Journal of Comparative Physiology B

, Volume 178, Issue 6, pp 729–734 | Cite as

Epigenetic silencers are enriched in dormant desert frog muscle

  • Nicholas J. Hudson
  • T. G. A. Lonhienne
  • Craig E. Franklin
  • Gregory S. Harper
  • S. A. Lehnert
Original Paper

Abstract

Green-striped burrowing frogs, Cycloranaalboguttata, survive droughts by entering a metabolic depression called aestivation, characterised by a reduction in resting oxygen consumption by 80%. Aestivation in C. alboguttata is manifest by transcriptional silencing of skeletal muscle bioenergetic genes, such as NADH ubiquinone oxidoreductase 1, ATP synthase and superoxide dismutase 2. In this study, we hypothesised that aestivation is associated with epigenetic change in frog muscle. We assessed mRNA transcript abundance of seven genes that code for proteins with established roles in epigenetically-mediated gene silencing [transcriptional co-repressor SIN3A, DNA (cytosine-5-) methyltransferase 1, methyl CpG binding protein 2, chromodomain helicase DNA binding protein 4, histone binding protein rbbp4, histone deacetylase 1 and nuclear receptor co-repressor 2] using qRT-PCR. These seven genes showed a modest (1.1–3.5-fold) but coordinated upregulation in 6-month aestivating muscle. This reached significance for SIN3A and DNA cytosine-5-methyltransferase 1 in standard pair-wise comparisons (p < 0.05), and the candidates as a whole when analysed by Fisher’s combined probability test (p < 0.01). These data are consistent with the hypothesis that the transcriptional silencing and metabolic depression that occurs during seasonal dormancy are associated with chromatin remodelling, and present a novel example of an environmentally induced epigenetic modification in an adult vertebrate.

Keywords

Epigenetic SIN3 co-repressor Aestivation Frog Muscle Dormancy Disuse 

References

  1. Berriel Diaz M, Lange M, Heldmaier G, Klingenspor M (2004) Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus). J Comp Physiol B 174:495–502PubMedCrossRefGoogle Scholar
  2. Eddy SF, Morin P Jr, Storey KB (2006) Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifigus. J Exp Zoolog A Comp Exp Biol 305:620–630PubMedCrossRefGoogle Scholar
  3. Flanigan JE, Withers PC, Fuery CJ, Guppy M (1993) Metabolic depression and Na+ K+ gradients in the aestivating Australian goldfields frog, Neobatrachus wilsmorei. J Comp Physiol B 163:587–593PubMedCrossRefGoogle Scholar
  4. Fleischer TC, Yun UJ, Ayer DE (2003) Identification and characterisation of three new components of the mSIN3A corepressor complex. Mol Cell Biol 23:3456–3467PubMedCrossRefGoogle Scholar
  5. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T (2000) DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24:88–91PubMedCrossRefGoogle Scholar
  6. Grundy JE, Storey KB (1999) Antioxidant defence and lipid peroxidation damage in estivating toads, Scaphiosus couchii. J Comp Physiol B 168:132–142CrossRefGoogle Scholar
  7. Hudson NJ, Franklin CE (2002a) Maintaining muscle mass during extended disuse: aestivating frogs as a model species. J Exp Biol 255:2297–2303Google Scholar
  8. Hudson NJ, Franklin CE (2002b) Effect of aestivation on muscle characteristics and locomotor performance in the green-striped burrowing frog, Cyclorana alboguttata. J Comp Physiol B 172:177–182PubMedCrossRefGoogle Scholar
  9. Hudson NJ, Lavidis NA, Choy PT, Franklin CE (2005) Effect of prolonged inactivity on skeletal motor nerve terminals during aestivation in the burrowing frog, Cyclorana alboguttata. J Comp Physiol A 191:373–379CrossRefGoogle Scholar
  10. Hudson NJ, Lehnert SA, Ingham AB, Symonds B, Franklin CE, Harper GS (2006) Lessons from an aestivating frog: sparing muscle protein despite starvation and disuse. Am J Physiol Regul Integr Comp 290:R836–843CrossRefGoogle Scholar
  11. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet Suppl 33:245–254CrossRefGoogle Scholar
  12. Larade K, Storey KB (2007) Arrest of transcription following anoxic exposure in a marine mollusc. Mol Cell Biochem 303:243–249PubMedCrossRefGoogle Scholar
  13. MacDonald JA Storey KB (2006) Identification of a 115kD MAP-kinase activated by freezing and anoxic stresses in the marine periwinkle, Littorina littorea. Arch Biochem Biophys 450:208–214PubMedCrossRefGoogle Scholar
  14. Morin P Jr, Storey KB (2006) Evidence for a reduced transcriptional state during hibernation in ground squirrels. Cryobiology 53:310–318PubMedCrossRefGoogle Scholar
  15. Pile LA, Spellman PT, Katzenberger RJ, Wassarman DA (2003) The SIN3 deacetylase complex represses genes encoding mitochondrial proteins: implications for the regulation of energy metabolism. J Biol Chem 278:37840–37848PubMedCrossRefGoogle Scholar
  16. Pyne S, Futcher B, Skiena S (2006) Meta-analysis based on control of false discovery rate: combining yeast ChIP-chip datasets. Bioinformatics 22(20):2516–2522PubMedCrossRefGoogle Scholar
  17. Rider MH, Hussain N, Horman S, Dilworth SM, Storey KB (2006) Stress-induced activation of the AMP-activated protein kinase in the freeze tolerant frog Rana sylvatica. Cryobiology 53:297–309PubMedCrossRefGoogle Scholar
  18. Rountree MR, Bachman KE, Baylin SB (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25:269–277PubMedCrossRefGoogle Scholar
  19. Sellars MJ, Vuocolo T, Leeton LA, Coman GJ, Degnan BM, Preston NP (2007) Real Time RT-PCR quantification of Kurama shrimp transcripts: a comparison of relative and absolute quantification methods. J Biotechnol 129(3):391–399PubMedCrossRefGoogle Scholar
  20. Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and aestivation. Q Rev Biol 65:145–174PubMedCrossRefGoogle Scholar
  21. Symonds BL, James RS, Franklin CE (2007) Getting the jump on skeletal muscle disuse atrophy: preservation of contractile performance in aestivating Cyclorana alboguttata (Gunther 1867). J Exp Biol 210:825–835PubMedCrossRefGoogle Scholar
  22. Tan SH, Reverter A, Wang Y, Byrne KA, McWilliam SM, Lehnert SA (2006) Gene expression profiling of bovine in vitro adipogenesis using a cDNA microarray. Funct Integr Genomics 6(3):235–249PubMedCrossRefGoogle Scholar
  23. Williams DR, Epperson LE, Li W, Hughes MA, Taylor R, Rogers J, Martin SL, Cossins AR, Gracy AY (2005) Seasonally hibernating phenotype assessed though transcript screening. Physiol Genomics 24:13–22PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Nicholas J. Hudson
    • 1
  • T. G. A. Lonhienne
    • 2
  • Craig E. Franklin
    • 3
  • Gregory S. Harper
    • 4
  • S. A. Lehnert
    • 1
  1. 1.CSIRO Livestock IndustriesBrisbaneAustralia
  2. 2.Centre for Integrative Legume ResearchBrisbaneAustralia
  3. 3.School of Integrative BiologyThe University of QueenslandBrisbaneAustralia
  4. 4.Meat and Livestock AustraliaBrisbaneAustralia

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