Dissociation of SERPINE1 mRNA from the translational repressor proteins Ago2 and TIA-1 upon platelet activation

Thrombosis and Haemostasis

Volumn 113, Issue 5, 2015, Pages 1046-1059

  Corduan, Aurélie ^a,b   Plé, Hélène ^a,b   Laffont, Benoit ^a,b   Wallon, Thérèse ^a,b   Plante, Isabelle ^a,b   Landry, Patricia ^a,b   Provost, Patrick ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Argonaute 2; MicroRNA; mRNA; Plasminogen activator inhibitor 1 (PAI 1); Platelet

Indexed keywords

ALPHA2 INTEGRIN; ARGONAUTE 2 PROTEIN; BETA3 INTEGRIN; IMMUNOGLOBULIN G; MESSENGER RNA; MICRORNA; MICRORNA 134; MICRORNA 143; MICRORNA 199B; MICRORNA 19A; MICRORNA 21; MICRORNA 22; MICRORNA 223; MICRORNA 24; MICRORNA 326; MICRORNA 503; PADGEM PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROSTAGLANDIN SYNTHASE; PROTEIN BCL 3; RNA BINDING PROTEIN; SERPINE 1 MESSENGER RNA; SODIUM ASCORBIC ACID COTRANSPORTER; T CELL RESTRICTED INTRACELLULAR ANTIGEN 1; T LYMPHOCYTE ANTIGEN; TALIN; THROMBIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; POLYADENYLIC ACID BINDING PROTEIN; REPRESSOR PROTEIN; SERPINE1 PROTEIN, HUMAN; TIA1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; GENE ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; NORMAL HUMAN; NORTHERN BLOTTING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOIMMUNOPRECIPITATION; RNA EXTRACTION; RNA TRANSLATION; THROMBOCYTE ACTIVATION; TRANSLATION REGULATION; 3' UNTRANSLATED REGION; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PROTEIN SYNTHESIS; THROMBOCYTE;

3' UNTRANSLATED REGIONS; ARGONAUTE PROTEINS; BLOOD PLATELETS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPRECIPITATION; MICRORNAS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLATELET ACTIVATION; POLY(A)-BINDING PROTEINS; POLYMERASE CHAIN REACTION; PROTEIN BIOSYNTHESIS; REPRESSOR PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; THROMBIN;

EID: 84931287776     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH14-07-0622     Document Type: Article

References (50)

