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The Platelet Transcriptome: Coding RNAs

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Platelets in Thrombotic and Non-Thrombotic Disorders

Abstract

Until recently platelets were categorized as simple anucleate cytoplasts that function solely in the hemostatic arena. However, the last decade has demonstrated that platelets have roles beyond primary hemostasis and they possess complex molecular information including a rich repertoire of messenger RNAs (mRNAs). Platelet mRNAs have features that mirror transcripts produced and translated in nucleated cells, and mRNAs for approximately half of the human genome have been identified in this terminally differentiated cell. The study of platelet mRNAs has expanded tremendously with the advent of next-generation RNA sequencing (NGS) and several groups have shown that platelets are capable of translating some megakaryocyte-derived mRNAs into protein. Platelet mRNA profiles have also been used to predict cellular function and platelets are capable of transferring intact mRNAs into microparticles and other cells. This chapter reviews our current understanding of platelet mRNAs and their potential contribution to biological and pathologic processes in humans. Roles for noncoding RNAs are described in Edelstein and Bray (2017).

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References

  • Alhasan AA, Izuogu OG, Al-Balool HH, Steyn JS, Evans A, Colzani M, Ghevaert C, Mountford JC, Marenah L, Elliott DJ, Santibanez-Koref M, Jackson MS (2016) Circular RNA enrichment in platelets is a signature of transcriptome degradation. Blood 127(9):e1–e11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anfossi G, Russo I, Trovati M (2009) Platelet dysfunction in central obesity. Nutr Metab Cardiovasc Dis 19:440–449

    Article  CAS  PubMed  Google Scholar 

  • Assinger A (2014) Platelets and infection—an emerging role of platelets in viral infection. Front Immunol 5:649

    Article  PubMed  PubMed Central  Google Scholar 

  • Auer PL, Doerge RW (2010) Statistical design and analysis of RNA sequencing data. Genetics 185:405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Béres BJ, Tóth-Zsámboki E, Vargová K, László A, Masszi T, Kerecsen G, Préda I, Kiss RG (2008) Analysis of platelet alpha2-adrenergic receptor activity in stable coronary artery disease patients on dual antiplatelet therapy. Thromb Haemost 100:829–838

    PubMed  Google Scholar 

  • Best MG, Sol N, Kooi I, Tannous J, Westerman BA, Rustenburg F, Schellen P, Verschueren H, Post E, Koster J, Ylstra B, Ameziane N, Dorsman J, Smit EF, Verheul HM, Noske DP, Reijneveld JC, Nilsson RJA, Tannous BA, Wesseling P, Wurdinger T (2015) RNA-Seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell 28:666–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatt DL (2008) What makes platelets angry: diabetes, fibrinogen, obesity, and impaired response to antiplatelet therapy? J Am Coll Cardiol 52:1060–1061

    Article  PubMed  Google Scholar 

  • Booyse FM, Rafelson ME (1967) Stable messenger RNA in the synthesis of contractile protein in human platelets. Biochim Biophys Acta 145:188–190

    Article  CAS  PubMed  Google Scholar 

  • Bray PF, McKenzie SE, Edelstein LC, Nagalla S, Delgrosso K, Ertel A, Kupper J, Jing Y, Londin E, Loher P, Chen H-W, Fortina P, Rigoutsos I (2013) The complex transcriptional landscape of the anucleate human platelet. BMC Genomics 14:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buxbaum AR, Haimovich G, Singer RH (2014) In the right place at the right time: visualizing and understanding mRNA localization. Nat Rev Mol Cell Biol 16:95–109

    Article  PubMed  PubMed Central  Google Scholar 

  • Catricala S, Torti M, Ricevuti G (2012) Alzheimer disease and platelets: how’s that relevant. Immun Ageing 9(1):20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cecchetti L, Tolley ND, Michetti N, Bury L, Weyrich AS, Gresele P (2011) Megakaryocytes differentially sort mRNAs for matrix metalloproteinases and their inhibitors into platelets: a mechanism for regulating synthetic events. Blood 118:1903–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chavda N, Mackie IJ, Porter JB, Harrison P, Patterson K, Machin SJ (1996) Rapid flow cytometric quantitation of reticulated platelets in whole blood. Platelets 7:189–194

