MicroRNAs in Cerebrovascular Diseases – from Pathophysiology to Potential Biomarkers
Authors:
O. Volný 1,2; L. Kašičková 3; D. Coufalová 2,3; P. Cimflová 2,4; J. Novák 5,6
Authors place of work:
I. neurologická klinika LF MU a FN u sv. Anny v Brně
1; ICRC – Mezinárodní centrum klinického výzkumu, FN u sv. Anny v Brně
2; Lékařská fakulta MU, Brno
3; Klinika zobrazovacích metod LF MU a FN u sv. Anny v Brně
4; II. interní klinika LF MU a FN U sv. Anny v Brně
5; Fyziologický ústav, LF MU, Brno
6
Published in the journal:
Cesk Slov Neurol N 2016; 79/112(3): 287-293
Category:
Review Article
Summary
Small non-coding molecules of ribonucleic acid are important regulators of gene expression and translation. One group of non-coding RNAs is represented by microRNA – 22-24 nucleotides long RNA molecules with effects on regulation of proteins synthesis. Many of them are tissue or organ specific (e. g. miR-206 in striated muscles or miR-122 in hepatocytes). These molecules are enzyme-resistant and detectable in both intracellular and extracellular space. Currently, these molecules are intensively studied as potential markers in many diseases including cerebrovascular diseases. In this review we provide insight into the recent knowledge from animal to human studies concerning miRNAs, with the special emphasis put on diagnostic, therapeutic and prognostic potentials in ischemic stroke (let-7, miR-7, miR-21, miR-29, miR-124, miR-181, miR-210, miR-223), intracranial aneurysms (miR-21, miR-26, miR-29, miR-143/145), and brain arterio-venous malformations (miR-18a).
Key words:
microRNA – ischemic stroke – intracranial aneurysma – cerebral arterio-venous malformations
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.
Zdroje
1. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011;12(12):861– 74. doi: 10.1038/nrg3074.
2. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116(2):281– 97.
3. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993;75(5):843– 54.
4. Reinhart BJ, Slack FJ, Basson M, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000;403(6772):901– 6.
5. Pasquinelli AE, Reinhart BJ, Slack F, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000;408(6808):86– 9.
6. Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 2002;99(24):15524– 9.
7. Weber JA, Baxter DH, Zhang S, et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010;56(11):1733– 41. doi: 10.1373/clinchem.2010.147405.
8. Kondkar AA, Abu-Amero KK. Utility of circulating microRNAs as clinical biomarkers for cardiovascular diseases. BioMed Res Int 2015;2015:821823. doi: 10.1155/2015/ 821823.
9. Zhang W, Qian P, Zhang X, et al. Autocrine/ Paracrine Human Growth Hormone-stimulated MicroRNA 96-182-183 Cluster Promotes Epithelial-Mesenchymal Transition and Invasion in Breast Cancer. J Biol Chem 2015;290(22):13812– 29. doi: 10.1074/jbc.M115.653261.
10. Madonna R, Cadeddu C, Deidda M, et al. Cardioprotection by gene therapy: a review paper on behalf of the Working Group on Drug Cardiotoxicity and Cardioprotection of the Italian Society of Cardiology. Int J Cardiol 2015;191:203– 10. doi: 10.1016/j.ijcard.2015.04.232.
11. Chen X, Zhang L, Su T, et al. Kinetics of plasma microRNA-499 expression in acute myocardial infarction. J Thorac Dis 2015;7(5):890– 6. doi: 10.3978/j.issn.2072-1439.2014.11.32.
12. Arrese M, Eguchi A, Feldstein AE. Circulating microRNAs: emerging biomarkers of liver disease. Semin Liver Dis 2015;35(1):43– 54. doi: 10.1055/s-0034-1397348.
13. van Rooij E, Olson EN. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 2012;11(11):860– 72. doi: 10.1038/nrd3864.
14. Rayner KJ, Esau CC, Hussain FN, et al. Inhibition of miR-33a/ b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 2011;478(7369):404– 7. doi: 10.1038/nature10486.
15. Rayner KJ, Sheedy FJ, Esau CC, et al. Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 2011;121(7):2921– 31. doi: 10.1172/JCI57275.
16. Wahlquist C, Jeong D, Rojas-Muñoz A, et al. Inhibition of miR-25 improves cardiac contractility in the failing heart. Nature 2014;508(7497):531– 5. doi: 10.1038/nature13073.
