An antagomir to microRNA let7f promotes neuroprotection in an ischemic stroke model

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Selvamani, Amutha ^a   Sathyan, Pratheesh ^a   Miranda, Rajesh C ^a   Sohrabji, Farida ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICRORNA; MICRORNA LET7F; MICRORNA LET7F ANTAGOMIR; MICRORNA MIR1; MICRORNA MIR1 ANTAGOMIR; NEUROPROTECTIVE AGENT; SEX HORMONE; SOMATOMEDIN C; UNCLASSIFIED DRUG; MIRN1 MICRORNA, RAT; MIRNLET7 MICRORNA, RAT;

3' UNTRANSLATED REGION; ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFICACY; FEMALE; GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE SILENCING; GENE TARGETING; GENETIC ANALYSIS; INSULIN LIKE GROWTH FACTOR 1 GENE; MALE; MICROGLIA; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SENSORIMOTOR INTEGRATION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL BEHAVIOR; CHEMISTRY; DISEASE MODEL; DRUG ANTAGONISM; GENETICS; ISCHEMIA; METABOLISM; RAT; REPERFUSION INJURY; STROKE;

ANIMALIA; RATTUS;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; ISCHEMIA; MALE; MICROGLIA; MICRORNAS; NEUROPROTECTIVE AGENTS; RATS; REPERFUSION INJURY; SEX FACTORS; STROKE;

EID: 84857683479     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032662     Document Type: Article

References (79)

