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Review Articles

Platelet protein synthesis, regulation, and post-translational modifications: mechanics and function

Pages 99-117 | Received 14 Mar 2023, Accepted 08 Jun 2023, Published online: 22 Jun 2023

References

  • Agam G, Bessler H, Djaldetti M. 1976b. In vitro DNA and RNA synthesis by human platelets. Biochim Biophys Acta. 425(1):41–48. doi: 10.1016/0005-2787(76)90214-8.
  • Agam G, Gasner S, Bessler H, Fishman P, Djaldetti M. 1976a. Chloramphenicol induced inhibition of platelet protein synthesis: in vitro and in vivo studies. Br J Haematol. 33(1):53–59. doi: 10.1111/j.1365-2141.1976.tb00971.x.
  • Allfrey VG, Faulkner R, Mirsky AE. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA. 51(5):786–794. doi: 10.1073/pnas.51.5.786.
  • Allam O, Samarani S, Jenabian M-A, Routy J-P, Tremblay C, Amre D, Ahmad A. 2017. Differential synthesis and release of IL-18 and IL-18 binding protein from human platelets and their implications for HIV infection. Cytokine. 90:144–154. doi: 10.1016/j.cyto.2016.10.016.
  • Anderson DM, Anderson KM, Chang C-L, Makarewich CA, Nelson BR, McAnally JR, Kasaragod P, Shelton JM, Liou J, Bassel-Duby R, et al. 2015. A micropeptide encoded by a putative long non-coding RNA regulates muscle performance. Cell. 160(4):595–606. doi: 10.1016/j.cell.2015.01.009.
  • Aslan JE. 2021. Platelets proteomes, pathways, and phenotypes as informants of vascular wellness and disease. Arterioscler Thromb Vasc Biol. 41(3):999–1011. doi: 10.1161/ATVBAHA.120.314647.
  • Aslan JE, Phillips KG, Healy LD, Itakura A, Pang J, McCarty OJT. 2013. Histone deacetylase 6-mediated deacetylation of α-tubulin coordinates cytoskeletal and signaling events during platelet activation. Am J Physiol Cell Physiol. 305(12):C1230–C1239. doi: 10.1152/ajpcell.00053.2013.
  • Aslan JE, Rigg RA, Nowak MS, Loren CP, Baker-Gro SM, Pang J, David LL, McCarty OJT. 2015. Lysine acetyltransferase supports platelet function. J Thromb Haemost. 13(10):1908–1917. doi: 10.1111/jth.13070.
  • Asselta R, Rimoldi V, Guella I, Solda G, De Cristofaro R, Peyvandi F, Duga S. 2010. Molecular characterization of in-frame and out-of-frame alternative splicings in coagulation factor XI pre-mRNA. Blood. 115(10):2065–2072. doi: 10.1182/blood-2009-09-245092.
  • Babur Ö, Melrose AR, Cunliffe JM, Klimek J, Pang J, Sepp A-LI, Zilberman-Rudenko J, Tassi Yunga S, Zheng T, Parra-Izquierdo I, et al. 2020. Phosphoproteomic quantitation and causal analysis reveal pathways in GPVI/ITAM-mediated platelet activation programs. Blood. 136(20):2346–2358. doi: 10.1182/blood.2020005496.
  • Barber AJ, Jamieson GA. 1971. Platelet collagen adhesion characterization of collagen glucosyltransferase of plasma membranes of human blood platelets. Biochim Biophys Acta. 252(3):533–545. doi: 10.1016/0304-4165(71)90156-5.
  • Bazzini AA, Johnstone TG, Christiano R, Mackowiak SD, Obermayer B, Fleming ES, Vejnar CE, Lee MT, Rajewsky N, Walther TC, et al. 2014. Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation. Embo J. 33(9):981–993. doi: 10.1002/embj.201488411.
  • Belloc F, Heilmann E, Combrie R, Boisseau MR, Nurden AT. 1987. Protein synthesis and storage in human platelets: a defective storage of fibrinogen in platelets in Glanzmann’s thrombasthenia. Biochim Biophys Acta. 925(2):218–225. doi: 10.1016/0304-4165(87)90112-7.
  • Bian W, Chen W, Jiang X, Qu H, Jiang J, Yang J, Liang X, Zhao B, Sun Y, Zhang C. 2020. Downregulation of long non-coding RNA nuclear paraspeckle assembly transcript 1 inhibits MEG-01 differentiation and platelet-like particles activity. Front Genet. 11:571467–571411. doi: 10.3389/fgene.2020.571467.
  • Bijak M, Dzieciol M, Rywaniak J, Saluk J, Zielinska M. 2016. Platelets miRNA as a prediction marker of thrombotic episodes. Dis Markers. 2016:2872507. doi: 10.1155/2016/2872507.
  • Bosmann HB. 1971. Platelet adhesiveness and aggregation: the collagen:glycosyl, polypeptide: N-acetylgalactosaminyl and glycoprotein:galactosyl transferases of human platelets. Biochem Biophys Res Commun. 43(5):1118–1124. doi: 10.1016/0006-291x(71)90578-x.
  • Brogren H, Karlsson L, Andersson M, Wang L, Erlinge D, Jern S. 2004. Platelets synthesize large amounts of active plasminogen activator inhibitor I. Blood. 104(13):3943–3948. doi: 10.1182/blood-2004-04-1439.
  • Brogren H, Sihlbom C, Wallmark K, Lönn M, Deinum J, Karlsson L, Jern S. 2008. Heterogeneous glycosylation patterns of human PAI-1 may reveal its cellular origin. Thromb Res. 122(2):271–281. doi: 10.1016/j.thromres.2008.04.008.
