Circulating Exosomes and Their Role in Stroke

Author(s): Reza Jafarzadeh-Esfehani, Mohammad Soudyab, Seyed Mostafa Parizadeh, Mohammad Ehsan Jaripoor, Payam Sasan Nejad, Mohammad Shariati, Ariane Sadr Nabavi*.

Journal Name: Current Drug Targets

Volume 21 , Issue 1 , 2020

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Abstract:

Stroke is an acute neurologic disorder which can be life-threatening if left untreated or diagnosed late. Various detecting techniques including neurologic imaging of the brain by computed tomography or magnetic resonance imaging can facilitate diagnosis of stroke. However, according to the recent advances in molecular detection techniques, new diagnostic and prognostic markers have emerged. Exosomes as an extra cellar particle are one of these markers which can have useful diagnostic, prognostic, and even therapeutic impact after stroke. We have previously discussed the role of exosomes in cardiovascular disease and in the present review we focus on the most common cerebrovascular disease. The aim of the present review is summarizing the recent diagnostic role of exosomes which are specifically secreted during a stroke and can guide clinicians to better diagnosis of stroke.

Keywords: microRNA, exosome, stroke, diagnosis, cerebrovascular disease, thrombosis.

[1]
Wang Z, He D, Zeng YY, et al. The spleen may be an important target of stem cell therapy for stroke. J Neuroinflammation 2019; 16(1): 20.
[http://dx.doi.org/10.1186/s12974-019-1400-0] [PMID: 30700305]
[2]
Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. Lancet Neurol 2009; 8(4): 355-69.
[http://dx.doi.org/10.1016/S1474-4422(09)70025-0] [PMID: 19233729]
[3]
Feigin VL, Forouzanfar MH, Krishnamurthi R, et al. global burden of diseases, injuries, and risk factors study 2010 (gbd 2010) and the gbd stroke experts group. global and regional burden of stroke during 1990-2010: findings from the global burden of disease study 2010. Lancet 2014; 383(9913): 245-54.
[http://dx.doi.org/10.1016/S0140-6736(13)61953-4] [PMID: 24449944]
[4]
Béjot Y, Daubail B, Giroud M. Epidemiology of stroke and transient ischemic attacks: Current knowledge and perspectives. Rev Neurol (Paris) 2016; 172(1): 59-68.
[http://dx.doi.org/10.1016/j.neurol.2015.07.013] [PMID: 26718592]
[5]
Burn J, Dennis M, Bamford J, Sandercock P, Wade D, Warlow C. Long-term risk of recurrent stroke after a first-ever stroke. The Oxfordshire Community Stroke Project. Stroke 1994; 25(2): 333-7.
[http://dx.doi.org/10.1161/01.STR.25.2.333] [PMID: 8303740]
[6]
Hardie K, Jamrozik K, Hankey GJ, Broadhurst RJ, Anderson C. Trends in five-year survival and risk of recurrent stroke after first-ever stroke in the Perth Community Stroke Study. Cerebrovasc Dis 2005; 19(3): 179-85.
[http://dx.doi.org/10.1159/000083253] [PMID: 15644631]
[7]
Hartmann A, Rundek T, Mast H, et al. Mortality and causes of death after first ischemic stroke: The northern manhattan stroke study. Neurology 2001; 57(11): 2000-5.
[http://dx.doi.org/10.1212/WNL.57.11.2000] [PMID: 11739816]
[8]
Mohan KM, Crichton SL, Grieve AP, Rudd AG, Wolfe CD, Heuschmann PU. Frequency and predictors for the risk of stroke recurrence up to 10 years after stroke: the South London Stroke Register. J Neurol Neurosurg Psychiatry 2009; 80(9): 1012-8.
[http://dx.doi.org/10.1136/jnnp.2008.170456] [PMID: 19465412]
[9]
Petty GW, Brown RD Jr, Whisnant JP, Sicks JD, O’Fallon WM, Wiebers DO. Survival and recurrence after first cerebral infarction: a population-based study in Rochester, Minnesota, 1975 through 1989. Neurology 1998; 50(1): 208-16.
