Alternatively spliced tissue factor synergizes with the estrogen receptor pathway in promoting breast cancer progression

Journal of Thrombosis and Haemostasis

Volumn 13, Issue 9, 2015, Pages 1683-1693

  Kocaturk B ^a   Tieken, C ^a   Vreeken, D ^a   Unlu B ^a   Engels, C C ^a   de Kruijf, E M ^a   Kuppen, P J ^a   Reitsma, P H ^a   Bogdanov, V Y ^b   Versteeg, H H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Blood coagulation; Cell movement; Cell proliferation; Integrin beta1; Tumors

Indexed keywords

ALTERNATIVELY SPLICED TISSUE FACTOR; BETA1 INTEGRIN; ESTRADIOL; ESTROGEN RECEPTOR; FULL LENGTH TISSUE FACTOR; ISOPROTEIN; THROMBOPLASTIN; UNCLASSIFIED DRUG; ESTROGEN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BREAST CANCER; BREAST CANCER CELL LINE; BREAST CARCINOGENESIS; CANCER GRADING; CANCER GROWTH; CANCER STAGING; CELL MIGRATION; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; ALTERNATIVE RNA SPLICING; BREAST TUMOR; CARCINOMA; CELL DIVISION; CELL MOTION; DISEASE COURSE; DRUG EFFECTS; FEMALE; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; SOFTWARE; TISSUE MICROARRAY; TUMOR CELL LINE;

ALTERNATIVE SPLICING; ANTIGENS, CD29; BREAST NEOPLASMS; CARCINOMA; CELL DIVISION; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; NEOPLASM GRADING; NEOPLASM PROTEINS; NEOPLASM STAGING; NEOPLASMS, HORMONE-DEPENDENT; PROTEIN ISOFORMS; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; SOFTWARE; THROMBOPLASTIN; TISSUE ARRAY ANALYSIS;

EID: 84940845766     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13049     Document Type: Article

References (39)

