Regulation of pro-angiogenic tissue factor expression in hypoxia-induced human lung cancer cells

Oncology Reports

Volumn 30, Issue 1, 2013, Pages 462-470

  Eisenreich, Andreas ^a   Zakrzewicz, Andreas ^a   Huber, Kilian ^b   Thierbach, Hannes ^a   Pepke, Wojciech ^a   Goldin Lang, Petra ^a   Schultheiss, Heinz Peter ^a   Pries, Axel ^a   Rauch, Ursula ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

A549; Angiogenesis; Chemokines; Splicing; Tissue factor

Indexed keywords

ALTERNATIVELY SPLICED TISSUE FACTOR; CYSTEINE RICH PROTEIN 61; FULL LENGTH TISSUE FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN CLK1; PROTEIN CLK4; REGULATOR PROTEIN; THROMBOPLASTIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VITRONECTIN RECEPTOR;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CELL COUNT; CELL HYPOXIA; CELL STRAIN A549; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUNG CARCINOMA; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINE CCL2; CYSTEINE-RICH PROTEIN 61; HUMANS; INTEGRIN ALPHAVBETA3; LUNG NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN ISOFORMS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; THROMBOPLASTIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84878200731     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2013.2413     Document Type: Article

References (39)

1. Eisenreich A, Celebi O, Goldin-Lang P, Schultheiss HP and Rauch U: Upregulation of tissue factor expression and thrombogenic activity in human aortic smooth muscle cells by irradiation, rapamycin and paclitaxel. Int Immunopharmacol 8: 307-311, 2008.
2. Giesen PL, Rauch U, Bohrman B, et al: Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 96: 2311-2315, 1999. (Pubitemid 29117911)
3. Rauch U, Antoniak S, Boots M, et al: Association of tissue-factor upregulation in squamous-cell carcinoma of the lung with increased tissue factor in circulating blood. Lancet Oncol 6: 254, 2005. (Pubitemid 40450719)
4. Szotowski B, Antoniak S, Poller W, Schultheiss HP and Rauch U: Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res 96: 1233-1239, 2005. (Pubitemid 40962100)
5. Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M and Nemerson Y: Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med 9: 458-462, 2003. (Pubitemid 36460081)
6. Eisenreich A, Bogdanov VY, Zakrzewicz A, et al: Cdc2-like kinases and DNA topoisomerase I regulate alternative splicing of tissue factor in human endothelial cells. Circ Res 104: 589-599, 2009.
7. Eisenreich A, Malz R, Pepke W, Ayral Y, Poller W, Schultheiss HP and 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 73: 1746-1752, 2009.
8. Tardos JG, Eisenreich A, Deikus G, et al: SR proteins ASF/SF2 and SRp55 participate in tissue factor biosynthesis in human monocytic cells. J Thromb Haemost 6: 877-884, 2008. (Pubitemid 351524551)
9. Rauch U and Antoniak S: Tissue factor-positive microparticles in blood associated with coagulopathy in cancer. Thromb Haemost 97: 9-10, 2007. (Pubitemid 46242380)
10. Eisenreich A, Boltzen U, Malz R, Schultheiss HP and Rauch U: Overexpression of alternatively spliced tissue factor induces the pro-angiogenic properties of murine cardiomyocytic HL-1 cells. Circ J 75: 1235-1242, 2011.
11. Eisenreich A and Rauch U: Regulation and differential role of the tissue factor isoforms in cardiovascular biology. Trends Cardiovasc Med 20: 199-203, 2010.
12. Hobbs JE, Zakarija A, Cundiff DL, et al: Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res 120 (Suppl 2) S13-S21, 2007. (Pubitemid 350101769)
13. van den Berg YW, van den Hengel LG, Myers HR, et al: Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci USA 106: 19497-19502, 2009.
14. Goldin-Lang P, Tran QV, Fichtner I, et al: Tissue factor expression pattern in human non-small cell lung cancer tissues indicate increased blood thrombogenicity and tumor metastasis. Oncol Rep 20: 123-128, 2008.
15. Zhang T, Koide N, Wada Y, et al: Significance of monocyte chemotactic protein-1 and thymidine phosphorylase in angiogenesis of human cardiac myxoma. Circ J 67: 54-60, 2003. (Pubitemid 36123989)
16. Zhang Y, Han J, Yang X, et al: Pigment epithelium-derived factor inhibits angiogenesis and growth of gastric carcinoma by down-regulation of VEGF. Oncol Rep 26: 681-686, 2011.
