RNA-seq identifies circulating MIR-125a-5p, MIR-125b-5p, and MIR-143-3p as potential biomarkers for acute ischemic stroke

Circulation Research

Volumn 121, Issue 8, 2017, Pages 970-980

  Tiedt, Steffen ^a,b   Prestel, Matthias ^a   Malik, Rainer ^a   Schieferdecker, Nicola ^a   Duering, Marco ^a   Kautzky, Veronika ^a   Stoycheva, Ivelina ^a   Böck, Julia ^a   Northoff, Bernd H ^a   Klein, Matthias ^a   Dorn, Franziska ^a   Krohn, Knut ^c   Teupser, Daniel ^a   Liesz, Arthur ^a,b   Plesnila, Nikolaus ^a,b   Holdt, Lesca Miriam ^a   Dichgans, Martin ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b Technische Universität München Munich Cluster for Systems Neurology   (Germany)

^c UNIVERSITY HOSPITAL LEIPZIG   (Germany)

Author keywords

Biomarkers; MicroRNAs; Stroke

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 6; MICRORNA; MICRORNA 125A 5P; MICRORNA 125B 5P; MICRORNA 143 3P; NEURON SPECIFIC ENOLASE; UNCLASSIFIED DRUG; ENOLASE; GENETIC MARKER; IL6 PROTEIN, HUMAN; MIRN125 MICRORNA, HUMAN; MIRN143 MICRORNA, HUMAN;

ADULT; AREA UNDER THE CURVE; ARTICLE; BLOOD ANALYSIS; BRAIN HYPOXIA; BRAIN ISCHEMIA; CLINICAL ARTICLE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DISEASE CLASSIFICATION; EARLY DIAGNOSIS; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; LONGITUDINAL STUDY; MALE; NEURO-2A CELL LINE; NEUROIMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA REPLICATION; RNA SEQUENCE; SENSITIVITY AND SPECIFICITY; THROMBOCYTE COUNT; TRANSIENT ISCHEMIC ATTACK; UPREGULATION; VALIDATION PROCESS; AGED; BLOOD; CASE CONTROL STUDY; CEREBROVASCULAR ACCIDENT; DIAGNOSTIC IMAGING; GENETIC MARKER; GENETICS; MIDDLE AGED; PREDICTIVE VALUE; PROGNOSIS; RECEIVER OPERATING CHARACTERISTIC; REPRODUCIBILITY; SEQUENCE ANALYSIS; TIME FACTOR; VALIDATION STUDY; VERY ELDERLY; X-RAY COMPUTED TOMOGRAPHY;

AGED; AGED, 80 AND OVER; AREA UNDER CURVE; BRAIN ISCHEMIA; CASE-CONTROL STUDIES; EARLY DIAGNOSIS; FEMALE; GENETIC MARKERS; HUMANS; INTERLEUKIN-6; MALE; MICRORNAS; MIDDLE AGED; PHOSPHOPYRUVATE HYDRATASE; PREDICTIVE VALUE OF TESTS; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; ROC CURVE; SEQUENCE ANALYSIS, RNA; STROKE; TIME FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 85025463892     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.311572     Document Type: Article

References (52)

1. GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1459–1544.
2. Hopyan J, Ciarallo A, Dowlatshahi D, Howard P, John V, Yeung R, Zhang L, Kim J, MacFarlane G, Lee TY, Aviv RI. Certainty of stroke diagnosis: incremental benefit with CT perfusion over noncontrast CT and CT angiography. Radiology. 2010;255:142–153. doi: 10.1148/radiol.09091021.
3. Wardlaw JM, Mielke O. Early signs of brain infarction at CT: observer reliability and outcome after thrombolytic treatment–systematic review. Radiology. 2005;235:444–453. doi: 10.1148/radiol.2352040262.
4. Whiteley W, Tseng MC, Sandercock P. Blood biomarkers in the diagnosis of ischemic stroke: a systematic review. Stroke. 2008;39:2902–2909. doi: 10.1161/STROKEAHA.107.511261.
5. Anand N, Stead LG. Neuron-specific enolase as a marker for acute ischemic stroke: a systematic review. Cerebrovasc Dis. 2005;20:213–219. doi: 10.1159/000087701.
6. Wunderlich MT, Wallesch CW, Goertler M. Release of glial fibrillary acidic protein is related to the neurovascular status in acute ischemic stroke. Eur J Neurol. 2006;13:1118–1123. doi: 10.1111/j.1468-1331.2006.01435.x.
7. Foerch C, Singer OC, Neumann-Haefelin T, du Mesnil de Rochemont R, Steinmetz H, Sitzer M. Evaluation of serum S100B as a surrogate marker for long-term outcome and infarct volume in acute middle cerebral artery infarction. Arch Neurol. 2005;62:1130–1134. doi: 10.1001/archneur.62.7.1130.
8. Smith CJ, Emsley HC, Gavin CM, Georgiou RF, Vail A, Barberan EM, del Zoppo GJ, Hallenbeck JM, Rothwell NJ, Hopkins SJ, Tyrrell PJ. Peak plasma interleukin-6 and other peripheral markers of inflammation in the first week of ischaemic stroke correlate with brain infarct volume, stroke severity and long-term outcome. BMC Neurol. 2004;4:2. doi: 10.1186/1471-2377-4-2.
9. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297.
10. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105:10513–10518.
11. Zampetaki A, Willeit P, Drozdov I, Kiechl S, Mayr M. Profiling of circulating microRNAs: from single biomarkers to re-wired networks. Cardiovasc Res. 2012;93:555–562. doi: 10.1093/cvr/cvr266.
12. He Y, Lin J, Kong D, Huang M, Xu C, Kim TK, Etheridge A, Luo Y, Ding Y, Wang K. Current state of circulating microRNAs as cancer biomarkers. Clin Chem. 2015;61:1138–1155. doi: 10.1373/clinchem.2015.241190.
13. Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 2012;110:483–495. doi: 10.1161/CIRCRESAHA.111.247452.
14. Mayr M, Zampetaki A, Willeit P, Willeit J, Kiechl S. MicroRNAs within the continuum of postgenomics biomarker discovery. Arterioscler Thromb Vasc Biol. 2013;33:206–214. doi: 10.1161/ATVBAHA.112.300141.
15. Bhalala OG, Srikanth M, Kessler JA. The emerging roles of microRNAs in CNS injuries. Nat Rev Neurol. 2013;9:328–339. doi: 10.1038/nrneurol.2013.67.
16. Tan KS, Armugam A, Sepramaniam S, Lim KY, Setyowati KD, Wang CW, Jeyaseelan K. Expression profile of microRNAs in young stroke patients. PLoS One. 2009;4:e7689. doi: 10.1371/journal.pone.0007689.
17. Li P, Teng F, Gao F, Zhang M, Wu J, Zhang C. Identification of circulating microRNAs as potential biomarkers for detecting acute ischemic stroke. Cell Mol Neurobiol. 2015;35:433–447. doi: 10.1007/s10571-014-0139-5.
18. Tsai PC, Liao YC, Wang YS, Lin HF, Lin RT, Juo SH. Serum microRNA-21 and microRNA-221 as potential biomarkers for cerebrovascular disease. J Vasc Res. 2013;50:346–354. doi: 10.1159/000351767.
19. Li M, Zhang J. Circulating microRNAs: potential and emerging biomarkers for diagnosis of cardiovascular and cerebrovascular diseases. Biomed Res Int. 2015;2015:730535. doi: 10.1155/2015/730535.
