MicroRNA in ischemic stroke etiology and pathology

Physiological Genomics

Volumn 43, Issue 10, 2011, Pages 521-528

  Rink, Cameron ^a   Khanna, Savita ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Atherosclerosis; Brain; Ischemia; MiRNA

Indexed keywords

CASPASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LOCKED NUCLEIC ACID; MESSENGER RNA; MICRORNA; MICRORNA 21; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TRANSCRIPTOME;

ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL SURVIVAL; DRUG TARGETING; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INCIDENCE; MICRORNAS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; STROKE;

EID: 79957649500     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00158.2010     Document Type: Review

References (90)

1. Baranova O, Miranda L.F, Pichiule P, Dragatsis I, Johnson R.S, Chavez J.C. Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 27: 6320-6332, 2007.
2. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, function. Cell 116: 281-297, 2004.
3. Bentwich I. Prediction and validation of microRNAs and their targets. FEBS Lett 579: 5904-5910, 2005.
4. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, Bentwich Z. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 37: 766-770, 2005.
5. Chen T, Huang Z, Wang L, Wang Y, Wu F, Meng S, Wang C. MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/macro-phages. Cardiovasc Res 83: 131-139, 2009.
6. Chen W.J, Lin K.H, Lai Y.J, Yang S.H, Pang J.H. Protective effect of propylthiouracil independent of its hypothyroid effect on atherogenesis in cholesterol-fed rabbits: PTEN induction and inhibition of vascular smooth muscle cell proliferation and migration. Circulation 110: 1313-1319, 2004.
7. Cheng C, de Crom R, van Haperen R, Helderman F, Mousavi Gourabi B, van Damme L.C, Kirschbaum S.W, Slager C.J, van der Steen A.F, Krams R. The role of shear stress in atherosclerosis: action through gene expression and inflammation? Cell Biochem Biophys 41: 279-294, 2004.
8. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen M.J, Krams R, de Crom R. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113: 2744-2753, 2006.
9. Christensen M, Schratt G.M. microRNA involvement in developmental and functional aspects of the nervous system and in neurological diseases. Neurosci Lett 466: 55-62, 2009.
10. De Oliveira-Sales E.B, Nishi E.E, Boim M.A, Dolnikoff M.S, Bergamas-chi C.T, Campos R.R. Upregulation of AT1R and iNOS in the rostral ventrolateral medulla (RVLM) is essential for the sympathetic hyperac-tivity and hypertension in the 2K-1C Wistar rat model. Am J Hypertens 23: 708-715, 2010.
11. Dentelli P, Rosso A, Orso F, Olgasi C, Taverna D, Brizzi M.F. microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5A expression. Arterioscler Thromb Vasc Biol 30: 1562-1568, 2010.
12. Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 29: 675-687, 2009.
13. Dhawan S.S, Avati Nanjundappa R.P, Branch J.R, Taylor W.R, Quyyumi A.A, Jo H, McDaniel M.C, Suo J, Giddens D, Samady H. Shear stress and plaque development. Expert Rev Cardiovasc Ther 8: 545-556, 2010.
14. Dirnagl U, Iadecola C, Moskowitz M.A, Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397, 1999. Dirnagl U, Simon R.P, Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26: 248-254, 2003.
15. Dirnagl U, Simon RP, Hallenbeck JM. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26: 248-254, 2003.
16. Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjarn M, Hansen H.F, Berger U, Gullans S, Kearney P, Sarnow P, Straarup E.M, Kauppinen S. LNA-mediated microRNA silencing in non-human primates. Nature 452: 896-899, 2008.
17. Eulalio A, Huntzinger E, Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 132: 9-14, 2008.
18. Fasanaro P, D'Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, Capogrossi M.C, Martelli F. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 283: 15878-15883, 2008.