17. Janssen HL, Reesink HW, Lawitz EJ, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med 2013;368(18):1685– 94. doi: 10.1056/NEJMoa1209026.
18. Soreq H, Wolf Y. NeurimmiRs: microRNAs in the neuroimmune interface. Trends Mol Med 2011;17(10):548– 55. doi: 10.1016/j.molmed.2011.06.009.
19. Kim JM, Jung KH, Chu K, et al. Atherosclerosis-related circulating microRNAs as a predictor of strokerecurrence. Transl Stroke Res 2015;6(3):191– 7. doi: 10.1007/s12975-015-0390-1.
20. Dharap A, Bowen K, Place R, et al. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 2009;29(4):675– 87. doi: 10.1038/jcbfm.2008.157.
21. Gubern C, Camós S, Ballesteros I, et al. miRNA expression is modulated over time after focal ischaemia: up-regulation of miR-347 promotes neuronal apoptosis. FEBS J 2013;280(23):6233– 46. doi: 10.1111/febs.12546.
22. Jeyaseelan K, Lim KY, Armugam A. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke J Cereb Circ 2008;39(3):959– 66.
23. Liu FJ, Lim KY, Kaur P, et al. microRNAs involved in regulating spontaneous recovery in embolic stroke model. PloS One 2013;8(6):e66393.
24. Selvamani A, Williams MH, Miranda RC, et al. Circulating miRNA profiles provide a biomarker for severity of stroke outcomes associated with age and sex in a rat model. Clin Sci Lond Engl 2014;127(2):77– 89. doi: 10.1042/CS20130565.
25. Weng H, Shen C, Hirokawa G, et al. Plasma miR--124 as a biomarker for cerebral infarction. Biomed Res 2011;32(2):135– 41.
26. Rehfeld F, Rohde AM, Nguyen DT, et al. Lin28 and let-7: ancient milestones on the road from pluripotency to neurogenesis. Cell Tissue Res 2015;359(1):145– 60. doi: 10.1007/s00441-014-1872-2.
27. Hulsmans M, Holvoet P. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res 2013;100(1):7– 18. doi: 10.1093/cvr/cvt161.
28. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9(6):654– 9.
29. Selvamani A, Sathyan P, Miranda RC, et al. An antagomir to microRNA Let7f promotes neuroprotection in an ischemic stroke model. PloS One 2012;7(2):e32662. doi: 10.1371/journal.pone.0032662.
30. Bienertova-Vasku J, Novak J, Vasku A. MicroRNAs in pulmonary arterial hypertension: pathogenesis, diagnosis and treatment. J Am Soc Hypertens 2015;9(3):221– 34. doi: 10.1016/j.jash.2014.12.011.
31. Tan KS, Armugam A, Se pramaniam S, et al. Expression profile of MicroRNAs in young stroke patients. PloS One 2009;4(11):e7689. doi: 10.1371/ journal.pone.0007689.
32. Buller B, Liu X, Wang X, et al. MicroRNA-21 protects neurons from ischemic death. FEBS J 2010;277(20):4299– 307. doi: 10.1111/j.1742-4658.2010.07818.x.
33. Zhou J, Zhang J. Identification of miRNA-21 and miRNA-24 in plasma as potential early stage markers of acute cerebral infarction. Mol Med Rep 2014;10(2):971– 6. doi: 10.3892/mmr.2014.2245.
34. Dong S, Cheng Y, Yang J, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 2009;284(43):29514– 25. doi: 10.1074/jbc.M109.027896.
35. Huang LG, Li JP, Pang XM, et al. MicroRNA-29c Correlates with Neuroprotection Induced by FNS by Targeting Both Birc2 and Bak1 in Rat Brain after Stroke. CNS Neurosci Ther 2015;21(6):496– 503. doi: 10.1111/cns.12383.
36. Khanna S, Rink C, Ghoorkhanian R, et al. Loss of miR-29b following acute ischemic stroke contributes to neural cell death and infarct size. J Cereb Blood Flow Metab 2013;33(8):1197– 206. doi: 10.1038/jcbfm.2013.68.
37. Pandi G, Nakka VP, Dharap A, et al. MicroRNA miR-29c down-regulation leading to de-repression of its target DNA methyltransferase 3a promotes ischemic brain damage. PloS One 2013;8(3):e58039. doi: 10.1371/journal.pone.0058039.
