MicroRNA responses to focal cerebral ischemia in male and female mouse brain

Frontiers in Molecular Neuroscience

Volumn 7, Issue FEB, 2014, Pages

  Lusardi, Theresa A ^a   Murphy, Stephanie J ^a   Phillips, Jay ^b   Chen, Yingxin ^b   Davis, Catherine M ^b   Young, Jennifer M ^b   Thompson, Simon J ^a   Saugstad, Julie A ^b  

^a LEGACY RESEARCH   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Array analysis; Cerebral ischemia; microRNA; Pathway analysis; qRT PCR; Sex differences; Stroke

Indexed keywords

COMPLEMENTARY DNA; MICRORNA; MICRORNA 1187; MICRORNA 1224; MICRORNA 125B; MICRORNA 145; MICRORNA 15B; MICRORNA 296; MICRORNA 509; MICRORNA 669; MICRORNA 675; MICRORNA 682; MICRORNA 686; MICRORNA 697; MICRORNA 770; MICRORNA 883A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DNA SEQUENCE; GENOME ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MICROARRAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

EID: 84894060837     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2014.00011     Document Type: Article

References (47)

1. Ambros, V. (2004). The functions of animal micrornas. Nature 431, 350-355. doi: 10.1038/nature02871
2. Appelros, P., Stegmayr, B., and Terent, A. (2009). Sex differences in stroke epidemiology: a systematic review. Stroke 40,1082-1090. doi: 10.1161/STR0KEAHA.108.540781.
3. Banerjee, A., Wang, J., Bodhankar, S., Vandenbark, A. A., Murphy, S. J., and Offner, H. (2013). Phenotypic changes in immune cell subsets reflect increased infarct volume in male vs. female mice. Trans. Stroke Res. 4, 554-563. doi: 10.1007/s12975-013-0268-z
4. Bushnell, C. D. (2008). Stroke and the female brain. Nat. Clin. Pract. Neurol. 4, 22-33. doi: 10.1038/ncpneuro0686
5. Cambronne, X. A., Shen, R., Auer, P. L., and Goodman, R. H. (2012). Capturing microrna targets using an rna-induced silencing complex (risc)-trap approach. Proc. Natl. Acad. Sci. U.S.A. 109, 20473-20478. doi: 10.1073/pnas.1218887109
6. Chen, Y., Bodhankar, S., Murphy, S. J., Vandenbark, A. A., Alkayed, N. J., Offner, H. (2012). Intrastriatal B-cell administration limits infarct size after stroke in B-cell deficient mice. Metab. Brain Dis. 27, 487-493. doi: 10.1007/s11011-012-9317-7
7. Cheng, J., and Hurn, P. D. (2010). Sex shapes experimental ischemic brain injury. Steroids 75, 754-759. doi: 10.1016/j.steroids.2009.10.014.
8. Chua, J. H., Armugam, A., and Jeyaseelan, K. (2009). Micrornas: biogenesis, function and applications. Curr. Opin. Mol. Ther.11,189-199.
9. Dharap, A., Bowen, K., Place, R., Li, L. C., and Vemuganti, R. (2009). Transient focal ischemia induces extensive temporal changes in rat cerebral micrornaome. J. Cereb. Blood Flow Metab. 29, 675-687. doi: 10.1038/jcbfm.2008.157.
10. Doench, J. G., and Sharp, P. A. (2004). Specificity of microrna target selection in translational repression. GenesDev.18, 504-511. doi: 10.1101/gad.1184404.
11. Eulalio, A., Mano, M., Dal Ferro, M., Zentilin, L., Sinagra, G., Zacchigna, S., et al. (2012). Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492, 376-381. doi: 10.1038/nature11739.
12. Fasanaro, P., Greco, S., Ivan, M., Capogrossi, M. C., and Martelli, F. (2010). Microrna: emerging therapeutic targets in acute ischemic diseases. Pharmacol. Ther. 125, 92-104. doi: 10.1016/j.pharmthera.2009.10.003.
13. Feng, W., and Feng, Y. (2011). Micrornas in neural cell development and brain diseases. Sci. ChinaLifeSci. 54,1103-1112. doi: 10.1007/s11427-011-4249-8.