1. Bushnell CD, (2008) Stroke in women: risk and prevention throughout the lifespan. Neurol Clin 26: 1161-1176.
2. Lisabeth LD, Brown DL, Morgenstern LB, (2006) Barriers to intravenous tissue plasminogen activator for acute stroke therapy in women. Gend Med 3: 270-278.
3. Ambros V, (2004) The functions of animal microRNAs. Nature 431: 350-355.
4. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
5. Kloosterman WP, Plasterk RH, (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-450.
6. Soifer HS, Rossi JJ, Saetrom P, (2007) MicroRNAs in disease and potential therapeutic applications. Mol Ther 15: 2070-2079.
7. Kocerha J, Kauppinen S, Wahlestedt C, (2009) microRNAs in CNS disorders. Neuromolecular Med 11: 162-172.
8. 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.
9. 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.
10. 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.
11. Zeng L, Liu J, Wang Y, Wang L, Weng S, et al. (2011) MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front Biosci (Elite Ed) 3: 1265-1272.
12. Yin KJ, Deng Z, Huang HR, Hamblin M, Xie CQ, et al. (2010) miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 38: 17-26.
13. Schwab S, Spranger M, Krempien S, Hacke W, Bettendorf M, (1997) Plasma insulin-like growth factor I and IGF binding protein 3 levels in patients with acute cerebral ischemic injury. Stroke 28: 1744-1748.
14. Laughlin GA, Barrett-Connor E, Criqui MH, Kritz-Silverstein D, (2004) The prospective association of serum insulin-like growth factor I (IGF-I) and IGF-binding protein-1 levels with all cause and cardiovascular disease mortality in older adults: the Rancho Bernardo Study. J Clin Endocrinol Metab 89: 114-120.
15. Johnsen SP, Hundborg HH, Sorensen HT, Orskov H, Tjonneland A, et al. (2005) Insulin-like growth factor (IGF) I,-II, and IGF binding protein-3 and risk of ischemic stroke. J Clin Endocrinol Metab 90: 5937-5941.
16. Gluckman P, Klempt N, Guan J, Mallard C, Sirimanne E, et al. (1992) A role for IGF-1 in the rescue of CNS neurons following hypoxic-ischemic injury. Biochem Biophys Res Commun 182: 593-599.
17. Liu XF, Fawcett JR, Hanson LR, Frey WH II, (2004) The window of opportunity for treatment of focal cerebral ischemic damage with noninvasive intranasal insulin-like growth factor-I in rats. J Stroke Cerebrovasc Dis 13: 16-23.
18. Johnston BM, Mallard EC, Williams CE, Gluckman PD, (1996) Insulin-like growth factor-1 is a potent neuronal rescue agent after hypoxic-ischemic injury in fetal lambs. J Clin Invest 97: 300-308.
19. Guan J, Bennet L, George S, Wu D, Waldvogel HJ, et al. (2001) Insulin-like growth factor-1 reduces postischemic white matter injury in fetal sheep. J Cereb Blood Flow Metab 21: 493-502.
20. Yan YP, Sailor KA, Vemuganti R, Dempsey RJ, (2006) Insulin-like growth factor-1 is an endogenous mediator of focal ischemia-induced neural progenitor proliferation. Eur J Neurosci 24: 45-54.
21. Smith LE, (2005) IGF-1 and retinopathy of prematurity in the preterm infant. Biol Neonate 88: 237-244.
22. Wang JM, Hayashi T, Zhang WR, Sakai K, Shiro Y, et al. (2000) Reduction of ischemic brain injury by topical application of insulin-like growth factor-I after transient middle cerebral artery occlusion in rats. Brain Res 859: 381-385.
23. Bartke A, (2008) Impact of reduced insulin-like growth factor-1/insulin signaling on aging in mammals: novel findings. Aging Cell 7: 285-290.
24. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Greenwald D, et al. (1997) Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg 87: 724-730.
25. Dubal DB, Kashon ML, Pettigrew LC, Ren JM, Finklestein SP, et al. (1998) Estradiol protects against ischemic injury. J Cereb Blood Flow Metab 18: 1253-1258.
26. Rusa R, Alkayed NJ, Crain BJ, Traystman RJ, Kimes AS, et al. (1999) 17beta-estradiol reduces stroke injury in estrogen-deficient female animals. Stroke 30: 1665-1670.
27. Schabitz WR, Hoffmann TT, Heiland S, Kollmar R, Bardutzky J, et al. (2001) Delayed neuroprotective effect of insulin-like growth factor-i after experimental transient focal cerebral ischemia monitored with mri. Stroke 32: 1226-1233.
28. Lin S, Fan LW, Rhodes PG, Cai Z, (2009) Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats. Exp Neurol 217: 361-370.
29. Selvamani A, Sohrabji F, (2010a) Reproductive age modulates the impact of focal ischemia on the forebrain as well as the effects of estrogen treatment in female rats. Neurobiol Aging 31 (9): 1618-28.
30. Selvamani A, Sohrabji F, (2010b) The neurotoxic effects of estrogen on ischemic stroke in older female rats is associated with age-dependent loss of insulin-like growth factor-1. J Neurosci 30: 6852-6861.
31. Borasio GD, Robberecht W, Leigh PN, Emile J, Guiloff RJ, et al. (1998) A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group. Neurology 51: 583-586.
32. Trojan LA, Kopinski P, Wei MX, Ly A, Glogowska A, et al. (2002) IGF-I: from diagnostic to triple-helix gene therapy of solid tumors. Acta Biochim Pol 49: 979-990.
33. Smith J, Axelrod D, Singh B, Kleinberg D, (2011) Prevention of breast cancer: the case for studying inhibition of IGF-1 actions. Ann Oncol 22 (Suppl 1): i50-52.
34. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
35. Elia L, Contu R, Quintavalle M, Varrone F, Chimenti C, et al. (2009) Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120: 2377-2385.
36. Granjon A, Gustin MP, Rieusset J, Lefai E, Meugnier E, et al. (2009) The microRNA signature in response to insulin reveals its implication in the transcriptional action of insulin in human skeletal muscle and the role of a sterol regulatory element-binding protein-1c/myocyte enhancer factor 2C pathway. Diabetes 58: 2555-2564.
37. Lu L, Katsaros D, de la Longrais IA, Sochirca O, Yu H, (2007) Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Res 67: 10117-10122.
38. Mongroo PS, Noubissi FK, Cuatrecasas M, Kalabis J, King CE, et al. (2011) IMP-1 displays cross-talk with K-Ras and modulates colon cancer cell survival through the novel proapoptotic protein CYFIP2. Cancer Res 71: 2172-2182.
