The role of DNA methylation during anoxia tolerance in a freshwater turtle (Trachemys scripta elegans)

详细信息    查看全文

• 作者：Sanoji Wijenayake ; Kenneth B. Storey
• 关键词：Metabolic rate depression ; Anoxia ; Trachemys scripta elegans ; Epigenetics ; DNA methyltransferases ; Methyl ; binding proteins
• 刊名：Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：186
• 期：3
• 页码：333-342
• 全文大小：730 KB
• 参考文献：Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21:87–96CrossRef PubMed
  Avvakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, Arrowsmith CH, Dhe-Paganon S (2008) Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455:822–825CrossRef PubMed
  Barlow DP (1993) Methylation and imprinting: from host defense to gene regulation? Science 260:309–310CrossRef PubMed
  Beall R, Privitera C (1973) Effects of cold exposure on cardiac metabolism of the turtle Chrysemys picta. Am J Physiol 224:435–441PubMed
  Bestor TH, Tycko B (1996) Creation of genomic methylation patterns. Nat Genet 12:363–367CrossRef PubMed
  Biggar KK, Storey KB (2012) Evidence of cell cycle suppression and microRNA regulation of cyclin D1 during anoxia exposure in turtles. Cell Cycle 9:1705–1713CrossRef
  Biggar KK, Groom AG, Storey KB (2011) Hypometabolism and turtles: physiological and molecular strategies of anoxic survival. In: Nowakowska A, Caputa M (eds) Hypometabolism: strategies of survival in vertebrates and invertebrates. Research Signpost, Kerala, pp 57–94
  Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(6):21
  Bird AP, Wolffe AP (1999) Methylation-induced repression belts, braces, and chromatin. Cell 99:451–454CrossRef PubMed
  Bogdanovic O, Veenstra JC (2009) DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118:549–565CrossRef PubMed PubMedCentral
  Boutilier R, Donohoe P, Tattersall G, West T (1997) Hypometabolic homeostasis in overwintering aquatic amphibians. J Exp Biol 200:387–400PubMed
  Boyes J, Bird A (1991) DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64:1123–1134CrossRef PubMed
  Buck LT, Land SC, Hochachka PW (1993) Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression. Am J Physiol 265:49–56
  Calvanese V, Lara E, Kahn A, Fraga MF (2009) The role of epigenetics in aging and age-related diseases. Ageing Res Rev 8:268–276CrossRef PubMed
  Chiacchiera F, Piunti A, Pasini D (2013) Epigenetic methylations and their connections with metabolism. Cell Mol Life Sci 70:1495–1508CrossRef PubMed
  Fraser K, Houlihan D, Lutz DP, Leone-Kabler S, Manuel L, Brechin J (2001) Complete suppression of protein synthesis during anoxia with no post-anoxia protein synthesis debt in the red-eared slider turtle Trachemys scripta elegans. J Exp Biol 204:4353–4360PubMed
  Goll MG, Bestor TG (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514CrossRef PubMed
  Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311:395–398CrossRef PubMed
  Grewal SIS, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 301:798–802CrossRef PubMed
  Herbert CV, Jackson DC (1985) Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes, and cardiovascular function in aerated and anoxic water. Physiol Zool 58:670–681CrossRef
  Hermes-Lima M, Zenteno-Savin T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C: Toxicol Pharmacol 133:537–556CrossRef
  Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493–9498CrossRef PubMed PubMedCentral
  Jackson DC (2002) Hibernating without oxygen: physiological adaptations of the painted turtle. J Physiol 543:731–737CrossRef PubMed PubMedCentral
  Jackson DC, Heisler N (1982) Plasma ion balance of submerged anoxic turtles at 3 °C: the role of calcium lactate formation. Respir Physiol 49:159–174CrossRef PubMed
  Jackson DC, Crocker CE, Ultsch GR (2000) Bone and shell contribution to lactic acid buffering of submerged turtles Chrysemys picta bellii at 3 °C. Am J Physiol Regul Integr Comp Physiol 278:1564–1571
  Jeltsch A, Nellen W, Lyko F (2006) Two substrates are better than one: dual specificities for DNMT2 methyltransferases. Trends Biochem Sci 31:306–308CrossRef PubMed
  Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP (1998) Methylated DNA and MeCP2 recruit histone deacetylas to repress transcription. Nat Ganet 19:187–191CrossRef
  Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31:89–97CrossRef PubMed
  Krivoruchko A, Storey KB (2010a) Epigenetics in anoxia tolerance: a role for histone deacetylases. Mol Cell Biochem 342:151–161CrossRef PubMed
  Krivoruchko A, Storey KB (2010b) Molecular mechanisms of turtle anoxia tolerance: a role for NF-kappaB. Gene 450:63–69CrossRef PubMed
  Krivoruchko A, Storey KB (2013) Anoxia-responsive regulation of the FoxO transcription factors in freshwater turtles, Trachemys scripta elegans. Biochim Biophys Acta 1830:4990–4998CrossRef PubMed
  Krivoruchko A, Storey KB (2014) Activation of the carbohydrate response element binding protein (ChREBP) in response to anoxia in the turtle (Trachemys scripta elegans). Biochim Biophys Acta 1840:3000–3005CrossRef PubMed
  Lutz PL, Milton SL (2004) Negotiating brain anoxia survival in the turtle. J Exp Biol 207:3141–3147CrossRef PubMed
  Lutz PL, Storey KB (1997) Adaptations to variations in oxygen tension by vertebrates and invertebrates. In: Dantzler WH (ed) Handbook of physiology, section 13, Comparative physiology, vol 2. Oxford University Press, Oxford, pp 1479–1522
  Macaluso M, Montanari M, Cinti C, Giordano A (2005) Modulation of cell cycle components by epigenetic and genetic events. Semin Oncol 32:452–457CrossRef PubMed
  Ng HH, Zhang Y, Hendrich B, Johnson CA, Turner BM, Erdjument-Bromage H, Tempest P, Reignberg D, Bird A (1999) MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1:58–61
  Okano M, Xie S, Li E (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19:219–220CrossRef PubMed
  Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257CrossRef PubMed
  Ramsahoye BH, Biniszkiewics D, Lyko F, Clark V, Bird AP, Jaenisch R (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 97:5237–5242CrossRef PubMed PubMedCentral
  Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758PubMed
  Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, Lyko F (2010) RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev 24:1590–1595CrossRef PubMed PubMedCentral
  Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M, Koseki H (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting DNMT1 to methylated DNA. Nature 7171:908–912CrossRef
  Storey KB (1975) Purification and properties of turtle heart creatine kinase: role for the enzyme in glycolytic control. Int J Biochem 6:53–59CrossRef
  Storey KB (2007) Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp Biochem Physiol A 147:263–276CrossRef
  Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174CrossRef PubMed
  Storey KB, Storey JM (2007) Tribute to P.L. Lutz: putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714CrossRef PubMed
  Ultsch GR (1985) The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 10 °C. Comp Biochem Physiol A 3:607–611CrossRef
  Ultsch GR (2006) The ecology of overwintering among turtles: where turtles overwinter and its consequences. Biol Rev 81:339–367CrossRef PubMed
  Ultsch GR, Jackson DC (1982) Long-term submergence at 3 °C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water: survival, gas exchange and acid-base status. J Exp Biol 96:11–28
  Van der Maarel SM (2008) Epigenetic mechanisms in health and disease. Ann Rheum Dis 67:97–100
  Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565CrossRef
  Watt F, Molloy PL (1998) Cytosine methylation prevents binding to DNA of HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 2:1136–1143CrossRef
  Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286:481–486CrossRef PubMed
  