  • Brown GT, McIntyre TM. 2011. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β rich microparticles. J Immunol. 186(9):5489–5496. doi: 10.4049/jimmunol.1001623.
  • Brown GT, Narayanan P, Li W, Silverstein RL, McIntyre TM. 2013. Lipopolysaccharides stimulate platelets through an IL-1β autocrine loop. J Immunol. 191(10):5196–51203. doi: 10.4049/jimmunol.1300354.
  • Bruce IJ, Kerry R. 1987. The effect of chloramphenicol and cycloheximide on platelet aggregation and protein synthesis. Biochem Pharmacol. 36(11):1769–1773. doi: 10.1016/0006-2952(87)90236-x.
  • Burkhart JM, Gambaryan S, Watson SP, Jurk K, Walter U, Sickmann A, Heemskerk JWM, Zahedi RP. 2014. What can proteomics tell us about platelets? Circ Res. 114(7):1204–1219. doi: 10.1161/CIRCRESAHA.114.301598.
  • Caron JM. 1997. Posttranslational modification of tubulin by palmitoylation: i. In vivo and cell-free studies. Mol Biol Cell. 8(4):621–636. doi: 10.1091/mbc.8.4.621.
  • Chattopadhyay M, Dahiya N, Atreya C. 2018. MicroRNA-223 regulates Septin-2 and Septin-6 in stored platelets. Microrna. 7(3):223–228. doi: 10.2174/2211536607666180626122750.
  • Cimmino G, Tarallo R, Nassa G, De Filippo MR, Giurato G, Ravo M, Rizzo F, Conte S, Pellegrino G, Cirillo P, et al. 2015. Activating stimuli induce platelet microRNA modulation and proteome reorganization. Thromb Haemost. 114(1):96–108. doi: 10.1160/TH14-09-0726.
  • Clancy L, Freedman JE. 2015. The role of circulating platelet transcripts. J Thromb Haemost. 13(Suppl 1):s33–S39. doi: 10.1111/jth.12922.
  • Colberg L, Cammann C, Greinacher A, Seifert U. 2020. Structure and function of the ubiquitin-proteosome system in platelets. J Thromb Haemost. 18(4):771–780. doi: 10.1111/jth.14730.
  • Corduan A, Plé H, Laffont B, Wallon T, Plante I, Landry P, Provost P. 2015. Dissociation of SERPINE1 mRNA from the translational repressor proteins Ago2 and TIA-1 upon platelet activation. Thromb Haemost. 113(5):1046–1059. doi: 10.1160/TH14-07-0622.
  • Dahiya N, Sarachana T, Kulkarni S, Wood WH, IIIZhang Y, Becker KG, Wang B-D, Atreya CD. 2017. miR-570 interacts with mitochondrial ATPase subunit g (ATP5L) encoding mRNA in stored platelets. Platelets. 28(1):74–81. doi: 10.1080/09537104.2016.1203405.
  • Dahiya N, Sarachana T, Vu L, Becker KG, Wood IW, Zhang Y, Atreya CD. 2015. Platelet microRNAs: an overview. Transfus Med Rev. 29(4):215–219. doi: 10.1016/j.tmrv.2015.08.002.
  • Dangwal S, Thum T. 2013. MicroRNAs in platelet physiology and pathology. Hamostaseologie. 33(1):17–20. doi: 10.5482/HAMO-13-01-0002.
  • Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, et al. 2005. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell. 122(3):379–391. doi: 10.1016/j.cell.2005.06.015.
  • Dong X, Ding S, Yu M, Niu L, Xue L, Zhao Y, Xie L, Song X, Song X. 2020. Small nuclear RNAs (U1, U2, U5) in tumor-educated platelets are downregulated and act as promising biomarkers in lung cancer. Front Oncol. 10:1627–1611. doi: 10.3389/fonc.2020.01627.
  • Dowal L, Yang W, Freeman MR, Steen H, Flaumenhaft R. 2011. Proteomic analysis of palmitoylated platelet proteins. Blood. 118(13):e62–e73. doi: 10.1182/blood-2011-05-353078.
  • Drazic A, Myklebust LM, Ree R, Arnesen T. 2016. The world of protein acetylation. Biochim Biophys Acta. 1864(10):1372–1401. doi: 10.1016/j.bbapap.2016.06.007.
  • Edelstein LC, McKenzie SE, Shaw C, Holinstat MA, Kunapuli SP, Bray PF. 2013a. MicroRNAs in platelet production and activation. J Thromb Haemost. 11(Supp1):340–350. doi: 10.1111/jth.12214.
  • Edelstein LC, Simon LM, Montoya RT, Holinstat M, Chen ES, Bergeron A, Kong X, Nagalla S, Mohandas N, Cohen DE, et al. 2013b. Racial difference in human platelet PAR4 reactivity reflects expression of PCTP and miR-367c. Nat Med. 19(12):1609–1616. doi: 10.1038/nm.3385.
  • Elgheznawy A, Shi L, Hu J, Wittig I, Laban H, Pircher J, Mann A, Provost P, Randriamboavonjy V, Fleming I. 2015. Dicer cleavage by calpain determines platelet microRNA levels and function in diabetes. Circ Res. 117(2):157–165. doi: 10.1161/CIRCRESAHA.117.305784.
  • El-Kadiry AE-H, Merhi Y. 2021. The role of the proteosome in platelet function. IJMS. 22(8):3999–3917. doi: 10.3390/ijms22083999.
