Evidence for tissue factor phosphorylation and its correlation with protease-activated receptor expression and the prognosis of primary breast cancer

International Journal of Cancer

Volumn 126, Issue 10, 2010, Pages 2330-2340

  Rydén, Lisa ^a   Grabau, Dorthe ^a   Schaffner, Florence ^b   Jönsson, Per Ebbe ^c   Ruf, Wolfram ^b   Belting, Mattias ^a  

^a LUND UNIVERSITY   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c HELSINGBORG HOSPITAL   (Sweden)

Author keywords

Breast cancer; Protease activated receptors; Tissue factor; VEGF A

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; THROMBOPLASTIN; VASCULOTROPIN A; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VEGFA PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER; BREAST TUMOR; CANCER RECURRENCE; CANCER SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FOLLOW UP; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENE; XENOGRAFT; ADENOCARCINOMA; ANIMAL; CANCER TRANSPLANTATION; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; KAPLAN MEIER METHOD; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; MOUSE MUTANT; PATHOLOGY; PHOSPHORYLATION; PREDICTION AND FORECASTING; PROSPECTIVE STUDY; SIGNAL TRANSDUCTION; SWEDEN; TUMOR CELL LINE;

ADENOCARCINOMA; ADULT; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIERS ESTIMATE; LYMPHATIC METASTASIS; MAMMARY NEOPLASMS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, SCID; MIDDLE AGED; NEOPLASM TRANSPLANTATION; PHOSPHORYLATION; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROSPECTIVE STUDIES; RECEPTOR, PAR-2; SIGNAL TRANSDUCTION; SWEDEN; THROMBOPLASTIN; TRANSPLANTATION, HETEROLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77951209407     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24921     Document Type: Article

References (37)