1. Michelson AD. How platelets work: platelet function and dysfunction. J Thromb Thrombolysis 2003; 16: 7-12.
2. Schulz C, Massberg S. Platelets in atherosclerosis and thrombosis. Handb Exp Pharmacol 2012(210): 111-33.
3. Roth GJ, Hickey MJ, Chung DW, et al. Circulating human blood platelets retain appreciable amounts of poly (A)+ RNA. Biochem Biophys Res Commun 1989; 160: 705-710.
4. Ts’ao CH. Rough endoplasmic reticulum and ribosomes in blood platelets. Scand J Haematol 1971; 8: 134-140.
5. Zimmerman GA, Weyrich AS. Signal-dependent protein synthesis by activated platelets: new pathways to altered phenotype and function. Arterioscler Thromb Vasc Biol 2008; 28: s17-24.
6. Brogren H, Karlsson L, Andersson M, et al. Platelets synthesize large amounts of active plasminogen activator inhibitor 1. Blood 2004; 104: 3943-3948.
7. Landry P, Plante I, Ouellet DL, et al. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol 2009; 16: 961-966.
8. Ple H, Landry P, Benham A, et al. The repertoire and features of human platelet microRNAs. PLoS One 2012; 7: e50746.
9. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
10. Meister G, Landthaler M, Patkaniowska A, et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004; 15: 185-197.
11. Fabian MR, Sundermeier TR, Sonenberg N. Understanding how miRNAs posttranscriptionally regulate gene expression. Prog Mol Subcell Biol 2010; 50: 1-20.
12. Kondkar AA, Bray MS, Leal SM, et al. VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost 2010; 8: 369-378.
13. Osman A, Falker K. Characterisation of human platelet microRNA by quantitative PCR coupled with an annotation network for predicted target genes. Platelets 2011; 22: 433-441.
14. Nagalla S, Shaw C, Kong X, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011; 117: 5189-5197.
15. Simon LM, Edelstein LC, Nagalla S, et al. Human platelet microRNA-mRNA networks associated with age and gender revealed by integrated plateletomics. Blood 2014; 123: e37-45.
16. Xu X, Gnatenko DV, Ju J, et al. Systematic analysis of microRNA fingerprints in thrombocythemic platelets using integrated platforms. Blood 2012; 120: 3575-3585.
17. Shi R, Ge L, Zhou X, et al. Decreased platelet miR-223 expression is associated with high on-clopidogrel platelet reactivity. Thromb Res 2013; 131: 508-513.
18. Laffont B, Corduan A, Ple H, et al. Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles. Blood 2013; 122: 253-261.
19. Ple H, Maltais M, Corduan A, Rousseau G, Madore F, Provost P. Alteration of the platelet transcriptome in chronic kidney disease. Thromb Haemost 2012; 108: 605-615.
20. Marchand A, Proust C, Morange PE, et al. miR-421 and miR-30c inhibit SERPINE 1 gene expression in human endothelial cells. PLoS One 2012; 7: e44532.
21. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004; 10: 1507-1517.
22. Osman A, Hitzler WE, Meyer CU, et al. Effects of pathogen reduction systems on platelet microRNAs, mRNAs, activation, and function. Platelets 2014; Epub ahead of print.
23. Beitzinger M, Peters L, Zhu JY, et al. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol 2007; 4: 76-84.
24. Frank F, Sonenberg N, Nagar B. Structural basis for 5’-nucleotide base-specific recognition of guide RNA by human AGO 2. Nature 2010; 465: 818-822.
25. Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-655.
26. Weyrich AS, Dixon DA, Pabla R, et al. Signal-dependent translation of a regulatory protein, Bcl-3, in activated human platelets. Proc Natl Acad Sci USA 1998; 95: 5556-5561.
27. Lindemann S, Tolley ND, Dixon DA, et al. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol 2001; 154: 485-490.
28. Ginsburg D, Zeheb R, Yang AY, et al. cDNA cloning of human plasminogen activator- inhibitor from endothelial cells. J Clin Invest 1986; 78: 1673-1680.
29. Weyrich AS, Lindemann S, Tolley ND, et al. Change in protein phenotype without a nucleus: translational control in platelets. Semin Thromb Hemost 2004; 30: 491-498.
30. Srikantan S, Tominaga K, Gorospe M. Functional interplay between RNA-binding protein HuR and microRNAs. Curr Protein Pept Sci 2012; 13: 372-379.
31. Piecyk M, Wax S, Beck AR, et al. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J 2000; 19: 4154-4163.
32. Kim HH, Kuwano Y, Srikantan S, et al. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev 2009; 23: 1743-1748.
33. Rowley JW, Oler AJ, Tolley ND, et al. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 2011; 118: e101-111.
34. Turchinovich A, Burwinkel B. Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol 2012; 9: 1066-1075.
35. Chu CY, Rana TM. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p 54. PLoS Biol 2006; 4: e210.
36. Iwasaki S, Kawamata T, Tomari Y. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol Cell 2009; 34: 58-67.
37. Hong W, Kondkar AA, Nagalla S, et al. Transfection of human platelets with short interfering RNA. Clin Transl Sci 2011; 4: 180-182.
38. Lai X, Schmitz U, Gupta SK, et al. Computational analysis of target hub gene repression regulated by multiple and cooperative miRNAs. Nucleic Acids Res 2012; 40: 8818-8834.
39. Evangelista V, Manarini S, Di Santo A, et al. De novo synthesis of cyclooxygenase- 1 counteracts the suppression of platelet thromboxane biosynthesis by aspirin. Circ Res 2006; 98: 593-595.
40. Wu X, Brewer G. The regulation of mRNA stability in mammalian cells: 2. 0. Gene 2012; 500: 10-21.
41. Kawai T, Lal A, Yang X, et al. Translational control of cytochrome c by RNAbinding proteins TIA-1 and HuR. Mol Cell Biol 2006; 26: 3295-3307.
42. Ho JJ, Marsden PA. Competition and collaboration between RNA-binding proteins and microRNAs. Wiley Interdiscip Rev RNA 2014; 5: 69-86.
43. Vasudevan S, Steitz JA. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 2007; 128: 1105-1118.
44. Mazan-Mamczarz K, Galban S, Lopez de Silanes I, et al. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc Natl Acad Sci USA 2003; 100: 8354-8359.
45. Bhattacharyya SN, Habermacher R, Martine U, et al. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006; 125: 1111-1124.
46. Dixon DA, Tolley ND, Bemis-Standoli K, et al. Expression of COX-2 in plateletmonocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signaling. J Clin Invest 2006; 116: 2727-2738.
47. Kieffer N, Guichard J, Farcet JP, et al. Biosynthesis of major platelet proteins in human blood platelets. Eur J Biochem 1987; 164: 189-195.
48. Thon JN, Devine DV. Translation of glycoprotein IIIa in stored blood platelets. Transfusion 2007; 47: 2260-2270.
49. Savini I, Catani MV, Arnone R, et al. Translational control of the ascorbic acid transporter SVCT2 in human platelets. Free Radic Biol Med 2007; 42: 608-616.
50. Thiele T, Steil L, Gebhard S, et al. Profiling of alterations in platelet proteins during storage of platelet concentrates. Transfusion 2007; 47: 1221-1233.