  • Evangelista V, Manarini S, Di Santo A, Capone ML, Ricciotti E, Di Francesco L, Tacconelli S, Sacchetti A, D’Angelo S, Scilimati A, et al. 2006. De novo synthesis of cyclooxygenase-1 counteracts the suppression of platelet thromboxane biosynthesis by aspirin. Circ Res. 98(5):593–595. doi: 10.1161/01.RES.0000214553.37930.3e.
  • Fields AT, Lee M-C, Mayer F, Santos YA, Bainton CMV, Matthay ZA, Callcut RA, Mayer N, Cuschieri J, Kober KM, et al. 2022. A new trauma frontier: exploratory pilot study of platelet transcriptomics in trauma patients. J Trauma Acute Care Surg. 92(2):313–322. doi: 10.1097/TA.0000000000003450.
  • Flaumenhaft R, Sim DS. 2005. Protein palmitoylation in signal transduction of hematopoietic cells. Hematology. 10(6):511–519. doi: 10.1080/10245330500141507.
  • Gallinari P, Di Marco S, Jones P, Pallaoro M, Steinkuhler C. 2007. HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res. 17(3):195–211. doi: 10.1038/sj.cr.7310149.
  • Garcia A, Dunoyer-Geindre S, Fontana P. 2021. Do miRNAs have a role in platelet function regulation? Hamostaseologie. 41(3):217–224. doi: 10.1055/a-1478-2105.
  • Gardiner EE, Andrews RK. 2019. Platelet ubiquitylation-it’s everywhere. Thromb Haemost. 119(1):6–8. doi: 10.1055/s-0038-1676650.
  • 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(6):2285–2293. doi: 10.1182/blood-2002-09-2797.
  • Groterhorst KG, Mannell H, Pircher J, Kraemer BF. 2019. Platelet proteosome activity and metabolism is upregulated during bacterial sepsis. IJMS. 20(23):5961–5969. doi: 10.3390/ijms2023561.
  • Gutmann C, Joshi A, Mayr M. 2020. Platelet ‘-omics’ in health and cardiovascular disease. Atherosclerosis. 307:87–96. doi: 10.1016/j.atherosclerosis.2020.05.022.
  • Guo B, Wu S, Zhu X, Zhang L, Deng J, Li F, Wang Y, Zhang S, Wu R, Lu J, et al. 2020. Micropeptide CIP2A-BP encoded by LINC00665 inhibits triple-negative breast cancer progression. Embo J. 39:e102190. 1–16.
  • Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS. 2002. Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-dependent calcium entry channel. Blood. 100(8):2801–2811. doi: 10.1182/blood-2002-03-0723.
  • Hayashi M, Suzuki H, Kawashima A, Saido TC, Inomata M. 1999. The behavior of calpain-generated N and C-terminal fragments of talin in integrin-mediated signalling pathways. Arch Biochem Biophys. 371(2):133–141. doi: 10.1006/abbi.1999.1427.
  • Higgins EA, Siminovitch KA, Zhuang D, Brockhausen I, Dennis JW. 1991. Aberrant O-linked oligosaccharide biosynthesis in lymphocytes and platelets from patients with the Wiskott-Aldrich syndrome. J Biol Chem. 266(10):6280–6290.
  • Huang EM. 1994. Palmitoylation of platelets proteins. Platelets. 5(2):61–69. doi: 10.3109/09537109409005515.
  • Huang J, Swieringa F, Solari FA, Provenzale I, Grassi L, De Simone I, Baaten C, Cavill R, Sickmann A, Frontini M, et al. 2021. Assessment of a complete and classified platelet proteome from genome-wide transcripts of human platelets and megakaryocytes covering platelet functions. Sci Rep. 11(1):12358–12318. doi: 10.1038/s41598-021-91661-x.
  • Huang J, Zhang P, Solari FA, Sickmann A, Garcia A, Jurk K, Heemskerk JWM. 2021. Molecular proteomics and signalling of human platelets in health and disease. IJMS. 22(18):9860–9821. doi: 10.3390/ijms22189860.
  • Inzulza-Tapia A, Alarcon M. 2022. Role of non-coding RNA of human platelet in cardiovascular disease. Curr Med Chem. 29(19):3420–3444. doi: 10.2174/0929867329666211230104955.
  • Israels SJ, McMillan-Ward E. 2010. Palmitoylation supports the association of tetraspanin CD63 and CD9 and integrin alphaIIbbeta3 in activated platelets. Thromb Res. 125(2):152–158. doi: 10.1016/j.thromres.2009.07.005.
  • Jones J, Krag SS, Betenbaugh MJ. 2005. Controlling N-linked glycan site occupancy. Biochim Biophys Acta. 1726(2):121–137. doi: 10.1016/j.bbagen.2005.07.003.
  • Joshi A, Schmidt LE, Burnap SA, Lu R, Chan MV, Armstrong PC, Baig F, Gutmann C, Willeit P, Santer P, et al. 2022. Neutrophil-derived protein S100A8/A9 alters the platelet proteome in acute myocardial infarction and is associated with changes in platelet reactivity. Arterioscler Thromb Vasc Biol. 42(1):49–62. doi: 10.1161/ATVBAHA.121.317113.
  • Khan AO, Slater A, Maclachlan A, Nicolson PLR, Pike JA, Reyat JS, Yule J, Stapley R, Rayes J, Thomas SG, et al. 2022. Post-translational polymodification of β1-tubulin regulates motor protein localization in platelet production and function. Haematologica. 107(1):243–259. doi: 10.3324/haematol.2020.270793.