1. Blom JW, Doggen CJ, Osanto S, Rosendaal FR. Malignancies, prothrombotic mutations, and the risk of venous thrombosis. JAMA 2005;293:715-722 (Pubitemid 40216041)
2. Rak J, Yu JL, Luyendyk J, Mackman N. Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans. Cancer Res 2006;66:10643-10646 (Pubitemid 44876956)
3. Belting M, Ahamed J, Ruf W. Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol 2005;25:1545-1550 (Pubitemid 41098920)
4. Rickles FR, Brenner B. Tissue factor and cancer. Semin Thromb Hemost 2008;34:143-145
5. Poon RT-P, Lau CP-Y, Ho JW-Y, Yu W-C, Fan S-T, Wong J. Tissue Factor expression correlates with tumor angiogenesis and invasiveness in human hepatocellular carcinoma. Clin Cancer Res 2003;9:5339-5345 (Pubitemid 37413589)
6. Nitori N, Ino Y, Nakanishi Y, Yamada T, Honda K, Yanagihara K, Kosuge T, Kanai Y, Kitajima M, Hirohashi S. Prognostic significance of tissue factor in pancreatic ductal adenocarcinoma. Clin Cancer Res 2005;11:2531-2539 (Pubitemid 40569450)
7. Patry G, Hovington H, Larue H, Harel F, Fradet Y, Lacombe L. Tissue factor expression correlates with disease-specific survival in patients with node-negative muscle-invasive bladder cancer. Int J Cancer 2008;122:1592-1597 (Pubitemid 351294968)
8. Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 2006;10:355-362 (Pubitemid 44693468)
9. Bromberg ME, Konigsberg WH, Madison JF, Pawashe A, Garen A. Tissue factor promotes melanoma metastasis by a pathway independent of blood coagulation. Proc Natl Acad Sci USA 1995;92:8205-8209
10. Abe K, Shoji M, Chen J, Bierhaus A, Danave I, Micko C, Casper K, Dillehay DL, Nawroth PP, Rickles FR. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc Natl Acad Sci USA 1999;96:8663-8668 (Pubitemid 29354848)
11. Riewald M, Ruf W. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc Natl Acad Sci USA 2001;98:7742-7747 (Pubitemid 32642631)
12. Hjortoe GM, Petersen LC, Albrektsen T, Sorensen BB, Norby PL, Mandal SK, Pendurthi UR, Rao LV. Tissue factor-factor VIIa specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated via PAR-2 and results in increased cell migration. Blood 2004;103:3029-3037 (Pubitemid 38451676)
13. Morris DR, Ding Y, Ricks TK, Gullapalli A, Wolfe BL, Trejo J. Protease-activated receptor-2 is essential for factor VIIa and Xa-induced signaling, migration, and invasion of breast cancer cells. Cancer Res 2006;66:307-314 (Pubitemid 43166037)
14. Liu Y, Mueller BM. Protease-activated receptor-2 regulates vascular endothelial growth factor expression in MDA-MB-231 cells via MAPK pathways. Biochem Biophys Res Commun 2006;344:1263-1270
15. Ahamed J, Ruf W. Protease-activated receptor 2-dependent phosphorylation of the tissue factor cytoplasmic domain. J Biol Chem 2004;279:23038-23044 (Pubitemid 38685607)
16. Dorfleutner A, Hintermann E, Tarui T, Takada Y, Ruf W. Crosstalk of integrin α3β1 and tissue factor in cell migration. Mol Biol Cell 2004;15:4416-4425 (Pubitemid 39299092)
17. Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A, Carmeliet P, Mueller BM, Friedlander M, Ruf W. Regulation of angiogenesis by tissue factor cytoplasmic domain signalling. Nat Med 2004;10:502-509 (Pubitemid 38667909)
18. Ge L, Shenoy SK, Lefkowitz RJ, DeFea K. Constitutive protease-activated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both beta-arrestin-1 and -2. J Biol Chem2004;279:55419-55424
19. Jiang X, Bailly MA, Panetti TS, Cappello M, Konigsberg WH, Bromberg ME. Formation of tissue factor-factor VIIa-factor Xa complex promotes cellular signaling and migration of human breast cancer cells. J Thromb Haemost 2004;2:93-101. (Pubitemid 40185625)
20. Kamath L, Meydani A, Foss F, Kuliopulos A. Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res 2001;61:5933-5940 (Pubitemid 32769114)
21. Booden MA, Eckert LB, Der CJ, Trejo J. Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion. Mol Cell Biol 2004;24:1990-1999
22. Arora P, Cuevas BD, Russo A, Johnson GL, Trejo J. Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion. Oncogene 2008;27:4434-4445
23. Versteeg HH, Schaffner F, Kerver M, Ellies LG, Andrade-Gordon P, Mueller BM, Ruf W. Protease activated receptor (PAR)2, but not PAR1 signaling promotes the development of mammary adenocarcinoma in PyMT mice. Cancer Res 2008;68:7219-7227
24. Albrektsen T, Sorensen BB, Hjortoe GM, Fleckner J, Rao LVM, Petersen LC. Transcriptional program induced by factor VIIa-tissue factor, PAR1 and PAR2 in MDA-MB-231 cells. J Thromb Haemost 2007;5:1588-1597 (Pubitemid 47091396)
25. Schaffner F, Ruf W. Tissue Factor and PAR2 Signaling in the Tumor Microenvironment. Arterioscler Thromb Vasc Biol, in press.
26. Ngo CV, Picha K, McCabe F, Millar H, Tawadros R, Tam SH, Nakada MT, Anderson GM. CNTO 859, a humanized anti-tissue factor monoclonal antibody, is a potent inhibitor of breast cancer metastasis and tumor growth in xenograft models. Int J Cancer 2007;120:1261-1267 (Pubitemid 46256779)
27. Versteeg HH, Schaffner F, Kerver M, Petersen HH, Ahamed J, Felding-Habermann B, Takada Y, Mueller BM, Ruf W. Inhibition of tissue factor signaling suppresses tumor growth. Blood 2008;111:190-199
28. Jessani N, Humphrey M, McDonald WH, Niessen S, Masuda K, Gangadharan B, Yates,JR, III, Mueller BM, Cravatt BF. Carcinoma and stromal enzyme activity profiles associated with breast tumor growth in vivo. Proc Natl Acad Sci USA 2004;101:13756-13761 (Pubitemid 39298480)
29. Ryden L, Chebil G, Sjostrom L, Pawlowski R, Jonsson PE. Determination of sentinel lymph node (SLN) status in primary breast cancer by prospective use of immunohistochemistry increases the rate of micrometastases and isolated tumor cells: analysis of 174 patients after SLN biopsy. Eur J Surg Oncol 2007;33:33-38 (Pubitemid 46131884)
30. Dorfleutner A, Ruf W. Regulation of tissue factor cytoplasmic domain phosphorylation by palmitoylation. Blood 2003;102:3998-4005. (Pubitemid 37486981)
31. Shoji M, Hancock WW, Abe K, Micko C, Casper KA, Baine RM, Wilcox JN, Danave I, Dillehay DL, Matthews E, Contrino J, Morrissey JH, et al. 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;152:399-411. (Pubitemid 28106386)
32. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403-410
33. Rakha EA, El-Sayed ME, Lee AH, Elston CW, Grainge MJ, Hodi Z, Blamey RW, Ellis IO. Prognostic significance of Nottingham histologic grade in invasive breast carcinoma. J ClinOncol 2008;26:3153-3158
34. Sturm U, Luther T, Albrecht S, Flössel C, Grossmann H, Müller M. Immunohistological detection of tissue factor in normal and abnormal human mammary glands using monoclonal antibodies. Virchows Arch A Pathol Anat Histopathol 1992;421:79-86.
35. Vrana JA, Stang MT, Grande JP, Getz MJ. 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;56:5063-5070
36. Ueno T, Toi M, Koike M, Nakamura S, Tominaga T. Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer 2000;83:164-170 (Pubitemid 30411712)
37. Koizume S, Jin M-S, Miyagi E, Hirahara F, Nakamura Y, Piao JH, Asai A, Yoshida A, Tsuchiya E, Ruf W, Miyagi Y. Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII. Cancer Res 2006;66:9453-9460 (Pubitemid 44623642)