Cell and Tissue Research

, Volume 359, Issue 3, pp 715–727 | Cite as

Evolutionary history and epigenetic regulation of the three paralogous pax7 genes in rainbow trout

  • Iban Seiliez
  • Jacob Michael Froehlich
  • Lucie Marandel
  • Jean-Charles Gabillard
  • Peggy R. Biga
Regular Article

Abstract

The extraordinary muscle growth potential of teleost fish, particular those of the Salmoninae clade, elicits questions about the regulation of the relatively highly conserved transcription factors of the myogenic program. The pseudotetraploid nature of the salmonid genome adds another layer of regulatory complexity that must be reconciled with epigenetic data to improve our understanding of the achievement of lifelong muscle growth in these fish. We identify three paralogous pax7 genes (pax7a1, pax7a2 and pax7b) in the rainbow trout genome. During in vitro myogenesis, pax7a1 transcripts remain stable, whereas pax7a2 and pax7b mRNAs increase in abundance, similarly to myogenin mRNAs but in contrast to the expression pattern of the mammalian ortholog. We also profile the distribution of repressive H3K27me3 and H3K9me3 and permissive H3K4me3 marks during in vitro myogenesis across these loci and find that pax7a2 expression is associated with decreased H3K27 trimethylation, whereas pax7b expression is correlated with decreased H3K9me3 and H3K27me3. These data link the unique differential expression of pax7 paralogs with epigenetic histone modifications in a vertebrate species displaying growth divergent from that of mammals and highlight an important divergence in the regulatory mechanisms of pax7 expression among vertebrates. The system described here provides a more comprehensive picture of the combinatorial control mechanisms orchestrating skeletal muscle growth in a salmonid, leading to a better understanding of myogenesis in this species and across Vertebrata more generally.