  • Kannan M, Mohan KVK, Kulkarni S, Atreya C. 2009. Membrane array-based differential profiling of platelets during storage for 52 miRNAs associated with apoptosis. Transfusion. 49(7):1443–1450. doi: 10.1111/j.1537-2995.2009.02140.x.
  • Kaudewitz D, Skroblin P, Bender LH, Barwari T, Willeit P, Pechlaner R, Sunderland NP, Willeit K, Morton AC, Armstrong PC, et al. 2016. Association of microRNAs and YRNAs with platelet function. Circ Res. 118(3):420–432. doi: 10.1161/CIRCRESAHA.114.305663.
  • Kieffer N, Guichard J, Farcet J-P, Vainchenker W, Breton-Gorius J. 1987. Biosynthesis of major platelet proteins in human blood platelets. Eur J Biochem. 164(1):189–195. doi: 10.1111/j.1432-1033.1987.tb11010.x.
  • Kondkar AA, Bray BS, Leal SM, Nagalla S, Liu DJ, Jin Y, Dong JF, Ren Q, Whiteheart SW, Shaw C, et al. 2010. VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost. 8(2):369–378. doi: 10.1111/j.1538-7836.2009.03700.x.
  • Kornblith LZ, Bainton CMV, Fields AT, Matthay ZA, Magid NT, Nunez-Garcia B, Prakash A, Kurien PA, Callcut RA, Cohen MJ, et al. 2020. A journey upstream: fluctuating platelet-specific genes in cell-free plasma as proof-of -concept for using ribonucleic acid sequencing to improve understanding of postinjury platelet biology. J Trauma Acute Care Surg. 88(6):742–751. doi: 10.1097/TA.0000000000002681.
  • Kouzarides T. 2000. Acetylation: a regulatory modification to rival phosphorylation? Embo J. 19(6):1176–1179. doi: 10.1093/emboj/19.6.1176.
  • Kovacs EG, Katona E, Bereczky Z, Homorodi N, Balogh L, Toth E, Peterfy H, Kiss RG, Edes I, Muszbek L. 2013. New direct and indirect methods for the detection of cyclooxygenase 1 acetylation by aspirin; the lack of aspirin resistance among healthy individuals. Thromb Res. 131(4):320–324. doi: 10.1016/j.thromres.2013.01.033.
  • Kraemer BF, Geimer M, Franz-Wachtel M, Lamkemeyer T, Mannell H, Lindemann S. 2020. Extracellular matrix-specific platelet activation leads to differential translational response and protein de novo synthesis in human platelets. IJMS. 21(21):8155–8115. doi: 10.3390/ijms21218155.
  • Kraemer BF, Weyrich AS, Lindemann S. 2013. Protein degradation systems in platelets. Thromb Haemost. 110(5):920–924. doi: 10.1160/TH13-03-0183.
  • Kumari S, Chaurasia SN, Nayak MK, Mallick RL, Dash D. 2015. Sirtuin inhibition induces apoptosis-like changes in platelets and thrombocytopenia. J Biol Chem. 290(19):12290–12299. doi: 10.1074/jbc.M114.615948.
  • Lan O, Du C, Xiong J, Wu Y, Liao W, Liu C, Chen J, Ran L, Wang Y, Wang J, et al. 2022. Renal Klotho safeguards platelet lifespan in advanced chronic kidney disease through restraining Bcl-xL ubiquitination and degradation. J Thromb Haemost. 20(12):2972–2987. doi: 10.1111/jth.15876.
  • Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. 2009. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol. 16(9):961–966. doi: 10.1038/nsmb.1651.
  • Latorre A, Moscardo A. 2016. Regulation of platelet function by acetylation/deacetylation mechanisms. Curr Med Chem. 23(35):3966–3974. doi: 10.2174/0929867323666160907112038.
  • Lee MM, Nasirikenari M, Manhardt CT, Ashline DJ, Hanneman AJ, Reinhold VN, Lau JTY. 2014. Platelets support extracellular sialylation by supporting the sugar donor substrate. J Biol Chem. 289(13):8742–8748. doi: 10.1074/jbc.C113.546713.
  • Lee-Sundlov MM, Ashline DJ, Hanneman AJ, Grozovsky R, Reinhold VN, Hoffmeister KM, Lau JTY. 2017. Circulating blood and platelets supply glycosyltransferases that enable extrinsic extracellular glycosylation. Glycobiology. 27(2):188–198. doi: 10.1093/glycob/cww108.
  • Lemaitre D, Vericel E, Polette A, Lagarde M. 1997. Effects of fatty acids on human platelet glutathione peroxidase: possible role of oxidative stress. Biochem Pharmacol. 53(4):479–486. doi: 10.1016/s0006-2952(96)00734-4.
  • Li Y, Fu J, Ling Y, Yago T, McDaniel JM, Song J, Bai X, Kondo Y, Qin Y, Hoover C, et al. 2017. Sialylation on O-glycans protects platelets from clearance by liver Kupffer cells. Proc Natl Acad Sci USA. 114(31):8360–8365. doi: 10.1073/pnas.1707662114.
  • Lian L, Suzuki A, Hayes V, Saha S, Han X, Xu T, Yates IJ, Poncz M, Kashina A, Abrams CS. 2014. Loss of ATE1-mediated arginylation leads to impaired platelet myosin phosphorylation, clot retraction, and in vivo thrombosis formation. Haematologica. 99(3):554–560. doi: 10.3324/haematol.2013.093047.
  • Lindemann S, Gawaz M. 2007. The active platelet: translation and protein synthesis in an anucleate cell. Semin Thromb Hemost. 33(2):144–150. doi: 10.1055/s-2007-969027.
