россия, 119991 Москва, ул. Косыгина, 4

Россия, 117997 Москва, ул. Саморы Машела, 1



А. Н. Свешникова
ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова»; ФГБУН «Центр теоретических проблем физико-химической фармакологии РАН»; ФГБУ «Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева» Минздрава России; ФГАОУ ВО Первый Московский государственный медицинский университет им. И.М. Сеченова Минздрава России (Сеченовский университет)
Россия

Россия, 119991 Москва, ул. Ленинские горы, 1, стр. 2

Россия, 119991 Москва, ул. Косыгина, 4

Россия, 117997 Москва, ул. Саморы Машела, 1

Россия, 119991 Москва, ул. Трубецкая, 8, стр. 2



Список литературы

1. Maciel E.O., Carvalhal G.F., da Silva V.D. et al. Increased tissue factor expression and poor nephroblastoma prognosis. J Urol 2009;182(4):1594–9. DOI: 10.1016/j.juro.2009.06.011.

2. Silva D.D., Noronha J.A.P., Silva V.D., Carvalhal G.F. Increased tissue factor expression is an independent predictor of mortality in clear cell carcinoma of the kidney. Int Braz J Urol 2014;40(4):499–506. DOI: 10.1590/S1677-5538.IBJU.2014.04.08.

3. Davis M.E. Glioblastoma: overview of disease and treatment. Clin J Oncol Nurs 2016;20(5 Suppl):S2–8. DOI: 10.1188/16.CJON.S1.2-8.

4. Tsui K.H., Shvarts O., Smith R.B. et al. Prognostic indicators for renal cell carcinoma: a multivariate analysis of 643 patients using the revised 1997 TNM staging criteria. J Urol 2000;163(4):1090–5.

5. Giesen P.L., Rauch U., Bohrmann B. et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 1999;96(5):2311–5. DOI: 10.1073/pnas.96.5.2311.

6. Falati S., Liu Q., Gross P. et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003;197(11):1585–98. DOI: 10.1084/jem.20021868.

7. Pyo R.T., Sato Y., Mackman N., Taubman M.B. Mice deficient in tissue factor demonstrate attenuated intimal hyperplasia in response to vascular injury and decreased smooth muscle cell migration. Thromb Haemost 2004;92(3):451–8. DOI: 10.1160/TH04-02-0122.

8. Bugge T.H., Xiao Q., Kombrinck K.W. et al. Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci USA 1996;93(13):6258–63. DOI: 10.1073/pnas.93.13.6258.

9. Carmeliet P., Mackman N., Moons L. et al. Role of tissue factor in embryonic blood vessel development. Nature 1996;383(6595): 73–5. DOI: 10.1038/383073a0.

10. Toomey J.R., Kratzer K.E., Lasky N.M. et al. Targeted disruption of the murine tissue factor gene results in embryonic lethality. Blood 1996;88(5):1583–7.

11. Hembrough T.A., Swartz G.M., Papathanassiu A. et al. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Res 2003;63(11):2997–3000.

12. Khorana A.A., Ahrendt S.A., Ryan C.K. et al. Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin Cancer Res 2007;13(10):2870–5. DOI: 10.1158/1078-0432.CCR-06-2351.

13. Sakurai M., Matsumoto K., Gosho M. et al. Expression of tissue factor in epithelial ovarian carcinoma is involved in the development of venous thromboembolism. Int J Gynecol Cancer 2017;27(1):37–43. DOI: 10.1097/IGC.0000000000000848.

14. Morrissey J.H., Fakhrai H., Edgington T.S. Molecular cloning of the cDNA for tissue factor, the cellular receptor for the initiation of the coagulation protease cascade. Cell 1987;50(1):129–35. DOI: 10.1016/0092-8674(87)90669-6.

15. Harlos K., Martin D.M., O’Brien D.P. et al. Crystal structure of the extracellular region of human tissue factor. Nature 1994;370(6491): 662–6. DOI: 10.1038/370662a0.

16. Ohkubo Y.Z., Morrissey J.H., Tajkhorshid E. Dynamical view of membrane binding and complex formation of human factor VIIa and tissue factor. J Thromb Haemost 2010;8(5):1044–3. DOI: 10.1111/j.1538-7836.2010.03826.x.

