Cdc2-like kinases and DNA topoisomerase I regulate alternative splicing of tissue factor in human endothelial cells

Circulation Research

Volumn 104, Issue 5, 2009, Pages 589-599

  Eisenreich, Andreas ^a   Bogdanov, Vladimir Y ^b   Zakrzewicz, Andreas ^a   Pries, Axel ^a   Antoniak, Silvio ^a   Poller, Wolfgang ^a   Schultheiss, Heinz Peter ^a   Rauch, Ursula ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiovascular research; Endothelial cells; Tissue factor; Tumor necrosis factor; Vascular biology

Indexed keywords

ARGININE; CHROMOGENIC SUBSTRATE; CYCLIN DEPENDENT KINASE 1; DNA TOPOISOMERASE; PROCOAGULANT; SERINE; THROMBOPLASTIN; TUMOR NECROSIS FACTOR ALPHA; BLOOD CLOTTING FACTOR 10A; CLK DUAL SPECIFICITY KINASES; CLK DUAL-SPECIFICITY KINASES; MESSENGER RNA; NUCLEAR PROTEIN; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; RNA BINDING PROTEIN; RNA PRECURSOR; SERINE ARGININE RICH SPLICING PROTEINS; SERINE-ARGININE-RICH SPLICING PROTEINS; SFRS1 PROTEIN, HUMAN; SFRS4 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN; WESTERN BLOTTING; BLOOD CLOTTING; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHOSPHORYLATION; RNA INTERFERENCE; TIME;

ALTERNATIVE SPLICING; BLOOD COAGULATION; CELLS, CULTURED; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; ENDOTHELIAL CELLS; FACTOR XA; GENE EXPRESSION REGULATION; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; RNA PRECURSORS; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; THROMBOPLASTIN; TIME FACTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 63649100364     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.183905     Document Type: Article

References (30)

1. Rauch U, Nemerson Y. Circulating tissue factor and thrombosis. Curr Opin Hematol. 2000;7:273-277.
2. Szotowski B, Antoniak S, Poller W, Schultheiss HP, Rauch U. Proco-agulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res. 2005;96:1233-1239.
3. Morel O, Toti F, Hugel B, Bakouboula B, Camoin-Jau L, Dignat-George F, Freyssinet JM. Procoagulant microparticles: disrupting the vascular homeostasis equation? Arterioscler Thromb Vasc Biol. 2006;26: 2594-2604.
4. Giesen PL, Rauch U, Bohrman B, Kling D, Roque M, Fallon JT, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A. 1999;96: 2311-2315.
5. Szotowski B, Antoniak S, Rauch U. Alternatively spliced tissue factor: a previously unknown piece in the puzzle of hemostasis. Trends Cardiovasc Med. 2006;16:177-182.
6. Rauch U, Bonderman D, Bohrmann B, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood. 2000b;96:170-175.
7. Mackman N. Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol. 2004;24:1015-1022.
8. 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.
9. Bogdanov VY. Blood coagulation and alternative pre-mRNA splicing: an overview. Curr Mol Med. 2006;6:859-869.
10. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem. 2003;72:291-336.
11. Valdivia HH. One gene, many proteins: alternative splicing of the ryanodine receptor gene adds novel functions to an already complex channel protein. Circ Res. 2007;100:761-763.
12. Bourgeois CF, Lejeune F, 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. 2004;78:37-88.
13. Muraki M, Ohkawara B, Hosoya T, Onogi H, Koizumi J, Koizumi T, Sumi K, Yomoda J, Murray MV, Kimura H, Furuichi K, Shibuya H, Krainer AR, Suzuki M, Hagiwara M. Manipulation of alternative splicing by a newly developed inhibitor of Clks. J Biol Chem. 2004;279: 24246-24254.
14. Soret J, Gabut M, Dupon C, Kohlhagen G, Stévenin J, Pommier Y, Tazi J. Altered serine/arginine-rich protein phosphorylation and exonic enhancer-dependent splicing in mammalian cells lacking topoisomerase I. Cancer Res. 2003;63:8203-8211.
15. Prasad J, Colwill K, Pawson T, Manley JL. The protein kinase Clk/Sty directly modulates SR protein activity: both hyper- and hypophosphorylation inhibit splicing. Mol Cell Biol. 1999;19:6991-7000.
16. Schwertz H, Tolley ND, Foulks JM, Denis MM, Risenmay BW, Buerke M, Tilley RE, Rondina MT, Harris EM, Kraiss LW, Mackman N, Zimmerman GA, Weyrich AS. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med. 2006;203:2433-2440.
17. Szotowski B, Goldin-Lang P, Antoniak S, Bogdanov VY, Pathirana D, Pauschinger M, Dörner A, Kuehl U, Coupland S, Nemerson Y, Hummel M, Poller W, Hetzer R, Schultheiss HP, Rauch U. Alterations in myo-cardial tissue factor expression and cellular localization in dilated cardiomyopathy. J Am Coll Cardiol. 2005;45:1081-1089.
18. Lawson JH, Kalafatis M, Stram S, Mann KG. A model for the tissue factor pathway to thrombin I. An empirical study. J Biol Chem. 1994; 269:23357-23366.
19. Duncan PI, Howell BW, Marius RM, Drmanic S, Douville EM, Bell JC. Alternative splicing of STY, a nuclear dual specificity kinase. J Biol Chem. 1995;270:21524-21531.
20. Duncan PI, Stojdl DF, Marius RM, Bell JC. In vivo regulation of alternative pre-mRNA splicing by the Clk1 protein kinase. Mol Cell Biol. 1997;17:5996-6001.
21. Chand HS, Ness SA, Kisie W. Identification of a novel human tissue factor splice variant that is upregulated in tumor cells. Int J Cancer. 2006;118:1713-1720.
22. Rauch U, Antoniak S, Boots M, Schulze K, Goldin-Lang P, Stein H. Association of tissue-factor upregulation in squamous-cell carcinoma of the lung with increased tissue factor in circulating blood. Lancet Oncol. 2005;6:254.
23. Sanford JR, Bruzik JP. Regulation of SR protein localization during development. Proc Natl Acad Sci U S A. 2001;98:10184-10189.
24. Kashima T, Rao N, David CJ, Manley JL. hnRNP A1 functions with specificity in repression of SMN2 exon 7 splicing. Hum Mol Genet. 2007;16:3149-3159.
25. Zahler AM, Neugebauer KM, Stolk JA, Roth MB. Human SR proteins and isolation of a cDNA encoding SRp75. Mol Cell Biol. 1993;13: 4023-4028.
26. Houslay MD, Baillie GS, Maurice DH. cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res. 2007;100: 950-966.
27. Solier S, Lansiaux A, Logette E, Wu J, Soret J, Tazi J. Topoisomerase I and II inhibitors control caspase-2 pre-messenger RNA splicing in human cells. Mol Cancer Res. 2004;2:53-61.
28. Stamm S. Regulation of alternative splicing by reversible protein phos-phorylation. J Biol Chem. 2008;283:1223-1227.
29. 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.
30. Tedgui A, Mallat Z. Anti-inflammatory mechanisms in the vascular wall. Circ Res. 2001;88:877-887.