Demethylation of circulating estrogen receptor alpha gene in cerebral ischemic stroke

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Lin, Hsiu Fen ^a,b   Hsi, Edward ^a,b   Liao, Yi Chu ^c,d   Chhor, Brian ^e   Hung, Jessica ^f   Juo, Suh Hang H ^a,b   Lin, Ruey Tay ^a,b   Chiariotti, Lorenzo ^g  

^a KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e STANFORD UNIVERSITY   (United States)

^f University of Washington   (United States)

^g UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; GENOMIC DNA; ESTROGEN RECEPTOR ALPHA, HUMAN;

AGE DISTRIBUTION; ARTICLE; BRAIN ATHEROSCLEROSIS; BRAIN ISCHEMIA; CARDIOEMBOLIC STROKE; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; PROMOTER REGION; PYROSEQUENCING; QUANTITATIVE ANALYSIS; RISK ASSESSMENT; SEX DIFFERENCE; STROKE PATIENT; ADULT; AGED; CEREBROVASCULAR ACCIDENT; GENETICS; METABOLISM; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CPG ISLANDS; DNA METHYLATION; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MALE; MIDDLE AGED; SEX FACTORS; STROKE;

EID: 84947777471     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139608     Document Type: Article

References (35)

1. Marsh BJ, Williams-Karnesky RL, Stenzel-Poore MP (2009) Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 158:1007-1020. doi: 10.1016/j.neuroscience.2008.07.067 PMID: 18809468
2. Trendelenburg G, Dirnagl U. (2005) Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 50: 307-320. PMID: 15846804
3. Simpkins JW, Rajakumar G, Zhang Y.Q., Simpkins CE, Greenwald D, Yu CJ, 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. PMID: 9347981
4. Toung TJ, Traystman RJ, Hurn P.D. (1998) Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke 29:1666-1670. PMID: 9707210
5. Schreihofer DA, Ma Y. (2013) Estrogen receptors and ischemic neuroprotection: who, what, where, and when? Brain Res 1514:107-122. doi: 10.1016/j.brainres.2013.02.051 PMID: 23500634
6. Dubal DB, Zhu H, Yu J., Rau SW, Shughrue PJ, Merchenthaler I, et al (2001) Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci U S A 98:1952-1957. PMID: 11172057
7. Dubal DB, Rau SW, Shughrue P.J., Zhu H., Yu J, Cashion AB, et al (2006) Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death. Endocrinology 147:3076-3084. PMID: 16527848
8. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21. PMID: 11782440
9. Li LC, Chui R, Nakajima K., Oh BR, Au HC, Dahiya R. (2000) Frequent methylation of estrogen receptor in prostate cancer: correlation with tumor progression. Cancer Res 60: 702-706. PMID: 10676656
10. Post WS, Goldschmidt-Clermont PJ, Wilhide CC, Heldman A.W., Sussman MS, Ouyang P, et al. (1999) Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res 43: 985-991. PMID: 10615426
11. Yoshida T, Eguchi H, Nakachi K., Tanimoto K, Higashi Y, Suemasu K., et al. (2000) Distinct mechanisms of loss of estrogen receptor alpha gene expression in human breast cancer: methylation of the gene and alteration of trans-acting factors. Carcinogenesis 21: 2193-2201. PMID: 11133808
12. Westberry JM, Prewitt AK, Wilson M.E. (2008) Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats. Neuroscience 152: 982-989. doi: 10.1016/j.neuroscience.2008.01.048 PMID: 18353557
13. Lavados PM, Sacks C, Prina L., Escobar A, Tossi C, Araya F., et al. (2007) Incidence, case-fatality rate, and prognosis of ischaemic stroke subtypes in a predominantly Hispanic-Mestizo population in Iquique, Chile (PISCIS project): a community-based incidence study. Lancet Neurol 6:140-148. PMID: 17239801
14. Lin HF, Tsai PC, Liao Y.C., Lin TH, Tai CT, Juo SH, et al (2011) Chromosome 9p21 genetic variants are associated with myocardial infarction but not with ischemic stroke in a Taiwanese population. J Investig Med 59: 926-930. doi: 10.231/JIM.0b013e318214ea49 PMID: 21415773
15. Adams HP Jr., Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DJ, et al. (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 24: 35-41. PMID: 7678184
16. Lin HF, Liu CK, Liao Y.C., Lin RT, Chen CS, Juo SH. (2010) The risk of the metabolic syndrome on carotid thickness and stiffness: sex and age specific effects. Atherosclerosis 210:155-159. doi: 10.1016/j.atherosclerosis.2009.11.027 PMID: 20035939