  • Lindemann S, Tolley ND, Dixon DA, McIntyre TM, Prescott SM, Zimmerman GA, Weyrich AS. 2001. Activated platelets mediate inflammatory signaling by regulated interleukin 1β synthesis. J Cell Biol. 154(3):485–490. doi: 10.1083/jcb.200105058.
  • Lindsay CR, Edelstein LC. 2016. MicroRNAs in platelet physiology and function. Semin Thromb Hemost. 42(3):215–222. doi: 10.1055/s-0035-1570077.
  • Livne A, Packham MA, Guccione MA, Mustard JF. 1988. Aggregation-related association of lipid with the cytoskeleton of rabbit and human platelets prelabeled with [3H] palmitic acid. J Clin Invest. 81(2):288–299. doi: 10.1172/JCI113320.
  • Maass PG, Glazar P, Memczak S, Dittmar G, Hollfinger I, Schreyer L, Sauer AV, Toka O, Aiuti A, Luft FC, et al. 2017. A map of human circular RNAs in clinically relevant tissues. J Mol Med. 95(11):1179–1189. doi: 10.1007/s00109-017-1582-9.
  • Macaulay IC, Carr P, Gusnanto A, Ouwehand WH, Fitzgerald D, Watkins NA. 2005. Platelet genomics and proteomic in human health and disease. J Clin Invest. 115(12):3370–3377. doi: 10.1172/JCI26885.
  • Magiera MM, Singh P, Janke C. 2018. SnapShot: functions of tubulin posttranslational modifications. Cell. 173(6):1552–1552.e1. doi: 10.1016/j.cell.2018.05.032.
  • Maguire PB, Moran N, Cagney G, Fitzgerald DJ. 2004. Application of proteomics to the study of platelet regulatory mechanisms. Trends Cardiovasc Med. 14(6):207–220. doi: 10.1016/j.tcm.2004.06.001.
  • Mammadova-Bach E, Jaeken J, Gudermann T, Braun A. 2020. Platelets and defective N-glycosylation. IJMS. 21(16):5630–5616. doi: 10.3390/ijms21165630.
  • Manne BK, Bhatlekar S, Middleton EA, Weyrich AS, Borst O, Rondina MT. 2020. Phospho-inositide-dependent kinase 1 regulates signal dependent translation in megakaryocytes and platelets. J Thromb Haemost. 18(5):1183–1196. doi: 10.1111/jth.14748.
  • Marsden AJ, Riley DR, Barry A, Khalil JS, Guinn B, Kemp NT, Rivero F, Beltran-Alvarez P. 2021. Inhibition of arginine methylation impairs platelet function. ACS Pharmacol Transl Sci. 4(5):1567–1577. doi: 10.1021/acsptsci.1c00135.
  • Miao X, Rahman MF-U, Jiang L, Min Y, Tan S, Xie H, Lee L, Wang M, Malmstrom RE, Lui W-O, et al. 2018. Thrombin-reduced miR-27b attenuates platelet angiogenic activities in vitro via enhancing platelet synthesis of anti-angiogenic thrombospondin-1. J Thromb Haemost. 16(4):791–801. doi: 10.1111/jth.13978.
  • Middleton EA, Rowley JW, Campbell RA, Grissom CK, Brown SM, Beesley SJ, Schwertz H, Kosaka Y, Manne BK, Krauel K, et al. 2019. Sepsis alters the transcriptional and translational landscape of human and murine platelets. Blood. 134(12):911–923. doi: 10.1182/blood.2019000067.
  • Moscardo A, Valles J, Latorre A, Jover R, Santos MT. 2015. The histone deacetylase sirtuin 2 is a new player in the regulation of platelet function. J Thromb Haemost. 13(7):1335–1344. doi: 10.1111/jth.13004.
  • Mossberg K, Olausson J, Fryk E, Jern S, Jansson A, Brogren H. 2022. The role of the platelet pool of Plasminogen Activator Inhibitor-1 in well-controlled type 2 diabetes patients. PLOS One. 17(8):e0267833. doi: 10.1371/journal.pone.0267833.
  • Mussbacher M, Pirabe A, Brunnthaler L, Schrottmaier WC, Assinger A. 2021. Horizontal microRNA transfer by platelets-evidence and implications. Front Physiol. 12:678362–678311. doi: 10.3389/fphys,2021.678362.
  • Muszbek L, Laposata M. 1989. Covalent modification of platelet proteins by palmitate. Blood. 74(4):1339–1347.
  • Muszbek L, Laposata M. 1993. Myristoylation of proteins in platelets occurs predominantly through thioester linkages. J Biol Chem. 268(11):8251–8255.
  • Nagalla S, Shaw C, Kong X, Kondkar AA, Edelstein LC, Ma L, Chen J, McKnight GS, Lopez JA, Yang L, et al. 2011. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood. 117(19):5189–5197. doi: 10.1182/blood-2010-09-299719.
  • Nassa G, Giurato G, Cimmino G, Rizzo F, Ravo M, Salvati A, Nyman TA, Zhu Y, Vesterlund M, Lehtio J, et al. 2018. Splicing of platelet resident pre-mRNA upon activation by physiological stimuli results in functionally relevant proteome modifications. Sci Rep. 8(1):498–412. doi: 10.1038/s41598-017-18985-5.
  • Neu CT, Gutschner T, Haemmerle M. 2020. Post-transcriptional expression control in platelet biogenesis and function. IJMS. 21(20):7614–7625. doi: 10.3390/ijms21207614.
