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Articles

Does hsa-miR-223-3p from platelet-derived extracellular vesicles regulate tissue factor expression in monocytic cells?

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Pages 1031-1042 | Received 22 Apr 2021, Accepted 30 Dec 2021, Published online: 08 Feb 2022

References

  • Cannell IG, Kong YW, Bushell M. How do microRNAs regulate gene expression? Biochem Soc Trans. 2008;36(6):1224–1231. doi:10.1042/BST0361224.
  • Diehl P, Fricke A, Sander L, Stamm J, Bassler N, Htun N, Ziemann M, Helbing T, El-Osta A, Jowett JB, et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res. 2012;93(4):633–644. doi:10.1093/cvr/cvs007.
  • Shan Z, Qin S, Li W, Wu W, Yang J, Chu M, Li X, Huo Y, Schaer GL, Wang S, et al. An endocrine genetic signal between blood cells and vascular smooth muscle cells: role of MicroRNA-223 in smooth muscle function and atherogenesis. J Am Coll Cardiol. 2015;65(23):2526–2537. doi:10.1016/j.jacc.2015.03.570.
  • Plé H, Landry P, Benham A, Coarfa C, Gunaratne PH, Provost P. The repertoire and features of human platelet microRNAs. PLoS One. 2012;7(12):e50746. doi:10.1371/journal.pone.0050746.
  • Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol. 2009;16(9):961–966. doi:10.1038/nsmb.1651.
  • Willeit P, Zampetaki A, Dudek K, Kaudewitz D, King A, Kirkby NS, Crosby-Nwaobi R, Prokopi M, Drozdov I, Langley SR, et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res. 2013;112(4):595–600. doi:10.1161/CIRCRESAHA.111.300539.
  • Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999;94(11):3791–3799. doi:10.1182/blood.V94.11.3791.
  • Ambrose AR, Alsahli MA, Kurmani SA, Goodall AH. Comparison of the release of microRNAs and extracellular vesicles from platelets in response to different agonists. Platelets. 2018;29(5):446–454. doi:10.1080/09537104.2017.1332366.
  • Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One. 2012;7(3):e30679. doi:10.1371/journal.pone.0030679.
  • Crescitelli R, Lässer C, Szabó TG, Kittel A, Eldh M, Dianzani I, Buzás EI, Lötvall J. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles. 2013;2(1):20677. doi:10.3402/jev.v2i0.20677.
  • Laffont B, Corduan A, Plé H, Duchez AC, Cloutier N, Boilard E, Provost P. Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles. Blood. 2013;122(2):253–261. doi:10.1182/blood-2013-03-492801.
  • Laffont B, Corduan A, Rousseau M, Duchez AC, Lee CH, Boilard E, Provost P. Platelet microparticles reprogram macrophage gene expression and function. Thromb Haemost. 2016;115(2):311–323. doi:10.1160/th15-05-0389.
  • Bao H, Chen YX, Huang K, Zhuang F, Bao M, Han Y, Chen XH, Shi Q, Yao QP, Qi YX. Platelet-derived microparticles promote endothelial cell proliferation in hypertension via miR-142–3p. FASEB J. 2018;32(7):3912–3923. doi:10.1096/fj.201701073R.
  • Zhang Y, Zhang W, Zha C, Liu Y. Platelets activated by the anti-β2GPI/β2GPI complex release microRNAs to inhibit migration and tube formation of human umbilical vein endothelial cells. Cell Mol Biol Lett. 2018;23(1):24. doi:10.1186/s11658-018-0091-3.
  • Anene C, Graham AM, Boyne J, Roberts W. Platelet microparticle delivered microRNA-Let-7a promotes the angiogenic switch. Biochim Biophys Acta Mol Basis Dis. 2018;1864(8):2633–2643. doi:10.1016/j.bbadis.2018.04.013.
  • Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S, Brisson AR. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014;12(5):614–627. doi:10.1111/jth.12554.
