Long-Lasting Changes in DNA Methylation Following Short-Term Hypoxic Exposure in Primary Hippocampal Neuronal Cultures

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Hartley, Iain ^a   Elkhoury, Fuad F ^a   Heon Shin, Joo ^b   Xie, Bin ^b   Gu, Xiangqun ^a   Gao, Yuan ^b   Zhou, Dan ^a   Haddad, Gabriel G ^a,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LIEBER INSTITUTE FOR BRAIN DEVELOPMENT   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d RADY CHILDREN'S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL HYPOXIA; CELL STRUCTURE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CPG ISLAND; DNA EXTRACTION; DNA METHYLATION; DOWN REGULATION; EMBRYO; EPIGENETICS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HIPPOCAMPAL NEURONAL CULTURE; MOUSE; NONHUMAN; PROMOTER REGION; RNA SEQUENCE; UPREGULATION;

ANIMALS; ANOXIA; BIOLOGICAL MARKERS; CELLS, CULTURED; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HIPPOCAMPUS; MICE; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84886415417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077859     Document Type: Article

References (44)

1. Obstetricians ACo, Encephalopathy GTFoN, Palsy C, Pediatrics AAo (2003) Neonatal encephalopathy and cerebral palsy: defining the pathogenesis and pathophysiology. American College of Obstetricians and Gynecologists.
2. MacLennan A, (1999) A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement. BMJ 319: 1054-1059. doi:10.1136/bmj.319.7216.1054. PubMed: 10521205.
3. Jögi A, Øra I, Nilsson H, Lindeheim A, Makino Y, et al. (2002) Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci USA 99: 7021-7026. doi:10.1073/pnas.102660199. PubMed: 12011461.
4. Ragel BT, Couldwell WT, Gillespie DL, Jensen RL, (2007) Identification of hypoxia-induced genes in a malignant glioma cell line (U-251) by cDNA microarray analysis. Neurosurg Rev 30: 181-187; discussion: 10.1007/s10143-007-0070-z. PubMed: 17486380.
5. Ralph GS, Parham S, Lee SR, Beard GL, Craigon MH, et al. (2004) Identification of potential stroke targets by lentiviral vector mediated overexpression of HIF-1 alpha and HIF-2 alpha in a primary neuronal model of hypoxia. J Cereb Blood Flow Metab 24: 245-258. PubMed: 14747751.
6. Jin K, Mao XO, Eshoo MW, del Rio G, Rao R, et al. (2002) cDNA microarray analysis of changes in gene expression induced by neuronal hypoxia in vitro. Neurochem Res 27: 1105-1112. doi:10.1023/A:1020913123054. PubMed: 12462408.
7. Amicarelli F, Colafarina S, Cattani F, Cimini A, Di Ilio C, et al. (2003) Scavenging system efficiency is crucial for cell resistance to ROS-mediated methylglyoxal injury. Free Radic Biol Med 35: 856-871. doi:10.1016/S0891-5849(03)00438-6. PubMed: 14556850.
8. Burgula S, Medisetty R, Jammulamadaka N, Musturi S, Ilavazhagan G, et al. (2010) Downregulation of PEBP1 in rat brain cortex in hypoxia. J Mol Neurosci 41: 36-47. doi:10.1007/s12031-009-9275-7. PubMed: 19705086.
9. Zhou D, Wang J, Zapala MA, Xue J, Schork NJ, et al. (2008) Gene expression in mouse brain following chronic hypoxia: role of sarcospan in glial cell death. Physiol Genomics 32: 370-379. PubMed: 18056785.
10. Feinberg AP, (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447: 433-440. doi:10.1038/nature05919. PubMed: 17522677.
11. Okano M, Bell DW, Haber DA, Li E, (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257. doi:10.1016/S0092-8674(00)81656-6. PubMed: 10555141.
12. Yoder JA, Soman NS, Verdine GL, Bestor TH, (1997) DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 270: 385-395. doi:10.1006/jmbi.1997.1125. PubMed: 9237905.