[http://dx.doi.org/10.1212/WNL.50.1.208] [PMID: 9443482]
[10]
Slam AU. Clinical pattern of stroke and distributions according to age, gender and potential risk factors. J Rawalpindi Medical College 2018; 22(S-1): 27-30.
[11]
Traylor M, Zhang CR, Adib-Samii P, et al. Genome-wide meta-analysis of cerebral white matter hyperintensities in patients with stroke 2016; 86(2): 146-53.
[http://dx.doi.org/10.1212/WNL.0000000000002263]
[12]
Darabi H, Salmaninejad A, Jaripour ME, Azarpazhooh MR, Mojarrad M, Sadr-Nabavi A. Association of the genetic polymorphisms in immunoinflammatory microRNAs with risk of ischemic stroke and subtypes in an Iranian population. J Cell Physiol 2019; 234(4): 3874-86.
[http://dx.doi.org/10.1002/jcp.27159]
[13]
Ghasemi MR. Is apolipoprotein genotype a reason for the excessive incidence of stroke in persian population? %. J Biomedicine and Health 2016; 1(1): 1-6.
[http://dx.doi.org/10.17795/jbm-5417]
[14]
Pirhoushiaran M, Ghasemi MR, Hami J, et al. The association of coagulation factor v (leiden) and factor ii (prothrombin) mutations with stroke. Iran Red Crescent Med J 2014; 16(11)e11548
[http://dx.doi.org/10.5812/ircmj.11548] [PMID: 25763204]
[15]
Parizadeh SM, Jafarzadeh-Esfehani R, Ghandehari M, et al. Circulating exosomes as potential biomarkers in cardiovascular disease. Curr Pharm Des 2018; 24(37): 4436-44.
[http://dx.doi.org/10.2174/1381612825666181219162655] [PMID: 30569849]
[16]
Hesari A, Golrokh Moghadam SA, Siasi A, et al. Tumor-derived exosomes: potential biomarker or therapeutic target in breast cancer? J Cell Biochem 2018; 119(6): 4236-40.
[PMID: 28833502]
[17]
Hosseini M, Khatamianfar S, Hassanian SM, et al. Exosome-encapsulated microRNAs as potential circulating biomarkers in colon cancer. Curr Pharm Des 2017; 23(11): 1705-9.
[http://dx.doi.org/10.2174/1381612822666161201144634] [PMID: 27908272]
[18]
Simons M, Raposo G. Exosomes--vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009; 21(4): 575-81.
[http://dx.doi.org/10.1016/j.ceb.2009.03.007] [PMID: 19442504]
[19]
Higashijima Y, Sonoda H, Takahashi S, Kondo H, Shigemura K, Ikeda M. Excretion of urinary exosomal AQP2 in rats is regulated by vasopressin and urinary pH. Am J Physiol Renal Physiol 2013; 305(10): F1412-21.
[http://dx.doi.org/10.1152/ajprenal.00249.2013] [PMID: 23986519]
[20]
Hugel B, Martínez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology (Bethesda) 2005; 20(1): 22-7.
[http://dx.doi.org/10.1152/physiol.00029.2004] [PMID: 15653836]
[21]
Horstman LL, Jy W, Minagar A, et al. Cell-derived microparticles and exosomes in neuroinflammatory disorders. Int Rev Neurobiol 2007; 79: 227-68.
[http://dx.doi.org/10.1016/S0074-7742(07)79010-4] [PMID: 17531844]
[22]
Borroto-Escuela DO, Agnati LF, Bechter K, Jansson A, Tarakanov AO, Fuxe K. The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural-glial networks. Philos Trans R Soc Lond B Biol Sci 2015; 370(1672)20140183
[http://dx.doi.org/10.1098/rstb.2014.0183] [PMID: 26009762]
[23]
EL Andaloussi S. Mäger I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013; 12(5): 347-57.
[http://dx.doi.org/10.1038/nrd3978] [PMID: 23584393]
[24]
Evans-Osses I, Reichembach LH, Ramirez MI. Exosomes or microvesicles? Two kinds of extracellular vesicles with different routes to modify protozoan-host cell interaction. Parasitol Res 2015; 114(10): 3567-75.