38. Dhiraj DK, Chrysanthou E, Mallucci GR, et al. miRNAs-19b, -29b-2* and -339-5p show an early and sustained up-regulation in ischemic models of stroke. PloS One 2013;8(12):e83717. doi: 10.1371/journal.pone.0083717.
39. Shi G, Liu Y, Liu T, et al. Upregulated miR-29b promotes neuronal cell death by inhibiting Bcl2L2 after ischemic brain injury. Exp Brain Res 2012;216(2):225– 30. doi: 10.1007/s00221-011-2925-3.
40. Laterza OF, Lim L, Garrett-Engele PW, et al. Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 2009;55(11):1977– 83. doi: 10.1373/clinchem.2009.131797.
41. Meza-Sosa KF, Pedraza-Alva G, Pérez-Martínez L. MicroRNAs: key triggers of neuronal cell fate. Front Cell Neurosci 2014;8:175. doi: 10.3389/fncel.2014.00175.
42. Doeppner TR, Doehring M, Bretschneider E, et al. MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradation. Acta Neuropathol 2013;126(2):251– 65. doi: 10.1007/s00401-013-1142-5.
43. Sun Y, Gui H, Li Q, et al. MicroRNA-124 protects neurons against apoptosis in cerebral ischemic stroke. CNS Neurosci Ther 2013;19(10):813– 9. doi: 10.1111/cns.12142.
44. Fang M, Wang J, Zhang X, et al. The miR-124 regulates the expression of BACE1/ β-secretase correlated with cell death in Alzheimer’s disease. Toxicol Lett 2012;209(1):94– 105. doi: 10.1016/j.toxlet.2011.11.032.
45. Liu XS, Chopp M, Zhang RL, et al. MicroRNA profiling in subventricular zone after stroke: MiR-124a regulates proliferation of neural progenitor cells through Notch signaling pathway. PloS One 2011;6(8):e23461. doi: 10.1371/journal.pone.0023461.
46. Zhu F, Liu JL, Li JP, et al. MicroRNA-124 (miR-124) regulates Ku70 expression and is correlated with neuronal death induced by ischemia/ reperfusion. J Mol Neurosci 2014;52(1):148– 55. doi: 10.1007/s12031-013-0155-9.
47. Miska EA, Alvarez-Saavedra E, Townsend M, et al.Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 2004;5(9):R68.
48. Ouyang YB, Giffard RG. MicroRNAs affect BCL-2 family proteins in the setting of cerebral ischemia. Neurochem Int 2014;77:2– 8. doi: 10.1016/j.neuint.2013.12.006.
49. Ouyang YB, Lu Y, Yue S, et al. miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis 2012;45(1):555– 63. doi: 10.1016/j.nbd.2011.09.012.
50. Ouyang YB, Giffard RG. MicroRNAs regulate the chaperone network in cerebral ischemia. Transl Stroke Res 2013;4(6):693– 703. doi: 10.1007/s12975-013-0280-3.
51. Ouyang YB, Xu L, Liu S, et al. Role of astrocytes in delayed neuronal death: GLT-1 and its novel regulation by MicroRNAs. Adv Neurobiol 2014;11:171– 88. doi: 10.1007/978-3-319-08894-5_9.
52. Chan YC, Banerjee J, Choi SY, et al. miR-210: the master hypoxamir. Microcirc 2012;19(3):215– 23. doi: 10.1111/j.1549-8719.2011.00154.x.
53. Fasanaro P, D’Alessandra Y, Di Stefano V, et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 2008;283(23):15878– 83. doi: 10.1074/jbc.M800731200.
54. Lou L, Guo F, Liu F, et al. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem 2012;370(1– 2):45– 51. doi: 10.1007/s11010-012-1396-6.
55. Zeng L, He X, Wang Y, et al. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther 2014;21(1):37– 43. doi: 10.1038/gt.2013.55.
56. Sepramaniam S, Ying LK, Armugam A, et al. MicroRNA-130a represses transcriptional activity of aquaporin 4 M1 promoter. J Biol Chem 2012;287(15):12006– 15. doi: 10.1074/jbc.M111.280701.
57. Pan Y, Liang H, Liu H, et al. 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 Baltim Md 2014;192(1):437– 46. doi: 10.4049/jimmunol.1301790.