13. Lu Y, Chu A, Turker MS, Glazer PM, (2011) Hypoxia-induced epigenetic regulation and silencing of the BRCA1 promoter. Mol Cell Biol 31: 3339-3350. doi:10.1128/MCB.01121-10. PubMed: 21670155.
14. Nanduri J, Makarenko V, Reddy VD, Yuan G, Pawar A, et al. (2012) Epigenetic regulation of hypoxic sensing disrupts cardiorespiratory homeostasis. Proc Natl Acad Sci USA 109: 2515-2520. doi:10.1073/pnas.1120600109. PubMed: 22232674.
15. Fath T, Ke YD, Gunning P, Götz J, Ittner LM, (2009) Primary support cultures of hippocampal and substantia nigra neurons. Nat Protoc 4: 78-85. PubMed: 19131959.
16. Ball MP, Li JB, Gao Y, Lee JH, LeProust EM, et al. (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 27: 361-368. doi:10.1038/nbt.1533. PubMed: 19329998.
17. Colaneri A, Staffa N, Fargo DC, Gao Y, Wang T, et al. (2011) Expanded methyl-sensitive cut counting reveals hypomethylation as an epigenetic state that highlights functional sequences of the genome. Proc Natl Acad Sci USA 108: 9715-9720. doi:10.1073/pnas.1105713108. PubMed: 21602498.
18. Grant GR, Farkas MH, Pizarro AD, Lahens NF, Schug J, et al. (2011) Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics 27: 2518-2528. PubMed: 21775302.
19. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106. doi:10.1186/gb-2010-11-10-r106. PubMed: 20979621.
20. Raspaglio G, Filippetti F, Prislei S, Penci R, De Maria I, et al. (2008) Hypoxia induces class III beta-tubulin gene expression by HIF-1alpha binding to its 3' flanking region. Gene 409: 100-108. doi:10.1016/j.gene.2007.11.015. PubMed: 18178340.
21. Rössler J, Stolze I, Frede S, Freitag P, Schweigerer L, et al. (2004) Hypoxia-induced erythropoietin expression in human neuroblastoma requires a methylation free HIF-1 binding site. J Cell Biochem 93: 153-161. doi:10.1002/jcb.20133. PubMed: 15352172.
22. Shahrzad S, Bertrand K, Minhas K, Coomber BL, (2007) Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2: 119-125. doi:10.4161/epi.2.2.4613. PubMed: 17965619.
23. Watson JA, Watson CJ, McCrohan AM, Woodfine K, Tosetto M, et al. (2009) Generation of an epigenetic signature by chronic hypoxia in prostate cells. Hum Mol Genet 18: 3594-3604. doi:10.1093/hmg/ddp307. PubMed: 19584087.
24. Wenger RH, Kvietikova I, Rolfs A, Camenisch G, Gassmann M, (1998) Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site. Eur J Biochem 253: 771-777. doi:10.1046/j.1432-1327.1998.2530771.x. PubMed: 9654078.
25. Jones PA, (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492. doi:10.1038/nrg3230. PubMed: 22641018.
26. Bird A, (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21. doi:10.1101/gad.947102. PubMed: 11782440.
27. Curristin SM, Cao A, Stewart WB, Zhang H, Madri JA, et al. (2002) Disrupted synaptic development in the hypoxic newborn brain. Proc Natl Acad Sci USA 99: 15729-15734. doi:10.1073/pnas.232568799. PubMed: 12438650.
28. Pocock R, Hobert O, (2008) Oxygen levels affect axon guidance and neuronal migration in Caenorhabditis elegans. Nat Neurosci 11: 894-900. doi:10.1038/nn.2152. PubMed: 18587389.
29. Ara J, Fekete S, Frank M, Golden JA, Pleasure D, et al. (2011) Hypoxic-preconditioning induces neuroprotection against hypoxia-ischemia in newborn piglet brain. Neurobiol Dis 43: 473-485. doi:10.1016/j.nbd.2011.04.021. PubMed: 21554956.