    Article  CAS  PubMed  Google Scholar 

  • Choi YH, Hagedorn CH (2003) Purifying mRNAs with a high-affinity eIF4E mutant identifies the short 3′ poly(A) end phenotype. Proc Natl Acad Sci U S A 100:7033–7038

    Article  PubMed  PubMed Central  Google Scholar 

  • Cimmino G, Tarallo R, Nassa G, De Filippo MR, Giurato G, Ravo M, Rizzo F, Conte S, Pellegrino G, Cirillo P, Calabro P, Öhman T, Nyman TA, Weisz A, Golino P (2015) Activating stimuli induce platelet microRNA modulation and proteome reorganisation. Thromb Haemost 114(1):96–108

    Article  PubMed  Google Scholar 

  • Clancy L, Freedman JE (2014) New paradigms in thrombosis: novel mediators and biomarkers platelet RNA transfer. J Thromb Thrombolysis 37:12–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costa V, Angelini C, De Feis I, Ciccodicola A (2010) Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol 2010:853916

    Article  PubMed  PubMed Central  Google Scholar 

  • Darnell JE (2013) Reflections on the history of pre-mRNA processing and highlights of current knowledge: a unified picture. RNA 19:443–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davila J, Manwani D, Vasovic L, Avanzi M, Uehlinger J, Ireland K, Mitchell WB (2015) A novel inflammatory role for platelets in sickle cell disease. Platelets 26:726–729

    Article  CAS  PubMed  Google Scholar 

  • De Stoppelaar SF, van ’t Veer C, van der Poll T (2014) The role of platelets in sepsis. Thromb Haemost 112:666–677

    Article  PubMed  Google Scholar 

  • Delaleau M, Borden KLB (2015) Multiple export mechanisms for mRNAs. Cells 4:452–473

    Article  PubMed  PubMed Central  Google Scholar 

  • Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, Fratto CM, Tolley E, Kraiss LW, McIntyre TM, Zimmerman GA, Weyrich AS (2005) Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 122:379–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dillies M-A, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, Keime C, Marot G, Castel D, Estelle J, Guernec G, Jagla B, Jouneau L, Laloë D, Le Gall C, Schaëffer B, Le Crom S, Guedj M, Jaffrézic F (2013) A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform 14(6):671–683

    Article  CAS  PubMed  Google Scholar 

  • Dittrich M, Birschmann I, Pfrang J, Herterich S, Smolenski A, Walter U, Dandekar T (2006) Analysis of SAGE data in human platelets: features of the transcriptome in an anucleate cell. Thromb Haemost 95:643–651

    CAS  PubMed  Google Scholar 

  • Edelstein LC, Simon LM, Montoya RT, Holinstat M, Chen ES, Bergeron A, Kong X, Nagalla S, Mohandas N, Cohen DE, Dong J, Shaw C, Bray PF (2013) Racial differences in human platelet PAR4 reactivity reflect expression of PCTP and miR-376c. Nat Med 19:1609–1616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edelstein LC, Bray PF (2017) Noncoding RNAs in platelet biology. In: Gresele P et al (eds) Platelets in thrombotic and non-thrombotic disorders. Springer, Cham, pp 239–252

    Google Scholar 

  • Eicher JD, Wakabayashi Y, Vitseva O, Esa N, Yang Y, Zhu J, Freedman JE, McManus DD, Johnson AD (2016) Characterization of the platelet transcriptome by RNA sequencing in patients with acute myocardial infarction. Platelets 27(3):230–239