• 作者单位：Sanoji Wijenayake (1)
  Kenneth B. Storey (2)
  
  1. Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON, K1S 5B6, Canada
  2. Department of Biology, Department of Chemistry, Canada Research Chair in Molecular Physiology, Institute of Biochemistry, 1125 Colonel By Drive, Ottawa, ON, K1S 5B6, Canada
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Biomedicine
  Human Physiology
  Zoology
  Animal Physiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-136X

文摘

Oxygen deprivation is a lethal stress that only a few animals can tolerate for extended periods. This study focuses on analyzing the role of DNA methylation in aiding natural anoxia tolerance in a champion vertebrate anaerobe, the red-eared slider turtle (Trachemys scripta elegans). We examined the relative expression and total enzymatic activity of four DNA methyltransferases (DNMT1, DNMT2, DNMT3a and DNMT3b), two methyl-binding domain proteins (MBD1 and MBD2), and relative genomic levels of 5-methylcytosine under control, 5 h anoxic, and 20 h anoxic conditions in liver, heart, and white skeletal muscle (n = 4, p < 0.05). In liver, protein expression of DNMT1, DNMT2, MBD1, and MBD2 rose significantly by two- to fourfold after 5 h anoxic submergence compared to normoxic-control conditions. In heart, 5 h anoxia submergence resulted in a 1.4-fold increase in DNMT3a levels and a significant decrease in MBD1 and MBD2 levels to ~30 % of control values. In white muscle, DNMT3a and DNMT3b increased threefold and MBD1 levels increased by 50 % in response to 5 h anoxia. Total DNMT activity rose by 0.6–2.0-fold in liver and white muscle and likewise global 5mC levels significantly increased in liver and white muscle under 5 and 20 h anoxia. The results demonstrate an overall increase in DNA methylation, DNMT protein expression and enzymatic activity in response to 5 and 20 h anoxia in liver and white muscle indicating a potential downregulation of gene expression via this epigenetic mechanism during oxygen deprivation.