Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration

Abstract

Tissue factor (TF), an initiator of the extrinsic coagulation cascade, is expressed in a wide range of cancer cells and plays important roles in cancer progression and metastasis. Recently, the intracellular function of TF has been revealed to be involved in cancer invasion, independent of the blood coagulation pathway. To evaluate the clinical significance of TF expression, we performed an enzyme-linked immunosorbent assay (ELISA) in the plasma of 67 breast cancer patients and immunohistochemistry in 213 breast cancer tissues. In the ELISA study, we showed an up-regulation of plasma TF concentration in breast cancer patients compared with normal controls. Immunohistochemistry demonstrated that TF was expressed in tumour cells and stromal cells and tumour TF expression closely correlated with stromal TF expression (P = 0.0005). The concentration of plasma TF was associated with tissue TF expression in both tumour and stroma. The multivariate analysis demonstrated that tumour TF expression was an independent prognostic indicator for overall survival (P = 0.0452). Our data show that plasma TF concentration reflects tissue TF expression and tumour TF expression can provide some predictive value for prognosis and distant metastasis, which indicates the importance of TF function in tumour progression.

References 49

1. 1.

   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):4007-4020.

   Not in our library10.1021/bi00362a005

2. 2.

   Bastida E., Ordinas A., Escolar G., Jamieson G. A. Tissue factor in microvesicles shed from U87MG human glioblastoma cells induces coagulation, platelet aggregation, and thrombogenesis. Blood. 1984;64(1):177-184.

   Not in our library

3. 3.

   Bevilacqua M. P., Pober J. S., Majeau G. R., Cotran R. S., Gimbrone M. A. Interleukin 1 (IL-1) induces biosynthesis and cell surface expression of procoagulant activity in human vascular endothelial cells. J Exp Med. 1984;160(2):618-623.

   Not in our library10.1084/jem.160.2.618

4. 4.

   Bevilacqua M. P., Pober J. S., Majeau G. R., Fiers W., Cotran R. S., Gimbrone M. A. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1. Proc Natl Acad Sci U S A. 1986;83(12):4533-4537.

   Not in our library10.1073/pnas.83.12.4533

5. 5.

   Bobrow M. N., Harris T. D., Shaughnessy K. J., Litt G. J. Catalyzed reporter deposition, a novel method of signal amplification. Application to immunoassays. J Immunol Methods. 1989;125(1-2):279-285.

   Not in our library10.1016/0022-1759(89)90104-x

6. 6.

   Bromberg M. E., Konigsberg W. H., Madison J. F., Pawashe A., Garen A. Tissue factor promotes melanoma metastasis by a pathway independent of blood coagulation. Proc Natl Acad Sci U S A. 1995;92(18):8205-8209.

   Not in our library10.1073/pnas.92.18.8205

7. 7.

   Brox J. H., Osterud B., Bjørklid E., Fenton J. W. Production and availability of thromboplastin in endothelial cells: the effects of thrombin, endotoxin and platelets. Br J Haematol. 1984;57(2):239-246.

   Not in our library10.1111/j.1365-2141.1984.tb02892.x

8. 8.

   Callander N. S., Varki N., Rao L. V. Immunohistochemical identification of tissue factor in solid tumors. Cancer. 1992;70(5):1194-1201.

   Not in our library10.1002/1097-0142(19920901)70:5<1194::aid-cncr2820700528>3.0.co;2-e

9. 9.

   Colucci M., Balconi G., Lorenzet R., Pietra A., Locati D., Donati M. B., Semeraro N. Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest. 1983;71(6):1893-1896.

   Not in our library10.1172/jci110945

10. 10.

    Conkling P. R., Greenberg C. S., Weinberg J. B. Tumor necrosis factor induces tissue factor-like activity in human leukemia cell line U937 and peripheral blood monocytes. Blood. 1988;72(1):128-133.

    Not in our library

11. 11.

    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):209-215.

    Not in our library10.1038/nm0296-209

12. 12.

    Cuadrado M. J., Dobado-Berrios P. M., López-Pedrera C., Gómez-Zumaquero J. M., Tinahones F., Jurado A., Camps T., Torres A., Velasco F. Variability of soluble tissue factor in primary antiphospholipid syndrome. Thromb Haemost. 1998;80(4):712-713.

    Not in our library

13. 13.

    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):1087-1097.

    Not in our library

14. 14.

    Esumi N., Fan D., Fidler I. J. Inhibition of murine melanoma experimental metastasis by recombinant desulfatohirudin, a highly specific thrombin inhibitor. Cancer Res. 1991;51(17):4549-4556.

    Not in our library

15. 15.

    Fadok V. A., Voelker D. R., Campbell P. A., Cohen J. J., Bratton D. L., Henson P. M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol. 1992;148(7):2207-2216.

    Not in our library

16. 16.

    Falciani M., Gori A. M., Fedi S., Chiarugi L., Simonetti I., Dabizzi R. P., Prisco D., Pepe G., Abbate R., Gensini G. F. Elevated tissue factor and tissue factor pathway inhibitor circulating levels in ischaemic heart disease patients. Thromb Haemost. 1998;79(3):495-499.