  • Hartopo AB, Puspitawati I, Gharini PP, Setianto BY. Platelet microparticle number is associated with the extent of myocardial damage in acute myocardial infarction. Arch Med Sci. 2016;12:529–537. doi:10.5114/aoms.2016.59926.
  • Lukasik M, Rozalski M, Luzak B, Michalak M, Ambrosius W, Watala C, Kozubski W. Enhanced platelet-derived microparticle formation is associated with carotid atherosclerosis in convalescent stroke patients. Platelets. 2013;24(1):63–70. doi:10.3109/09537104.2011.654292.
  • Stępień E, Stankiewicz E, Zalewski J, Godlewski J, Zmudka K, Wybrańska I. Number of microparticles generated during acute myocardial infarction and stable angina correlates with platelet activation. Arch Med Res. 2012;43(1):31–35. doi:10.1016/j.arcmed.2012.01.006.
  • Chiva-Blanch G, Laake K, Myhre P, Bratseth V, Arnesen H, Solheim S, Badimon L, Seljeflot I. Platelet-, monocyte-derived and tissue factor-carrying circulating microparticles are related to acute myocardial infarction severity. PLoS One. 2017;12(2):e0172558. doi:10.1371/journal.pone.0172558.
  • Jung C, Sörensson P, Saleh N, Arheden H, Rydén L, Pernow J. Circulating endothelial and platelet derived microparticles reflect the size of myocardium at risk in patients with ST-elevation myocardial infarction. Atherosclerosis. 2012;221(1):226–231. doi:10.1016/j.atherosclerosis.2011.12.025.
  • Tan KT, Tayebjee MH, Lim HS, Lip GY. Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels. Diabet Med. 2005;22(12):1657–1662. doi:10.1111/j.1464-5491.2005.01707.x.
  • Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard JM, Mayr A, Weger S, Schett G, Shah A, et al. Prospective study on circulating MicroRNAs and risk of myocardial infarction. J Am Coll Cardiol. 2012;60(4):290–299. doi:10.1016/j.jacc.2012.03.056.
  • Li S, Chen H, Ren J, Geng Q, Song J, Lee C, Cao C, Zhang J, Xu N. MicroRNA-223 inhibits tissue factor expression in vascular endothelial cells. Atherosclerosis. 2014;237(2):514–520. doi:10.1016/j.atherosclerosis.2014.09.033.
  • Brand K, Fowler BJ, Edgington TS, Mackman N. Tissue factor mRNA in THP-1 monocytic cells is regulated at both transcriptional and posttranscriptional levels in response to lipopolysaccharide. Mol Cell Biol. 1991;11(9):4732–4738. doi:10.1128/mcb.11.9.4732-4738.1991.
  • Zhang X, Yu H, Lou JR, Zheng J, Zhu H, Popescu NI, Lupu F, Lind SE, Ding WQ. MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem. 2011;286(2):1429–1435. doi:10.1074/jbc.M110.146530.
  • Chuang TD, Luo X, Panda H, Chegini N. miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Mol Endocrinol. 2012;26(6):1028–1042. doi:10.1210/me.2012-1075.
  • Witkowski M, Weithauser A, Tabaraie T, Steffens D, Kränkel N, Witkowski M, Stratmann B, Tschoepe D, Landmesser U, Rauch-Kroehnert U. Micro-RNA-126 reduces the blood thrombogenicity in diabetes mellitus via targeting of tissue factor. Arterioscler Thromb Vasc Biol. 2016;36(6):1263–1271. doi:10.1161/ATVBAHA.f115.306094.
  • Sahu A, Jha PK, Prabhakar A, Singh HD, Gupta N, Chatterjee T, Tyagi T, Sharma S, Kumari B, Singh S, et al. MicroRNA-145 impedes thrombus formation via targeting tissue factor in venous thrombosis. EBioMedicine. 2017;26:175–186. doi:10.1016/j.ebiom.2017.11.022.
  • Gregory SA, Morrissey JH, Edgington TS. Regulation of tissue factor gene expression in the monocyte procoagulant response to endotoxin. Mol Cell Biol. 1989;9(6):2752–2755. doi:10.1128/mcb.9.6.2752-2755.1989.