  • Obeso D, Mera-Berriatua L, Rodriguez-Coira J, Rosace D, Fernandez P, Martin-Antoniano I, Santaolalla M, Martin GM, Chivato T, Fernandez-Rivas M, et al. 2018. Multi-omics analysis points to altered platelet functions in severe food-associated respiratory allergy. Allergy. 73(11):2137–2149. doi: 10.1111/all.13563.
  • Octave M, Pirotton L, Ginion A, Robaux V, Lepropre S, Ambroise J, Bouzin C, Guigas B, Giera M, Foretz M, et al. 2021. Acetyl-CoA carboxylase inhibitor CP640.186 increases tubulin acetylation and impairs thrombin-induced platelet aggregation. IJMS. 22(23):13129. doi: 10.3390/ijms222313129.
  • O’Kane P, Xie L, Liu Z, Queen L, Jackson G, Ji Y, Ferro A. 2009. Aspirin acetylates nitric oxide synthase type 3 in platelets thereby increasing its activity. Cardiovasc Res. 83(1):123–130. doi: 10.1093/cvr/cvp120.
  • Pabla R, Weyrich AS, Dixon DA, Bray PF, McIntyre TM, Prescott SM, Zimmerman GA. 1999. Integrin-dependent control of translation: engagement of integrin αIIbβ3 regulates synthesis of proteins in activated platelets. J Cell Biol. 144(1):175–184. doi: 10.1083/jcb.144.1.175.
  • Panes O, Matus V, Saez CG, Quiroga T, Pereira J, Mezzano D. 2007. Human platelets synthesize and express functional tissue factor. Blood. 109(12):5242–5250. doi: 10.1182/blood-2006-06-030619.
  • Patel-Hett S, Richardson JL, Schulze H, Drabek K, Isaac NA, Hoffmeister K, Shivdasani RA, Bulinski JC, Galjart N, Hartwig JH, et al. 2008. Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood. 111(9):4605–4616. doi: 10.1182/blood-2007-10-118844.
  • Prendes MJ, Bielek E, Zechmeister-Machhart M, Vanyek-Zavadil E, Carroll VA, Breuss J, Binder BR, Geiger M. 1999. Synthesis and ultrastructural localization of protein C inhibitor in human platelets and megakaryocytes. Blood. 94(4):1300–1312.
  • Preußer C, Hung L-H, Schneider T, Schreiner S, Hardt M, Moebus A, Santoso S, Bindereif A. 2018. Selective release of circRNAs in platelet-derived extracellular vesicles. J Extracell Vesicles. 7(1):1424473–1424412. doi: 10.1080/20013078.2018.1424473.
  • Ribba A-S, Batzenschlager M, Rabat c, Buchou T, Moog S, Khochbin S, Bourova-Flin E, Lafanechere L, Lanza F, Sadoul K. 2021. Marginal band microtubules are acetylated by αTAT1. Platelets. 32(4):568–572. doi: 10.1080/09537104.2020.1759791.
  • Rocheleau AD, Melrose AR, Cunliffe JM, Klimek J, Babur O, Yunga ST, Ngo ATP, Pang J, David LL, McCarty OJT, et al. 2019. Identification, quantification and systems analysis of protein N-ε lysine methylation in anucleate blood platelets. Proteomics. 19(11):e1900001. doi: 10.1002/pmic.201900001.
  • Rodriguez P, Bello O, Tablante A, Apitz-Castro R. 1988. Galactosylation of endogenous proteins from human platelets. Biochem Med Metab Biol. 40(2):151–161. doi: 10.1016/0885-4505(88)90116-8.
  • Rodriguez P, Durante P. 1990. Characterization of a protein:glucosyltransferase activity in human platelets. Biochem Med Metab Biol. 43(2):147–158. doi: 10.1016/0885-4505(90)90020-2.
  • Rondina MT, Schwertz H, Harris ES, Kraemer BF, Campbell RA, Mackman N, Grissom CK, Weyrich AS, Zimmerman GA. 2011. The septic milieu triggers expression of spliced tissue factor mRNA in human platelets. J Thromb Haemost. 9(4):748–758. doi: 10.1111/j.1538-7836.2011.04208.x.
  • Rondina MT, Voora D, Simon LM, Schwertz H, Harper JF, Lee O, Bhatlekar SC, Li Q, Eustes AS, Montenont E, et al. 2020. Longitudinal RNA-seq analysis of the repeatability of gene expression and splicing in human platelets identifies a platelet SELP splice QTL. Circ Res. 126(4):501–516. doi: 10.1161/CIRCRESAHA.119.315215.
  • Roth GJ, Majerus PW. 1975. The mechanism of the effect of aspirin on human platelets 1. Acetylation of a particulate fraction protein. J Clin Invest. 56(3):624–632. doi: 10.1172/JCI108132.
  • Rowley JW, Chappaz S, Corduan A, Chong MMW, Campbell R, Khoury A, Manne BK, Wurtzel JG, Michael JV, Goldfinger LE, et al. 2016. Dicer 1-mediated miRNA processing shapes the mRNA profile and function of murine platelets. Blood. 127(14):1743–1751. doi: 10.1182/blood-2015-07-661371.
  • Sadoul K, Wang J, Diagouraga B, Vitte A-L, Buchou T, Rossini T, Polack B, Xi X, Matthias P, Khochbin S. 2012. HDAC6 controls the kinetics of platelet activation. Blood. 120(20):4215–4218. doi: 10.1182/blood-2012-05-428011.
