Journal of Hematology & Oncology | |
Tissue factor in tumor microenvironment: a systematic review | |
Bo Zhu3  Yongsheng Li1  Bo Guo2  Xiao Han2  | |
[1] Harvard Institutes of Medicine, Department of Anesthesiology, Center for Experimental Therapeutics and Reperfusion Injury, Perioperative and Pain Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston 02115, MA, USA;Institute of Cancer, Xinqiao Hospital, Third Military Medical University, Chongqing 400037, PR China;Biomedical Analysis Center, Third Military Medical University, Chongqing 400038, China | |
关键词: Coagulation; Microparticles; Venous thromboembolism; Tumor microenvironment; Tissue factor; | |
Others : 1233321 DOI : 10.1186/s13045-014-0054-8 |
|
received in 2014-06-18, accepted in 2014-07-09, 发布年份 2014 | |
【 摘 要 】
The aberrant hemostasis is a common manifestation of cancer, and venous thromboembolism (VTE) is the second leading cause of cancer patients’ mortality. Tissue factor (TF), comprising of a 47-kDa transmembrane protein that presents in subendothelial tissues and leukocytes and a soluble isoform, have distinct roles in the initiation of extrinsic coagulation cascade and thrombosis. Laboratory and clinical evidence showed the deviant expression of TF in several cancer systems and its tumor-promoting effects. TF contributes to myeloid cell recruitment in tumor stroma, thereby remodeling of tumor microenvironment. Additionally, the number of TF-positive-microparticles (TF+MP) from tumor origins correlates with the VTE rates in cancer patients. In this review, we summarize our current understanding of the TF regulation and roles in tumor progression and clinical complications.
【 授权许可】
2014 Han et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20151119112033452.pdf | 2128KB | download | |
Figure 3. | 121KB | Image | download |
Figure 2. | 86KB | Image | download |
Figure 1. | 70KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
【 参考文献 】
- [1]Spicer EK, Horton R, Bloem L, Bach R, Williams KR, Guha A, Kraus J, Lin TC, Nemerson Y, Konigsberg WH: Isolation of cDNA clones coding for human tissue factor: primary structure of the protein and cDNA. Proc Natl Acad Sci U S A 1987, 84:5148-5152.
- [2]Versteeg HH, Peppelenbosch MP, Spek CA: The pleiotropic effects of tissue factor: a possible role for factor VIIa-induced intracellular signalling? Thromb Haemost 2001, 86:1353-1359.
- [3]Tardos JG, Eisenreich A, Deikus G, Bechhofer DH, Chandradas S, Zafar U, Rauch U, Bogdanov VY: SR proteins ASF/SF2 and SRp55 participate in tissue factor biosynthesis in human monocytic cells. J Thromb Haemost 2008, 6:877-884.
- [4]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, 9:458-462.
- [5]Szotowski B, Antoniak S, Poller W, Schultheiss HP, Rauch U: Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res 2005, 96:1233-1239.
- [6]Eisenreich A, Bogdanov VY, Zakrzewicz A, Pries A, Antoniak S, Poller W, Schultheiss HP, Rauch U: Cdc2-like kinases and DNA topoisomerase I regulate alternative splicing of tissue factor in human endothelial cells. Circ Res 2009, 104:589-599.
- [7]Censarek P, Bobbe A, Grandoch M, Schror K, Weber AA: Alternatively spliced human tissue factor (asHTF) is not pro-coagulant. Thromb Haemost 2007, 97:11-14.
- [8]Srinivasan R, Bogdanov VY: Alternatively spliced tissue factor: discovery, insights, clinical implications. Front Biosci 2011, 16:3061-3071.
- [9]Bick RL: Cancer-associated thrombosis. N Engl J Med 2003, 349:109-111.
- [10]Yu YJ, Li YM, Hou XD, Guo C, Cao N, Jiao ZY: Effect of tissue factor on invasion inhibition and apoptosis inducing effect of oxaliplatin in human gastric cancer cell. Asian Pac J Cancer Prev 2012, 13:1845-1849.
- [11]Eisenreich A, Boltzen U, Malz R, Schultheiss HP, Rauch U: Overexpression of alternatively spliced tissue factor induces the pro-angiogenic properties of murine cardiomyocytic HL-1 cells. Circ J 2011, 75:1235-1242.
- [12]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, 110:11517-11522.
- [13]Liu Y, Jiang P, Capkova K, Xue D, Ye L, Sinha SC, Mackman N, Janda KD, Liu C: Tissue factor-activated coagulation cascade in the tumor microenvironment is critical for tumor progression and an effective target for therapy. Cancer Res 2011, 71:6492-6502.