Keywords

pax7 Epigenetic regulation Histone methylation ChIP Rainbow trout 

References

  1. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–1714CrossRefPubMedGoogle Scholar
  2. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, Bento P, Da Silva C, Labadie K, Alberti A, Aury JM, Louis A, Dehais P, Bardou P, Montfort J, Klopp C, Cabau C, Gaspin C, Thorgaard GH, Boussaha M, Quillet E, Guyomard R, Galiana D, Bobe J, Volff JN, Genet C, Wincker P, Jaillon O, Roest Crollius H, Guiguen Y (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bower NI, Johnston IA (2010) Paralogs of Atlantic salmon myoblast determination factor genes are distinctly regulated in proliferating and differentiating myogenic cells. Am J Physiol Regul Integr Comp Physiol 298:R1615–R1626CrossRefPubMedGoogle Scholar
  4. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039–1043CrossRefPubMedGoogle Scholar
  5. Diao Y, Guo X, Li Y, Sun K, Lu L, Jiang L, Fu X, Zhu H, Sun H, Wang H, Wu Z (2012) Pax3/7BP is a Pax7- and Pax3-binding protein that regulates the proliferation of muscle precursor cells by an epigenetic mechanism. Cell Stem Cell 11:231–241CrossRefPubMedGoogle Scholar
  6. Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 12:1052–1058CrossRefPubMedGoogle Scholar
  7. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedCentralPubMedGoogle Scholar
  8. Froehlich JM, Fowler ZG, Galt NJ, Smith DL Jr, Biga PR (2013a) Sarcopenia and piscines: the case for indeterminate-growing fish as unique genetic model organisms in aging and longevity research. Front Genet 4:159CrossRefPubMedCentralPubMedGoogle Scholar
  9. Froehlich JM, Galt NJ, Charging MJ, Meyer BM, Biga PR (2013b) In vitro indeterminate teleost myogenesis appears to be dependent on Pax3. Vitro Cell Dev Biol Anim 49:371–385CrossRefGoogle Scholar
  10. Froehlich JM, Seiliez I, Gabillard JC, Biga PR (2014) Preparation of primary myogenic precursor cell/myoblast cultures from basal vertebrate lineages. J Vis Exp 86:(in press)Google Scholar
  11. Gabillard JC, Sabin N, Paboeuf G (2010) In vitro characterization of proliferation and differentiation of trout satellite cells. Cell Tissue Res 342:471–477CrossRefPubMedGoogle Scholar
  12. Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, Reshef R, Rozenboim I, Wleklinski-Lee M, Yablonka-Reuveni Z (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231:489–502CrossRefPubMedGoogle Scholar
  13. Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, Prince VE, Yang Z, Thomas MG, Coates MI (2007) A new time-scale for ray-finned fish evolution. Proc Biol Sci 274:489–498CrossRefPubMedCentralPubMedGoogle Scholar
  14. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957CrossRefPubMedGoogle Scholar
  15. Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–1628CrossRefPubMedGoogle Scholar
  16. Kawabe Y, Wang YX, McKinnell IW, Bedford MT, Rudnicki MA (2012) Carm1 regulates Pax7 transcriptional activity through MLL1/2 recruitment during asymmetric satellite stem cell divisions. Cell Stem Cell 11:333–345CrossRefPubMedCentralPubMedGoogle Scholar
  17. Kitzmann M, Carnac G, Vandromme M, Primig M, Lamb NJ, Fernandez A (1998) The muscle regulatory factors MyoD and myf-5 undergo distinct cell cycle-specific expression in muscle cells. J Cell Biol 142:1447–1459CrossRefPubMedCentralPubMedGoogle Scholar
  18. Konstantinides N, Averof M (2014) A common cellular basis for muscle regeneration in arthropods and vertebrates. Science 343:788–791CrossRefPubMedGoogle Scholar
  19. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, Greenblatt JF, Shilatifard A (2003a) The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11:721–729CrossRefPubMedGoogle Scholar
  20. Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, Richards DP, Beattie BK, Emili A, Boone C, Shilatifard A, Buratowski S, Greenblatt J (2003b) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23:4207–4218CrossRefPubMedCentralPubMedGoogle Scholar
  21. Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646CrossRefPubMedCentralPubMedGoogle Scholar
  22. Ling BM, Gopinadhan S, Kok WK, Shankar SR, Gopal P, Bharathy N, Wang Y, Taneja R (2012) G9a mediates Sharp-1-dependent inhibition of skeletal muscle differentiation. Mol Biol Cell 23:4778–4785CrossRefPubMedCentralPubMedGoogle Scholar
  23. Macqueen DJ, Johnston IA (2014) A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc Biol Sci 281:20132881CrossRefPubMedCentralPubMedGoogle Scholar
  24. Mal AK (2006) Histone methyltransferase Suv39h1 represses MyoD-stimulated myogenic differentiation. EMBO J 25:3323–3334CrossRefPubMedCentralPubMedGoogle Scholar
  25. Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Physiol B Biochem Mol Biol 129:207–219CrossRefPubMedGoogle Scholar
  26. Mozzetta C, Consalvi S, Saccone V, Forcales SV, Puri PL, Palacios D (2011) Selective control of Pax7 expression by TNF-activated p38alpha/polycomb repressive complex 2 (PRC2) signaling during muscle satellite cell differentiation. Cell Cycle 10:191–198CrossRefPubMedGoogle Scholar
  27. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110–113CrossRefPubMedGoogle Scholar
  28. Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA, Davis MP, Wainwright PC, Friedman M, Smith WL (2012) Resolution of ray-finned fish phylogeny and timing of diversification. Proc Natl Acad Sci U S A 109:13698–13703CrossRefPubMedCentralPubMedGoogle Scholar