17. Mackman N., Morrissey J.H., Fowler B., Edgington T.S. Complete sequence of the human tissue factor gene, a highly regulated cellular receptor that initiates the coagulation protease cascade. Biochemistry 1989;28(4):1755–62.

18. Paborsky L.R., Harris R.J. Post-translational modifications of recombinant human tissue factor. Thromb Res 1990;60(5):367–76. DOI: 10.1016/0049-3848(90)90219-3.

19. Bogdanov V.Y., Balasubramanian V., Hathcock J. et al. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med 2003;9(4):458–62. DOI: 10.1038/nm841.

20. Bogdanov V.Y., Kirk R.I., Miller C. et al. Identification and characterization of murine alternatively spliced tissue factor. J Thromb Haemost 2006;4(1):158–67. DOI: 10.1111/j.1538-7836.2005.01680.x.

21. Fair D.S. Quantitation of factor VII in the plasma of normal and warfarintreated individuals by radioimmunoassay. Blood 1983;62(4):784–91.

22. Morrissey J.H., Macik B.G., Neuenschwander P.F., Comp P.C. Quantitation of activated factor VII levels in plasma using a tissue factor mutant selectively deficient in promoting factor VII activation. Blood 1993;81(3):734–44.

23. Zwaal R.F., Comfurius P., Bevers E.M. Lipid-protein interactions in blood coagulation. Biochim Biophys Acta 1998;1376(3):433–53. DOI: 10.1016/S0304-4157(98)00018-5

24. Bach R., Gentry R., Nemerson Y. Factor VII binding to tissue factor in reconstituted phospholipid vesicles: induction of cooperativity by phosphatidylserine. Biochemistry 1986;25(14):4007–20.

25. O’Brien D.P., Kemball-Cook G., Hutchinson A.M. et al. Surface plasmon resonance studies of the interaction between factor VII and tissue factor. Demonstration of defective tissue factor binding in a variant FVII molecule (FVII-R79Q). Biochemistry 1994;33(47):14162–9.

26. McCallum C.D., Hapak R.C., Neuenschwander P.F. et al. The location of the active site of blood coagulation factor VIIa above the membrane surface and its reorientation upon association with tissue factor. A fluorescence energy transfer study. J Biol Chem 1996;271(45):28168–75.

27. Kelley R.F., Costas K.E., O’Connell M.P., Lazarus R.A. Analysis of the factor VIIa binding site on human tissue factor: effects of tissue factor mutations on the kinetics and thermodynamics of binding. Biochemistry 1995;34(33):10383–92.

28. Gibbs C.S., McCurdy S.N., Leung L.L., Paborsky L.R. Identification of the factor VIIa binding site on tissue factor by homologous loop swap and alanine scanning mutagenesis. Biochemistry 1994;33(47):14003–10.

29. Schullek J.R., Ruf W., Edgington T.S. Key ligand interface residues in tissue factor contribute independently to factor VIIa binding. J Biol Chem 1994;269(30):19399–403.

30. Banner D.W., D’Arcy A., Chene C. et al. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996;380(6569):41–6. DOI: 10.1038/380041a0.

31. Vadivel K., Agah S., Messer A.S. et al. Structural and functional studies of gamma-carboxyglutamic acid domains of factor VIIa and activated Protein C: role of magnesium at physiological calcium. J Mol Biol 2013;425(11):1961–81. DOI: 10.1016/j.jmb.2013.02.017.

32. Drake T.A., Morrissey J.H., Edgington T.S. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol 1989;134(5):1087–97.

33. Fleck R.A., Rao L.V., Rapaport S.I., Varki N. Localization of human tissue factor antigen by immunostaining with monospecific, polyclonal anti-human tissue factor antibody. Thromb Res 1990;59(2):421–37.

34. Osterud B., Tindall A., Brox J.H., Olsen J.O. Thromboplastin content in the vessel walls of different arteries and organs of rabbits. Thromb Res 1986;42(3):323–29.

35. Wilcox J.N., Smith K.M., Schwartz S.M., Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci USA 1989;86(8):2839–43. DOI: 10.1073/pnas.86.8.2839.