20. Sacco RL, Kasner SE, Broderick JP, et al; American Heart Association Stroke Council, Council on Cardiovascular Surgery and Anesthesia; Council on Cardiovascular Radiology and Intervention; Council on
21. Cardiovascular and Stroke Nursing; Council on Epidemiology and Prevention; Council on Peripheral Vascular Disease; Council on Nutrition, Physical Activity and Metabolism. An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013;44:2064–2089. doi: 10.1161/STR.0b013e318296aeca.
22. Braun J, Misiak D, Busch B, Krohn K, Hüttelmaier S. Rapid identification of regulatory microRNAs by miTRAP (miRNA trapping by RNA in vitro affinity purification). Nucleic Acids Res. 2014;42:e66. doi: 10.1093/nar/gku127.
23. Stokowy T, Eszlinger M, Świerniak M, Fujarewicz K, Jarząb B, Paschke R, Krohn K. Analysis options for high-throughput sequencing in miRNA expression profiling. BMC Res Notes. 2014;7:144. doi: 10.1186/1756-0500-7-144.
24. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8.
25. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616.
26. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993;24:35–41.
27. Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard JM, Mayr A, Weger S, Schett G, Shah A, Boulanger CM, Willeit J, Chowienczyk PJ, Kiechl S, Mayr M. Prospective study on circulating microRNAs and risk of myocardial infarction. J Am Coll Cardiol. 2012;60:290–299. doi: 10.1016/j.jacc.2012.03.056.
28. Kaudewitz D, Skroblin P, Bender LH, et al. Association of microRNAs and YRNAs with platelet function. Circ Res. 2016;118:420–432. doi: 10.1161/CIRCRESAHA.114.305663.
29. Worthmann H, Tryc AB, Goldbecker A, Ma YT, Tountopoulou A, Hahn A, Dengler R, Lichtinghagen R, Weissenborn K. The temporal profile of inflammatory markers and mediators in blood after acute ischemic stroke differs depending on stroke outcome. Cerebrovasc Dis. 2010;30:85–92. doi: 10.1159/000314624.
30. Glickman SW, Phillips S, Anstrom KJ, Laskowitz DT, Cairns CB. Discriminative capacity of biomarkers for acute stroke in the emergency department. J Emerg Med. 2011;41:333–339. doi: 10.1016/j.jemermed.2010.02.025.
31. Dvorak F, Haberer I, Sitzer M, Foerch C. Characterisation of the diagnostic window of serum glial fibrillary acidic protein for the differentiation of intracerebral haemorrhage and ischaemic stroke. Cerebrovasc Dis. 2009;27:37–41. doi: 10.1159/000172632.
32. González-García S, González-Quevedo A, Peña-Sánchez M, Menéndez-Saínz C, Fernández-Carriera R, Arteche-Prior M, Pando-Cabrera A, Fernández-Concepción O. Serum neuron-specific enolase and S100 calcium binding protein B biomarker levels do not improve diagnosis of acute stroke. J R Coll Physicians Edinb. 2012;42:199–204. doi: 10.4997/JRCPE.2012.302.
33. Liebetrau C, Möllmann H, Dörr O, Szardien S, Troidl C, Willmer M, Voss S, Gaede L, Rixe J, Rolf A, Hamm C, Nef H. Release kinetics of circulating muscle-enriched microRNAs in patients undergoing transcoronary ablation of septal hypertrophy. J Am Coll Cardiol. 2013;62:992–998. doi: 10.1016/j.jacc.2013.05.025.
34. Jauch EC, Saver JL, Adams HP Jr, Bruno A, Connors JJ, Demaerschalk BM, Khatri P, McMullan PW Jr, Qureshi AI, Rosenfield K, Scott PA, Summers DR, Wang DZ, Wintermark M, Yonas H; American Heart Association Stroke Council; Council on Cardiovascular Nursing; Council on Peripheral Vascular Disease; Council on Clinical Cardiology. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013;44:870–947. doi: 10.1161/STR.0b013e318284056a.