14. Git, A., Dvinge, H., Salmon-Divon, M., Osborne, M., Kutter, C., Hadfield, J., et al. (2010). Systematic comparison of microarray profiling, real-time pcr, and next-generation sequencing technologies for measuring differential microrna expression. RNA 16,991-1006. doi: 10.1261/rna.1947110.
15. Guarnieri, D. J., and DiLeone, R. J. (2008). Micrornas: a new class of gene regulators. Ann. Med. 40,197-208. doi: 10.1080/07853890701771823.
16. Ilnytskyy, Y., Zemp, F. J., Koturbash, I., and Kovalchuk, O. (2008). Altered microrna expression patterns in irradiated hematopoietic tissues suggest a sex- specific protective mechanism. Biochem. Biophys. Res. Commun. 377,41-45. doi: 10.1016/j.bbrc.2008.09.080.
17. Jeyaseelan, K., Lim, K. Y., and 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. doi: 10.1161/strokeaha.107.500736.
18. Johnsen, D., and Murphy, S. J. (2011). Isoflurane preconditioning protects neurons from male and female mice against oxygen and glucose deprivation and is modulated by estradiol only in neurons from female mice. Neuroscience 199, 368-374. doi: 10.1016/j.neuroscience.2011.09.053
19. Kitano, H., Young, J. M., Cheng, J., Wang, L., Hurn, P. D., and Murphy, S. J. (2007). Gender-specific response to isoflurane preconditioning in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 27,1377-1386. doi: 10.1038/sj.jcbfm.9600444.
20. Koerner, I., Murphy, S. J., and Hurn, P. D. (2007). "Gender, sex steroids, and cerebral ischemic pathobiology," in Acute Ischemic Injury and Repair in the Nervous System, ed P. Chan (New York, NY: Kluwer Academic/Plenum Publishers), 186-207.
21. Koturbash, I., Zemp, F., Kolb, B., and Kovalchuk, O. (2011). Sex-specific radiation-induced micrornaome responses in the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat. Res. 722, 114-118. doi: 10.1016/j.mrgentox.2010.05.007.
22. Lang, J. T., and McCullough, L. D. (2008). Pathways to ischemic neuronal cell death: are sex differences relevant? J. Transl. Med. 6, 33. doi: 10.1186/1479-5876-6-33.
23. Li, H., Pin, S., Zeng, Z., Wang, M. M., Andreasson, K. A., and McCullough, L. D. (2005). Sex differences in cell death. Ann. Neurol. 58, 317-321. doi: 10.1002/ana.20538
24. Liu, D. Z., Tian, Y., Ander, B. P., Xu, H., Stamova, B. S., Zhan, X., 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. doi: 10.1038/jcbfm.2009.186.
25. Liu, M., Hurn, P. D., Roselli, C. E., andAlkayed, N. J. (2007). Role ofp450 aromatase in sex-specific astrocytic cell death. J. Cereb. Blood Flow Metab. 27,135-141. doi: 10.1038/sj.jcbfm.9600331.
26. Liu, M., Oyarzabal, E. A., Yang, R., Murphy, S. J., and Hurn, P. D. (2008). A novel method for assessing sex-specific and genotype-specific response to injury in astrocyte culture. J. Neurosci. Methods 171, 214-217. doi: 10.1016/j.jneumeth.2008.03.002.
27. Liu, X. S., Chopp, M., Zhang, R. L., and Zhang, Z. G. (2013). Micrornas in cerebral ischemia-induced neurogenesis. J. Neuropathol. Exp. Neurol. 72, 718-722. doi: 10.1097/NEN.0b013e31829e4963.
28. Lusardi, T. A., Farr, C. D., Faulkner, C. L., Pignataro, G., Yang, T., Lan, J., et al. (2010). Ischemic preconditioning regulates expression of micrornas and a predicted target, mecp2, in mouse cortex. J. Cereb. Blood Flow Metab. 30, 744-756. doi: 10.1038/jcbfm.2009.253.
29. Lusardi, T. A., Thompson, S. J., Macdonald, I. C., Lan, J. Q., Theofilas, P., and Saugstad, J. A. (2012). Effect of (s)-3,5-dhpg on microrna expression in mouse brain. Exp. Neurol. 235, 497-507. doi: 10.1016/j.expneurol.2012.01.018.