39. Reid JG, Nagaraja AK, Lynn FC, Drabek RB, Muzny DM, et al. (2008) Mouse let-7 miRNA populations exhibit RNA editing that is constrained in the 5′-seed/cleavage/anchor regions and stabilize predicted mmu-let-7a:mRNA duplexes. Genome Res 18: 1571-1581.
40. 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.
41. Yu XY, Song YH, Geng YJ, Lin QX, Shan ZX, et al. (2008) Glucose induces apoptosis of cardiomyocytes via microRNA-1 and IGF-1. Biochem Biophys Res Commun 376: 548-552.
42. Hua Y, Zhang Y, Ren J, (2011) IGF-1 Deficiency Resists Cardiac Hypertrophy and Myocardial Contractile Dysfunction: Role of microRNA-1 and microRNA-133a. J Cell Mol Med.
43. Roush S, Slack FJ, (2008) The let-7 family of microRNAs. Trends Cell Biol 18: 505-516.
44. Biernaskie J, Corbett D, Peeling J, Wells J, Lei H, (2001) A serial MR study of cerebral blood flow changes and lesion development following endothelin-1-induced ischemia in rats. Magn Reson Med 46: 827-830.
45. Makeyev EV, Zhang J, Carrasco MA, Maniatis T, (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27: 435-448.
46. Rizk NN, Myatt-Jones J, Rafols J, Dunbar JC, (2007) Insulin like growth factor-1 (IGF-1) decreases ischemia-reperfusion induced apoptosis and necrosis in diabetic rats. Endocrine 31: 66-71.
47. Takane K, Fujishima K, Watanabe Y, Sato A, Saito N, et al. (2010) Computational prediction and experimental validation of evolutionarily conserved microRNA target genes in bilaterian animals. BMC Genomics 11: 101.
48. Siegel C, Turtzo C, McCullough LD, (2010) Sex differences in cerebral ischemia: possible molecular mechanisms. J Neurosci Res 88: 2765-2774.
49. Renolleau S, Fau S, Goyenvalle C, Charriaut-Marlangue C, (2007) 'Sex, neuroprotection, and neonatal ischemia'. Dev Med Child Neurol 49: 477; author reply 477-478.
50. Liu F, Li Z, Li J, Siegel C, Yuan R, et al. (2009) Sex differences in caspase activation after stroke. Stroke 40: 1842-1848.
51. Hagberg H, Dammann O, Mallard C, Leviton A, (2004) Preconditioning and the developing brain. Semin Perinatol 28: 389-395.
52. Li J, McCullough LD, (2009) Sex differences in minocycline-induced neuroprotection after experimental stroke. J Cereb Blood Flow Metab 29: 670-674.
53. Colton CA, (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4: 399-418.
54. O'Donnell SL, Frederick TJ, Krady JK, Vannucci SJ, Wood TL, (2002) IGF-I and microglia/macrophage proliferation in the ischemic mouse brain. Glia 39: 85-97.
55. Kitamura Y, Takata K, Inden M, Tsuchiya D, Yanagisawa D, et al. (2004) Intracerebroventricular injection of microglia protects against focal brain ischemia. J Pharmacol Sci 94: 203-206.
56. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J, (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27: 2596-2605.
57. Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M, (2005) Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol Cell Neurosci 29: 381-393.
58. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, et al. (2006) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31: 149-160.
59. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O, (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100: 13632-13637.
60. Monje ML, Toda H, Palmer TD, (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
61. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
62. Nimmerjahn A, Kirchhoff F, Helmchen F, (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
63. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J, (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29: 3974-3980.
64. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105.
65. Bhat-Nakshatri P, Wang G, Collins NR, Thomson MJ, Geistlinger TR, et al. (2009) Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res 37: 4850-4861.
66. Budhu A, Ji J, Wang XW, (2010) The clinical potential of microRNAs. J Hematol Oncol 3: 37.
67. Wang G, van der Walt JM, Mayhew G, Li YJ, Zuchner S, et al. (2008) Variation in the miRNA-433 binding site of FGF20 confers risk for Parkinson disease by overexpression of alpha-synuclein. Am J Hum Genet 82: 283-289.
68. Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, et al. (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci USA 105: 6415-6420.
69. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, et al. (2007) A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317: 1220-1224.
70. Wang S, van der Walt JM, Mayhew G, Li YJ, Zuchner S, et al. (2008) The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15: 261-271.
71. Johnson R, Zuccato C, Belyaev ND, Guest DJ, Cattaneo E, et al. (2008) A microRNA-based gene dysregulation pathway in Huntington's disease. Neurobiol Dis 29: 438-445.
72. Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL, (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci 28: 14341-14346.
73. Beveridge NJ, Tooney PA, Carroll AP, Gardiner E, Bowden N, et al. (2008) Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum Mol Genet 17: 1156-1168.
74. Hutchison ER, Okun E, Mattson MP, (2009) The therapeutic potential of microRNAs in nervous system damage, degeneration, and repair. Neuromolecular Med 11: 153-161.
75. Paxinos G, Watson C, Pennisi M, Topple A, (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13: 139-143.
76. Krützfeldt J, Kuwajima S, Braich R, Rajeev KG, Pena J, et al. (2007) Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res 35: 2885-2892.
77. Woodlee MT, Asseo-Garcia AM, Zhao X, Liu SJ, Jones TA, et al. (2005) Testing forelimb placing "across the midline" reveals distinct, lesion-dependent patterns of recovery in rats. Exp Neurol 191: 310-317.
78. Sayeed I, Wali B, Stein DG, (2007) Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Restor Neurol Neurosci 25: 151-159.
79. Johnson AB, Sohrabji F, (2005) Estrogen's effects on central and circulating immune cells vary with reproductive age. Neurobiol Aging 26: 1365-1374.