CpG preconditioning regulates miRNA expression that modulates genomic reprogramming associated with neuroprotection against ischemic injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 2, 2015, Pages 257-266

  Vartanian, Keri B ^a   Mitchell, Hugh D ^b   Stevens, Susan L ^a   Conrad, Valerie K ^a   McDermott, Jason E ^b   Stenzel Poore, Mary P ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

microRNA; neuroprotection; preconditioning; reprogramming; stroke

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; MICRORNA; SODIUM CHLORIDE; CPG-OLIGONUCLEOTIDE; IMMUNOLOGICAL ADJUVANT; NEUROPROTECTIVE AGENT; OLIGODEOXYRIBONUCLEOTIDE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE CONTROL; GENE MUTATION; GENE TARGETING; ISCHEMIC PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEAR REPROGRAMMING; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; STATISTICAL ANALYSIS; UPREGULATION; ANIMAL; BIOSYNTHESIS; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; STROKE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BRAIN ISCHEMIA; GENE EXPRESSION REGULATION; MALE; MICE; MICRORNAS; NEUROPROTECTIVE AGENTS; OLIGODEOXYRIBONUCLEOTIDES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STROKE;

EID: 84922337356     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.193     Document Type: Article

References (39)

1. Adeoye O, Hornung R, Khatri P, Kleindorfer D. Recombinant tissue-type plasminogen activator use for ischemic stroke in the United States: a doubling of treatment rates over the course of 5 years. Stroke 2011; 42: 1952-1955.
2. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009; 8: 398-412.
3. Stevens SL, Leung PY, Vartanian KB, Gopalan B, Yang T, Simon RP et al. Multiple preconditioning paradigms converge on interferon regulatory factor-dependent signaling to promote tolerance to ischemic brain injury. J Neurosci 2011; 31: 8456-8463.
4. Vartanian KB, Stevens SL, Marsh B, Williams-Karnesky RL, Lessov NS, Stenzel-Poore MP. LPS preconditioning redirects TLR signaling following stroke: TRIF-IRF3 plays a seminal role in mediating tolerance to ischemic injury. J Neuroinflammation 2011; 8: 140.
5. Dhodda VK, Sailor KA, Bowen KK, Vemuganti R. Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis. J Neurochem 2004; 89: 73-89.
6. Yenari MA, Liu J, Zheng Z, Vexler ZS, Lee JE, Giffard RG. Antiapoptotic and antiinflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci 2005; 1053: 74-83.
7. Kawahara N, Wang Y, Mukasa A, Furuya K, Shimizu T, Hamakubo T et al. Genomewide gene expression analysis for induced ischemic tolerance and delayed neuronal death following transient global ischemia in rats. J Cereb Blood Flow Metab 2004; 24: 212-223.
8. Meller R, Minami M, Cameron JA, Impey S, Chen D, Lan JQ et al. CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 2005; 25: 234-246.
9. Peng Z, Li J, Li Y, Yang X, Feng S, Han S et al. Downregulation of miR-181b in mouse brain following ischemic stroke induces neuroprotection against ischemic injury through targeting heat shock protein A5 and ubiquitin carboxyl-terminal hydrolase isozyme L1. J Neurosci Res 2013; 91: 1349-1362.
10. Yin KJ, Deng Z, Huang H, Hamblin M, Xie C, Zhang J et al. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 2010; 38: 17-26.
11. Lee ST, Chu K, Jung KH, Yoon HJ, Jeon D, Kang KM et al. MicroRNAs induced during ischemic preconditioning. Stroke 2010; 41: 1646-1651.
12. Lusardi TA, Farr CD, Faulkner CL, Pignataro G, Yang T, Lan J et al. Ischemic preconditioning regulates expression of microRNAs and a predicted target, MeCP2, in mouse cortex. J Cereb Blood Flow Metab 2010; 30: 744-756.
13. Bahjat FR, Williams-Karnesky RL, Kohama SG, West GA, Doyle KP, Spector MD et al. Proof of concept: pharmacological preconditioning with a Toll-like receptor agonist protects against cerebrovascular injury in a primate model of stroke. J Cereb Blood Flow Metab 2011; 31: 1229-1242.
14. Stevens SL, Ciesielski TM, Marsh BJ, Yang T, Homen DS, Boule JL et al. Toll-like receptor 9: a new target of ischemic preconditioning in the brain. J Cereb Blood Flow Metab 2008; 28: 1040-1047.
15. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30: 207-210.
16. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk - database: prediction of possible miRNA binding sites by 'walking' the genes of three genomes. J Biomed Inform 2011; 44: 839-847.
17. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, Cook SA et al. Editingdefective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 2006; 443: 50-55.
18. Stum M, McLaughlin HM, Kleinbrink EL, Miers KE, Ackerman SL, Seburn KL et al. An assessment of mechanisms underlying peripheral axonal degeneration caused by aminoacyl-tRNA synthetase mutations. Mol Cell Neurosci 2011; 46: 432-443.
19. Patel S, Huang YW, Reheman A, Pluthero FG, Chaturvedi S, Mukovozov IM et al. The cell motility modulator Slit2 is a potent inhibitor of platelet function. Circulation 2012; 126: 1385-1395.
20. Hamidi T, Cano CE, Grasso D, Garcia MN, Sandi MJ, Calvo EL et al. Nupr1-aurora kinase A pathway provides protection against metabolic stressmediated autophagic-associated cell death. Clin Cancer Res 2012; 18: 5234-5246.
21. Hamidi T, Cano CE, Grasso D, Garcia MN, Sandi MJ, Calvo EL et al. NUPR1 works against the metabolic stress-induced autophagy-associated cell death in pancreatic cancer cells. Autophagy 2013; 9: 95-97.
22. Cai J, Zhu Q, Zheng K, Li H, Qi Y, Cao Q et al. Co-localization of Nkx6.2 and Nkx2.2 homeodomain proteins in differentiated myelinating oligodendrocytes. Glia 2010; 58: 458-468.
23. Chen Z, Ge B, Hudson TJ, Rozen R. Microarray analysis of brain RNA in mice with methylenetetrahydrofolate reductase deficiency and hyperhomocysteinemia. Brain Res Gene Expr Patterns 2002; 1: 89-93.
24. Lapchak PA, Doyan S, Fan X, Woods CM. Synergistic effect of AJW200, a von Willebrand factor neutralizing antibody with low dose (0.9 mg/mg) thrombolytic therapy following embolic stroke in rabbits. J Neurol Neurophysiol 2013; 4: 146.
25. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, Leung PY et al. Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: a critical role for IRF3. J Neurosci 2009; 29: 9839-9849.
26. Nijboer CH, Heijnen CJ, Groenendaal F, May MJ, van Bel F, Kavelaars A. Strong neuroprotection by inhibition of NF-kappaB after neonatal hypoxia-ischemia involves apoptotic mechanisms but is independent of cytokines. Stroke 2008; 39: 2129-2137.
27. Jiang W, Zhang S, Fu F, Zhu H, Hou J. Inhibition of nuclear factor-kappaB by 6-Oacetyl shanzhiside methyl ester protects brain against injury in a rat model of ischemia and reperfusion. J Neuroinflammation 2010; 7: 55.
28. Vartanian KB, Stevens SL, Marsh BJ, Williams-Karnesky R, Lessov NS, Stenzel-Poore MP. LPS preconditioning redirects TLR signaling following stroke: TRIF-IRF3 plays a seminal role in mediating tolerance to ischemic injury. J Neuroinflammation 2011; 8: 140.
29. Lee YJ, Hallenbeck JM. Insights into cytoprotection from ground squirrel hibernation, a natural model of tolerance to profound brain oligaemia. Biochem Soc Trans 2006; 34: 1295-1298.
30. Lee YJ, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S et al. Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metab 2007; 27: 950-962.
31. Nathaniel TI. Brain-regulated metabolic suppression during hibernation: a neuroprotective mechanism for perinatal hypoxia-ischemia. Int J Stroke 2008; 3: 98-104.
32. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M et al. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 2003; 362: 1028-1037.
33. Iwakuma M, Anzai T, Kobayashi S, Ogata M, Kaneda Y, Ohno K et al. Antisense in vivo knockdown of synaptotagmin I and synapsin I by HVJ-liposome mediated gene transfer modulates ischemic injury of hippocampus in opposing ways. Neurosci Res 2003; 45: 285-296.
34. Greenberg DA, Jin K. Vascular endothelial growth factors (VEGFs) and stroke. Cell Mol Life Sci 2013; 70: 1753-1761.
35. Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci U S A 2000; 97: 10242-10247.
36. Tole S, Mukovozov IM, Huang YW, Magalhaes MA, Yan M, Crow MR et al. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J Leukoc Biol 2009; 86: 1403-1415.
37. Poppert H, Sadikovic S, Sander K, Wolf O, Sander D. Embolic signals in unselected stroke patients: prevalence and diagnostic benefit. Stroke 2006; 37: 2039-2043.
38. Gronberg NV, Johansen FF, Kristiansen U, Hasseldam H. Leukocyte infiltration in experimental stroke. J Neuroinflammation 2013; 10: 115.
39. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11: 597-610.