MicroRNAs Involved in Regulating Spontaneous Recovery in Embolic Stroke Model

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Liu, Fu Jia ^a   Lim, Kai Ying ^a   Kaur, Prameet ^a   Sepramaniam, Sugunavathi ^a   Armugam, Arunmozhiarasi ^a   Wong, Peter Tsun Hon ^a   Jeyaseelan, Kandiah ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 142 3P; MICRORNA 142 5P; MICRORNA 146; MICRORNA 196A; MICRORNA 196B; MICRORNA 196C; MICRORNA 206; MICRORNA 21; MICRORNA 224; MICRORNA 290; MICRORNA 291A 5P; MICRORNA 30C 1; MICRORNA 324 3P; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN TISSUE; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CONVALESCENCE; DISEASE COURSE; EMBOLIC STROKE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; MALE; MICROARRAY ANALYSIS; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REPERFUSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL CULTURE; COMPLICATION; DISEASE MODEL; EMBOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STROKE; VALIDATION STUDY; WISTAR RAT;

ANIMALIA; ERINACEIDAE; RODENTIA;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EMBOLISM; MALE; MICE; MICRORNAS; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; STROKE; TRANSCRIPTOME;

EID: 84879156930     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066393     Document Type: Article

References (86)

1. Wardlaw JM, Warlow CP, Counsell C, (1997) Systematic review of evidence on thrombolytic therapy for acute ischaemic stroke. Lancet 350: 607-614.
2. Cramer SC, Riley JD, (2008) Neuroplasticity and brain repair after stroke. Curr Opin Neurol 21: 76-82.
3. Wightman B, Ha I, Ruvkun G, (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.
4. Jeyaseelan K, Lim KY, Armugam A, (2008) MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 39: 959-966.
5. Lim KY, Chua JH, Tan JR, Swaminathan P, Sepramaniam S, et al. (2010) MicroRNAs in Cerebral Ischemia. Translational Stroke Research 1: 287-303.
6. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, et al. (2010) Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30: 92-101.
7. Dharap A, Bowen K, Place R, Li LC, Vemuganti R, (2009) Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 29: 675-687.
8. Tan KS, Armugam A, Sepramaniam S, Lim KY, Setyowati KD, et al. (2009) Expression profile of MicroRNAs in young stroke patients. PLoS One 4: e7689.
9. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR, (1997) A rat model of focal embolic cerebral ischemia. Brain Res 766: 83-92.
10. Armugam A, Cher CD, Lim K, Koh DC, Howells DW, et al. (2009) A secretory phospholipase A2-mediated neuroprotection and anti-apoptosis. BMC Neurosci 10: 120.
11. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, et al. (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab. 10: 290-3.
12. Lin TN, He YY, Wu G, Khan M, Hsu CY, (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke. 24: 117-21.
13. Longa EZ, Weinstein PR, Carlson S, Cummins R, (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91.
14. Karolina DS, Armugam A, Tavintharan S, Wong MT, Lim SC, et al. (2011) MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus. PLoS One 6: e22839.
15. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-10.
16. Hirai S, Banba Y, Satake T, Ohno S, (2011) Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-Jun N-terminal kinase pathway. J Neurosci 31: 6468-6480.
17. Ziu M, Fletcher L, Rana S, Jimenez DF, Digicaylioglu M, (2011) Temporal differences in microRNA expression patterns in astrocytes and neurons after ischemic injury. PLoS One 6: e14724.
18. Sepramaniam S, Armugam A, Lim KY, Karolina DS, Swaminathan P, et al. (2010) MicroRNA 320a functions as a novel endogenous modulator of aquaporins 1 and 4 as well as a potential therapeutic target in cerebral ischemia. J Biol Chem 285: 29223-30.
19. Nakayama H, Jorgensen H, Raaschou H, Olsen T, (1994) Recovery of upper extremity function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil 75: 394-398.
20. Pedersen PM, Jørgensen HS, Nakayama H, Raaschou HO, Olsen TS, (1995) Aphasia in acute stroke: incidence, determinants, and recovery. Ann Neurol 38: 659-666.