[http://dx.doi.org/10.1007/s00436-015-4659-9] [PMID: 26272631]
[25]
Boulanger CM, Loyer X, Rautou PE, Amabile N. Extracellular vesicles in coronary artery disease. Nat Rev Cardiol 2017; 14(5): 259-72.
[http://dx.doi.org/10.1038/nrcardio.2017.7] [PMID: 28150804]
[26]
Ailawadi S, Wang X, Gu H, Fan GC. Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochim Biophys Acta 2015; 1852(1): 1-11.
[http://dx.doi.org/10.1016/j.bbadis.2014.10.008] [PMID: 25463630]
[27]
Malik ZA, Kott KS, Poe AJ, et al. Cardiac myocyte exosomes: stability, HSP60, and proteomics. Am J Physiol Heart Circ Physiol 2013; 304(7): H954-65.
[http://dx.doi.org/10.1152/ajpheart.00835.2012] [PMID: 23376832]
[28]
Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010; 73(10): 1907-20.
[http://dx.doi.org/10.1016/j.jprot.2010.06.006] [PMID: 20601276]
[29]
Mollaei H, Safaralizadeh R, Pouladi N. A brief review of exosomes and their roles in cancer. Meta Gene 2017; 11: 70-4.
[http://dx.doi.org/10.1016/j.mgene.2016.11.010]
[30]
Parizadeh SM, Ferns GA, Ghandehari M, et al. The diagnostic and prognostic value of circulating microRNAs in coronary artery disease: A novel approach to disease diagnosis of stable CAD and acute coronary syndrome. J Cell Physiol 2018; 233(9): 6418-24.
[http://dx.doi.org/10.1002/jcp.26324] [PMID: 29215707]
[31]
Kim D-K, Kang B, Kim OY, et al. EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2013; 2(1): 20384.
[http://dx.doi.org/10.3402/jev.v2i0.20384] [PMID: 24009897]
[32]
Mathivanan S, Simpson RJ. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 2009; 9(21): 4997-5000.
[http://dx.doi.org/10.1002/pmic.200900351] [PMID: 19810033]
[33]
de Jong OG, Verhaar MC, Chen Y, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles 2012; 1: 1.
[http://dx.doi.org/10.3402/jev.v1i0.18396] [PMID: 24009886]
[34]
Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol 2014; 28: 3-13.
[http://dx.doi.org/10.1016/j.semcancer.2014.04.009]
[35]
Ibrahim A, Marbán E. Exosomes: fundamental biology and roles in cardiovascular physiology. Annu Rev Physiol 2016; 78: 67-83.
[http://dx.doi.org/10.1146/annurev-physiol-021115-104929] [PMID: 26667071]
[36]
Zhang ZG, Buller B, Chopp M. Exosomes - beyond stem cells for restorative therapy in stroke and neurological injury. Nat Rev Neurol 2019; 15(4): 193-203.
[http://dx.doi.org/10.1038/s41582-018-0126-4] [PMID: 30700824]
[37]
Street JM, Barran PE, Mackay CL, et al. Identification and proteomic profiling of exosomes in human cerebrospinal fluid. J Transl Med 2012; 10: 5.
[http://dx.doi.org/10.1186/1479-5876-10-5] [PMID: 22221959]
[38]
Taylor DD, Gerçel-Taylor C. Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects. Br J Cancer 2005; 92(2): 305-11.
[http://dx.doi.org/10.1038/sj.bjc.6602316] [PMID: 15655551]
[39]
Palma J, Yaddanapudi SC, Pigati L, et al. MicroRNAs are exported from malignant cells in customized particles. Nucleic Acids Res 2012; 40(18): 9125-38.
[http://dx.doi.org/10.1093/nar/gks656] [PMID: 22772984]
[40]
Tauro BJ, Greening DW, Mathias RA, Mathivanan S, Ji H, Simpson RJ. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics 2013; 12(3): 587-98.
[http://dx.doi.org/10.1074/mcp.M112.021303] [PMID: 23230278]
[41]
Nedaeinia R, Manian M, Jazayeri MH, et al. Circulating exosomes and exosomal microRNAs as biomarkers in gastrointestinal cancer. Cancer Gene Ther 2017; 24(2): 48-56.