30. Mi, H., Muruganujan, A., Casagrande, J. T., and Thomas, P. D. (2013). Large-scale gene function analysis with the panther classification system. Nat. Protoc. 8, 1551-1566. doi: 10.1038/nprot.2013.092.
31. Mi, H., and Thomas, P. (2009). Panther pathway: an ontology-based pathway database coupled with data analysis tools. Methods Mol. Biol. 563, 123-140. doi: 10.1007/978-1-60761-175-2-7.
32. Murchison, E. P., and Hannon, G. J. (2004). MiRNAs on the move: miRNA biogenesis and the rnai machinery. Curr. Opin. Cell Biol. 16, 223-229. doi: 10.1016/j.ceb.2004.04.003.
33. Murphy, S. J., McCullough, L. D., and Smith, J. M. (2004). Stroke in the female: role of biological sex and estrogen. ILAR J. 45, 147-159. doi: 10.1093/ilar.45.2.147.
34. Niwa, R., and Slack, F. J. (2007). The evolution of animal microrna function. Curr. Opin. Genet. Dev.17,145-150. doi: 10.1016/j.gde.2007.02.004.
35. Ouyang, Y. B., Stary, C. M., Yang, G. Y., and Giffard, R. (2013). Micrornas: innovative targets for cerebral ischemia and stroke. Curr. Drug Targets 14, 90-101. doi: 10.2174/138945013804806424
36. Ovbiagele, B., Goldstein, L. B., Higashida, R. T., Howard, V. J., Johnston, S. C., Khavjou, O. A., et al. (2013). Forecasting the future of stroke in the united states: a policy statement from the american heart association and american stroke association. Stroke 44, 2361-2375. doi: 10.1161/STR.0b013e31829 734f2
37. Persky, R. W., Turtzo, L. C., and McCullough, L. D. (2010). Stroke in women: disparities and outcomes. Curr. Cardiol. Rep. 12, 6-13. doi: 10.1007/s11886-009- 0080-2
38. Reeves, M. J., Bushnell, C. D., Howard, G., Gargano, J. W., Duncan, P. W., Lynch, G., et al. (2008). Sex differences in stroke: epidemiology, clinical presentation, medical care, and outcomes. Lancet Neurol. 7, 915-926. doi: 10.1016/S1474-4422(08)70193-5
39. Rink, C., and Khanna, S. (2011). MicroRNA in ischemic stroke etiology and pathology. Physiol. Genomics. 43, 521-528. doi: 10.1152/physiolgenomics.00158.2010.
40. Saini, M., and Shuaib, A. (2008). Stroke in women. Recent Pat. Cardiovasc. Drug Discov. 3,209-221. doi: 10.2174/157489008786264032.
41. Saugstad, J. A. (2010). Micrornas as effectors of brain function with roles in ischemia and injury, neuroprotection, and neurodegeneration. J. Cereb. Blood Flow Metab. 30,1564-1576. doi: 10.1038/jcbfm.2010.101.
42. Siegel, C., Li, J., Liu, F., Benashski, S. E., and McCullough, L. D. (2011). Mir-23a regulation of x-linked inhibitor of apoptosis (xiap) contributes to sex differences in the response to cerebral ischemia. Proc. Natl. Acad. Sci. U.S.A. 108, 11662-11667. doi: 10.1073/pnas.1102635108.
43. Siegel, C., Turtzo, C., and McCullough, L. D. (2010). Sex differences in cerebral ischemia: possible molecular mechanisms. J. Neurosci. Res. 88, 2765-2774. doi: 10.1002/jnr.22406
44. Tan, J. R., Koo, Y. X., Kaur, P., Liu, F., Armugam, A., Wong, P. T., et al. (2011). Micrornas in stroke pathogenesis. Curr. Mol. Med.11,76-92.
45. Towfighi, A., Markovic, D., and Ovbiagele, B. (2013). Sex differences in revascularization interventions after acute ischemic stroke. J. Stroke Cerebrovasc. Dis. 22, e347-e353. doi: 10.1016/j.jstrokecerebrovasdis.2013.03.018.
46. Vagnerova, K., Koerner, I. P., and Hurn, P. D. (2008). Gender and the injured brain. Anesth. Analg. 107, 201-214. doi: 10.1213/ane.0b013e31817326a5.
47. Vejnar, C. E., Blum, M., and Zdobnov, E. M. (2013). Mirmap web: comprehensive microrna target prediction online. Nucleic Acids Res. 41, W165-W168. doi: 10.1093/nar/gkt430