- [14]Saito Y, Hashimoto Y, Kuroda J, Yasunaga M, Koga Y, Takahashi A, Matsumura Y: 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, 47:2230-2239.
- [15]Schaffner F, Yokota N, Ruf W: Tissue factor proangiogenic signaling in cancer progression. Thromb Res 2012, 129(Suppl 1):S127-S131.
- [16]Welsh J, Smith JD, Yates KR, Greenman J, Maraveyas A, Madden LA: Tissue factor expression determines tumour cell coagulation kinetics. Int J Lab Hematol 2012, 34:396-402.
- [17]Hong H, Zhang Y, Nayak TR, Engle JW, Wong HC, Liu B, Barnhart TE, Cai W: Immuno-PET of tissue factor in pancreatic cancer. J Nucl Med 2012, 53:1748-1754.
- [18]Cocco E, Varughese J, Buza N, Bellone S, Glasgow M, Bellone M, Todeschini P, Carrara L, Silasi DA, Azodi M, Schwartz PE, Rutherford TJ, Pecorelli S, Lockwood CJ, Santin AD: Expression of tissue factor in adenocarcinoma and squamous cell carcinoma of the uterine cervix: implications for immunotherapy with hI-con1, a factor VII-IgGFc chimeric protein targeting tissue factor. BMC Cancer 2011, 11:263. BioMed Central Full Text
- [19]Owens AP 3rd, Mackman N: Microparticles in hemostasis and thrombosis. Circ Res 2011, 108:1284-1297.
- [20]Rak J: Microparticles in cancer. Semin Thromb Hemost 2010, 36:888-906.
- [21]Castellana D, Toti F, Freyssinet JM: Membrane microvesicles: macromessengers in cancer disease and progression. Thromb Res 2010, 125(Suppl 2):S84-S88.
- [22]Pabinger I, Thaler J, Ay C: Biomarkers for prediction of venous thromboembolism in cancer. Blood 2013, 122:2011-2018.
- [23]Bharthuar A, Khorana AA, Hutson A, Wang JG, Key NS, Mackman N, Iyer RV: Circulating microparticle tissue factor, thromboembolism and survival in pancreaticobiliary cancers. Thromb Res 2013, 132:180-184.
- [24]Ma Z, Zhang T, Wang R, Cheng Z, Xu H, Li W, Wang Y, Wang X: Tissue factor-factor VIIa complex induces epithelial ovarian cancer cell invasion and metastasis through a monocytes-dependent mechanism. Int J Gynecol Cancer 2011, 21:616-624.
- [25]Cole M, Bromberg M: Tissue factor as a novel target for treatment of breast cancer. Oncologist 2013, 18:14-18.
- [26]Perry JR: Thromboembolic disease in patients with high-grade glioma. Neuro Oncol 2012, 14(Suppl 4):iv73-iv80.
- [27]Thaler J, Ay C, Mackman N, Metz-Schimmerl S, Stift J, Kaider A, Mullauer L, Gnant M, Scheithauer W, Pabinger I: Microparticle-associated tissue factor activity in patients with pancreatic cancer: correlation with clinicopathological features. Eur J Clin Invest 2013, 43:277-285.
- [28]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, 95:324-331.
- [29]Lwaleed BA, Lam L, Lasebai M, Cooper AJ: Expression of tissue factor and tissue factor pathway inhibitor in microparticles and subcellular fractions of normal and malignant prostate cell lines. Blood Coagul Fibrinolysis 2013, 24:339-343.
- [30]Li H, Tian ML, Yu G, Liu YC, Wang X, Zhang J, Ji SQ, Zhu J, Wan YL, Tang JQ: Hyperthermia synergizes with tissue factor knockdown to suppress the growth and hepatic metastasis of colorectal cancer in orthotopic tumor model. J Surg Oncol 2012, 106:689-695.
- [31]Eisenreich A, Zakrzewicz A, Huber K, Thierbach H, Pepke W, Goldin-Lang P, Schultheiss HP, Pries A, Rauch U: Regulation of pro-angiogenic tissue factor expression in hypoxia-induced human lung cancer cells. Oncol Rep 2013, 30:462-470.
- [32]Zhao Y, Zhang D, Wang S, Tao L, Wang A, Chen W, Zhu Z, Zheng S, Gao X, Lu Y: Holothurian glycosaminoglycan inhibits metastasis and thrombosis via targeting of nuclear factor-kappaB/tissue factor/Factor Xa pathway in melanoma B16F10 cells. PLoS One 2013, 8:e56557.
