Tissue factor induced by epithelial-mesenchymal transition triggers a procoagulant state that drives metastasis of circulating tumor cells

Cancer Research

Volumn 76, Issue 14, 2016, Pages 4270-4282

  Bourcy, Morgane ^a   Suarez Carmona, Meggy ^a   Lambe, Justine ^a   Francart, Marie Emilie ^a   Schroeder, Hélène ^a   Delierneux, Céline ^b   Skrypek, Nicolas ^c,d   Thompson, Erik W ^e   Jérusalem, Guy ^a   Berx, Geert ^c,d   Thiry, Marc ^b   Blacher, Silvia ^a   Hollier, Brett G ^e   Noël, Agnòs ^a   Oury, Cécile ^b   Polette, Myriam ^f   Gilles, Christine ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

^e QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^f UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SHORT HAIRPIN RNA; THROMBOPLASTIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; VIMENTIN; ZEB1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; BREAST CANCER; CANCER PATIENT; CARCINOGENESIS; CELL SURVIVAL; CIRCULATING TUMOR CELL; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG METASTASIS; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; FEMALE; LUNG TUMOR; PATHOLOGY; PHYSIOLOGY; SECONDARY; TUMOR CELL LINE; TUMOR EMBOLISM;

ANIMALS; BLOOD COAGULATION; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; NEOPLASTIC CELLS, CIRCULATING; THROMBOPLASTIN; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 84978634561     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2263     Document Type: Article

References (50)