  • Saini V, Dawar R, Suneja S, Gangopadhyay S, Kaur C. 2021. Can microRNA become next-generation tools in molecular diagnostics and therapeutics? A systematic review. Egypt J Med Hum Genet. 22(1):1–9. doi: 10.1186/s43042-020-00125-w.
  • Salaun C, Greaves J, Chamberlain LH. 2010. The intracellular dynamic of protein palmitoylation. J Cell Biol. 191(7):1229–1238. doi: 10.1083/jcb.201008160.
  • Savini I, Catani MV, Arnone R, Rossi A, Frega G, Del Principe D, Avigliano L. 2007. Translational control of the ascorbic acid transporter SVCT2 in human platelets. Free Radic Biol Med. 42(5):608–616. doi: 10.1016/j.freeradbiomed.2006.11.028.
  • Schwertz H, Tolley ND, Foulks JM, Denis MM, Risenmay BW, Buerke M, Tilley RE, Rondina MT, Harris EM, Kraiss LW, et al. 2006. Signal-dependent splicing of tissue factor per-mRNA modulates the thrombogenecity of human platelets. J Exp Med. 203(11):2433–2440. doi: 10.1084/jem.20061302.
  • Shashkin PN, Brown GT, Ghosh A, Marathe GK, McIntyre TM. 2008. Lipopolysaccharide is a direct agonist for platelet RNA splicing. J Immunol. 181(5):3495–3502. doi: 10.4049/jimmunol.181.5.3495.
  • Shevchuk O, Begonja AJ, Gambaryan S, Totzeck M, Rassaf T, Huber TB, Greinacher A, Renne T, Sickmann A. 2021. Proteomics: a tool to study platelet function. IJMS. 22(9):4776–4725. doi: 10.3390/ijms22094776.
  • Sim DS, Dilks JR, Flaumenhaft R. 2007. Platelets possess and require an active protein palmitoylation pathway for agonist-mediated activation and in vivo thrombus formation. Arterioscler Thromb Vasc Biol. 27(6):1478–1485. doi: 10.1161/ATVBAHA.106.139287.
  • Singh J, Kaul D. 1997. RNA-mediated regulation of receptor-Ck gene in human platelets. Mol Cell Biochem. 173(1/2):189–192. doi: 10.1023/A:1006872904778.
  • Soslau G. 1982. Cytochrome levels and activity in stored human platelets. Arch Biochem Biophys. 215(2):532–538. doi: 10.1016/0003-9861(82)90112-6.
  • Soslau G. 1983. De novo synthesis of DNA in human platelets. Arch Biochem Biophys. 226(1):252–256. doi: 10.1016/0003-9861(83)90291-6.
  • Soslau G. 2018. Circular RNA (circRNA) was an important bridge in the switch from the RNA world to the DNA world. J Theor Biol. 447:32–40. doi: 10.1016/j.jtbi.2018.03.021.
  • Soslau G. 2020. The role of the red blood cell and platelet in the evolution of mammalian and avian endothermy. J Exp Zool B Mol Dev Evol. 334(2):113–127. doi: 10.1002/jez.b.22922.
  • Soslau G, Giles J. 1982. The loss of sialic acid and its prevention in stored human platelets. Thromb Res. 26(6):443–455. doi: 10.1016/0049-3848(82)90316-4.
  • Soslau G, Mason C, Lynch S, Benjamin J, Ashak D, Prakash JM, Moore A, Bagsiyao P, Albert T, Mathew LM, et al. 2014. Intracellular matrix metalloproteinase-2 (MMP-2) regulates human platelet activation via hydrolysis of talin. Thromb Haemost. 111(1):140–153. doi: 10.1160/TH13-03-0248.
  • Soslau G, Parker J. 1989. Modulation of platelet function by extracellular ATP. Blood. 74(3):984–993.
  • Soslau G, Rybicki A. 1982. In vitro incorporation of fucose and methionine into human platelet proteins. Biochem Biophys Res Commun. 109(4):1256–1263. doi: 10.1016/0006-291x(82)91912-x.
  • Stakos DA, Gatsiou A, Stamatelopoulos K, Tselepis AD, Stellos K. 2013. Platelet microRNAs: from platelet biology to possible disease biomarkers and therapeutic targets. Platelets. 24(8):579–589. doi: 10.3109/09537104.2012.724483.
  • Sun Y, Liu R, Xia X, Xing L, Jiang J, Bian W, Zhang W, Wang C, Zhang C. 2022. Large-scale profiling on lncRNAs in human platelets: correlation with platelet reactivity. Cells. 11(14):2256–2215. doi: 10.3390/cells11142256.
  • Thon JN, Devine DV. 2007. Translation of glycoprotein IIIa in stored blood platelets. Transfusion. 47(12):2260–2270. doi: 10.1111/j.1537-2995.2007.01455.x.
  • Unsworth AJ, Bombik I, Pinto-Fernandez A, McGouran JF, Konietzny R, Zahedi RP, Watson SP, Kessler BM, Pears CJ. 2019. Human platelet protein ubiquitylaltion and changes following GPVI activation. Thromb Haemost. 119(1):104–116. doi: 10.1055/s-0038-1676344.
  • Vidal M, Murgue B, Basse F, Bienvenue A. 1991. Fatty acylation of human platelet proteins: evidence for myristoylation of a 50 kDa peptide. Biochem Int. 6:1175–1184.
  • Vieira PCM, da Silva Maues JH, Lamarao LM, Moreira-Nunes CA, Burbano RMR. 2022. MiroRNA 320a and membrane antigens as tools to evaluate the pathophysiology of platelets stored in blood banks. Curr Issues Mol Biol. 44(5):1838–1850. doi: 10.3390/cimb44050126.