36. Bom V.J., Bertina R.M. The contributions of Ca2+, phospholipids and tissue-factor apoprotein to the activation of human blood-coagulation factor X by activated factor VII. Biochem J 1990;265(2): 327–36. DOI: 10.1042/bj2650327.

37. Rao L.V., Rapaport S.I. Activation of factor VII bound to tissue factor: a key early step in the tissue factor pathway of blood coagulation. Proc Natl Acad Sci USA 1988;85(18):6687–91. DOI: 10.1073/pnas.85.18.668.7

38. Kisiel W., Fujikawa K., Davie E.W. Activation of bovine factor VII (proconvertin) by factor XIIa (activated Hageman factor). Biochemistry 1977;16(19):4189–94.

39. Butenas S., Mann K.G. Kinetics of human factor VII activation. Biochemistry 1996;35(6):1904–10. DOI: 10.1021/bi951768c.

40. Nemerson Y., Repke D. Tissue factor accelerates the activation of coagulation factor VII: the role of a bifunctional coagulation cofactor. Thromb Res 1985;40(3):351–8. DOI: 10.1016/0049-3848(85)90270-1.

41. Waters E.K., Morrissey J.H. Restoring full biological activity to the isolated ectodomain of an integral membrane protein. Biochemistry 2006;45(11):3769–74. DOI: 10.1021/bi052600m.

42. Neuenschwander P.F., Morrissey J.H. Deletion of the membrane anchoring region of tissue factor abolishes autoactivation of factor VII but not cofactor function. Analysis of a mutant with a selective deficiency in activity. J Biol Chem 1992;267(20):14477–82.

43. Neuenschwander P.F., Fiore M.M., Morrissey J.H. Factor VII autoactivation proceeds via interaction of distinct proteasecofactor and zymogen-cofactor complexes. Implications of a two-dimensional enzyme kinetic mechanism. J Biol Chem 1993;268(29):21489–92.

44. Ke K., Yuan J., Morrissey J.H. Tissue factor residues that putatively interact with membrane phospholipids. PLoS One 2014;9(2):e88675. DOI: 10.1371/journal.pone.0088675.

45. Komiyama Y., Pedersen A.H., Kisiel W. Proteolytic activation of human factors IX and X by recombinant human factor VIIa: effects of calcium, phospholipids, and tissue factor. Biochemistry 1990;29(40):9418–25.

46. Versteeg H.H., Heemskerk J.W.M., Levi M., Reitsma P.H. New fundamentals in hemostasis. Physiol Rev 2013;93(1):327–58. DOI: 10.1152/physrev.00016.2011.

47. Шатурный В.И., Шахиджанов С.С., Свешникова А.Н., Пантелеев М.А. Активаторы, рецепторы и пути внутриклеточной сигнализации в тромбоцитах крови. Биомедицинская химия 2014;60(2):198–200. DOI: 10.18097/PBMC20146002182.

48. Sato Y., Kataoka H., Asada Y. et al. Overexpression of tissue factor pathway inhibitor in aortic smooth muscle cells inhibits cell migration induced by tissue factor/factor VIIa complex. Thromb Res 1999;94(6):401–6. DOI: 10.1016/S0049-3848(99)00032-8.

49. Ueno T., Toi M., Koike M. et al. Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer 2000;83(2):164–70. DOI: 10.1054/bjoc.2000.1272.

50. Regina S., Rollin J., Blechet C. et al. Tissue factor expression in non-small cell lung cancer: relationship with vascular endothelial growth factor expression, microvascular density, and K-ras mutation. J Thorac Oncol 2008;3(7):689–97. DOI: 10.1097/JTO.0b013e31817c1b21.

51. Kakkar A.K., Lemoine N.R., Scully M.F. et al. Tissue factor expression correlates with histological grade in human pancreatic cancer. Br J Surg 1995;82(8):1101–4. DOI: 10.1002/bjs.1800820831.

52. Walker T.M., Van Ginkel P.R., Gee R.L. et al. Expression of angiogenic factors Cyr61 and tissue factor in uveal melanoma. Arch Ophthalmol 2002;120(12):1719–25. DOI: 10.1001/archopht.120.12.1719.