21. Zhang ZG, Zhang L, Jiang Q, Zhang R, Davies K, et al. (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106: 829-838.
22. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA, (2001) Collateral growth and angiogenesis around cortical stroke. Stroke 32: 2179-2184.
23. Nudo RJ, (2007) Postinfarct cortical plasticity and behavioral recovery. Stroke 38: 840-845.
24. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, et al. (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533.
25. Lu XC, Williams AJ, Yao C, Berti R, Hartings JA, et al. (2004) Microarray analysis of acute and delayed gene expression profile in rats after focal ischemic brain injury and reperfusion. J Neurosci Res 77: 843-57.
26. Buller B, Liu X, Wang X, Zhang RL, Zhang L, et al. (2010) MicroRNA-21 protects neurons from ischemic death. FEBS J 277: 4299-4307.
27. Zhang L, Chopp M, Liu X, Teng H, Tang T, et al. (2012) Combination therapy with VELCADE and tissue plasminogen activator is neuroprotective in aged rats after stroke and targets microRNA-146a and the toll-like receptor signaling pathway. Arterioscler Thromb Vasc Biol 32: 1856-1864.
28. Li H, Huang J, Du W, Jia C, Yao H, et al. (2012) TRPC6 inhibited NMDA receptor activities and protected neurons from ischemic excitotoxicity. J Neurochem 123: 1010-8.
29. Li P, Hu X, Gan Y, Gao Y, Liang W, et al. (2011) Mechanistic insight into DNA damage and repair in ischemic stroke: exploiting the base excision repair pathway as a model of neuroprotection. Antioxid Redox Signal 14: 1905-1918.
30. Schwartz-Bloom RD, Sah R, (2001) gamma-Aminobutyric acid (A) neurotransmission and cerebral ischemia. J Neurochem 77: 353-371.
31. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, et al. (2004) Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24: 441-448.
32. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP, (1996) Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 10: 301-312.
33. Savage C, Das P, Finelli AL, Townsend SR, Sun CY, et al. (1996) Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factor beta pathway components. Proc Natl Acad Sci U S A 93: 790-794.
34. Artavanis-Tsakonas S, Rand MD, Lake RJ, (1999) Notch signaling: Cell fate control and signal integration in development. Science 284: 770-776.
35. Logan CY, Nusse R, (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
36. Gross CE, Bednar MM, Howard DB, Sporn MB, (1993) Transforming growth factor-beta 1 reduces infarct size after experimental cerebral ischemia in a rabbit model. Stroke 24: 558-562.
37. Pang L, Ye W, Che XM, Roessler BJ, Betz AL, et al. (2001) Reduction of inflammatory response in the mouse brain with adenoviral-mediated transforming growth factor-ss1 expression. Stroke 32: 544-552.
38. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, et al. (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442: 823-826.
39. Sims JR, Lee SW, Topalkara K, Qiu J, Xu J, et al. (2009) Sonic hedgehog regulates ischemia/hypoxia-induced neural progenitor proliferation. Stroke 40: 3618-3626.
40. Bambakidis NC, Petrullis M, Kui X, Rothstein B, Karampelas I, et al. (2012) Improvement of neurological recovery and stimulation of neural progenitor cell proliferation by intrathecal administration of Sonic hedgehog. J Neurosurg 116: 1114-1120.
41. Shruster A, Ben-Zur T, Melamed E, Offen D, (2012) Wnt signaling enhances neurogenesis and improves neurological function after focal ischemic injury. PLoS One 7: e40843.
42. Ferretti E, De Smaele E, Miele E, Laneve P, Po A, et al. (2008) Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J 27: 2616-2627.
43. Kefas B, Comeau L, Floyd DH, Seleverstov O, Godlewski J, et al. (2009) The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J Neurosci 29: 15161-15168.
44. Saydam O, Shen Y, Wurdinger T, Senol O, Boke E, et al. (2009) Downregulated microRNA-200a in meningiomas promotes tumor growth by reducing E-cadherin and activating the Wnt/beta-catenin signaling pathway. Mol Cell Biol 29: 5923-5940.
45. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, et al. (2009) miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res 104: 170-178.
46. Kato M, Putta S, Wang M, Yuan H, Lanting L, et al. (2009) TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 11: 881-889.
47. Yu Y, Kanwar SS, Patel BB, Oh PS, Nautiyal J, et al. (2012) MicroRNA-21 induces stemness by downregulating transforming growth factor beta receptor 2 (TGFβR2) in colon cancer cells. Carcinogenesis 33: 68-76.
48. Han L, Yue X, Zhou X, Lan FM, You G, et al. (2012) MicroRNA-21 expression is regulated by β-catenin/STAT3 pathway and promotes glioma cell invasion by direct targeting RECK. CNS Neurosci Ther 18: 573-583.
49. Krichevsky AM, Gabriely G, (2009) miR-21: a small multi-faceted RNA. J Cell Mol Med 13: 39-53.
50. Davis BN, Hilyard AC, Lagna G, Hata A, (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61.
51. Dey BK, Gagan J, Dutta A, (2011) miR-206 and miR-486 induce myoblast differentiation by downregulating Pax7. Mol Cell Biol. 31: 203-14.
52. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, et al. (2008) MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 27: 4373-4379.
53. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, et al. (2011) p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 4: ra71.
54. Hughes DP, (2009) How the NOTCH pathway contributes to the ability of osteosarcoma cells to metastasize. Cancer Treat Res 152: 479-496.
55. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, et al. (2010) MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 31: 1037-1044.
56. Hashimi ST, Fulcher JA, Chang MH, Gov L, Wang S, et al. (2009) MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114: 404-414.
57. Genovese G, Ergun A, Shukla SA, Campos B, Hanna J, et al. (2012) microRNA regulatory network inference identifies miR-34a as a novel regulator of TGF-β signaling in glioblastoma. Cancer Discov 2: 736-749.
58. Stecca B, Ruiz i Altaba A, (2009) A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers. EMBO J 28: 663-676.
59. Yang X, Feng M, Jiang X, Wu Z, Li Z, et al. (2009) miR-449a and miR-449b are direct transcriptional targets of E2F1 and negatively regulate pRb-E2F1 activity through a feedback loop by targeting CDK6 and CDC25A. Genes Dev 23: 2388-2393.
60. Lizé M, Pilarski S, Dobbelstein M, (2010) E2F1-inducible microRNA 449a/b suppresses cell proliferation and promotes apoptosis. Cell Death Differ 17: 452-458.
61. Franklin TJ, (1997) Therapeutic approaches to organ fibrosis. Int J Biochem Cell Biol 29: 79-89.
62. Macconi D, Tomasoni S, Romagnani P, Trionfini P, Sangalli F, et al. (2012) MicroRNA-324-3p Promotes Renal Fibrosis and Is a Target of ACE Inhibition. J Am Soc Nephrol 23: 1496-1505.
63. Wang B, Koh P, Winbanks C, Coughlan MT, McClelland A, et al. (2011) miR-200a Prevents renal fibrogenesis through repression of TGF-β2 expression. Diabetes 60: 280-287.
64. Dey N, Ghosh-Choudhury N, Kasinath BS, Choudhury GG, (2012) TGFβ-Stimulated MicroRNA-21 Utilizes PTEN to Orchestrate AKT/mTORC1 Signaling for Mesangial Cell Hypertrophy and Matrix Expansion. PLoS One 7: e42316.
65. Guo Y, Xiao L, Sun L, Liu F, (2012) Wnt/beta-catenin signaling: a promising new target for fibrosis diseases. Physiol Res 61: 337-346.
66. Doyle KP, Cekanaviciute E, Mamer LE, Buckwalter MS, (2010) TGFβ signaling in the brain increases with aging and signals to astrocytes and innate immune cells in the weeks after stroke. J Neuroinflamm 7: 62.
67. Jalali S, Ramanathan GK, Parthasarathy PT, Aljubran S, Galam L, et al. (2012) Mir-206 regulates pulmonary artery smooth muscle cell proliferation and differentiation. PLoS One. 7: e46808.