- [33]Yu JL, Rak JW: 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, 2:2065-2067.
- [34]Contrino J, Hair G, Kreutzer DL, Rickles FR: In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996, 2:209-215.
- [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]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, 106:19497-19502.
- [37]Godby RC, Van Den Berg YW, Srinivasan R, Sturm R, Hui DY, Konieczny SF, Aronow BJ, Ozhegov E, Ruf W, Versteeg HH, Bogdanov VY: Nonproteolytic properties of murine alternatively spliced tissue factor: implications for integrin-mediated signaling in murine models. Mol Med 2012, 18:771-779.
- [38]Rao LV, Pendurthi UR: Regulation of tissue factor coagulant activity on cell surfaces. J Thromb Haemost 2012, 10:2242-2253.
- [39]Rautou PE, Mackman N: Microvesicles as risk markers for venous thrombosis. Expert Rev Hematol 2013, 6:91-101.
- [40]Rao B, Gao Y, Huang J, Gao X, Fu X, Huang M, Yao J, Wang J, Li W, Zhang J, Liu H, Wang L: Mutations of p53 and K-ras correlate TF expression in human colorectal carcinomas: TF downregulation as a marker of poor prognosis. Int J Colorectal Dis 2011, 26:593-601.
- [41]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, 105:1734-1741.
- [42]Magnus N, Garnier D, Rak J: Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells. Blood 2010, 116:815-818.
- [43]Rong Y, Belozerov VE, Tucker-Burden C, Chen G, Durden DL, Olson JJ, Van Meir EG, Mackman N, Brat DJ: Epidermal growth factor receptor and PTEN modulate tissue factor expression in glioblastoma through JunD/activator protein-1 transcriptional activity. Cancer Res 2009, 69:2540-2549.
- [44]Eisenreich A, Malz R, Pepke W, Ayral Y, Poller W, Schultheiss HP, Rauch U: Role of the phosphatidylinositol 3-kinase/protein kinase B pathway in regulating alternative splicing of tissue factor mRNA in human endothelial cells. Circ J 2009, 73:1746-1752.
- [45]Provencal M, Labbe D, Veitch R, Boivin D, Rivard GE, Sartelet H, Robitaille Y, Gingras D, Beliveau R: c-Met activation in medulloblastoma induces tissue factor expression and activity: effects on cell migration. Carcinogenesis 2009, 30:1089-1096.
- [46]Vieira KB, Goldstein DJ, Villa LL: Tumor necrosis factor alpha interferes with the cell cycle of normal and papillomavirus-immortalized human keratinocytes. Cancer Res 1996, 56:2452-2457.
- [47]Vogelstein B, Kinzler KW: Cancer genes and the pathways they control. Nat Med 2004, 10:789-799.
- [48]Lee BJ, Kim JH, Woo SH, Kim JH, Kim DH, Yu YS: Tissue factor is involved in retinoblastoma cell proliferation via both the Akt and extracellular signal-regulated kinase pathways. Oncol Rep 2011, 26:665-670.
- [49]Sun L, Liu Y, Lin S, Shang J, Liu J, Li J, Yuan S, Zhang L: Early growth response gene-1 and hypoxia-inducible factor-1alpha affect tumor metastasis via regulation of tissue factor. Acta Oncol 2013, 52:842-851.
- [50]Bastarache JA, Sebag SC, Grove BS, Ware LB: Interferon-gamma and tumor necrosis factor-alpha act synergistically to up-regulate tissue factor in alveolar epithelial cells. Exp Lung Res 2011, 37:509-517.
- [51]Wygrecka M, Zakrzewicz D, Taborski B, Didiasova M, Kwapiszewska G, Preissner KT, Markart P: TGF-beta1 induces tissue factor expression in human lung fibroblasts in a PI3K/JNK/Akt-dependent and AP-1-dependent manner. Am J Respir Cell Mol Biol 2012, 47:614-627.
- [52]Fedorov O, Huber K, Eisenreich A, Filippakopoulos P, King O, Bullock AN, Szklarczyk D, Jensen LJ, Fabbro D, Trappe J, Rauch U, Bracher F, Knapp S: Specific CLK inhibitors from a novel chemotype for regulation of alternative splicing. Chem Biol 2011, 18:67-76.
- [53]Eisenreich A: Regulation of vascular function on posttranscriptional level. Thrombosis 2013, 2013:948765.