53. Guan M., Jin J., Su B. et al. Tissue factor expression and angiogenesis in human glioma. Clin Biochem 2002;35(4):321–5. DOI: 10.1016/S0009-9120(02)00312-0.

54. Koizume S., Jin M.-S., Miyagi E. et al. Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII. Cancer Res 2006;66(19): 9453–60. DOI: 10.1158/0008-5472.CAN-06-1803.

55. Poon R.T.P., Lau C.P.Y., Ho J.W.Y. et al. Tissue factor expression correlates with tumor angiogenesis and invasiveness in human hepatocellular carcinoma. Clin Cancer Res 2003;9(14):5339–45.

56. Zhao L., Bi Y., Kou J. et al. Phosphatidylserine exposing-platelets and microparticles promote procoagulant activity in colon cancer patients. J Exp Clin Cancer Res 2016;35:54. DOI: 10.1186/s13046-016-0328-9.

57. Campello E., Spiezia L., Radu C.M. et al. Endothelial, platelet, and tissue factorbearing microparticles in cancer patients with and without venous thromboembolism. Thromb Res 2011;127(5):473–7. DOI: 10.1016/j.thromres.2011.01.002.

58. Del Conde I., Bharwani L.D., Dietzen D.J. et al. Microvesicle-associated tissue factor and Trousseau’s syndrome. J Thromb Haemost 2007;5(1):70–4. DOI: 10.1111/j.1538-7836.2006.02301.x.

59. Hron G., Kollars M., Weber H. et al. Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemost 2007;97(1):119–23.

60. Levitan N., Dowlati A., Remick S.C. et al. Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine (Baltimore) 1999;78(5):285–91.

61. Brandes A.A., Scelzi E., Salmistraro G. et al. Incidence of risk of thromboembolism during treatment high-grade gliomas: a prospective study. Eur J Cancer 1997;33(10):1592–6. DOI: 10.1016/S0959-8049(97)00167-6.

62. Connolly G.C., Menapace L., Safadjou S. et al. Prevalence and clinical significance of incidental and clinically suspected venous thromboembolism in lung cancer patients. Clin Lung Cancer 2013;14(6): 713–8. DOI: 10.1016/j.cllc.2013.06.003.

63. Sorensen H.T., Mellemkjaer L., Steffensen F.H. et al. The risk of a diagnosis of cancer after primary deep venous thrombosis or pulmonary embolism. N Engl J Med 1998;338(17):1169–73. DOI: 10.1056/NEJM199804233381701.

64. Manly D.A., Wang J., Glover S.L. et al. Increased microparticle tissue factor activity in cancer patients with venous thromboembolism. Thromb Res 2010;125(6):511–2. DOI: 10.1016/j.thromres.2009.09.019.

65. Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 1990;82(1):4–6.

66. Ollivier V., Bentolila S., Chabbat J. et al. Tissue factor-dependent vascular endothelial growth factor production by human fibroblasts in response to activated factor VII. Blood 1998;91(8):2698–703.

67. Uusitalo-Jarvinen H., Kurokawa T., Mueller B.M. et al. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler Thromb Vasc Biol 2007;27(6):1456–62. DOI: 10.1161/ATVBAHA.107.142539.

68. Belting M., Dorrell M.I., Sandgren S. et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med 2004;10(5):502–9. DOI: 10.1038/nm1037.

69. Thaler J., Preusser M., Ay C. et al. Intratumoral tissue factor expression and risk of venous thromboembolism in brain tumor patients. Thromb Res 2013;131(2):162–5. DOI: 10.1016/j.thromres.2012.09.020.

70. Unruh D., Sagin F., Adam M. et al. Levels of alternatively spliced tissue factor in the plasma of patients with pancreatic cancer may help predict aggressive tumor phenotype. Ann Surg Oncol 2015;22(Suppl 3):1206–11. DOI: 10.1245/s10434-015-4592-2.

71. de Meis E., Azambuja D., Ayres-Silva J.P. et al. Increased expression of tissue factor and protease-activated receptor-1 does not correlate with thrombosis in human lung adenocarcinoma. Brazilian J Med Biol Res 2010;43(4):403–8. DOI: 10.1590/S0100-879X2010007500017.