19. Fasanaro P, Greco S, Lorenzi M, Pescatori M, Brioschi M, Kulshreshtha R, Banfi C, Stubbs A, Calin G.A, Ivan M, Capogrossi M.C, Martelli F. An integrated approach for experimental target identification of hypoxia-induced miR-210. J Biol Chem 284: 35134-35143, 2009.
20. Floris S, Ruuls S.R, Wierinckx A, van der Pol S.M, Dopp E, van der Meide P.H, Dijkstra C.D, De Vries H.E. Interferon-beta directly influences monocyte infiltration into the central nervous system. J Neuroim-munol 127: 69-79, 2002.
21. Griffiths-Jones S, Grocock R.J, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-D144, 2006.
22. Harris T.A, Yamakuchi M, Ferlito M, Mendell J.T, Lowenstein C.J. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 105: 1516-1521, 2008.
23. Haver V.G, Slart R.H, Zeebregts C.J, Peppelenbosch M.P, Tio R.A. Rupture of vulnerable atherosclerotic plaques: microRNAs conducting the orchestra? Trends Cardiovasc Med 20: 65-71, 2010.
24. He L, He X, Lim L.P, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson A.L, Linsley P.S, Chen C, Lowe S.W, Cleary M.A, Hannon G.J. A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134, 2007.
25. Hellings W.E, Peeters W, Moll F.L, Pasterkamp G. From vulnerable plaque to vulnerable patient: the search for biomarkers of plaque destabi-lization. Trends Cardiovasc Med 17: 162-171, 2007.
26. Humphries S.E, Morgan L. Genetic risk factors for stroke and carotid atherosclerosis: insights into pathophysiology from candidate gene approaches. Lancet Neurol 3: 227-235, 2004.
27. Hurst R.T, Lee R.W. Increased incidence of coronary atherosclerosis in type 2 diabetes mellitus: mechanisms and management. Ann Intern Med 139: 824-834, 2003.
28. Jeyaseelan K, Lim K.Y, Armugam A. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 39: 959-966, 2008.
29. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, Dean D.B, Zhang C. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100: 1579-1588, 2007.
30. Kloosterman W.P, Plasterk R.H. The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-450, 2006.
31. Krutzfeldt J, Kuwajima S, Braich R, Rajeev K.G, Pena J, Tuschl T, Manoharan M, Stoffel M. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res 35: 2885-2892, 2007.
32. Kuhn D.E, Martin M.M, Feldman D.S, Terry A.V Jr, Nuovo G.J, Elton T.S. Experimental validation of miRNA targets. Methods 44: 47-54, 2008.
33. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol 12: 735-739, 2002.
34. Lee S.T, Chu K, Jung K.H, Yoon H.J, Jeon D, Kang K.M, Park K.H, Bae E.K, Kim M, Lee S.K, Roh J.K. MicroRNAs induced during ischemic preconditioning. Stroke 41: 1646-1651, 2010.
35. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature 425: 415-419, 2003.
36. Lee Y.W, Kuhn H, Hennig B, Neish A.S, Toborek M. IL-4-induced oxidative stress upregulates VCAM-1 gene expression in human endothelial cells. J Mol Cell Cardiol 33: 83-94, 2001.
37. Lewis B.P, Burge C.B, Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20, 2005.
38. Ley K, Huo Y. VCAM-1 is critical in atherosclerosis. J Clin Invest 107: 1209-1210, 2001.
39. Liu D.Z, Tian Y, Ander B.P, Xu H, Stamova B.S, Zhan X, Turner R.J, Jickling G, Sharp F.R. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30: 92-101, 2010.
40. Lloyd-Jones D, Adams R.J, Brown T.M, Carnethon M, Dai S, De Simone G, Ferguson T.B, Ford E, Furie K, Gillespie C, Go A, Green-lund K, Haase N, Hailpern S, Ho P.M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M.M, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong N.D, Wylie-Rosett J. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121: e46-e215, 2010.
41. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H, Knyazev P, Diebold J, Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7: 2591-2600, 2008.
42. Lukiw W.J, Pogue A.I. Induction of specific micro RNA (miRNA) species by ROS-generating metal sulfates in primary human brain cells. J Inorg Biochem 101: 1265-1269, 2007.
43. Mackay J, Mensah GA, Mendis S, Greenlund K; World Health Organization. The Atlas of Heart Disease and Stroke. Geneva: World Health Organization, 2004, p. 112.
44. Martin G, Schouest K, Kovvuru P, Spillane C. Prediction and validation of microRNA targets in animal genomes. J Biosci 32: 1049-1052, 2007.