- [54]Eisenreich A, Leppert U: The impact of microRNAs on the regulation of tissue factor biology. Trends Cardiovasc Med 2014, 24:128-132.
- [55]A E, Rauch U: Regulation of the tissue factor isoform expression and thrombogenicity of HMEC-1 by miR-126 and miR-19a. Cell Biol: Res Ther 2013, 2:1. doi:10.4172/2324-9293.1000101
- [56]Yu G, Li H, Wang X, Wu T, Zhu J, Huang S, Wan Y, Tang J: MicroRNA-19a targets tissue factor to inhibit colon cancer cells migration and invasion. Mol Cell Biochem 2013, 380:239-247.
- [57]Teruel R, Perez-Sanchez C, Corral J, Herranz MT, Perez-Andreu V, Saiz E, Garcia-Barbera N, Martinez-Martinez I, Roldan V, Vicente V, Lopez-Pedrera C, Martinez C: Identification of miRNAs as potential modulators of tissue factor expression in patients with systemic lupus erythematosus and antiphospholipid syndrome. J Thromb Haemost 2011, 9:1985-1992.
- [58]Garnier D, Magnus N, D’Asti E, Hashemi M, Meehan B, Milsom C, Rak J: Genetic pathways linking hemostasis and cancer. Thromb Res 2012, 129(Suppl 1):S22-S29.
- [59]Leppert U, Eisenreich A: The role of tissue factor isoforms in cancer biology.Int J Cancer 2014, doi:10.1002/ijc.28959.
- [60]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, 119:924-932.
- [61]Wu B, Zhou H, Hu L, Mu Y, Wu Y: Involvement of PKCalpha activation in TF/VIIa/PAR2-induced proliferation, migration, and survival of colon cancer cell SW620. Tumour Biol 2013, 34:837-846.
- [62]Hu L, Xia L, Zhou H, Wu B, Mu Y, Wu Y, Yan J: TF/FVIIa/PAR2 promotes cell proliferation and migration via PKCalpha and ERK-dependent c-Jun/AP-1 pathway in colon cancer cell line SW620. Tumour Biol 2013, 34:2573-2581.
- [63]Aberg M, Johnell M, Wickstrom M, Siegbahn A: Tissue Factor/FVIIa prevents the extrinsic pathway of apoptosis by regulation of the tumor suppressor Death-Associated Protein Kinase 1 (DAPK1). Thromb Res 2011, 127:141-148.
- [64]Signaevsky M, Hobbs J, Doll J, Liu N, Soff GA: Role of alternatively spliced tissue factor in pancreatic cancer growth and angiogenesis. Semin Thromb Hemost 2008, 34:161-169.
- [65]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-S21.
- [66]Maeda S, Maeda S, Ohno K, Kaji N, Hori M, Fujino Y, Tsujimoto H: Protease-activated receptor-2 induces proinflammatory cytokine and chemokine gene expression in canine keratinocytes. Vet Immunol Immunopathol 2013, 153:17-25.
- [67]Dorfleutner A, Hintermann E, Tarui T, Takada Y, Ruf W: Cross-talk of integrin alpha3beta1 and tissue factor in cell migration. Mol Biol Cell 2004, 15:4416-4425.
- [68]Ott I, Weigand B, Michl R, Seitz I, Sabbari-Erfani N, Neumann FJ, Schomig A: Tissue factor cytoplasmic domain stimulates migration by activation of the GTPase Rac1 and the mitogen-activated protein kinase p38. Circulation 2005, 111:349-355.
- [69]Muller M, Albrecht S, Golfert F, Hofer A, Funk RH, Magdolen V, Flossel C, Luther T: Localization of tissue factor in actin-filament-rich membrane areas of epithelial cells. Exp Cell Res 1999, 248:136-147.
- [70]Palumbo JS: Mechanisms linking tumor cell-associated procoagulant function to tumor dissemination. Semin Thromb Hemost 2008, 34:154-160.
- [71]Ruf W, Mueller BM: Thrombin generation and the pathogenesis of cancer. Semin Thromb Hemost 2006, 32(Suppl 1):61-68.
- [72]Degen JL, Palumbo JS: Hemostatic factors, innate immunity and malignancy. Thromb Res 2012, 129(Suppl 1):S1-S5.
- [73]Palumbo JS, Barney KA, Blevins EA, Shaw MA, Mishra A, Flick MJ, Kombrinck KW, Talmage KE, Souri M, Ichinose A, Degen JL: Factor XIII transglutaminase supports hematogenous tumor cell metastasis through a mechanism dependent on natural killer cell function. J Thromb Haemost 2008, 6:812-819.