35. Zhu G, Michel P, Aghaebrahim A, Patrie JT, Xin W, Eskandari A, Zhang W, Wintermark M. Computed tomography workup of patients suspected of acute ischemic stroke: perfusion computed tomography adds value compared with clinical evaluation, noncontrast computed tomography, and computed tomography angiogram in terms of predicting outcome. Stroke. 2013;44:1049–1055. doi: 10.1161/STROKEAHA.111.674705.
36. Sommer CJ. Ischemic stroke: experimental models and reality. Acta Neuropathol. 2017;133:245–261. doi: 10.1007/s00401-017-1667-0.
37. Zampetaki A, Mayr M. MicroRNAs in vascular and metabolic disease. Circ Res. 2012;110:508–522. doi: 10.1161/CIRCRESAHA.111.247445.
38. Ramanujam D, Engelhardt S. Intercellular miRNA traffic. Circ Res. 2015;116:1726–1728. doi: 10.1161/CIRCRESAHA.115.306519.
39. Deng L, Blanco FJ, Stevens H, et al. MicroRNA-143 activation regulates smooth muscle and endothelial cell crosstalk in pulmonary arterial hypertension. Circ Res. 2015;117:870–883. doi: 10.1161/CIRCRESAHA.115.306806.
40. Climent M, Quintavalle M, Miragoli M, Chen J, Condorelli G, Elia L. TGFβ triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ Res. 2015;116:1753–1764. doi: 10.1161/CIRCRESAHA.116.305178.
41. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 2009;460:705–710. doi: 10.1038/nature08195.
42. Che P, Liu J, Shan Z, Wu R, Yao C, Cui J, Zhu X, Wang J, Burnett MS, Wang S, Wang J. miR-125a-5p impairs endothelial cell angiogenesis in aging mice via RTEF-1 downregulation. Aging Cell. 2014;13:926–934. doi: 10.1111/acel.12252.
43. Muramatsu F, Kidoya H, Naito H, Sakimoto S, Takakura N. MicroRNA-125b inhibits tube formation of blood vessels through translational suppression of VE-cadherin. Oncogene. 2013;32:414–421. doi: 10.1038/onc.2012.68.
44. Reijerkerk A, Lopez-Ramirez MA, van Het Hof B, Drexhage JA, Kamphuis WW, Kooij G, Vos JB, van der Pouw Kraan TC, van Zonneveld AJ, Horrevoets AJ, Prat A, Romero IA, de Vries HE. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: implications for multiple sclerosis. J Neurosci. 2013;33:6857–6863. doi: 10.1523/JNEUROSCI.3965-12.2013.
45. Pan W, Zhu S, Dai D, et al. MiR-125a targets effector programs to stabilize Treg-mediated immune homeostasis. Nat Commun. 2015;6:7096. doi: 10.1038/ncomms8096.
46. Banerjee S, Cui H, Xie N, Tan Z, Yang S, Icyuz M, Thannickal VJ, Abraham E, Liu G. miR-125a-5p regulates differential activation of macrophages and inflammation. J Biol Chem. 2013;288:35428–35436. doi: 10.1074/jbc.M112.426866.
47. Graff JW, Dickson AM, Clay G, McCaffrey AP, Wilson ME. Identifying functional microRNAs in macrophages with polarized phenotypes. J Biol Chem. 2012;287:21816–21825. doi: 10.1074/jbc.M111.327031.
48. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron. 2010;65:373–384. doi: 10.1016/j.neuron.2010.01.005.
49. Willeit P, Zampetaki A, Dudek K, et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res. 2013;112:595–600. doi: 10.1161/CIRCRESAHA.111.300539.
50. McAlexander MA, Phillips MJ, Witwer KW. Comparison of methods for miRNA extraction from plasma and quantitative recovery of RNA from ce-rebrospinal fluid. Front Genet. 2013;4:83. doi: 10.3389/fgene.2013.00083.
51. Hafner M, Renwick N, Brown M, Mihailović A, Holoch D, Lin C, Pena JT, Nusbaum JD, Morozov P, Ludwig J, Ojo T, Luo S, Schroth G, Tuschl T. RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. RNA. 2011;17:1697–1712. doi: 10.1261/rna.2799511.
52. Mestdagh P, Hartmann N, Baeriswyl L, et al. Evaluation of quantitative miRNA expression platforms in the microRNA quality control (miRQC) study. Nat Methods. 2014;11:809–815. doi: 10.1038/nmeth.3014.