72. Regina S., Valentin J.B., Lachot S. et al. Increased tissue factor expression is associated with reduced survival in non-small cell lung cancer and with mutations of TP53 and PTEN. Clin Chem 2009;55(10):1834–42. DOI: 10.1373/clinchem.2009.123695.

73. Nitori N., Ino Y., Nakanishi Y. et al. Prognostic significance of tissue factor in pancreatic ductal adenocarcinoma. Clin Cancer Res 2005;11(7):2531–9. DOI: 10.1158/1078-0432.CCR-04-0866.

74. Yamashita H., Kitayama J., Ishikawa M., Nagawa H. Tissue factor expression is a clinical indicator of lymphatic metastasis and poor prognosis in gastric cancer with intestinal phenotype. J Surg Oncol 2007;95:324–31. DOI: 10.1002/jso.20680.

75. Abdulkadir S.A., Carvalhal G.F., Kaleem Z. et al. Tissue factor expression and angiogenesis in human prostate carcinoma. Hum Pathol 2000;31(4):443–7. DOI: 10.1053/hp.2000.6547.

76. van den Berg Y.W., van den Hengel L.G., Myers H.R. et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci USA 2009;106(46):19497–502. DOI: 10.1073/pnas.0905325106.

77. Bieker R., Kessler T., Schwoppe C. et al. Infarction of tumor vessels by NGR-peptide-directed targeting of tissue factor: experimental results and first-in-man experience. Blood 2009;113(20):5019–27. DOI: 10.1182/blood-2008-04-150318.

78. Nilsson F., Kosmehl H., Zardi L., Neri D. Targeted delivery of tissue factor to the ED-B domain of fibronectin, a marker of angiogenesis, mediates the infarction of solid tumors in mice. Cancer Res 2001;61(2):711–6.

79. Sawada M., Miyake S., Ohdama S. et al. Expression of tissue factor in non-smallcell lung cancers and its relationship to metastasis. Br J Cancer 1999;79(3–4): 472–7. DOI: 10.1038/sj.bjc.6690073.

80. Jiang X., Bailly M.A., Panetti T.S. et al. Formation of tissue factor-factor VIIafactor Xa complex promotes cellular signaling and migration of human breast cancer cells. J Thromb Haemost 2004;2(1):93–101. DOI: 10.1111/j.1538-7836.2004.00545.x.

81. Morris D.R., Ding Y., Ricks T.K. et al. Protease-activated receptor-2 is essential for factor VIIa and Xa-induced signaling, migration, and invasion of breast cancer cells. Cancer Res 2006;66(1):307–14. DOI: 10.1158/0008-5472.CAN-05-1735.

82. Hjortoe G.M., Petersen L.C., Albrektsen T. et al. Tissue factor-factor VIIa-specific upregulation of IL-8 expression in MDAMB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood 2004;103(8):3029–37. DOI: 10.1182/blood-2003-10-3417.

83. Tieken C., Verboom M.C., Ruf W. et al. Tissue factor associates with survival and regulates tumour progression in osteosarcoma. Thromb Haemost 2016;115(5):1025–33. DOI: 10.1160/TH15-07-0541.

84. Contrino J., Hair G., Kreutzer D.L., Rickles F.R. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996;2(2):209–15.

85. Ettelaie C., Collier M.E., Featherby S. et al. Analysis of the potential of cancer cell lines to release tissue factor-containing microvesicles: correlation with tissue factor and PAR2 expression. Thromb J 2016;14:2. DOI: 10.1186/s12959-016-0075-3.

86. Berny-Lang M.A., Aslan J.E., Tormoen G.W. et al. Promotion of experimental thrombus formation by the procoagulant activity of breast cancer cells. Phys Biol 2011;8(1):15014. DOI: 10.1088/1478-3975/8/1/015014.

87. Goldin-Lang P., Tran Q.V., Fichtner I. et al. Tissue factor expression pattern in human non-small cell lung cancer tissues indicate increased blood thrombogenicity and tumor metastasis. Oncol Rep 2008;20(1):123–8. DOI: 10.3892/or.20.1.123.