68. Li L, Sarver AL, Alamgir S, Subramanian S, (2012) Downregulation of microRNAs miR-1,-206 and-29 stabilizes PAX3 and CCND2 expression in rhabdomyosarcoma. Lab Invest. 92: 571-83.
69. Inose H, Ochi H, Kimura A, Fujita K, Xu R, et al. (2009) A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci U S A. 106: 20794-9.
70. Zhang T, Liu M, Wang C, Lin C, Sun Y, et al. (2011) Down-regulation of MiR-206 promotes proliferation and invasion of laryngeal cancer by regulating VEGF expression. Anticancer Res. 31: 3859-63.
71. Song G, Zhang Y, Wang L, (2009) MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J Biol Chem. 284: 31921-7.
72. Shan ZX, Lin QX, Fu YH, Deng CY, Zhou ZL, et al. (2009) Upregulated expression of miR-1/miR-206 in a rat model of myocardial infarction. Biochem Biophys Res Commun. 381: 597-601.
73. Liu W, D'Ercole JA, Ye P, (2011) Blunting type 1 insulin-like growth factor receptor expression exacerbates neuronal apoptosis following hypoxic/ischemic injury. BMC Neurosci. 12: 64.
74. Lee ST, Chu K, Jung KH, Kim JH, Huh JY, et al. (2012) miR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model. Ann Neurol. 72: 269-77.
75. Gibson CL, Gray LJ, Murphy SP, Bath PM, (2006) Estrogens and experimental ischemic stroke: a systematic review. J Cereb Blood Flow Metab. 26: 1103-1113.
76. Leivonen SK, Mäkelä R, Ostling P, Kohonen P, Haapa-Paananen S, et al. (2009) Protein lysate microarray analysis to identify microRNAs regulating estrogen receptor signaling in breast cancer cell lines. Oncogene. 28: 3926-36.
77. Wang R, Hu Y, Song G, Hao CJ, Cui Y, et al. (2012) MiR-206 regulates neural cells proliferation and apoptosis via Otx2. Cell Physiol Biochem. 29: 381-90.
78. Rhinn M, Dierich A, Shawlot W, Behringer RR, Le Meur M, et al. (1998) Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development 125: 845-856.
79. Li JY, Joyner AL, (2001) Otx2 and Gbx2 are required for refinement and not induction of mid-hindbrain gene expression. Development. 128: 4979-4991.
80. Torero Ibad R, Rheey J, Mrejen S, Forster V, Picaud S, et al. (2011) Otx2 promotes the survival of damaged adult retinal ganglion cells and protects against excitotoxic loss of visual acuity in vivo. J Neurosci 31: 5495-5503.
81. Lo CW, Cohen MF, Huang GY, Lazatin BO, Patel N, et al. (1997) Cx43 gap junction gene expression and gap junctional communication in mouse neural crest cells. Dev Genet. 20: 119-32.
82. Huang GY, Cooper ES, Waldo K, Kirby ML, Gilula NB, et al. (1998) Gap junction-mediated cell-cell communication modulates mouse neural crest migration. J Cell Biol. 143: 1725-34.
83. Blanc EM, Bruce-Keller AJ, Mattson MP, (1998) Astrocytic gap junctional communication decreases neuronal vulnerability to oxidative stress induced disruption of Ca2+ homeostasis and cell death. J Neurochem. 70: 958-970.
84. Ozog MA, Siushansian R, Naus CCG, (2002) Blocking gap junctions increases glutamate cytotoxicity. J Neuropathol Exp Neurol. 61: 132-141.
85. Siushansian R, Bechberger JF, Cechetto DF, Hachinski VC, Naus CCG, (2001) Connexin43 null mutation increases infarct size after stroke. J Comp Neurol. 440: 387-394.
86. Nakase T, Fushiki S, Naus CC, (2003) Astrocytic gap junctions composed of connexin 43 reduce apoptotic neuronal damage in cerebral ischemia. Stroke. 34: 1987-93.