    Article  CAS  PubMed  Google Scholar 

  • Fallahi P, Katz R, Toma I, Li R, Reiner J, Vanhouten K, Carpio L, Marshall L, Lian Y, Bupp S, Fu SW, Rickles F, Leitenberg D, Lai Y, Weksler BB, Rebling F, Yang Z, McCaffrey TA (2013) Aspirin insensitive thrombophilia: transcript profiling of blood identifies platelet abnormalities and HLA restriction. Gene 520(2):131–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fink L, Hölschermann H, Kwapiszewska G, Muyal JP, Lengemann B, Bohle RM, Santoso S (2003) Characterization of platelet-specific mRNA by real-time PCR after laser-assisted microdissection. Thromb Haemost 90:749–756

    CAS  PubMed  Google Scholar 

  • Floyd CN, Ferro A (2014) Mechanisms of aspirin resistance. Pharmacol Ther 141:69–78

    Article  CAS  PubMed  Google Scholar 

  • Geiger J, Burkhart JM, Gambaryan S, Walter U, Sickmann A, Zahedi RP (2013) Response: platelet transcriptome and proteome—relation rather than correlation. Blood 121:5257–5258

    Article  CAS  PubMed  Google Scholar 

  • Gnatenko DV, Dunn JJ, McCorkle SR, Weissmann D, Perrotta PL, Bahou WF (2003) Transcript profiling of human platelets using microarray and serial analysis of gene expression. Blood 101:2285–2293

    Article  CAS  PubMed  Google Scholar 

  • Gnatenko DV, Zhu W, Xu X, Samuel ET, Monaghan M, Zarrabi MH, Kim C, Dhundale A, Bahou WF (2010) Class prediction models of thrombocytosis using genetic biomarkers. Blood 115:7–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodall AH, Burns P, Salles I, Macaulay IC, Jones CI, Ardissino D, de Bono B, Bray SL, Deckmyn H, Dudbridge F, Fitzgerald DJ, Garner SF, Gusnanto A, Koch K, Langford C, O’Connor MN, Rice CM, Stemple D, Stephens J, Trip MD, Zwaginga J-J, Samani NJ, Watkins NA, Maguire PB, Ouwehand WH (2010) Transcription profiling in human platelets reveals LRRFIP1 as a novel protein regulating platelet function. Blood 116:4646–4656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Healy AM, Pickard MD, Pradhan AD, Wang Y, Chen Z, Croce K, Sakuma M, Shi C, Zago AC, Garasic J, Damokosh AI, Dowie TL, Poisson L, Lillie J, Libby P, Ridker PM, Simon DI (2006) Platelet expression profiling and clinical validation of myeloid-related protein-14 as a novel determinant of cardiovascular events. Circulation 113:2278–2284

    Article  CAS  PubMed  Google Scholar 

  • Heber S, Volf I (2015) Effects of physical (in)activity on platelet function. Biomed Res Int 2015:165078

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennekens CH, Dalen JE (2014) Aspirin in the primary prevention of cardiovascular disease: current knowledge and future research needs. Trends Cardiovasc Med 24:360–366

    Article  PubMed  Google Scholar 

  • Herter JM, Rossaint J, Zarbock A (2014) Platelets in inflammation and immunity. J Thromb Haemost 12:1764–1775

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim H, Nadipalli S, DeLao T, Guthikonda S, Kleiman NS (2012) Immature platelet fraction (IPF) determined with an automated method predicts clopidogrel hyporesponsiveness. J Thromb Thrombolysis 33:137–142

    Article  CAS  PubMed  Google Scholar 

  • Ishihara H, Connolly AJ, Zeng D, Kahn ML, Zheng YW, Timmons C, Tram T, Coughlin SR (1997) Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 386:502–506

    Article  CAS  PubMed  Google Scholar 

  • Junt T, Schulze H, Chen Z, Massberg S, Goerge T, Krueger A, Wagner DD, Graf T, Italiano JE, Shivdasani RA, von Andrian UH (2007) Dynamic visualization of thrombopoiesis within bone marrow. Science 317:1767–1770