    Not in our library

17. 17.

    Fischer E. G., Ruf W., Mueller B. M. Tissue factor-initiated thrombin generation activates the signaling thrombin receptor on malignant melanoma cells. Cancer Res. 1995;55(8):1629-1632.

    Not in our library

18. 18.

    Greeno E. W., Bach R. R., Moldow C. F. Apoptosis is associated with increased cell surface tissue factor procoagulant activity. Lab Invest. 1996;75(2):281-289.

    Not in our library

19. 19.

    Hamada K., Kuratsu J., Saitoh Y., Takeshima H., Nishi T., Ushio Y. Expression of tissue factor correlates with grade of malignancy in human glioma. Cancer. 1996;77(9):1877-1883.

    Not in our library10.1002/(sici)1097-0142(19960501)77:9<1877::aid-cncr18>3.0.co;2-x

20. 20.

    Imamura T., Iyama K., Takeya M., Kambara T., Nakamura S. Role of macrophage tissue factor in the development of the delayed hypersensitivity reaction in monkey skin. Cell Immunol. 1993;152(2):614-622.

    Not in our library10.1006/cimm.1993.1317

21. 21.

    Kakkar A. K., DeRuvo N., Chinswangwatanakul V., Tebbutt S., Williamson R. C. Extrinsic-pathway activation in cancer with high factor VIIa and tissue factor. Lancet. 1995;346(8981):1004-1005.

    Not in our library10.1016/s0140-6736(95)91690-3

22. 22.

    Kakkar A. K., Lemoine N. R., Scully M. F., Tebbutt S., Williamson R. C. Tissue factor expression correlates with histological grade in human pancreatic cancer. Br J Surg. 1995;82(8):1101-1104.

    Not in our library10.1002/bjs.1800820831

23. 23.

    Koomägi 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.

    Not in our library10.1002/(sici)1097-0215(19980220)79:1<19::aid-ijc4>3.0.co;2-z

24. 24.

    Koyama T., Nishida K., Ohdama S., Sawada M., Murakami N., Hirosawa S., Kuriyama R., Matsuzawa K., Hasegawa R., Aoki N. Determination of plasma tissue factor antigen and its clinical significance. Br J Haematol. 1994;87(2):343-347.

    Not in our library10.1111/j.1365-2141.1994.tb04919.x

25. 25.

    Masuda M., Nakamura S., Murakami T., Komiyama Y., Takahashi H. Association of tissue factor with a gamma chain homodimer of the IgE receptor type I in cultured human monocytes. Eur J Immunol. 1996;26(10):2529-2532.

    Not in our library10.1002/eji.1830261037

26. 26.

    Miller D. L., Yaron R., Yellin M. J. CD40L-CD40 interactions regulate endothelial cell surface tissue factor and thrombomodulin expression. J Leukoc Biol. 1998;63(3):373-379.

    Not in our library10.1002/jlb.63.3.373

27. 27.

    Misumi K., Ogawa H., Yasue H., Soejima H., Suefuji H., Nishiyama K., Takazoe K., Kugiyama K., Tsuji I., Kumeda K. Comparison of plasma tissue factor levels in unstable and stable angina pectoris. Am J Cardiol. 1998;81(1):22-26.

    Not in our library10.1016/s0002-9149(97)00801-1

28. 28.

    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):129-135.

    Not in our library10.1016/0092-8674(87)90669-6

29. 29.

    Mueller B. M., Reisfeld R. A., Edgington T. S., Ruf W. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc Natl Acad Sci U S A. 1992;89(24):11832-11836.

    Not in our library10.1073/pnas.89.24.11832

30. 30.

    Mueller B. M., Ruf W. Requirement for binding of catalytically active factor VIIa in tissue factor-dependent experimental metastasis. J Clin Invest. 1998;101(7):1372-1378.

    Not in our library10.1172/jci930

31. 31.

    Nemerson Y., Bach R. Tissue factor revisited. Prog Hemost Thromb. 1982;6:237-261.

    Not in our library

32. 32.

    Ollivier V., Bentolila S., Chabbat J., Hakim J., de Prost D. Tissue factor-dependent vascular endothelial growth factor production by human fibroblasts in response to activated factor VII. Blood. 1998;91(8):2698-2703.

    Not in our library

33. 33.

    Ott I., Fischer E. G., Miyagi Y., Mueller B. M., Ruf W. A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. J Cell Biol. 1998;140(5):1241-1253.

    Not in our library10.1083/jcb.140.5.1241

34. 34.

    Pendurthi U. R., Alok D., Rao L. V. Binding of factor VIIa to tissue factor induces alterations in gene expression in human fibroblast cells: up-regulation of poly(A) polymerase. Proc Natl Acad Sci U S A. 1997;94(23):12598-12603.

    Not in our library10.1073/pnas.94.23.12598

35. 35.

    Poulsen L. K., Jacobsen N., Sørensen B. B., Bergenhem N. C., Kelly J. D., Foster D. C., Thastrup O., Ezban M., Petersen L. C. Signal transduction via the mitogen-activated protein kinase pathway induced by binding of coagulation factor VIIa to tissue factor. J Biol Chem. 1998;273(11):6228-6232.