  • Oeth P, Parry GC, Mackman N. Regulation of the tissue factor gene in human monocytic cells. Role of AP-1, NF-kappa B/Rel, and Sp1 proteins in uninduced and lipopolysaccharide-induced expression. Arterioscler Thromb Vasc Biol. 1997;17(2):365–374. doi:10.1161/01.ATV.17.2.365.
  • Celi A, Pellegrini G, Lorenzet R, De Blasi A, Ready N, Furie BC, Furie B. P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci U S A. 1994;91(19):8767–8771. doi:10.1073/pnas.91.19.8767.
  • Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH. The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One. 2010;5(1):e8668. doi:10.1371/journal.pone.0008668.
  • Chung J, Koyama T, Ohsawa M, Shibamiya A, Hoshi A, Hirosawa S. 1,25(OH)(2)D(3) blocks TNF-induced monocytic tissue factor expression by inhibition of transcription factors AP-1 and NF-kappaB. Lab Invest. 2007;87(6):540–547. doi:10.1038/labinvest.3700550.
  • Koyama T, Shibakura M, Ohsawa M, Kamiyama R, Hirosawa S. Anticoagulant effects of 1alpha,25-dihydroxyvitamin D3 on human myelogenous leukemia cells and monocytes. Blood. 1998;92(1):160–167. doi:10.1182/blood.V92.1.160.413k16_160_167.
  • Gardiner C, Ferreira YJ, Dragovic RA, Redman CW, Sargent IL. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013;2(1):10. doi:10.3402/jev.v2i0.19671.
  • Collier MEW, Akinmolayan A, Goodall AH. Comparison of tissue factor expression and activity in foetal and adult endothelial cells. Blood Coagul Fibrinolysis. 2017;28(6):452–459. doi:10.1097/MBC.0000000000000621.
  • Conkling PR, Greenberg CS, Weinberg JB. Tumor necrosis factor induces tissue factor-like activity in human leukemia cell line U937 and peripheral blood monocytes. Blood. 1988;72(1):128–133. doi:10.1182/blood.V72.1.128.bloodjournal721128.
  • Herbert JM, Savi P, Laplace MC, Lale A. IL-4 inhibits LPS-, IL-1 beta- and TNF alpha-induced expression of tissue factor in endothelial cells and monocytes. FEBS Lett. 1992;310(1):31–33. doi:10.1016/0014-5793(92)81139-D.
  • Pinder PB, Hunt JA, Zacharski LR. In vitro stimulation of monocyte tissue factor activity by autologous platelets. Am J Hematol. 1985;19(4):317–325. doi:10.1002/ajh.2830190402.
  • Witkowski M, Tabaraie T, Steffens D, Friebel J, Dörner A, Skurk C, Witkowski M, Stratmann B, Tschoepe D, Landmesser U, et al. MicroRNA-19a contributes to the epigenetic regulation of tissue factor in diabetes. Cardiovasc Diabetol. 2018;17(1):34. doi:10.1186/s12933-018-0678-z.
  • Teruel R, Pérez-Sánchez C, Corral J, Herranz MT, Pérez-Andreu V, Saiz E, García-Barberá N, Martínez-Martínez I, Roldán V, Vicente V, et al. Identification of miRNAs as potential modulators of tissue factor expression in patients with systemic lupus erythematosus and antiphospholipid syndrome. J Thromb Haemost. 2011;9(10):1985–1992. doi:10.1111/j.1538-7836.2011.04451.x.
  • Mandal SK, Pendurthi UR, Rao LV. Cellular localization and trafficking of tissue factor. Blood. 2006;107(12):4746–4753. doi:10.1182/blood-2005-11-4674.
  • Mandal SK, Pendurthi UR, Rao LV. Tissue factor trafficking in fibroblasts: involvement of protease-activated receptor-mediated cell signaling. Blood. 2007;110(1):161–170. doi:10.1182/blood-2006-10-050476.