    Article  CAS  PubMed  Google Scholar 

  • Kahn ML, Zheng YW, Huang W, Bigornia V, Zeng D, Moff S, Farese RV, Tam C, Coughlin SR (1998) A dual thrombin receptor system for platelet activation. Nature 394:690–694

    Article  CAS  PubMed  Google Scholar 

  • Kahr WH, Hinckley J, Li L, Schwertz H, Christensen H, Rowley JW, Pluthero FG, Urban D, Fabbro S, Nixon B, Gadzinski R, Storck M, Wang K, Ryu G-Y, Jobe SM, Schutte BC, Moseley J, Loughran NB, Parkinson J, Weyrich AS, Di Paola J (2011) Mutations in NBEAL2, encoding a BEACH protein, cause gray platelet syndrome. Nat Genet 43:738–740

    Article  CAS  PubMed  Google Scholar 

  • Karpouza AP, Vakirtzi-Lemonias C (1997) The platelet-activating factor acetylhydrolase of mouse platelets. Biochim Biophys Acta 1323:12–22

    Article  CAS  PubMed  Google Scholar 

  • Kieffer N, Guichard J, Farcet JP, Vainchenker W, Breton-Gorius J (1987) Biosynthesis of major platelet proteins in human blood platelets. Eur J Biochem 164:189–195

    Article  CAS  PubMed  Google Scholar 

  • Kissopoulou A, Jonasson J, Lindahl TL, Osman A (2013) Next generation sequencing analysis of human platelet PolyA+ mRNAs and rRNA-depleted total RNA. PLoS One 8:e81809

    Article  PubMed  PubMed Central  Google Scholar 

  • Kondkar AA, Bray MS, Leal SM, Nagalla S, Liu DJ, Jin Y, Dong JF, Ren Q, Whiteheart SW, Shaw C, Bray PF (2010) VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost 8:369–378

    Article  CAS  PubMed  Google Scholar 

  • Laffont B, Corduan A, Plé H, Duchez A-C, Cloutier N, Boilard E, Provost P (2013) Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles. Blood 122:253–261

    Article  CAS  PubMed  Google Scholar 

  • Londin ER, Hatzimichael E, Loher P, Edelstein L, Shaw C, Delgrosso K, Fortina P, Bray PF, McKenzie SE, Rigoutsos I (2014) The human platelet: strong transcriptome correlations among individuals associate weakly with the platelet proteome. Biol Direct 9:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Lood C, Amisten S, Gullstrand B, Jönsen A, Allhorn M, Truedsson L, Sturfelt G, Erlinge D, Bengtsson AA (2010) Platelet transcriptional profile and protein expression in patients with systemic lupus erythematosus: up-regulation of the type I interferon system is strongly associated with vascular disease. Blood 116:1951–1957

    Article  CAS  PubMed  Google Scholar 

  • Mao Y, Lei L, Su J, Yu Y, Liu Z, Huo Y (2014) Regulators of G protein signaling are up-regulated in aspirin-resistant platelets from patients with metabolic syndrome. Pharmazie 69:371–373

    CAS  PubMed  Google Scholar 

  • Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nat Rev Genet 12:671–682

    Article  CAS  PubMed  Google Scholar 

  • Mason KD, Carpinelli MR, Fletcher JI, Collinge JE, Hilton AA, Ellis S, Kelly PN, Ekert PG, Metcalf D, Roberts AW, Huang DCS, Kile BT (2007) Programmed anuclear cell death delimits platelet life span. Cell 128:1173–1186

    Article  CAS  PubMed  Google Scholar 

  • Massimi I, Guerriero R, Lotti LV, Lulli V, Borgognone A, Romani F, Barillà F, Gaudio C, Gabbianelli M, Frati L, Pulcinelli FM (2014) Aspirin influences megakaryocytic gene expression leading to up-regulation of multidrug resistance protein-4 in human platelets. Br J Clin Pharmacol 78:1343–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEwen BJ (2014) The influence of diet and nutrients on platelet function. Semin Thromb Hemost 40:214–226