[http://dx.doi.org/10.1038/cgt.2016.77] [PMID: 27982021]
[42]
Yuyama K, Igarashi Y. Physiological and pathological roles of exosomes in the nervous system. Biomol Concepts 2016; 7(1): 53-68.
[http://dx.doi.org/10.1515/bmc-2015-0033] [PMID: 26812803]
[43]
Keller S, Sanderson MP, Stoeck A, Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett 2006; 107(2): 102-8.
[http://dx.doi.org/10.1016/j.imlet.2006.09.005] [PMID: 17067686]
[44]
Möbius W, Ohno-Iwashita Y, van Donselaar EG, et al. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J Histochem Cytochem 2002; 50(1): 43-55.
[http://dx.doi.org/10.1177/002215540205000105] [PMID: 11748293]
[45]
Stuffers S, Sem Wegner C, Stenmark H, Brech A. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 2009; 10(7): 925-37.
[http://dx.doi.org/10.1111/j.1600-0854.2009.00920.x] [PMID: 19490536]
[46]
Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014; 29: 116-25.
[http://dx.doi.org/10.1016/j.ceb.2014.05.004] [PMID: 24959705]
[47]
Giricz Z, Varga ZV, Baranyai T, et al. Cardioprotection by remote ischemic preconditioning of the rat heart is mediated by extracellular vesicles. J Mol Cell Cardiol 2014; 68: 75-8.
[http://dx.doi.org/10.1016/j.yjmcc.2014.01.004] [PMID: 24440457]
[48]
Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 2018; 75(2): 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[49]
McLellan A. Exosome release by primary B cells. Crit Rev Immunol 2009; 29(3): 203-17.
[http://dx.doi.org/10.1615/CritRevImmunol.v29.i3.20]
[50]
Nazari-Shafti M-T. A Monocyte Inspired Guiding System: Targeting of Exosomes to Ischemia Activated Microvascular Endothelium. The Thoracic and Cardiovascular Surgeon In: 2019. 67: p. (S 01)DGTHG-KV152.
[51]
McKelvey KJ, Powell KL, Ashton AW, Morris JM, McCracken SA. Exosomes: Mechanisms of Uptake. J Circ Biomark 2015; 4: 7.
[http://dx.doi.org/10.5772/61186] [PMID: 28936243]
[52]
Zhu R, Liu X, He Z. Association of miR-122, miR-124 miR-126 and miR-143 gene polymorphisms with ischemic stroke in the northern Chinese Han population. Int J Neurosci 2019; 129(9): 916-22.
[http://dx.doi.org/10.1080/00207454.2019.1593979] [PMID: 30895838]
[53]
Gao J, Yang S, Wang K, Zhong Q, Ma A, Pan X. Plasma miR-126 and miR-143 as Potential Novel Biomarkers for Cerebral Atherosclerosis. J Stroke Cerebrovasc Dis 2019; 28(1): 38-43.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2018.09.008] [PMID: 30309729]
[54]
Long G, Wang F, Li H, et al. Circulating miR-30a, miR-126 and let-7b as biomarker for ischemic stroke in humans. BMC Neurol 2013; 13: 178.
[http://dx.doi.org/10.1186/1471-2377-13-178] [PMID: 24237608]
[55]
Chen F, Du Y, Esposito E, et al. Effects of Focal Cerebral Ischemia on Exosomal Versus Serum mir126. Transl Stroke Res 2015; 6(6): 478-84.
[http://dx.doi.org/10.1007/s12975-015-0429-3] [PMID: 26449616]
[56]
Weng H, Shen C, Hirokawa G, et al. Plasma miR-124 as a biomarker for cerebral infarction. Biomed Res 2011; 32(2): 135-41.
[http://dx.doi.org/10.2220/biomedres.32.135] [PMID: 21551949]
[57]
Wang Z, Lu G, Sze J, et al. Plasma miR-124 Is a Promising Candidate Biomarker for Human Intracerebral Hemorrhage Stroke. Mol Neurobiol 2018; 55(7): 5879-88.