58. Tabet F, Vickers KC, Cuesta Torres LF, et al. HDL--transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat Commun 2014;5:3292. doi: 10.1038/ncomms4292.
59. Vickers KC, Landstreet SR, Levin MG, et al. MicroRNA-223 coordinates cholesterol homeostasis. Proc Natl Acad Sci U S A 2014;111(40):14518– 23. doi: 10.1073/pnas.1215767111.
60. Harraz MM, Eacker SM, Wang X, et al. MicroRNA-223 is neuroprotective by targeting glutamate receptors. Proc Natl Acad Sci U S A 2012;109(46):18962– 7. doi: 10.1073/ pnas.1121288109.
61. Duan X, Zhan Q, Song B, et al. Detection of platelet microRNA expression in patients with diabetes mellitus with or without ischemic stroke. J Diabetes Complications 2014;28(5):705– 10. doi: 10.1016/j.jdiacomp.2014.04.012.
62. Leung LY, Chan CP, Leung YK, et al. Comparison of miR-124-3p and miR-16 for early diagnosis of hemorrhagic and ischemic stroke. Clin Chim Acta 2014;433:139– 44. doi: 10.1016/j.cca.2014.03.007.
63. Liu Y, Zhang J, Han R, et al. Downregulation of serum brain specific microRNA is associated with inflammation and infarct volume in acute ischemic stroke. J Clin Neurosci 2015;22(2):291– 5. doi: 10.1016/j.jocn.2014.05.042.
64. 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. doi: 10.1186/1471-2377-13-178.
65. Tsai PC, Liao YC, Wang Y-S, et al. Serum microRNA-21 and microRNA-221 as potential biomarkers for cerebrovascular disease. J Vasc Res 2013;50(4):346– 54. doi: 10.1159/000351767.
66. Zeng L, Liu J, Wang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front Biosci 2011;3:1265– 72.
67. Wang Y, Zhang Y, Huang J, et al. Increase of circulating miR-223 and insulin-like growth factor-1 is associated with the pathogenesis of acute ischemic stroke in patients. BMC Neurol 2014;14:77. doi: 10.1186/1471-2377-14-77.
68. Vinciguerra A, Formisano L, Cerullo P, et al. MicroRNA--103-1 selectively downregulates brain NCX1 and its inhibition by anti-miRNA ameliorates stroke damage and neurological deficits. Mol Ther 2014;22(10):1829– 38. doi: 10.1038/mt.2014.113.
69. Yang ZB, Zhang Z, Li TB, et al. Up-regulation of brain-enriched miR-107 promotes excitatory neurotoxicity through down-regulation of glutamate transporter-1 expression following ischaemic stroke. Clin Sci Lond Engl 2014;127(12):679– 89. doi: 10.1042/CS20140084.
70. Chi W, Meng F, Li Y, et al. Downregulation of miRNA--134 protects neural cells against ischemic injury in N2A cells and mouse brain with ischemic stroke by targeting HSPA12B. Neuroscience 2014;277:111– 22. doi: 10.1016/j.neuroscience.2014.06.062.
71. Chi W, Meng F, Li Y, et al. Impact of microRNA-134 on neural cell survival against ischemic injury in primary cultured neuronal cells and mouse brain with ischemic stroke by targeting HSPA12B. Brain Res 2014;1592:22– 33. doi: 10.1016/j.brainres.2014.09.072.
72. Stary CM, Xu L, Sun X, et al. MicroRNA-200c contributes to injury from transient focal cerebral ischemia by targeting Reelin. Stroke 2015;46(2):551– 6. doi: 10.1161/STROKEAHA.114.007041.
73. Li LJ, Huang Q, Zhang N, et al. miR-376b-5p regulates angiogenesis in cerebral ischemia. Mol Med Rep 2014;10(1):527– 35. doi: 10.3892/mmr.2014.2172.
74. Liu P, Zhao H, Wang R, et al. MicroRNA-424 protects against focal cerebral ischemia and reperfusion injury in mice by suppressing oxidative stress. Stroke 2015;46(2):513– 9. doi: 10.1161/STROKEAHA.114.007482.
75. Zhao H, Wang J, Gao L, et al. MiRNA-424 protects against permanent focal cerebral ischemia injury in mice involving suppressing microglia activation. Stroke 2013;44(6):1706– 13. doi: 10.1161/STROKEAHA.111.000504.