- [74]Amirkhosravi A, Meyer T, Chang JY, Amaya M, Siddiqui F, Desai H, Francis JL: Tissue factor pathway inhibitor reduces experimental lung metastasis of B16 melanoma. Thromb Haemost 2002, 87:930-936.
- [75]Gil-Bernabe AM, Ferjancic S, Tlalka M, Zhao L, Allen PD, Im JH, Watson K, Hill SA, Amirkhosravi A, Francis JL, Pollard JW, Ruf W, Muschel RJ: Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood 2012, 119:3164-3175.
- [76]Ma S: Biology and clinical implications of CD133(+) liver cancer stem cells. Exp Cell Res 2013, 319:126-132.
- [77]Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, Korkaya H, Heath A, Dutcher J, Kleer CG, Jung Y, Dontu G, Taichman R, Wicha MS: Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 2011, 71:614-624.
- [78]Long H, Xie R, Xiang T, Zhao Z, Lin S, Liang Z, Chen Z, Zhu B: Autocrine CCL5 signaling promotes invasion and migration of CD133+ ovarian cancer stem-like cells via NF-kappaB-mediated MMP-9 upregulation. Stem Cells 2012, 30:2309-2319.
- [79]Milsom CC, Yu JL, Mackman N, Micallef J, Anderson GM, Guha A, Rak JW: Tissue factor regulation by epidermal growth factor receptor and epithelial-to-mesenchymal transitions: effect on tumor initiation and angiogenesis. Cancer Res 2008, 68:10068-10076.
- [80]Sade-Feldman M, Kanterman J, Ish-Shalom E, Elnekave M, Horwitz E, Baniyash M: Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 2013, 38:541-554.
- [81]Krisinger MJ, Goebeler V, Lu Z, Meixner SC, Myles T, Pryzdial EL, Conway EM: Thrombin generates previously unidentified C5 products that support the terminal complement activation pathway. Blood 2012, 120:1717-1725.
- [82]Markiewski MM, DeAngelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, Gerard C, Coukos G, Lambris JD: Modulation of the antitumor immune response by complement. Nat Immunol 2008, 9:1225-1235.
- [83]Ferjancic S, Gil-Bernabe AM, Hill SA, Allen PD, Richardson P, Sparey T, Savory E, McGuffog J, Muschel RJ: VCAM-1 and VAP-1 recruit myeloid cells that promote pulmonary metastasis in mice. Blood 2013, 121:3289-3297.
- [84]Falanga A, Russo L: Epidemiology, risk and outcomes of venous thromboembolism in cancer. Hamostaseologie 2012, 32:115-125.
- [85]Lazo-Langner A, Goss GD, Spaans JN, Rodger MA: The effect of low-molecular-weight heparin on cancer survival: a systematic review and meta-analysis of randomized trials. J Thromb Haemost 2007, 5:729-737.
- [86]Klerk CP, Smorenburg SM, Otten HM, Lensing AW, Prins MH, Piovella F, Prandoni P, Bos MM, Richel DJ, van Tienhoven G, Buller HR: The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol 2005, 23:2130-2135.
- [87]Hull RD, Townshend G: Long-term treatment of deep-vein thrombosis with low-molecular-weight heparin: an update of the evidence. Thromb Haemost 2013, 110:14-22.
- [88]Morel O, Jesel L, Freyssinet JM, Toti F: Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011, 31:15-26.
- [89]Hron G, Kollars M, Weber H, Sagaster V, Quehenberger P, Eichinger S, Kyrle PA, Weltermann A: Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemost 2007, 97:119-123.
- [90]Del Conde I, Bharwani LD, Dietzen DJ, Pendurthi U, Thiagarajan P, Lopez JA: Microvesicle-associated tissue factor and Trousseau’s syndrome. J Thromb Haemost 2007, 5:70-74.
- [91]Tesselaar ME, Romijn FP, Van Der Linden IK, Prins FA, Bertina RM, Osanto S: Microparticle-associated tissue factor activity: a link between cancer and thrombosis? J Thromb Haemost 2007, 5:520-527.
- [92]Tesselaar ME, Romijn FP, van der Linden IK, Bertina RM, Osanto S: Microparticle-associated tissue factor activity in cancer patients with and without thrombosis. J Thromb Haemost 2009, 7:1421-1423.
- [93]Zwicker JI, Liebman HA, Neuberg D, Lacroix R, Bauer KA, Furie BC, Furie B: Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res 2009, 15:6830-6840.