88. Koomagi R., Volm M. Tissue-factor expression in human non-small-cell lung carcinoma measured by immunohistochemistry: correlation between tissue factor and angiogenesis. Int J Cancer 1998;79(1):19–22. DOI: 10.1002/(SICI)1097-0215(19980220)79:1<19::AIDIJC4>3.0.CO;2-Z.

89. Hobbs J.E., Zakarija A., Cundiff D.L. et al. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res 2007;120(Suppl 2):13–21. DOI: 10.1016/S0049-3848(07)70126-3.

90. Khorana A.A., Francis C.W., Menzies K.E. et al. Plasma tissue factor may be predictive of venous thromboembolism in pancreatic cancer. J Thromb Haemost 2008;6(11):1983–5. DOI: 10.1111/j.1538-7836.2008.03156.x.

91. Thomas G.M., Brill A., Mezouar S. et al. Tissue factor expressed by circulating cancer cell-derived microparticles drastically increases the incidence of deep vein thrombosis in mice. J Thromb Haemost 2015;13(7):1310–9. DOI: 10.1111/jth.13002.

92. Yu J.L., Rak J.W. Shedding of tissue factor (TF)-containing microparticles rather than alternatively spliced TF is the main source of TF activity released from human cancer cells. J Thromb Haemost 2004;2(11):2065–7. DOI: 10.1111/j.1538-7836.2004.00972.x.

93. Zhang J., Ding J., Zhang X. et al. Regulation of vascular endothelial growth factor (VEGF) production and angiogenesis by tissue Factor (TF) in SGC-7901 gastric cancer cells. Cancer Biol Ther 2005;4(7):769–72.

94. Chand H.S., Ness S.A., Kisiel W. Identification of a novel human tissue factor splice variant that is upregulated in tumor cells. Int J Cancer 2006;118(7):1713–20. DOI: 10.1002/ijc.21550.

95. Del Conde I., Shrimpton C.N., Thiagarajan P., Lopez J.A. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005;106(5):1604–11. DOI: 10.1182/blood-2004-03-1095.

96. Rauch U., Bonderman D., Bohrmann B. et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000;96(1):170–5.

97. Hisada Y., Auriemma A.C., Alexander W. et al. Detection of tissue factor-positive extracellular vesicles by laser scanning confocal microscopy. Thromb Res 2017;150:65–72. DOI: 10.1016/j.thromres.2016.12.021.

98. Ichikawa J., Cole H.A., Magnussen R.A. et al. Thrombin induces osteosarcoma growth, a function inhibited by low molecular weight heparin in vitro and in vivo: procoagulant nature of osteosarcoma. Cancer 2012;118(9):2494–506. DOI: 10.1002/cncr.26518.

99. Zhang Y., Deng Y., Luther T. et al. Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest 1994;94(3):1320–7. DOI: 10.1172/JCI117451.

100. Palumbo J.S., Talmage K.E., Massari J.V et al. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent andindependent mechanisms. Blood 2007;110(1):133–41. DOI: 10.1182/blood-2007-01-065995.

101. Abe K., Shoji M., Chen J. et al. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc Natl Acad Sci USA 1999;96(15):8663–8. DOI: 10.1073/pnas.96.15.8663.

102. Bromberg M.E., Sundaram R., Homer R.J. et al. Role of tissue factor in metastasis: functions of the cytoplasmic and extracellular domains of the molecule. Thromb Haemost 1999;82(1):88–92.


Для цитирования:


Коваленко Т.А., Пантелеев М.А., Свешникова А.Н. Роль тканевого фактора в метастазировании, неоангиогенезе и гемостазе при онкологических заболеваниях. Онкогематология. 2019;14(2):70-85. https://doi.org/10.17650/1818-8346-2019-14-2-70-85

For citation:


Kovalenko T.A., Panteleev M.A., Sveshnikova A.N. The role of tissue factor in metastasising, neoangiogenesis and hemostasis in cancer. Oncohematology. 2019;14(2):70-85. (In Russ.) https://doi.org/10.17650/1818-8346-2019-14-2-70-85

Просмотров: 67


Creative Commons License
Контент доступен под лицензией Creative Commons Attribution 4.0 License.


ISSN 1818-8346 (Print)
ISSN 2413-4023 (Online)