1. Lumachi F, Brunello A, Maruzzo M, Basso U, Basso SM. Treatment of estrogen receptor-positive breast cancer. Curr Med Chem 2013; 20: 596-604.
2. Masood S. Estrogen and progesterone receptors in cytology: a comprehensive review. Diagn Cytopathol 1992; 8: 475-91.
3. Huang B, Omoto Y, Iwase H, Yamashita H, Toyama T, Coombes RC, Filipovic A, Warner M, Gustafsson JA. Differential expression of estrogen receptor alpha, beta1, and beta2 in lobular and ductal breast cancer. Proc Natl Acad Sci U S A 2014; 111: 1933-8.
4. Kumar V, Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell 1988; 55: 145-56.
5. Pratt WB. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 1998; 217: 420-34.
6. Mann M, Cortez V, Vadlamudi RK. Epigenetics of estrogen receptor signaling: role in hormonal cancer progression and therapy. Cancers (Basel) 2011; 3: 1691-707.
7. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 2011; 11: 558-72.
8. Qin L, Liao L, Redmond A, Young L, Yuan Y, Chen H, O'Malley BW, Xu J. The AIB1 oncogene promotes breast cancer metastasis by activation of PEA3-mediated matrix metalloproteinase 2 (MMP2) and MMP9 expression. Mol Cell Biol 2008; 28: 5937-50.
9. Renoir JM, Marsaud V, Lazennec G. Estrogen receptor signaling as a target for novel breast cancer therapeutics. Biochem Pharmacol 2013; 85: 449-65.
10. Leary A, Dowsett M. Combination therapy with aromatase inhibitors: the next era of breast cancer treatment? Br J Cancer 2006; 95: 661-6.
11. Monroe DM, Hoffman M. What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol 2006; 26: 41-8.
12. Camerer E, Huang W, Coughlin SR. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci U S A 2000; 97: 5255-60.
13. 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: 190-9.
14. Maciel EO, Carvalhal GF, da Silva VD, Batista EL Jr, Garicochea B. Increased tissue factor expression and poor nephroblastoma prognosis. J Urol 2009; 182: 1594-9.
15. 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: 164-70.
16. Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med 2003; 9: 458-62.
17. Boing AN, Hau CM, Sturk A, Nieuwland R. Human alternatively spliced tissue factor is not secreted and does not trigger coagulation. J Thromb Haemost 2009; 7: 1423-6.
18. Censarek P, Bobbe A, Grandoch M, Schror K, Weber AA. Alternatively spliced human tissue factor (asHTF) is not pro-coagulant. Thromb Haemost 2007; 97: 11-4.
19. van den Berg YW, van den Hengel LG, Myers HR, Ayachi O, Jordanova E, Ruf W, Spek CA, Reitsma PH, Bogdanov VY, Versteeg HH. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci U S A 2009; 106: 19497-502.
20. Hobbs JE, Zakarija A, Cundiff DL, Doll JA, Hymen E, Cornwell M, Crawford SE, Liu N, Signaevsky M, Soff GA. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res 2007; 120(Suppl 2): S13-21.
21. Kocaturk B, van den Berg YW, Tieken C, Mieog JS, de Kruijf EM, Engels CC, van der Ent MA, Kuppen PJ, van de Velde CJ, Ruf W, Reitsma PH, Osanto S, Liefers GJ, Bogdanov VY, Versteeg HH. 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.
22. van Nes JG, de Kruijf EM, Faratian D, van de Velde CJ, Putter H, Falconer C, Smit VT, Kay C, van de Vijver MJ, Kuppen PJ, Bartlett JM. COX2 expression in prognosis and in prediction to endocrine therapy in early breast cancer patients. Breast Cancer Res Treat 2011; 125: 671-85.
23. Srinivasan R, Ozhegov E, van den Berg YW, Aronow BJ, Franco RS, Palascak MB, Fallon JT, Ruf W, Versteeg HH, Bogdanov VY. Splice variants of tissue factor promote monocyte-endothelial interactions by triggering the expression of cell adhesion molecules via integrin-mediated signaling. J Thromb Haemost 2011; 9: 2087-96.
24. Unruh D, Turner K, Srinivasan R, Kocatürk B, Qi X, Chu Z, Aronow BJ, Plas DR, Gallo CA, Kalthoff H, Kirchhofer D, Ruf W, Ahmad SA, Lucas FV, Versteeg HH, Bogdanov VY. Alternatively spliced tissue factor contributes to tumor spread and activation of coagulation in pancreatic ductal adenocarcinoma. Int J Cancer 2014; 134: 9-20.
25. Katzenellenbogen BS, Norman MJ, Eckert RL, Peltz SW, Mangel WF. Bioactivities, estrogen receptor interactions, and plasminogen activator-inducing activities of tamoxifen and hydroxy-tamoxifen isomers in MCF-7 human breast cancer cells. Cancer Res 1984; 44: 112-9.
26. Xu J, Chen Y, Olopade OI. MYC and breast cancer. Genes Cancer 2010; 1: 629-40.
27. Katzenellenbogen BS, Kendra KL, Norman MJ, Berthois Y. Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Res 1987; 47: 4355-60.
28. Key T, Appleby P, Barnes I, Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002; 94: 606-16.
29. van den Berg YW, Osanto S, Reitsma PH, Versteeg HH. The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood 2012; 119: 924-32.
30. Carson SD, Pirruccello SJ. Tissue factor and cell morphology variations in cell lines subcloned from U87-MG. Blood Coagul Fibrinolysis 1998; 9: 539-47.
31. Yu JL, May L, Lhotak V, Shahrzad S, Shirasawa S, Weitz JI, Coomber BL, Mackman N, Rak JW. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 2005; 105: 1734-41.
32. Choudhury A, Kiessling R. Her-2/neu as a paradigm of a tumor-specific target for therapy. Breast Dis 2004; 20: 25-31.
33. Berthois Y, Katzenellenbogen JA, Katzenellenbogen BS. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. Proc Natl Acad Sci U S A 1986; 83: 2496-500.
34. Lyytinen H, Pukkala E, Ylikorkala O. Breast cancer risk in postmenopausal women using estrogen-only therapy. Obstet Gynecol 2006; 108: 1354-60.
35. Liao XH, Lu DL, Wang N, Liu LY, Wang Y, Li YQ, Yan TB, Sun XG, Hu P, Zhang TC. Estrogen receptor alpha mediates proliferation of breast cancer MCF-7 cells via a p21/PCNA/E2F1-dependent pathway. FEBS J 2014; 281: 927-42.
36. Li Y, Wang JP, Santen RJ, Kim TH, Park H, Fan P, Yue W. Estrogen stimulation of cell migration involves multiple signaling pathway interactions. Endocrinology 2010; 151: 5146-56.
37. Alvaro D, Onori P, Metalli VD, Svegliati-Baroni G, Folli F, Franchitto A, Alpini G, Mancino MG, Attili AF, Gaudio E. Intracellular pathways mediating estrogen-induced cholangiocyte proliferation in the rat. Hepatology 2002; 36: 297-304.
38. Pontiggia O, Sampayo R, Raffo D, Motter A, Xu R, Bissell MJ, Joffe EB, Simian M. The tumor microenvironment modulates tamoxifen resistance in breast cancer: a role for soluble stromal factors and fibronectin through beta1 integrin. Breast Cancer Res Treat 2012; 133: 459-71.
39. Lannigan DA. Estrogen receptor phosphorylation. Steroids 2003; 68: 1-9.