45. Martin M.M, Buckenberger J.A, Jiang J, Malana G.E, Nuovo G.J, Chotani M, Feldman D.S, Schmittgen T.D, Elton T.S. The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microRNA-155 binding. J Biol Chem 282: 24262-24269, 2007.
46. Matsui J, Wakabayashi T, Asada M, Yoshimatsu K, Okada M. Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J Biol Chem 279: 18600-18607, 2004.
47. Maziere P, Enright A.J. Prediction of microRNA targets. Drug Discov Today 12: 452-458, 2007.
48. Mehta J.L, Sanada N, Hu C.P, Chen J, Dandapat A, Sugawara F, Satoh H, Inoue K, Kawase Y, Jishage K, Suzuki H, Takeya M, Schnacken-berg L, Beger R, Hermonat P.L, Thomas M, Sawamura T. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ Res 100: 1634-1642, 2007.
49. Mettimano M, Romano-Spica V, Ianni A, Specchia M, Migneco A, Savi L. AGT and AT1R gene polymorphism in hypertensive heart disease. Int J Clin Pract 56: 574-577, 2002.
50. Meyer J.S, Rogers R.L, Mortel K.F, Judd B.W. Hyperlipidemia is a risk factor for decreased cerebral perfusion and stroke. Arch Neurol 44: 418-422, 1987.
51. Moulton K.S. Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol 17: 548-555, 2006.
52. Nakashima Y, Raines E.W, Plump A.S, Breslow J.L, Ross R. Upregu-lation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler Thromb Vasc Biol 18: 842-851, 1998.
53. Nemenoff R.A, Simpson P.A, Furgeson S.B, Kaplan-Albuquerque N, Crossno J, Garl P.J, Cooper J, Weiser-Evans M.C. Targeted deletion of PTEN in smooth muscle cells results in vascular remodeling and recruitment of progenitor cells through induction of stromal cell-derived factor-1alpha. Circ Res 102: 1036-1045, 2008.
54. O'Brien E.R, Garvin M.R, Dev R, Stewart D.K, Hinohara T, Simpson J.B, Schwartz S.M. Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol 145: 883-894, 1994.
55. O'Brien K.D, Allen M.D, McDonald T.O, Chait A, Harlan J.M, Fishbein D, McCarty J, Ferguson M, Hudkins K, Benjamin C.D, Lobb R, Alpers C.E. Vascular cell adhesion molecule-1 is expressed in human coronary atherosclerotic plaques Implications for the mode of progression of advanced coronary atherosclerosis. J Clin Invest 92: 945-951, 1993.
56. Osterud B, Bjorklid E. Role of monocytes in atherogenesis. Physiol Rev 83: 1069-1112, 2003.
57. Papadopoulos G.L, Reczko M, Simossis V.A, Sethupathy P, Hatzigeor-giou A.G. The database of experimentally supported targets: a functional update of TarBase. Nucleic Acids Res 37: D155-D158, 2009.
58. Persson J, Nilsson J, Lindholm M.W. Cytokine response to lipoprotein lipid loading in human monocyte-derived macrophages. Lipids Health Dis 5: 17, 2006.
59. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108: 3068-3071, 2006.
60. Rayner K.J, Suarez Y, Davalos A, Parathath S, Fitzgerald M.L, Tame-hiro N, Fisher E.A, Moore K.J, Fernandez-Hernando C. MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328: 1570- 1573, 2010.
61. Rink C, Khanna S. Significance of brain tissue oxygenation and the arachidonic acid cascade in stroke. Antioxid Redox Signal (Epub ahead of print).
62. Rodriguez J.J, Olabarria M, Chvatal A, Verkhratsky A. Astroglia in dementia and Alzheimeŕs disease. Cell Death Differ 16: 378-385, 2009.
63. Roy S, Khanna S, Hussain S.R, Biswas S, Azad A, Rink C, Gnyawali S, Shilo S, Nuovo G.J, Sen C.K. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metallopro-tease-2 via phosphatase and tensin homologue. Cardiovasc Res 82: 21-29, 2009.
64. Sacks F.M, Pfeffer M.A, Moye L.A, Rouleau J.L, Rutherford J.D, Cole T.G, Brown L, Warnica J.W, Arnold J.M, Wun C.C, Davis B.R, Braun-wald E. The effect of pravastatin on coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events Trial investigators. N Engl J Med 335: 1001-1009, 1996.
65. Sen C.K, Gordillo G.M, Khanna S, Roy S. Micromanaging vascular biology: tiny microRNAs play big band. J Vasc Res 46: 527-540, 2009.
66. Sethupathy P, Megraw M, Hatzigeorgiou A.G. A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Methods 3: 881-886, 2006.