17. Grau AJ, Weimar C, Buggle F., Heinrich A, Goertler M, Neumaier S., et al. (2001) Risk factors, outcome, and treatment in subtypes of ischemic stroke: the German stroke data bank. Stroke 32: 2559-2566. PMID: 11692017
18. Liu R, Liu Q, He S., Simpkins JW, Yang S.H. (2010) Combination therapy of 17beta-estradiol and recombinant tissue plasminogen activator for experimental ischemic stroke. J Pharmacol ExpTher 332: 1006-1012. doi: 10.1124/jpet.109.160937 PMID: 19952306
19. Chan GC, Fish JE, Mawji I.A., Leung DD, Rachlis AC, Marsden PA (2005) Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells. J Immunol 175: 3846-3861. PMID: 16148131
20. Wang YS, Chou WW, Chen K.C., Cheng HY, Lin RT, Juo SH. (2012) MicroRNA-152 mediates DNMT1-regulated DNA methylation in the estrogen receptor alpha gene. PLoS One 7: e30635. doi: 10.1371/journal.pone.0030635 PMID: 22295098
21. Baccarelli A, Wright R, Bollati V., Litonjua A, Zanobetti A., Tarantini L, et al. (2010) Ischemic heart disease and stroke in relation to blood DNA methylation. Epidemiology 21: 819-828. doi: 10.1097/EDE. 0b013e3181f20457 PMID: 20805753
22. Kim JM, Stewart R, Park M.S., Kang HJ, Kim SW, Shin IS, et al (2012) Associations of BDNF genotype and promoter methylation with acute and long-term stroke outcomes in an East Asian cohort. PLoS One 7: e51280. doi: 10.1371/journal.pone.0051280 PMID: 23240009
23. Lin RT, Hsi E, Lin H.F., Liao YC, Wang Y.S., Juo SH. (2014) LINE-1 methylation is associated with an increased risk of ischemic stroke in men. Curr Neurovasc Res 11: 4-9. PMID: 24295503
24. Dubal DB, Kashon ML, Pettigrew L.C., Ren JM, Finklestein SP, Rau SW, et al (1998) Estradiol protects against ischemic injury. J Cereb Blood FlowMetab 18:1253-1258. PMID: 9809515
25. Wise PM, Dubal D.B. (2000) Estradiol protects against ischemic brain injury in middle-aged rats. Biol Reprod 63: 982-985. PMID: 10993817
26. Westberry JM, Trout AL, Wilson M.E. (2010) Epigenetic regulation of estrogen receptor alpha gene expression in the mouse cortex during early postnatal development. Endocrinology 151: 731-740. doi: 10.1210/en.2009-0955 PMID: 19966177
27. Chang PY, Chen YJ, Chang F.H., Lu J., Huang WH, Yang TC, et al. (2013) Aspirin protects human coronary artery endothelial cells against atherogenic electronegative LDL via an epigenetic mechanism: a novel cytoprotective role of aspirin in acute myocardial infarction. Cardiovasc Res 99:137-145. doi: 10.1093/cvr/cvt062 PMID: 23519265
28. Pereira MA, Tao L, Wang W., Li Y, Umar A, Steele V.E., et al. (2004) Modulation by celecoxibanddifluor-omethylornithine of the methylation of DNA and the estrogen receptor-alpha gene in rat colon tumors. Carcinogenesis 25:1917-1923. PMID: 15205357
29. Lodder J, Boiten J. (1993) Incidence, natural history, and risk factors in lacunar infarction. Adv Neurol 62:213-227. PMID: 8517211
30. Alkayed NJ, Harukuni I, Kimes A.S., London ED, Traystman RJ, Hurn PD. (1998) Gender-linked brain injury in experimental stroke. Stroke 29:159-165; discussion 166. PMID: 9445346
31. Hall ED, Pazara KE, Linseman KL(1991) Sex differences in postischemic neuronal necrosis ingerbils. J Cereb Blood Flow Metab 11: 292-298. PMID: 1997500
32. Turtzo LC, McCullough L.D. (2010) Sex-specific responses to stroke. Future Neurol 5: 47-59. PMID: 20190872
33. Tian Y, Stamova B, Jickling G.C., Liu D., Ander BP, Bushnell C, et al. (2012) Effects of gender on gene expression in the blood of ischemic stroke patients. J Cereb Blood Flow Metab 32: 780-791. doi: 10.1038/jcbfm.2011.179 PMID: 22167233
34. Fuso A, Ferraguti G, Grandoni F., Ruggeri R, Scarpa S, Strom R., et al. (2010) Early demethylation of non-Cp G, CpC-rich, elements in the myogenin 5'-flanking region: a priming effect on the spreading of active demethylation. Cell Cycle 9: 3965-3976. PMID: 20935518
35. Fuso A, Ferraguti G, Scarpa S., Ferrer I, Lucarelli M. (2015) Disclosing bias in bisulfite assay: MethPrimers underestimate high DNA methylation. PLoSOne 10: e0118318. doi: 10.1371/journal.pone. 0118318 PMID: 25692551