[http://dx.doi.org/10.1007/s12035-017-0808-8] [PMID: 29101647]
[58]
Ji Q, Ji Y, Peng J, et al. Increased brain-specific mir-9 and mir-124 in the serum exosomes of acute ischemic stroke patients. PLoS One 2016; 11(9)e0163645
[http://dx.doi.org/10.1371/journal.pone.0163645] [PMID: 27661079]
[59]
Zhang X, Sun P, Yin K-J. MicroRNA biomarkers for stroke Translational research in stroke. Singapore: Springer Singapore 2017; pp. 319-56.
[http://dx.doi.org/10.1007/978-981-10-5804-2_15]
[60]
Chen Y, Song Y, Huang J, et al. Increased Circulating Exosomal miRNA-223 Is Associated with Acute Ischemic Stroke. Front Neurol 2017; 8: 57.
[http://dx.doi.org/10.3389/fneur.2017.00057] [PMID: 28289400]
[61]
Zhou J, Chen L, Chen B, et al. Increased serum exosomal miR-134 expression in the acute ischemic stroke patients. BMC Neurol 2018; 18(1): 198.
[http://dx.doi.org/10.1186/s12883-018-1196-z] [PMID: 30514242]
[62]
Wang W, Li DB, Li RY, et al. Diagnosis of hyperacute and acute ischaemic stroke: the potential utility of exosomal microrna-21-5p and microrna-30a-5p. Cerebrovasc Dis 2018; 45(5-6): 204-12.
[http://dx.doi.org/10.1159/000488365] [PMID: 29627835]
[63]
Ahmadi-Ahangar A. Predictive ability of C-reactive protein for stroke. Caspian J Intern Med 2016; 7(3): 151-2.
[PMID: 27757197]
[64]
Couch Y, Akbar N, Davis S, et al. Inflammatory stroke extracellular vesicles induce macrophage activation. Stroke 2017; 48(8): 2292-6.
[http://dx.doi.org/10.1161/STROKEAHA.117.017236] [PMID: 28536169]
[65]
Parizadeh SM, Jafarzadeh-Esfehani R, Ghandehari M, et al. Circulating exosomes as potential biomarkers in cardiovascular disease. Curr Pharm Des 2018; 24(37): 4436-44.
[http://dx.doi.org/10.2174/1381612825666181219162655] [PMID: 30569849]
[66]
Zagrean AM, Hermann DM, Opris I, Zagrean L, Popa-Wagner A. Multicellular crosstalk between exosomes and the neurovascular unit after cerebral ischemia. Therapeutic implications. Front Neurosci 2018; 12: 811.
[http://dx.doi.org/10.3389/fnins.2018.00811] [PMID: 30459547]
[67]
Bang OY, Chung JW, Lee MJ, et al. Cancer cell-derived extracellular vesicles are associated with coagulopathy causing ischemic stroke via tissue factor-independent way: The OASIS-CANCER study. PLoS One 2016; 11(7)e0159170
[http://dx.doi.org/10.1371/journal.pone.0159170] [PMID: 27427978]
[68]
Ji Q, Ji Y, Peng J, et al. Increased brain-specific MiR-9 and MiR-124 in the serum exosomes of acute ischemic stroke patients. PLoS One 2016; 11(9)e0163645
[http://dx.doi.org/10.1371/journal.pone.0163645] [PMID: 27661079]
[69]
Zhou J, Chen L, Chen B, et al. Increased serum exosomal miR-134 expression in the acute ischemic stroke patients. BMC Neurol 2018; 18(1): 198.
[http://dx.doi.org/10.1186/s12883-018-1196-z] [PMID: 30514242]
[70]
Li DB, Liu JL, Wang W, et al. Plasma exosomal miRNA-122-5p and miR-300-3p as potential markers for transient ischaemic attack in rats. Front Aging Neurosci 2018; 10(FEB): 24.
[http://dx.doi.org/10.3389/fnagi.2018.00024] [PMID: 29467645]
[71]
Wang W, Li DB, Li RY, et al. Diagnosis of hyperacute and acute ischaemic stroke: The potential utility of exosomal microRNA-21-5p and MicroRNA-30a-5p. Cerebrovasc Dis 2018; 45(5-6): 204-12.
[http://dx.doi.org/10.1159/000488365] [PMID: 29627835]


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VOLUME: 21
ISSUE: 1
Year: 2020
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DOI: 10.2174/1389450120666190821153557
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