    Article  PubMed  Google Scholar 

  • Merlo Pich M, Raule N, Catani L, Fagioli ME, Faenza I, Cocco L, Lenaz G (2004) Increased transcription of mitochondrial genes for Complex I in human platelets during ageing. FEBS Lett 558:19–22

    Article  CAS  PubMed  Google Scholar 

  • Mohebali D, Kaplan D, Carlisle M, Supiano MA, Rondina MT (2014) Alterations in platelet function during aging: clinical correlations with thromboinflammatory disease in older adults. J Am Geriatr Soc 62:529–535

    Article  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Pääbo S, Mann M (2011) Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol 7:548

    Article  PubMed  PubMed Central  Google Scholar 

  • Nekrutenko A, Taylor J (2012) Next-generation sequencing data interpretation: enhancing reproducibility and accessibility. Nat Rev Genet 13:667–672

    Article  CAS  PubMed  Google Scholar 

  • Newman PJ, Gorski J, White GC, Gidwitz S, Cretney CJ, Aster RH (1988) Enzymatic amplification of platelet-specific messenger RNA using the polymerase chain reaction. J Clin Invest 82:739–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson RJA, Balaj L, Hulleman E, van Rijn S, Pegtel DM, Walraven M, Widmark A, Gerritsen WR, Verheul HM, Vandertop WP, Noske DP, Skog J, Würdinger T (2011) Blood platelets contain tumor-derived RNA biomarkers. Blood 118:3680–3683

    Article  PubMed  Google Scholar 

  • Nilsson RJ, Karachaliou N, Berenguer J, Gimenez-Capitan A, Schellen P, Teixido C, Tannous J, Kuiper JL, Drees E, Grabowska M, van Keulen M, Heideman DAM, Thunnissen E, Dingemans AM, Viteri S, Tannous BA, Drozdowskyj A, Rosell R, Smit EF, Wurdinger T (2016) Rearranged EML4-ALK fusion transcripts sequester in circulating blood platelets and enable blood-based crizotinib response monitoring in non-small-cell lung cancer. Oncotarget 7(1):1066–1075

    PubMed  Google Scholar 

  • Nishimura S, Nagasaki M, Kunishima S, Sawaguchi A, Sakata A, Sakaguchi H, Ohmori T, Manabe I, Italiano JE, Ryu T, Takayama N, Komuro I, Kadowaki T, Eto K, Nagai R (2015) IL-1α induces thrombopoiesis through megakaryocyte rupture in response to acute platelet needs. J Cell Biol 209:453–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noetzli L, Lo RW, Lee-Sherick AB, Callaghan M, Noris P, Savoia A, Rajpurkar M, Jones K, Gowan K, Balduini CL, Pecci A, Gnan C, De Rocco D, Doubek M, Li L, Lu L, Leung R, Landolt-Marticorena C, Hunger S, Heller P, Gutierrez-Hartmann A, Xiayuan L, Pluthero FG, Rowley JW, Weyrich AS, Kahr WHA, Porter CC, Di Paola J (2015) Germline mutations in ETV6 are associated with thrombocytopenia, red cell macrocytosis and predisposition to lymphoblastic leukemia. Nat Genet 47:535–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osman A, Hitzler WE, Ameur A, Provost P (2015) Differential expression analysis by RNA-Seq reveals perturbations in the platelet mRNA transcriptome triggered by pathogen reduction systems. PLoS One 10:e0133070

    Article  PubMed  PubMed Central  Google Scholar 

  • Pagliari MT, Baronciani L, Garcìa Oya I, Solimando M, La Marca S, Cozzi G, Stufano F, Canciani MT, Peyvandi F (2013) A synonymous (c.3390C>T) or a splice-site (c.3380-2A>G) mutation causes exon 26 skipping in four patients with von Willebrand disease (2A/IIE). J Thromb Haemost 11:1251–1259

