Activating stimuli induce platelet microRNA modulation and proteome reorganisation

Thrombosis and Haemostasis

Volumn 114, Issue 1, 2015, Pages 96-108

  Cimmino, Giovanni ^a   Tarallo, Roberta ^b   Nassa, Giovanni ^b   De Filippo, Maria Rosaria ^b,c   Giurato, Giorgio ^b   Ravo, Maria ^b   Rizzo, Francesca ^b   Conte, Stefano ^a   Pellegrino, Grazia ^d   Cirillo, Plinio ^d   Calabrò, Paolo ^a   Öhman, Tiina ^e   Nyman, Tuula A ^e   Weisz, Alessandro ^b,f   Golino, Paolo ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e UNIVERSITY OF HELSINKI   (Finland)

^f S Giovanni di Dio e Ruggi d'Aragona Hospital   (Italy)

Author keywords

MicroRNA; Platelet activation; Platelet system biology; Quantitative proteomics; RNA Seq

Indexed keywords

ADENOSINE DIPHOSPHATE; COLLAGEN; INTEGRIN; MICRORNA; THROMBIN RECEPTOR ACTIVATING PEPTIDE; TRANSCRIPTOME; PEPTIDE; PROTEOME;

ARTICLE; BLOOD ANALYSIS; BLOOD CLOTTING; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; HUMAN; INFLAMMATION; MALE; MASS SPECTROMETRY; MRNA EXPRESSION ASSAY; NORMAL HUMAN; NUCLEAR REPROGRAMMING; PLATELET MICRORNA MODULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEOME REORGANISATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION; WESTERN BLOTTING; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; PROCEDURES; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SYSTEMS BIOLOGY; THROMBOCYTE; TIME;

ADENOSINE DIPHOSPHATE; BLOOD PLATELETS; COLLAGEN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HEALTHY VOLUNTEERS; HUMANS; MALE; MICRORNAS; PEPTIDES; PLATELET ACTIVATION; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TIME FACTORS; TRANSCRIPTOME;

EID: 84934783581     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH14-09-0726     Document Type: Article

References (52)