76. Brown RD, Wiebers DO, Forbes GS. Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. J Neurosur 1990;73(6):859– 63.
77. Brown RD, Broderick JP. Unruptured intracranial aneurysms: epidemiology, natural history, management options, and familial screening. Lancet Neurol 2014;13(4):393– 404. doi: 10.1016/S1474-4422(14)70015-8.
78. Shiue I, Arima H, Hankey GJ, et al. Modifiable lifestyle behaviours account for most cases of subarachnoid haemorrhage: a population-based case-control study in Australasia. J Neurol Sci 2012;313(1– 2):92– 4. doi: 10.1016/j.jns.2011.09.017.
79. Vernooij MW, Ikram MA, Tanghe HL, et al. Incidental findings on brain MRI in the general population. N Engl J Med 2007;357(18):1821– 8.
80. Lee HJ, Yi JS, Lee HJ, et al. Dysregulated expression profiles of microRNAs of experimentally induced cerebral aneurysms in rats. J Korean Neurosurg Soc 2013;53(2):72– 6. doi: 10.3340/jkns.2013.53.2.72.
81. Jiang Y, Zhang M, He H, et al. MicroRNA/ mRNA profiling and regulatory network of intracranial aneurysm. BMC Med Genomics 2013;6:36. doi: 10.1186/1755-8794-6-36.
82. Liu D, Han L, Wu X, et al. Genome-wide microRNA changes in human intracranial aneurysms. BMC Neurol 2014;14(1):188. doi: 10.1186/s12883-014-0188-x.
83. Jin H, Li C, Ge H, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of intracranial aneurysm rupture a case control study. J Transl Med 2013;11:296. doi: 10.1186/1479-5876-11-296.
84. Li P, Zhang Q, Wu X, et al. Circulating microRNAs serve as novel biological markers for intracranial aneurysms. J Am Heart Assoc 2014;3(5):e000972. doi: 10.1161/JAHA.114.000972.
85. Maegdefessel L, Azuma J, Toh R, et al. MicroRNA-21 blocks abdominal aortic aneurysm development and nicotine-augmented expansion. Sci Transl Med 2012;4(122):22. doi: 10.1126/scitranslmed.3003441.
86. Boon RA, Seeger T, Heydt S, et al. MicroRNA-29 in aortic dilation: implications for aneurysm formation. Circ Res 2011;109(10):1115– 9. doi: 10.1161/CIRCRESAHA.111.255737.
87. Maegdefessel L, Azuma J, Tsao PS. MicroRNA-29b regulation of abdominal aortic aneurysm development. Trends Cardiovasc Med 2014;24(1):1– 6. doi: 10.1016/j.tcm.2013.05.002.
88. Merk DR, Chin JT, Dake BA, et al. MiR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 2012;110(2):312– 24. doi: 10.1161/CIRCRESAHA.111.253740.
89. Elia L, Quintavalle M, Zhang J, et al. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 2009;16(12):1590– 8. doi: 10.1038/cdd.2009.153.
90. Doebele C, Bonauer A, Fischer A, et al. Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood 2010;115(23):4944– 50. doi: 10.1182/blood-2010-01-264812.
91. Ferreira R, Santos T, Amar A, et al. Argonaute-2 promotes miR-18a entry in human brain endothelial cells. J Am Heart Assoc 2014;3(3):e000968. doi: 10.1161/JAHA.114.000968.
92. Ferreira R, Santos T, Amar A, et al. MicroRNA-18a improves human cerebral arteriovenous malformation endothelial cell function. Stroke 2014;45(1):293– 7. doi: 10.1161/STROKEAHA.113.003578.
Štítky
Paediatric neurology Neurosurgery NeurologyČlánok vyšiel v časopise
Czech and Slovak Neurology and Neurosurgery
2016 Číslo 3
- Advances in the Treatment of Myasthenia Gravis on the Horizon
- Memantine Eases Daily Life for Patients and Caregivers
- Spasmolytic Effect of Metamizole
Najčítanejšie v tomto čísle
- Sympathetic Chain Schwannoma – a Case Report
- Clinical Guideline for the Diagnostics and Treatment of Patients with Ischemic Stroke and Transitory Ischemic Attack – Version 2016
- Validity Study of the Boston Naming Test Czech Version
- Pre-motor and Non-motor Symptoms of Parkinson’s Disease – Taxonomy, Clinical Manifestation and Neuropathological Correlates