    Article  CAS  PubMed  Google Scholar 

  • Park Y, Franchi F, Rollini F, Angiolillo DJ (2015) Update on oral antithrombotic therapy for secondary prevention following non-ST segment elevation myocardial infarction. Trends Cardiovasc Med 26(4):321–334

    Article  PubMed  Google Scholar 

  • Plé H, Landry P, Benham A, Coarfa C, Gunaratne PH, Provost P (2012a) The repertoire and features of human platelet microRNAs. PLoS One 7:e50746

    Article  PubMed  PubMed Central  Google Scholar 

  • Plé H, Maltais M, Corduan A, Rousseau G, Madore F, Provost P (2012b) Alteration of the platelet transcriptome in chronic kidney disease. Thromb Haemost 108(4):605–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Raghavachari N, Xu X, Harris A, Villagra J, Logun C, Barb J, Solomon MA, Suffredini AF, Danner RL, Kato G, Munson PJ, Morris SM, Gladwin MT (2007) Amplified expression profiling of platelet transcriptome reveals changes in arginine metabolic pathways in patients with sickle cell disease. Circulation 115:1551–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao AK, Freishtat RJ, Jalagadugula G, Singh A, Mao G, Wiles A, Cheung P, Boden G (2014) Alterations in insulin-signaling and coagulation pathways in platelets during hyperglycemia-hyperinsulinemia in healthy non-diabetic subject. Thromb Res 134:704–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raslova H, Roy L, Vourc’h C, Le Couedic JP, Brison O, Metivier D, Feunteun J, Kroemer G, Debili N, Vainchenker W (2003) Megakaryocyte polyploidization is associated with a functional gene amplification. Blood 101:541–544

    Article  CAS  PubMed  Google Scholar 

  • Risitano A, Beaulieu LM, Vitseva O, Freedman JE (2012) Platelets and platelet-like particles mediate intercellular RNA transfer. Blood 119:6288–6295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowley JW, Weyrich AS (2013) Coordinate expression of transcripts and proteins in platelets. Blood 121:5255–5256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowley JW, Oler A, Tolley ND, Hunter B, Low EN, Nix DA, Yost CC, Zimmerman GA, Weyrich AS (2011) Genome wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 118:e101–e111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowley JW, Schwertz H, Weyrich AS (2012) Platelet mRNA: the meaning behind the message. Curr Opin Hematol 19:385–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russo I, Traversa M, Bonomo K, De Salve A, Mattiello L, Del Mese P, Doronzo G, Cavalot F, Trovati M, Anfossi G (2010) In central obesity, weight loss restores platelet sensitivity to nitric oxide and prostacyclin. Obesity (Silver Spring) 18:788–797

    Article  CAS  Google Scholar 

  • Santilli F, Paloscia L, Liani R, Di Nicola M, Di Marco M, Lattanzio S, La Barba S, Pascale S, Mascellanti M, Davì G (2014) Circulating myeloid-related protein-8/14 is related to thromboxane-dependent platelet activation in patients with acute coronary syndrome, with and without ongoing low-dose aspirin treatment. J Am Heart Assoc 3(4):e000903

    Article  PubMed  PubMed Central  Google Scholar 

  • Schubert S, Weyrich AS, Rowley JW (2014) A tour through the transcriptional landscape of platelets. Blood 124:493–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 (2006) Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med 203:2433–2440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw T, Chesterman CN, Morgan FJ (1984) In vitro synthesis of low molecular weight proteins in human platelets: absence of labelled release products. Thromb Res 36:619–631

    Article  CAS  PubMed  Google Scholar 

  • Shendure J (2008) The beginning of the end for microarrays? Nat Methods 5:585–587

    Article  CAS  PubMed  Google Scholar 

  • Shi R, Ge L, Zhou X, Ji W-J, Lu R-Y, Zhang Y-Y, Zeng S, Liu X, Zhao J-H, Zhang W-C, Jiang T-M, Li Y-M (2013) Decreased platelet miR-223 expression is associated with high on-clopidogrel platelet reactivity. Thromb Res 131:508–513