    Not in our library10.1074/jbc.273.11.6228

36. 36.

    Røttingen J. A., Enden T., Camerer E., Iversen J. G., Prydz H. Binding of human factor VIIa to tissue factor induces cytosolic Ca2+ signals in J82 cells, transfected COS-1 cells, Madin-Darby canine kidney cells and in human endothelial cells induced to synthesize tissue factor. J Biol Chem. 1995;270(9):4650-4660.

    Not in our library10.1074/jbc.270.9.4650

37. 37.

    Shigemori C., Wada H., Matsumoto K., Shiku H., Nakamura S., Suzuki H. Tissue factor expression and metastatic potential of colorectal cancer. Thromb Haemost. 1998;80(6):894-898.

    Not in our library

38. 38.

    Shoji M., Hancock W. W., Abe K., Micko C., Casper K. A., Baine R. M., Wilcox J. N., Danave I., Dillehay D. L., Matthews E. 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. 1998;152(2):399-411.

    Not in our library

39. 39.

    Slupsky J. R., Kalbas M., Willuweit A., Henn V., Kroczek R. A., Müller-Berghaus G. Activated platelets induce tissue factor expression on human umbilical vein endothelial cells by ligation of CD40. Thromb Haemost. 1998;80(6):1008-1014.

    Not in our library

40. 40.

    Suefuji H., Ogawa H., Yasue H., Kaikita K., Soejima H., Motoyama T., Mizuno Y., Oshima S., Saito T., Tsuji I. Increased plasma tissue factor levels in acute myocardial infarction. Am Heart J. 1997;134(2 Pt 1):253-259.

    Not in our library10.1016/s0002-8703(97)70132-7

41. 41.

    Takahashi H., Satoh N., Wada K., Takakuwa E., Seki Y., Shibata A. Tissue factor in plasma of patients with disseminated intravascular coagulation. Am J Hematol. 1994;46(4):333-337.

    Not in our library10.1002/ajh.2830460414

42. 42.

    Taniguchi T., Kakkar A. K., Tuddenham E. G., Williamson R. C., Lemoine N. R. Enhanced expression of urokinase receptor induced through the tissue factor-factor VIIa pathway in human pancreatic cancer. Cancer Res. 1998;58(19):4461-4467.

    Not in our library

43. 43.

    Vrana J. A., Stang M. T., Grande J. P., Getz M. J. Expression of tissue factor in tumor stroma correlates with progression to invasive human breast cancer: paracrine regulation by carcinoma cell-derived members of the transforming growth factor beta family. Cancer Res. 1996;56(21):5063-5070.

    Not in our library

44. 44.

    Wada H., Nakase T., Nakaya R., Minamikawa K., Wakita Y., Kaneko T., Ohiwa M., Deguchi K., Shirakawa S. Elevated plasma tissue factor antigen level in patients with disseminated intravascular coagulation. Am J Hematol. 1994;45(3):232-236.

    Not in our library10.1002/ajh.2830450307

45. 45.

    Wojtukiewicz M. Z., Zacharski L. R., Memoli V. A., Kisiel W., Kudryk B. J., Rousseau S. M., Stump D. C. Indirect activation of blood coagulation in colon cancer. Thromb Haemost. 1989;62(4):1062-1066.

    Not in our library

46. 46.

    Yamamoto N., Watanabe T., Katsumata N., Omuro Y., Ando M., Fukuda H., Takue Y., Narabayashi M., Adachi I., Takashima S. Construction and validation of a practical prognostic index for patients with metastatic breast cancer. J Clin Oncol. 1998;16(7):2401-2408.

    Not in our library10.1200/jco.1998.16.7.2401

47. 47.

    Zacharski L. R., Schned A. R., Sorenson G. D. Occurrence of fibrin and tissue factor antigen in human small cell carcinoma of the lung. Cancer Res. 1983;43(8):3963-3968.

    Not in our library

48. 48.

    Zhang Y., Deng Y., Luther T., Müller M., Ziegler R., Waldherr R., Stern D. M., Nawroth P. P. Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest. 1994;94(3):1320-1327.

    Not in our library10.1172/jci117451

49. 49.

    Zhou L., Stordeur P., de Lavareille A., Thielemans K., Capel P., Goldman M., Pradier O. CD40 engagement on endothelial cells promotes tissue factor-dependent procoagulant activity. Thromb Haemost. 1998;79(5):1025-1028.

    Not in our library

Cited by papers we hold 5

• Characterization of a novel bispecific antibody targeting tissue factor-positive tumors with T cell engagement · 2022
  Not checked
• Tumor Cell-Induced Platelet Aggregation as an Emerging Therapeutic Target for Cancer Therapy · 2022
  Not checked
• Neutrophil extracellular traps in breast cancer and beyond: current perspectives on NET stimuli, thrombosis and metastasis, and clinical utility for diagnosis and treatment · 2019
  No notice
• Tissue Factor, Blood Coagulation, and Beyond: An Overview · 2011
  No notice
• Tissue factor expression as a possible determinant of thromboembolism in ovarian cancer · 2007
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.