17. Shimizu T, Okayama A, Inoue T and Takeda K: Analysis of gene expression during staurosporine-induced neuronal differentiation of human prostate cancer cells. Oncol Rep 14: 441-448, 2005.
18. 3 binding site in CCN1 (CYR61) critical for pro-angiogenic activities in vascular endothelial cells. J Biol Chem 279: 44166-44176, 2004.
19. Hutchings H, Ortega N and Plouët J: Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 17: 1520-1522, 2003.
20. Löbel M, Bauer S, Meisel C, et al: CCN1: CCN1: a novel inflammation-regulated biphasic immune cell migration modulator. Cell Mol Life Sci 69: 3101-3113, 2012.
21. Schaffner F, Versteeg HH, Schillert A, Yokota N, Petersen LC, Mueller BM and Ruf W: Cooperation of tissue factor cytoplasmic domain and PAR2 signaling in breast cancer development. Blood 116: 6106-6113, 2010.
22. Fedorov O, Huber K, Eisenreich A, et al: Specific CLK inhibitors from a novel chemotype for regulation of alternative splicing. Chem Biol 18: 67-76, 2011.
23. Schwertz H, Tolley ND, Foulks JM, et al: Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med 203: 2433-2440, 2006. (Pubitemid 44664613)
24. Kim SH, Kim KW and Jeong JW: Inhibition of hypoxia-induced angiogenesis by sodium butyrate, a histone deacetylase inhibitor, through hypoxia-inducible factor-1α suppression. Oncol Rep 17: 793-797, 2007.
25. Łuczak MW, Roszak A, Pawlik P, Kȩdzia H, Lianeri M and Jagodziński PP: Increased expression of HIF-1A and its implication in the hypoxia pathway in primary advanced uterine cervical carcinoma. Oncol Rep 26: 1259-1264, 2011.
26. Gang H, Hai Y, Dhingra R, et al: A novel hypoxia-inducible spliced variant of mitochondrial death gene Bnip3 promotes survival of ventricular myocytes. Circ Res 108: 1084-1092, 2011.
27. Hirschfeld M, zur Hausen A, Bettendorf H, Jäger M and Stickeler E: Alternative splicing of Cyr61 is regulated by hypoxia and significantly changed in breast cancer. Cancer Res 69: 2082-2090, 2009.
28. Tazi J, Bakkour N and Stamm S: Alternative splicing and disease. Biochim Biophys Acta 1792: 14-26, 2009.
29. Xu F, Shi J, Yu B, Ni W, Wu X and Gu Z: Chemokines mediate mesenchymal stem cell migration toward gliomas in vitro. Oncol Rep 23: 1561-1567, 2010.
30. Zhao X, Li DC, Zhao H, et al: A study of the suppressive effect on human pancreatic adenocarcinoma cell proliferation and angiogenesis by stable plasmid-based siRNA silencing of c-Src gene expression. Oncol Rep 27: 628-636, 2012.
31. Arderiu G, Peña E, Aledo R, Juan-Babot O and Badimon L: Tissue factor regulates microvessel formation and stabilization by induction of chemokine (C-C motif) ligand 2 expression. Arterioscler Thromb Vasc Biol 31: 2607-2615, 2011.
32. Ollivier V, Bentolila S, Chabbat J, Hakim J and de Prost D: Tissue factor-dependent vascular endothelial growth factor production by human fibroblasts in response to activated factor VII. Blood 91: 2698-2703, 1998. (Pubitemid 28227518)
33. Roberts JR, Perkins GD, Fujisawa T, Pettigrew KA, Gao F, Ahmed A and Trickett DR: Vascular endothelial growth factor promotes physical wound repair and is anti-apoptotic in primary distal lung epithelial and A549 cells. Crit Care Med 35: 2164-2170, 2007. (Pubitemid 47326455)
34. Loges S, Butzal M, Otten J, et al: Cilengitide inhibits proliferation and differentiation of human endothelial progenitor cells in vitro. Biochem Biophys Res Commun 357: 1016-1020, 2007. (Pubitemid 46695889)
35. Cirillo P, Calì G, Golino P, et al: Tissue factor binding of activated factor VII triggers smooth muscle cell proliferation via extracellular signal-regulated kinase activation. Circulation 109: 2911-2916, 2004. (Pubitemid 38780307)
36. Bourgeois CF, Lejeune F and Stévenin J: Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA. Prog Nucleic Acids Res Mol Biol 78: 37-88, 2004. (Pubitemid 39753917)
37. Eisenreich A, Boltzen U, Poller W, Schultheiss HP and Rauch U: Effects of the Cdc2-like kinase-family and DNA topoisomerase I on the alternative splicing of eNOS in TNF-α-stimulated human endothelial cells. Biol Chem 389: 1333-1338, 2008.
38. Eisenreich A and Rauch U: PI3K inhibitors in cardiovascular disease. Cardiovasc Ther 29: 29-36, 2011.
39. Prasad J, Colwill K, Pawson T and Manley JL: The protein kinase Clk/Sty directly modulates SR protein activity: both hyper- and hypophosphorylation inhibit splicing. Mol Cell Biol 19: 6991-7000, 1999. (Pubitemid 29441881)