67. Shashkin P, Dragulev B, Ley K. Macrophage differentiation to foam cells. Curr Pharm Des 11: 3061-3072, 2005.
68. Siri-Tarino P.W, Sun Q, Hu F.B, Krauss R.M. Saturated fat, carbohydrate, and cardiovascular disease. Am J Clin Nutr 91: 502-509, 2010.
69. Starzyk R.M, Rosenow C, Frye J, Leismann M, Rodzinski E, Putney S, Tuomanen E.I. Cerebral cell adhesion molecule: a novel leukocyte adhe- sion determinant on blood-brain barrier capillary endothelium. J Infect Dis 181: 181-187, 2000.
70. Stenzel-Poore M.P, Stevens S.L, King J.S, Simon R.P. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38: 680-685, 2007.
71. Suarez Y. Microregulation of plaque neovascularization. Arterioscler Thromb Vasc Biol 30: 1500-1501, 2010.
72. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6: 1586-1593, 2007.
73. Trogan E, Fisher E.A. Laser capture microdissection for analysis of macrophage gene expression from atherosclerotic lesions. Methods Mol Biol 293: 221-231, 2005.
74. Truettner J, Busto R, Zhao W, Ginsberg M.D, Perez-Pinzon M.A. Effect of ischemic preconditioning on the expression of putative neuro-protective genes in the rat brain. Brain Res Mol Brain Res 103: 106-115, 2002.
75. Van den Berg A, Mols J, Han J. RISC-target interaction: cleavage and translational suppression. Biochim Biophys Acta 1779: 668-677, 2008.
76. Van Wagoner N.J, Benveniste E.N. Interleukin-6 expression and regulation in astrocytes. J Neuroimmunol 100: 124-139, 1999.
77. Veldhuis W.B, Derksen J.W, Floris S, Van Der Meide P.H, De Vries H.E, Schepers J, Vos I.M, Dijkstra C.D, Kappelle L.J, Nicolay K, Bar P.R. Interferon-beta blocks infiltration of inflammatory cells and reduces infarct volume after ischemic stroke in the rat. J Cereb Blood Flow Metab 23: 1029-1039, 2003.
78. Wang S, Aurora A.B, Johnson B.A, Qi X, McAnally J, Hill J.A, Richardson J.A, Bassel-Duby R, Olson E.N. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15: 261-271, 2008.
79. Wang S, Wang L, Zhu T, Gao X, Li J, Wu Y, Zhu H. Improvement of tissue preparation for laser capture microdissection: application for cell type-specific miRNA expression profiling in colorectal tumors. BMC Genomics 11: 163, 2010.
80. Warsch J.R, Wright C.B. Stroke: hyperlipidemia and cerebral small-vessel disease. Nat Rev Neurol 6: 307-308, 2010.
81. Watson K.E, Peters Harmel A.L, Matson G. Atherosclerosis in type 2 diabetes mellitus: the role of insulin resistance. J Cardiovasc Pharmacol Ther 8: 253-260, 2003.
82. Weber M, Baker M.B, Moore J.P, Searles C.D. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 393: 643-648, 2010.
83. White H.D, Simes R.J, Anderson N.E, Hankey G.J, Watson J.D, Hunt D, Colquhoun D.M, Glasziou P, MacMahon S, Kirby A.C, West M.J, Tonkin A.M. Pravastatin therapy and the risk of stroke. N Engl J Med 343: 317-326, 2000.
84. Wiggins J.F, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, Bader AG. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 70: 5923-5930, 2010.
85. Witwer K.W, Sisk J.M, Gama L, Clements J.E. MicroRNA regulation of IFN-beta protein expression: rapid and sensitive modulation of the innate immune response. J Immunol 184: 2369-2376, 2010.
86. Xu C.C, Han W.Q, Xiao B, Li N.N, Zhu D.L, Gao P.J. [Differential expression of microRNAs in the aorta of spontaneously hypertensive rats.]. Sheng Li Xue Bao 60: 553-560, 2008.
87. Yin K.J, Deng Z, Hamblin M, Xiang Y, Huang H, Zhang J, Jiang X, Wang Y, Chen Y.E. Peroxisome proliferator-activated receptor delta regulation of miR-15a in ischemia-induced cerebral vascular endothelial injury. J Neurosci 30: 6398-6408, 2010.
88. Yin K.J, Deng Z, Huang H, Hamblin M, Xie C, Zhang J, Chen YE. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 38: 17-26, 2010.
89. Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E, Shah A, Willeit J, Mayr M. Plasma microRNA profiling reveals loss of endothelial MiR-126 and other microRNAs in type 2 diabetes. Circ Res 107: 810-817, 2010.
90. Zhang H.X, Du G.H, Zhang J.T. Ischemic pre-conditioning preserves brain mitochondrial functions during the middle cerebral artery occlusion in rat. Neurol Res 25: 471-476, 2003.