  29. Palacios D, Mozzetta C, Consalvi S, Caretti G, Saccone V, Proserpio V, Marquez VE, Valente S, Mai A, Forcales SV, Sartorelli V, Puri PL (2010) TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7:455–469CrossRefPubMedCentralPubMedGoogle Scholar
  30. Perdiguero E, Sousa-Victor P, Ballestar E, Munoz-Canoves P (2009) Epigenetic regulation of myogenesis. Epigenetics 4:541–550CrossRefPubMedGoogle Scholar
  31. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefPubMedCentralPubMedGoogle Scholar
  32. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36CrossRefPubMedCentralPubMedGoogle Scholar
  33. Rampalli S, Li L, Mak E, Ge K, Brand M, Tapscott SJ, Dilworth FJ (2007) p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation. Nat Struct Mol Biol 14:1150–1156CrossRefPubMedCentralPubMedGoogle Scholar
  34. Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599CrossRefPubMedGoogle Scholar
  35. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  36. Saccone V, Puri PL (2010) Epigenetic regulation of skeletal myogenesis. Organogenesis 6:48–53CrossRefPubMedCentralPubMedGoogle Scholar
  37. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, Guenou H, Malissen B, Tajbakhsh S, Galy A (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–3656CrossRefPubMedGoogle Scholar
  38. Santini F, Harmon LJ, Carnevale G, Alfaro ME (2009) Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol Biol 9:194CrossRefPubMedCentralPubMedGoogle Scholar
  39. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262CrossRefPubMedCentralPubMedGoogle Scholar
  40. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ 3rd (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16:919–932CrossRefPubMedCentralPubMedGoogle Scholar
  41. Sdek P, Oyama K, Angelis E, Chan SS, Schenke-Layland K, MacLellan WR (2013) Epigenetic regulation of myogenic gene expression by heterochromatin protein 1 alpha. PLoS One 8:e58319CrossRefPubMedCentralPubMedGoogle Scholar
  42. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786CrossRefPubMedGoogle Scholar
  43. Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, Pavlath GK, Dhawan J (2009) MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci U S A 106:4719–4724CrossRefPubMedCentralPubMedGoogle Scholar
  44. Seenundun S, Rampalli S, Liu QC, Aziz A, Palii C, Hong S, Blais A, Brand M, Ge K, Dilworth FJ (2010) UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J 29:1401–1411CrossRefPubMedCentralPubMedGoogle Scholar
  45. Stickland NC (1983) Growth and development of muscle fibres in the rainbow trout (Salmo gairdneri). J Anat 137:323–333PubMedCentralPubMedGoogle Scholar
  46. Stojic L, Jasencakova Z, Prezioso C, Stutzer A, Bodega B, Pasini D, Klingberg R, Mozzetta C, Margueron R, Puri PL, Schwarzer D, Helin K, Fischle W, Orlando V (2011) Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells. Epigenetics Chromatin 4:16CrossRefPubMedCentralPubMedGoogle Scholar
  47. Taberlay PC, Kelly TK, Liu CC, You JS, De Carvalho DD, Miranda TB, Zhou XJ, Liang G, Jones PA (2011) Polycomb-repressed genes have permissive enhancers that initiate reprogramming. Cell 147:1283–1294CrossRefPubMedCentralPubMedGoogle Scholar
  48. Tachibana M, Sugimoto K, Fukushima T, Shinkai Y (2001) Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem 276:25309–25317CrossRefPubMedGoogle Scholar
  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedCentralPubMedGoogle Scholar
  50. Tao Y, Neppl RL, Huang ZP, Chen J, Tang RH, Cao R, Zhang Y, Jin SW, Wang DZ (2011) The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly. J Cell Biol 194:551–565CrossRefPubMedCentralPubMedGoogle Scholar
  51. Verrier L, Escaffit F, Chailleux C, Trouche D, Vandromme M (2011) A new isoform of the histone demethylase JMJD2A/KDM4A is required for skeletal muscle differentiation. PLoS Genet 7:e1001390CrossRefPubMedCentralPubMedGoogle Scholar
  52. Wang AH, Zare H, Mousavi K, Wang C, Moravec CE, Sirotkin HI, Ge K, Gutierrez-Cruz G, Sartorelli V (2013) The histone chaperone Spt6 coordinates histone H3K27 demethylation and myogenesis. EMBO J 32:1075–1086CrossRefPubMedCentralPubMedGoogle Scholar
  53. Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, Zhang Y (2001) Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8:1207–1217CrossRefPubMedGoogle Scholar
  54. Wardle FC, Odom DT, Bell GW, Yuan B, Danford TW, Wiellette EL, Herbolsheimer E, Sive HL, Young RA, Smith JC (2006) Zebrafish promoter microarrays identify actively transcribed embryonic genes. Genome Biol 7:R71CrossRefPubMedCentralPubMedGoogle Scholar
  55. Yamane H, Nishikawa A (2013) Differential muscle regulatory factor gene expression between larval and adult myogenesis in the frog Xenopus laevis: adult myogenic cell-specific myf5 upregulation and its relation to the notochord suppression of adult muscle differentiation. Vitro Cell Dev Biol Anim 49:524–536CrossRefGoogle Scholar
  56. Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y (1998) Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates “reserve cells”. J Cell Sci 111:769–779PubMedGoogle Scholar
  57. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Iban Seiliez
    • 1
  • Jacob Michael Froehlich
    • 2
  • Lucie Marandel
    • 1
  • Jean-Charles Gabillard
    • 3
  • Peggy R. Biga
    • 2
  1. 1.INRA, UR1067 Nutrition Métabolisme AquacultureSt-Pée-sur-NivelleFrance
  2. 2.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.INRA, UR1037 Laboratoire de Physiologie et Génomique des PoissonsRennesFrance

Personalised recommendations