  • Egorina EM, Sovershaev MA, Bjørkøy G, Gruber FX, Olsen JO, Parhami-Seren B, Mann KG, Østerud B. Intracellular and surface distribution of monocyte tissue factor: application to intersubject variability. Arterioscler Thromb Vasc Biol. 2005;25(7):1493–1498. doi:10.1161/01.ATV.0000168413.29874.d7.
  • Gantier MP, McCoy CE, Rusinova I, Saulep D, Wang D, Xu D, Irving AT, Behlke MA, Hertzog PJ, Mackay F, et al. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res. 2011;39(13):5692–5703. doi:10.1093/nar/gkr148.
  • Guo Y, Liu J, Elfenbein SJ, Ma Y, Zhong M, Qiu C, Ding Y, Lu J. Characterization of the mammalian miRNA turnover landscape. Nucleic Acids Res. 2015;43(4):2326–2341. doi:10.1093/nar/gkv057.
  • Pan Y, Liang H, Liu H, Li D, Chen X, Li L, Zhang CY, Zen K. Platelet-secreted microRNA-223 promotes endothelial cell apoptosis induced by advanced glycation end products via targeting the insulin-like growth factor 1 receptor. J Immunol. 2014;192(1):437–446. doi:10.4049/jimmunol.1301790.
  • Li J, Tan M, Xiang Q, Zhou Z, Yan H. Thrombin-activated platelet-derived exosomes regulate endothelial cell expression of ICAM-1 via microRNA-223 during the thrombosis-inflammation response. Thromb Res. 2017;154:96–105. doi:10.1016/j.thromres.2017.04.016.
  • Zeng Z, Xia L, Fan X, Ostriker AC, Yarovinsky T, Su M, Zhang Y, Peng X, Xie Y, Pi L, et al. Platelet-derived miR-223 promotes a phenotypic switch in arterial injury repair. J Clin Invest. 2019;129(3):1372–1386. doi:10.1172/JCI124508.
  • Tan M, Yan HB, Li JN, Li WK, Fu YY, Chen W, Zhou Z. Thrombin stimulated platelet-derived exosomes inhibit platelet-derived growth factor receptor-beta expression in vascular smooth muscle cells. Cell Physiol Biochem. 2016;38(6):2348–2365. doi:10.1159/000445588.
  • Li S, Ren J, Xu N, Zhang J, Geng Q, Cao C, Lee C, Song J, Li J, Chen H. MicroRNA-19b functions as potential anti-thrombotic protector in patients with unstable angina by targeting tissue factor. J Mol Cell Cardiol. 2014;75:49–57. doi:10.1016/j.yjmcc.2014.06.017.
  • Lu J, Clark AG. Impact of microRNA regulation on variation in human gene expression. Genome Res. 2012;22(7):1243–1254. doi:10.1101/gr.132514.111.
  • Hayon Y, Dashevsky O, Shai E, Varon D, Leker RR. Platelet microparticles promote neural stem cell proliferation, survival and differentiation. J Mol Neurosci. 2012;47(3):659–665. doi:10.1007/s12031-012-9711-y.
  • Kim HK, Song KS, Chung JH, Lee KR, Lee SN. Platelet microparticles induce angiogenesis in vitro. Br J Haematol. 2004;124(3):376–384. doi:10.1046/j.1365-2141.2003.04773.x.
  • Risitano A, Beaulieu LM, Vitseva O, Freedman JE. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood. 2012;119(26):6288–6295. doi:10.1182/blood-2011-12-396440.
  • Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008;3(11):e3694. doi:10.1371/journal.pone.0003694.
  • Allantaz F, Cheng DT, Bergauer T, Ravindran P, Rossier MF, Ebeling M, Badi L, Reis B, Bitter H, D’Asaro M, et al. Expression profiling of human immune cell subsets identifies miRNA-mRNA regulatory relationships correlated with cell type specific expression. PLoS One. 2012;7(1):e29979. doi:10.1371/journal.pone.0029979.