  • Wandall HH, Rumjantseva V, Sørensen ALT, Patel-Hett S, Josefsson EC, Bennett EP, Italiano JE, Clausen H, Hartwig JH, Hoffmeister KM. 2012. The origin and function of platelet glycosyltransferases. Blood. 120(3):626–635. doi: 10.1182/blood-2012-02-409235.
  • Weber A-A, Przytulski B, Schumacher M, Zimmermann N, Gams E, Hohlfeld T, Schror K. 2002. Flow cytometry analysis of platelet cyclooxygenase-2: induction of platelet cyclooxygenase-2 in patients undergoing coronary artery bypass grafting. Br J Haematol. 117(2):424–426. doi: 10.1046/j.1365-2141.2002.03423.x.
  • 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 platelets. Proc Natl Acad Sci USA. 95(10):5556–5561. doi: 10.1073/pnas.95.10.5556.
  • Weyrich AS, Lindemann S, Tolley ND, Kraiss LW, Dixon DA, Mahoney TM, Prescott SP, McIntyre TM, Zimmerman GA. 2004. Change in protein phenotype without a nucleus: translational control in platelets. Semin Thromb Hemost. 30(4):491–498. doi: 10.1055/s-2004-833484.
  • Weyrich AS, Schwertz H, Kraiss LW, Zimmerman GA. 2009. Protein synthesis by platelets: historical and new perspectives. J Thromb Haemost. 7(2):241–246. doi: 10.1111/j.1538-7836.2008.03211.x.
  • Wicik Z, Czajka P, Eyileten C, Fitas A, Wolska M, Jakubik D, von Lewinski D, Sourij H, Siller-Matula J, Postula M. 2022. The role of miRNAs in regulation of platelet activity and related diseases- a bioinformatic analysis. Platelets. 33(7):1052–1064. doi: 10.1080/09537104.2022.2042233.
  • Woodhoo A, Iruarrizaga-Lejarreta M, Beraza N, Garcia-Rodriguez JL, Embade N, Fernandez-Ramos D, Matinez-Lopez N, Gutierrez V, Arteta B, Caballeria J, et al. 2012. HuR contributes to hepatic stellate cell activation and liver fibrosis. Hepatology. 56(5):1870–1882. doi: 10.1002/hep.25828.
  • Xavier-Ferrucio J, Krause DS. 2018. Bipotent megakaryocytic-erythroid progenitors: concepts and controversies. Stem Cells. 36(8):1138–1145. doi: 10.1002/stem.2834.
  • Xia L, Zeng Z, Tang WH. 2018. The role of platelet microparticle associated microRNAs in cellular crosstalk. Front Cardiovasc Med. 5:1–5. doi: 10.3389/fcvm.2018.00029.
  • Xu M, Du R, Xing W, Chen X, Wan J, Wang S, Xiong L, Nandakumar KS, Holmdahl R, Geng H. 2023. Platelets derived citrullinated proteins and microparticles are potential autoantibodies ACPA targets in RA patients. Front Immunol. 14:1084283. doi: 10.3389/fimmu.2023.1084283.
  • Yan Y, Xie R, Zhang Q, Zhu X, Han J, Xia R. 2019. Bcl-xL/Bak interaction and regulation by miRNA let-7b in the intrinsic apoptotic pathway of stored platelets. Platelets. 30(1):75–80. doi: 10.1080/09537104.2017.1371289.
  • Yu S, Huang H, Deng G, Xie Z, Ye Y, Guo R, Cai X, Hong J, Qian D, Zhou X, et al. 2015. miR-326 targets antiapoptotic Bcl-xL and mediates apoptosis in human platelets. PLoS One. 10(4):eO122784. doi: 10.1371/journal.pone.0122784.
  • Yunga ST, Gower AJ, Melrose AR, Fitzgerald MK, Rajendran A, Lusardi TA, Armstrong RJ, Minnier J, Jordan KR, McCarty OJT, et al. 2022. Effects of ex vivo anticoagulation and preanalytical processing time on the proteome content of platelets. J Thromb Haemost. 20(6):1437–1450. doi: 10.1111/jth.15694.
  • Zahedi RP, Begonja AJ, Gambaryan S, Sickmann A. 2006. Phosphoproteomics of human platelets: a quest for novel activation pathways. Biochim Biophys Acta. 1764(12):1963–1976. doi: 10.1016/j.bbapap.2006.08.017.
  • Zhou M, Gao M, Luo Y, Gui R, Ji H. 2019. Long non-coding RNA metallothionein 1 pseudogene 3 promotes P2Y12 expression by sponging miR-126 to activate platelet in diabetic animal model. Platelets. 30(4):452–459. doi: 10.1080/09537104.2018.1457781.
  • Zimmerman GA, Weyrich AS. 2008. Signal-dependent protein synthesis by activated platelets new pathways to altered phenotype and function. Arterioscler Thromb Vasc Biol. 28:s17–s24.
  • Zucker M, Hauschner H, Seligsohn U, Rosenberg N. 2018. Platelet factor XI: intracellular localization and mRNA splicing following platelet activation. Blood Cells Mol Dis. 69:30–37. doi: 10.1016/j.bcmd.2017.04.006.
  • Zucker M, Rosenberg N, Peretz HJ, Green D, Bauduer F, Zivelin A, Seligsohn U. 2011. Point mutations regarded as missense mutations cause splicing defects in the factor XI gene. J Thromb Haemost. 9(10):1977–1984. doi: 10.1111/j.1538-7836.2011.04426.x.

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