    Article  CAS  PubMed  Google Scholar 

  • Simon LM, Edelstein LC, Nagalla S, Woodley AB, Chen ES, Kong X, Ma L, Fortina P, Kunapuli S, Holinstat M, McKenzie SE, Dong J-F, Shaw CA, Bray PF (2014) Human platelet microRNA-mRNA networks associated with age and gender revealed by integrated plateletomics. Blood 123(16):e37–e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steiner M, Baldini M (1969) Protein synthesis in aging blood platelets. Blood 33:628–633

    CAS  PubMed  Google Scholar 

  • Suls J (2013) Anger and the heart: perspectives on cardiac risk, mechanisms and interventions. Prog Cardiovasc Dis 55:538–547

    Article  PubMed  Google Scholar 

  • Tang K, Liu J, Yang Z, Zhang B, Zhang H, Huang C, Ma J, Shen G-X, Ye D, Huang B (2010) Microparticles mediate enzyme transfer from platelets to mast cells: a new pathway for lipoxin A4 biosynthesis. Biochem Biophys Res Commun 400:432–436

    Article  CAS  PubMed  Google Scholar 

  • Vignini A, Morganti S, Salvolini E, Sartini D, Luzzi S, Fiorini R, Provinciali L, Di Primio R, Mazzanti L, Emanuelli M (2013) Amyloid precursor protein expression is enhanced in human platelets from subjects with Alzheimer’s disease and frontotemporal lobar degeneration: a real-time PCR study. Exp Gerontol 48:1505–1508

    Article  CAS  PubMed  Google Scholar 

  • Voora D, Cyr D, Lucas J, Chi J-T, Dungan J, McCaffrey TA, Katz R, Newby LK, Kraus WE, Becker RC, Ortel TL, Ginsburg GS (2013) Aspirin exposure reveals novel genes associated with platelet function and cardiovascular events. J Am Coll Cardiol 62:1267–1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner GP, Kin K, Lynch VJ (2012) Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 131(4):281–285

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Fang C, Gao H, Bilodeau ML, Zhang Z, Croce K, Liu S, Morooka T, Sakuma M, Nakajima K, Yoneda S, Shi C, Zidar D, Andre P, Stephens G, Silverstein RL, Hogg N, Schmaier AH, Simon DI (2014) Platelet-derived S100 family member myeloid-related protein-14 regulates thrombosis. J Clin Invest 124:2160–2171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warshaw AL, Laster L, Shulman NR (1967) Protein synthesis by human platelets. J Biol Chem 242:2094–2097

    CAS  PubMed  Google Scholar 

  • Weyrich AS, Dixon DA, Pabla R, Elstad MR, McIntyre TM, Prescott SM, Zimmerman GA (1998) Signal-dependent translation of a regulatory protein, Bcl-3, in activated human platelets. Proc Natl Acad Sci U S A 95:5556–5561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weyrich AS, Schwertz H, Kraiss LW, Zimmerman GA (2009) Protein synthesis by platelets: historical and new perspectives. J Thromb Haemost 7:241–246

    Article  CAS  PubMed  Google Scholar 

  • Yadegari H, Driesen J, Pavlova A, Biswas A, Hertfelder H-J, Oldenburg J (2012) Mutation distribution in the von Willebrand factor gene related to the different von Willebrand disease (VWD) types in a cohort of VWD patients. Thromb Haemost 108:662–671

    Article  CAS  PubMed  Google Scholar 

  • Zimmet J, Ravid K (2000) Polyploidy. Exp Hematol 28:3–16

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Jesse W. Rowley or Andrew S. Weyrich .

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Rowley, J.W., Manne, B.K., Weyrich, A.S. (2017). The Platelet Transcriptome: Coding RNAs. In: Gresele, P., Kleiman, N., Lopez, J., Page, C. (eds) Platelets in Thrombotic and Non-Thrombotic Disorders. Springer, Cham. https://doi.org/10.1007/978-3-319-47462-5_17

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