1. Fuster V, Badimon L, Badimon JJ, et al. The pathogenesis of coronary artery disease and the acute coronary syndromes (1). N Engl J Med 1992; 326: 242-250.
2. Bennett JS, Mousa S. Platelet function inhibitors in the Year 2000. Thromb Haemost 2001; 85: 395-400.
3. Trip MD, Cats VM, van Capelle FJ, et al. Platelet hyperreactivity and prognosis in survivors of myocardial infarction. N Engl J Med 1990; 322: 1549-1554.
4. Newman PJ, Gorski J, White GC, 2nd, et al. Enzymatic amplification of plateletspecific messenger RNA using the polymerase chain reaction. J Clin Invest 1988; 82: 739-743.
5. Gnatenko DV, Dunn JJ, Schwedes J, et al. Transcript profiling of human platelets using microarray and serial analysis of gene expression (SAGE). Meth Mol Biol 2009; 496: 245-272.
6. Freedman JE. A platelet transcriptome revolution. Blood 2011; 118: 3760-3761.
7. Ple H, Maltais M, Corduan A, et al. Alteration of the platelet transcriptome in chronic kidney disease. Thromb Haemost 2012; 108: 605-615.
8. Bray PF, McKenzie SE, Edelstein LC, et al. The complex transcriptional landscape of the anucleate human platelet. BMC Genom 2013; 14: 1.
9. Kieffer N, Guichard J, Farcet JP, et al. Biosynthesis of major platelet proteins in human blood platelets. Eur J Biochem 1987; 164: 189-195.
10. 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.
11. Denis MM, Tolley ND, Bunting M, et al. Escaping the nuclear confines: signaldependent pre-mRNA splicing in anucleate platelets. Cell 2005; 122: 379-391.
12. 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 2006; 203: 2433-2440.
13. Baek D, Villen J, Shin C, et al. The impact of microRNAs on protein output. Nature 2008; 455: 64-71.
14. Landry P, Plante I, Ouellet DL, et al. Existence of a microRNA pathway in anucleate platelets. Nature Struct Mol Biol 2009; 16: 961-966.
15. Ple H, Landry P, Benham A, et al. The repertoire and features of human platelet microRNAs. PloS one 2012; 7: e50746.
16. Simon LM, Edelstein LC, Nagalla S, et al. Human platelet microRNA-mRNA networks associated with age and gender revealed by integrated plateletomics. Blood 2014; Epub ahead of print.
17. Brambilla M, Camera M, Colnago D, et al. Tissue factor in patients with acute coronary syndromes: expression in platelets, leukocytes, and platelet-leukocyte aggregates. Arterioscl Thromb Vasc Biol 2008; 28: 947-953.
18. Amisten S. A rapid and efficient platelet purification protocol for platelet gene expression studies. Meth Mol Biol 2012; 788: 155-172.
19. Sener A, Egemen G, Cevik O, et al. In vitro effects of nitric oxide donors on apoptosis and oxidative/nitrative protein modifications in ADP-activated platelets. Human Exp Toxicol 2013; 32: 225-235.
20. Cirillo P, Golino P, Ragni M, et al. Activated platelets and leucocytes cooperatively stimulate smooth muscle cell proliferation and proto-oncogene expression via release of soluble growth factors. Cardiovasc Res 1999; 43: 210-218.
21. Mangalpally KK, Siqueiros-Garcia A, Vaduganathan M, et al. Platelet activation patterns in platelet size sub-populations: differential responses to aspirin in vitro. J Thromb Thrombol 2010; 30: 251-262.
22. Nassa G, Tarallo R, Giurato G, et al. Post-transcriptional regulation of human breast cancer cell proteome by unliganded estrogen receptor beta via microRNAs. Mol Cell Proteom 2014; 13: 1076-1090.
23. Shilov IV, Seymour SL, Patel AA, et al. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteom 2007; 6: 1638-1655.
24. Vizcaino JA, Cote RG, Csordas A, et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucl Acids Res 2013; 41 (Database issue): D1063-1069.
25. D'Andrea D, Grassi L, Mazzapioda M, et al. FIDEA: a server for the functional interpretation of differential expression analysis. Nucl Acids Res 2013; 41 (Web Server issue): W84-88.
26. Rolf N, Knoefler R, Suttorp M, et al. Optimized procedure for platelet RNA profiling from blood samples with limited platelet numbers. Clin Chem 2005; 51: 1078-1080.
27. Rox JM, Bugert P, Muller J, et al. Gene expression analysis in platelets from a single donor: evaluation of a PCR-based amplification technique. Clin Chem 2004; 50: 2271-2278.
28. Pfaff J, Meister G. Argonaute and GW182 proteins: an effective alliance in gene silencing. Biochem Soc Transact 2013; 41: 855-860.
29. Chekulaeva M, Mathys H, Zipprich JT, et al. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nature Struct Mol Biol 2011; 18: 1218-1226.
30. Stratz C, Nuhrenberg TG, Binder H, et al. Micro-array profiling exhibits remarkable intra-individual stability of human platelet micro-RNA. Thromb Haemost 2012; 107: 634-641.
31. 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.
32. Nagalla S, Shaw C, Kong X, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011; 117: 5189-5197.
33. Giurato G, De Filippo MR, Rinaldi A, et al. iMir: an integrated pipeline for high-throughput analysis of small non-coding RNA data obtained by smallRNA-Seq. BMC Bioinform 2013; 14: 362.
34. Fawcett J, Caberos LP, Littleton JM. The potentiation of platelet aggregation by mechanical stimuli is inhibited by ethanol in vitro. Alcohol Alcoholism 1987; 1: 573-576.
35. Cattaneo M, Tenconi PM, Lecchi A, et al. In vitro effects of picotamide on human platelet aggregation, the release reaction and thromboxane B2 production. Thromb Res 1991; 62: 717-724.
36. Born GV, Cross MJ. The Aggregation of Blood Platelets. J Physiol 1963; 168: 178-195.
37. Cheloufi S, Dos Santos CO, Chong MM, et al. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010; 465: 584-589.
38. Merkerova M, Belickova M, Bruchova H. Differential expression of microRNAs in hematopoietic cell lineages. Eur J Haematol 2008; 81: 304-310.
39. Cimmino G, Nassa RT, De Filippo MR, et al. Platelet activation results in modulation of miRNA expression profile: new insights into the pathophysiology of platelet activation. Circulation 2012; 126 (Suppl): Abstract.
40. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000; 407: 258-264.
41. Gidlof O, van der Brug M, Ohman J, et al. Platelets activated during myocardial infarction release functional miRNA, which can be taken up by endothelial cells and regulate ICAM1 expression. Blood 2013; 121: 3908-3917, S1-26.
42. Willeit P, Zampetaki A, Dudek K, et al. Circulating microRNAs as novel biomarkers for platelet activation. Circulation Res 2013; 112: 595-600.
43. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297.
44. Hammond SM, Bernstein E, Beach D, et al. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000; 404: 293-296.
45. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297: 2056-2060.
46. Mourelatos Z, Dostie J, Paushkin S, et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Develop 2002; 16: 720-728.
47. Meister G, Landthaler M, Patkaniowska A, et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004; 15: 185-197.
48. Rivas FV, Tolia NH, Song JJ, et al. Purified Argonaute2 and an siRNA form recombinant human RISC. Nature Struct Mol Biol 2005; 12: 340-349.
49. Chi SW, Hannon GJ, Darnell RB. An alternative mode of microRNA target recognition. Nature Struct Mol Biol 2012; 19: 321-327.
50. Sattler M, Salgia R, Shrikhande G, et al. Differential signaling after beta1 integrin ligation is mediated through binding of CRKL to p120 (CBL) and p110 (HEF1). J Biol Chem 1997; 272: 14320-14326.
51. Hirota T, Morisaki T, Nishiyama Y, et al. Zyxin, a regulator of actin filament assembly, targets the mitotic apparatus by interacting with h-warts/LATS1 tumor suppressor. J Cell Biol 2000; 149: 1073-1086.
52. Verschoor A, Langer HF. Crosstalk between platelets and the complement system in immune protection and disease. Thromb Haemost 2013; 110: 910-919.