1. McInnes LM, Jacobson N, Redfern A, Dowling A, Thompson EW, Saunders CM. Clinical implications of circulating tumor cells of breast cancer patients: role of epithelial-mesenchymal plasticity. Front Oncol 2015;5:42.
2. Pantel K, Speicher MR. The biology of circulating tumor cells. Oncogene 2016;35:1216-24.
3. Toss A, Mu Z, Fernandez S, Cristofanilli M. CTC enumeration and characterization : moving toward personalized medicine. Ann Transl Med 2014;2:108.
4. Bonnomet A, Brysse A, Tachsidis A, Waltham M, Thompson EW, Polette M, et al. Epithelial-to-mesenchymal transitions and circulating tumor cells. J Mammary Gland Biol Neoplasia 2010;15:261-73.
5. Krawczyk N, Meier-stiegen F, Banys M, Neubauer H, Ruckhaeberle E, Fehm T. Expression of stem cell and epithelial-mesenchymal transition markers in circulating tumor cells of breast cancer patients. Biomed Res Int 2014;2014:415721.
6. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013;13:97-110.
7. Nieto MA, Cano A. The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol 2012;22:361-8.
8. Puisieux A, Brabletz T, Caramel J. Oncogenic roles of EMT-inducing transcription factors. Nat Cell Biol 2014;16:488-94.
9. Suarez-Carmona M, Bourcy M, Lesage J, Leroi N, Syne L, Blacher S, et al. Soluble factors regulated by epithelial-mesenchymal transition mediate tumour angiogenesis and myeloid cell recruitment. J Pathol 2015;236: 491-504.
10. Bonnomet A, Syne L, Brysse A, Feyereisen E, Thompson EW, Noëel A, et al. A dynamic in vivo model of epithelial-to-mesenchymal transitions in circulating tumor cells and metastases of breast cancer. Oncogene 2012;31: 3741-53.
11. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 2009;11:R46.
12. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013;339:580-4.
13. Palumbo JS, Degen JL. Mechanisms linking tumor cell-associated procoagulant function to tumor metastasis. ThrombRes 2007;120:S22-8.
14. Gil-Bernabe AM, Lucotti S, Muschel RJ. Coagulation and metastasis: what does the experimental literature tell us? Br J Haematol 2013;162: 433-41.
15. Esumi N, Fan D, Fidler IJ. Inhibition of murine melanoma experimental metastasis by recombinant desulfatohirudin, a highly specific thrombin inhibitor. Cancer Res 1991;51:4549-56.
16. Hu L, Lee M, Campbell W, Perez-Soler R, Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood 2004;104:2746-51.
17. Mousa SA, Linhardt R, Francis JL, Amirkhosravi A. Anti-metastatic effect of a non-anticoagulant low-molecular-weight heparin versus the standard low-molecular-weight heparin, enoxaparin. Thromb Haemost 2006;96: 816-21.
18. Lee AY. Thrombosis in cancer: an update on prevention, treatment, and survival benefits of anticoagulants. Hematology Am Soc Hematol Educ Program 2010;2010:144-9.
19. Crissman JD, Hatfield JS, Menter DG, Sloane B, Honn KV. Morphological study of the interaction of intravascular tumor cells with endothelial cells and subendothelial matrix. Cancer Res 1988;48:4065-72.
20. Im JH, Fu W, Wang H, Bhatia SK, Hammer DA, Kowalska MA, et al. Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation. Cancer Res 2004;64:8613-9.
21. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and -independent mechanisms. Blood 2007;110:133-41.
22. Ruf W. Tissue factor and cancer. Thromb Res 2012;130:S84-7.
23. Ünlü B, Versteeg HH. Effects of tumor-expressed coagulation factors on cancer progression and venous thrombosis: is there a key factor? Thromb Res 2014;133:S76-84.
24. Magnus N, D'Asti E, Meehan B, Garnier D, Rak J. Oncogenes and the coagulation system - forces that modulate dormant and aggressive states in cancer. Thromb Res 2014;133:S1-9.
25. Williams JC, Mackman N. Tissue factor in health and disease. Front Biosci 2012;4:358-72.
26. Cole M, Bromberg M. Tissue factor as a novel target for treatment of breast cancer. Oncologist 2013;18:14-8.
27. Rautou PE, Mackman N. Microvesicles as risk markers for venous thrombosis. Expert Rev Hematol 2013;6:91-101.
28. Åberg M, Siegbahn A. Tissue factor non-coagulant signaling - molecular mechanisms and biological consequences with a focus on cell migration and apoptosis. J Thromb Haemost 2013;11:817-25.
29. Ackland ML, Newgreen DF, Fridman M, Waltham MC, Arvanitis A, Minichiello J, et al. Epidermal growth factor-induced epithelio-mesenchymal transition in human breast carcinoma cells. Lab Invest 2003; 83:435-48.
30. Cursons J, Leuchowius KJ, Waltham M, Tomaskovic-Crook E, Foroutan M, Bracken CP, et al. Stimulus-dependent differences in signalling regulate epithelial-mesenchymal plasticity and change the effects of drugs in breast cancer cell lines. Cell Commun Signal 2015;13:26.
31. Jeong H, Ryu YJ, An J, Lee Y, Kim A. Epithelial-mesenchymal transition in breast cancer correlates with high histological grade and triple-negative phenotype. Histopathology 2012;60:E87-95.
32. Alix-Panabieres C, Pantel K. Technologies for detection of circulating tumor cells: facts and vision. Lab Chip 2014;14:57-62.
33. Milsom CC, Yu JL, Mackman N, Micallef J, Anderson GM, Guha A, et al. Tissue factor regulation by epidermal growth factor receptor and epithelialto-mesenchymal transitions: effect on tumor initiation and angiogenesis. Cancer Res 2008;68:10068-76.
34. Garnier D, Magnus N, Lee TH, Bentley V, Meehan B, Milsom C, et al. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem 2012;287: 43565-72.
35. Garnier D, Milsom C, Magnus N, Meehan B, Weitz J, Yu J, et al. Role of the tissue factor pathway in the biology of tumor initiating cells. Thromb Res 2010;125:S44-50.
36. Orellana R, Kato S, Erices R, Bravo ML, Gonzalez P, Oliva B, et al. Platelets enhance tissue factor protein and metastasis initiating cell markers, and act as chemoattractants increasing the migration of ovarian cancer cells. BMC Cancer 2015;15:290.
37. Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci U S A 2014;111:E3053-61.
38. Breij EC, De Goeij BE, Verploegen S, Schuurhuis DH, Amirkhosravi A, Francis J, et al. An antibody - drug conjugate that targets tissue factor exhibits potent therapeutic activity against a broad range of solid tumors. Cancer Res 2014;74:1214-26.
39. Mueller BM, Reisfeld RA, Edgington TS, Ruf W. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc Natl Acad Sci U S A 1992;89:11832-6.
40. Ngo CV, Picha K, McCabe F, Millar H, Tawadros R, Tam SH, et al. 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;120:1261-7.
41. Saito Y, Hashimoto Y, Kuroda J, Yasunaga M, Koga Y, Takahashi A, et al. The inhibition of pancreatic cancer invasion-metastasis cascade in both cellular signal and blood coagulation cascade of tissue factor by its neutralisation antibody. Eur J Cancer 2011;47:2230-9.
42. Amarzguioui M, Peng Q, Wiiger MT, Vasovic V, Babaie E, Holen T, et al. Ex vivo and in vivo delivery of anti-tissue factor short interfering RNA inhibits mouse pulmonary metastasis of B16 melanoma cells. Clin Cancer Res 2006;12:4055-61.
43. 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 U S A 1995;92:8205-9.
44. Palumbo JS, Kombrinck KW, Drew AF, Grimes TS, Kiser JH, Degen JL, et al. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 2000;96:3302-9.
45. Nieswandt B, Hafner M, Echtenacher B, Männel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 1999;59: 1295-300.
46. Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 2005;105:178-85.
47. Biggerstaff JP, Seth N, Amirkhosravi A, Amaya M, Fogarty S, Meyer TV, et al. Soluble fibrin augments platelet/tumor cell adherence in vitro and in vivo, and enhancesexperimentalmetastasis. ClinExp Metastasis 1999;17:723-30.
48. Gorelik E, Bere WW, Herberman RB. Role of NK cells in the antimetastatic effect of anticoagulant drugs. Int J Cancer 1984;33:87-94.
49. Gil-Bernabe AM, Ferjancic S, Tlalka M, Zhao L, Allen PD, Im JH, et al. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood 2012;119:3164-75.
50. Aceto N, Toner M, Maheswaran S, Haber DA. En route to metastasis: circulating tumor cell clusters and epithelial-to- mesenchymal transition. Trends Cancer 2015;1:44-52.