30. Lin JS, Chen YS, Chiang HS, Ma MC, (2008) Hypoxic preconditioning protects rat hearts against ischaemia-reperfusion injury: role of erythropoietin on progenitor cell mobilization. J Physiol 586: 5757-5769. doi:10.1113/jphysiol.2008.160887. PubMed: 18845609.
31. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, et al. (2004) Hypoxic preconditioning protects against ischemic brain injury. NeuroRx 1: 26-35. doi:10.1602/neurorx.1.1.26. PubMed: 15717005.
32. Tang YL, Zhu W, Cheng M, Chen L, Zhang J, et al. (2009) Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res 104: 1209-1216. doi:10.1161/CIRCRESAHA.109.197723. PubMed: 19407239.
33. Arany Z, Huang LE, Eckner R, Bhattacharya S, Jiang C, et al. (1996) An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci USA 93: 12969-12973. doi:10.1073/pnas.93.23.12969. PubMed: 8917528.
34. Carrero P, Okamoto K, Coumailleau P, O'Brien S, Tanaka H, et al. (2000) Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1alpha. Mol Cell Biol 20: 402-415. doi:10.1128/MCB.20.1.402-415.2000. PubMed: 10594042.
35. Ema M, Hirota K, Mimura J, Abe H, Yodoi J, et al. (1999) Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 18: 1905-1914. doi:10.1093/emboj/18.7.1905. PubMed: 10202154.
36. Ruas JL, Poellinger L, Pereira T, (2002) Functional analysis of hypoxia-inducible factor-1 alpha-mediated transactivation. Identification of amino acid residues critical for transcriptional activation and/or interaction with CREB-binding protein. J Biol Chem 277: 38723-38730. doi:10.1074/jbc.M205051200. PubMed: 12133832.
37. Ruas JL, Poellinger L, Pereira T, (2005) Role of CBP in regulating HIF-1-mediated activation of transcription. J Cell Sci 118: 301-311. doi:10.1242/jcs.01617. PubMed: 15615775.
38. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y, (2007) The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod 13: 273-279. doi:10.1093/molehr/gam006. PubMed: 17327266.
39. Hua Z, Lv Q, Ye W, Wong CK, Cai G, et al. (2006) MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLOS ONE 1: e116. doi:10.1371/journal.pone.0000116. PubMed: 17205120.
40. Nakamura T, Hamada F, Ishidate T, Anai K, Kawahara K, et al. (1998) Axin, an inhibitor of the Wnt signalling pathway, interacts with beta-catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes Cells 3: 395-403. doi:10.1046/j.1365-2443.1998.00198.x. PubMed: 9734785.
41. Sekiya T, Nakamura T, Kazuki Y, Oshimura M, Kohu K, et al. (2002) Overexpression of Icat induces G(2) arrest and cell death in tumor cell mutants for adenomatous polyposis coli, beta-catenin, or Axin. Cancer Res 62: 3322-3326. PubMed: 12036951.
42. Spires TL, Molnár Z, Kind PC, Cordery PM, Upton AL, et al. (2005) Activity-dependent regulation of synapse and dendritic spine morphology in developing barrel cortex requires phospholipase C-beta1 signalling. Cereb Cortex 15: 385-393. doi:10.1093/cercor/bhh141. PubMed: 15749982.
43. Mazumdar J, O'Brien WT, Johnson RS, LaManna JC, Chavez JC, et al. (2010) O2 regulates stem cells through Wnt/[beta]-catenin signalling. Nat Cell Biol 12: 1007-1013. doi:10.1038/ncb2102. PubMed: 20852629.
44. Huang W, Zhu PJ, Zhang S, Zhou H, Stoica L, et al. (2013) mTORC2 controls actin polymerization required for consolidation of long-term memory. Nat Neurosci 16: 441-448. doi:10.1038/nn.3351. PubMed: 23455608.