Temperature affects methylation of the myogenin putative promoter, its expression and muscle cellularity in Senegalese sole larvae

Epigenetics

Volumn 8, Issue 4, 2013, Pages

  Campos, Catarina ^a,b,c   Valente, Luísa M P ^a   Conceição, Luís E C ^b   Engrola, Sofia ^b   Fernandes, Jorge M O ^c  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF ALGARVE   (Portugal)

^c NORD UNIVERSITY   (Norway)

Author keywords

Epigenetic regulation; Methylation; Myogenesis; Myogenin; Solea senegalensis; Thermal plasticity

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYTOSINE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; MYOCYTE ENHANCER FACTOR 2; MYOGENIN; TRANSCRIPTION FACTOR SOX6; 5' UNTRANSLATED REGION; DNA (CYTOSINE 5) METHYLTRANSFERASE;

5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL HUSBANDRY; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CPG ISLAND; EMBRYO; GENE SEQUENCE; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN METHYLATION; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SOLEA SENEGALENSIS; TATA BOX; TELEOST; TEMPERATURE; TRANSCRIPTION INITIATION SITE; ANIMAL; CYTOLOGY; FLATFISH; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; METHYLATION; MOLECULAR GENETICS; MUSCLE CELL; PROMOTER REGION; SKELETAL MUSCLE;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; FLATFISHES; LARVA; METHYLATION; MOLECULAR SEQUENCE DATA; MUSCLE CELLS; MUSCLE, SKELETAL; MYOGENIN; PROMOTER REGIONS, GENETIC; TEMPERATURE;

EID: 84875869640     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.24178     Document Type: Article

References (31)

1. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005; 74:481-514; PMID:15952895; http://dx.doi.org/10.1146/annurev. biochem.74.010904.153721.
2. Rai K, Nadauld LD, Chidester S, Manos EJ, James SR, Karpf AR, et al. Zebra fish Dnmt1 and Suv39h1 regulate organ-specific terminal differentiation during development. Mol Cell Biol 2006; 26:7077-85; PMID:16980612; http://dx.doi.org/10.1128/ MCB.00312-06.
3. Chen T, Ueda Y, Dodge JE, Wang Z, Li E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 2003; 23:5594-605; PMID:12897133; http://dx.doi.org/10.1128/ MCB.23.16.5594-5605.2003.
4. Li JY, Pu MT, Hirasawa R, Li BZ, Huang YN, Zeng R, et al. Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol Cell Biol 2007; 27:8748-59; PMID:17938196; http://dx.doi.org/10.1128/ MCB.01380-07.
5. Bergstrom DA, Tapscott SJ. Molecular distinction between specification and differentiation in the myogenic basic helix-loop-helix transcription factor family. Mol Cell Biol 2001; 21:2404-12; PMID:11259589; http://dx.doi.org/10.1128/MCB.21.7.2404-2412.2001.
6. Du SJ, Gao J, Anyangwe V. Muscle-specific expression of myogenin in zebrafish embryos is controlled by multiple regulatory elements in the promoter. Comp Biochem Physiol B Biochem Mol Biol 2003; 134:123-34; PMID:12524040; http://dx.doi.org/10.1016/ S1096-4959(02)00194-X.
7. Tan X, Hoang L, Du S. Characterization of muscle-regulatory genes, Myf5 and myogenin, from striped bass and promoter analysis of muscle-specific expression. Mar Biotechnol (NY) 2002; 4:537-45; PMID:14961228; http://dx.doi.org/10.1007/s10126-002-0013-1.
8. Spitz F, Demignon J, Porteu A, Kahn A, Concordet JP, Daegelen D, et al. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc Natl Acad Sci U S A 1998; 95:14220-5; PMID:9826681; http://dx.doi.org/10.1073/ pnas.95.24.14220.
9. Cheng TC, Wallace MC, Merlie JP, Olson EN. Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science 1993; 261:215-8; PMID:8392225; http://dx.doi. org/10.1126/science.8392225.
10. Yee SP, Rigby PW. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev 1993; 7(7A):1277-89; PMID:8391506; http://dx.doi.org/10.1101/ gad.7.7a.1277.
11. Fuso A, Ferraguti G, Grandoni F, Ruggeri R, Scarpa S, Strom R, et al. Early demethylation of non-CpG, CpCrich, elements in the myogenin 5'-flanking region: a priming effect on the spreading of active demethylation. Cell Cycle 2010; 9:3965-76; PMID:20935518; http://dx.doi.org/10.4161/cc.9.19.13193.
12. Palacios D, Summerbell D, Rigby PWJ, Boyes J. Interplay between DNA methylation and transcription factor availability: implications for developmental activation of the mouse Myogenin gene. Mol Cell Biol 2010; 30:3805-15; PMID:20498275; http://dx.doi. org/10.1128/MCB.00050-10.
13. Hupkes M, Jonsson MK, Scheenen WJ, van Rotterdam W, Sotoca AM, van Someren EP, et al. Epigenetics: DNA demethylation promotes skeletal myotube maturation. FASEB J 2011; 25:3861-72; PMID:21795504; http://dx.doi.org/10.1096/fj.11-186122.
14. Fernandes JM, Mackenzie MG, Wright PA, Steele SL, Suzuki Y, Kinghorn JR, et al. Myogenin in model pufferfish species: Comparative genomic analysis and thermal plasticity of expression during early development. Comp Biochem Physiol Part D Genomics Proteomics 2006; 1:35-45; PMID:20483233; http:// dx.doi.org/10.1016/j.cbd.2005.09.003.
15. Wilkes D, Xie SQ, Stickland NC, Alami-Durante H, Kentouri M, Sterioti A, et al. Temperature and myogenic factor transcript levels during early development determines muscle growth potential in rainbow trout (Oncorhynchus mykiss) and sea bass (Dicentrarchus labrax). J Exp Biol 2001; 204:2763-71; PMID:11683432.
16. Vinagre C, Fonseca V, Cabral H, Costa MJ. Habitat suitability index models for the juvenile soles, Solea solea and Solea senegalensis, in the Tagus estuary: Defining variables for species management. Fish Res 2006; 82:140-9; http://dx.doi.org/10.1016/j. fishres.2006.07.011.
17. Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, et al. A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fish 2003; 13:379-407; http://dx.doi.org/10.1007/ s11160-004-1632-6.
18. Campos C, Valente LMP, Conceição LE, Engrola S, Sousa V, Rocha E, et al. Incubation temperature induces changes in muscle cellularity and gene expression in Senegalese sole (Solea senegalensis). Gene 2013; 516:209-17; http://dx.doi.org/10.1016/j. gene.2012.12.074; PMID:23291415.
19. Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009; 10:189-98; PMID:19723495; http://dx.doi.org/10.1016/j.cmet.2009.07.011.
20. Verrijzer CP, Tjian R. TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem Sci 1996; 21:338-42; PMID:8870497; http://dx.doi. org/10.1016/0968-0004(96)10044-X.
21. Faralli H, Dilworth FJ. Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp Funct Genomics 2012; 2012:836374; PMID:22811619; http://dx.doi. org/10.1155/2012/836374.
22. Codina M, Bian YH, Gutiérrez J, Du SJ. Cloning and characterization of myogenin from seabream (Sparus aurata) and analysis of promoter muscle specificity. Comp Biochem Physiol Part D Genomics Proteomics 2008; 3:128-39; PMID:20483214; http://dx.doi. org/10.1016/j.cbd.2007.12.001.
23. Salero E, Giménez C, Zafra F. Identification of a non-canonical E-box motif as a regulatory element in the proximal promoter region of the apolipoprotein E gene. Biochem J 2003; 370:979-86; PMID:12444925; http://dx.doi.org/10.1042/BJ20021142.
24. Lüscher B, Larsson LG. The basic region/helix-loophelix/ leucine zipper domain of Myc proto-oncoproteins: function and regulation. Oncogene 1999; 18:2955-66; PMID:10378692; http://dx.doi. org/10.1038/sj.onc.1202750.
25. Johnston IA. Environment and plasticity of myogenesis in teleost fish. J Exp Biol 2006; 209:2249-64; PMID:16731802; http://dx.doi.org/10.1242/ jeb.02153.
26. Steinbacher P, Haslett JR, Obermayer A, Marschallinger J, Bauer HC, Sänger AM, et al. MyoD and Myogenin expression during myogenic phases in brown trout: a precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev Dyn 2007; 236:1106-14; PMID:17315228; http://dx.doi.org/10.1002/ dvdy.21103.
27. Campos C, Valente LM, Borges P, Bizuayehu T, Fernandes JM. Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 2010; 213:200-9; PMID:20038653; http://dx.doi. org/10.1242/jeb.033126.
28. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007; 447:425-32; PMID:17522676; http://dx.doi. org/10.1038/nature05918.
29. Campos C, Valente LM, Fernandes JM. Molecular evolution of zebrafish dnmt3 genes and thermal plasticity of their expression during embryonic development. Gene 2012; 500:93-100; PMID:22450363; http:// dx.doi.org/10.1016/j.gene.2012.03.041.
30. Fernandez-Diaz C, Yufera M, Canavate JP, Moyano FJ, Alarcon FJ, Diaz M. Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J Fish Biol 2001; 58:1086-97; http://dx.doi. org/10.1111/j.1095-8649.2001.tb00557.x.
31. Fernandes JMO, Mommens M, Hagen O, Babiak I, Solberg C. Selection of suitable reference genes for real-time PCR studies of Atlantic halibut development. Comp Biochem Physiol B Biochem Mol Biol 2008; 150:23-32; PMID:18302990; http://dx.doi. org/10.1016/j.cbpb.2008.01.003.