Multiple cis-elements in the 5'-flanking region of embryonic/larval fast-type of the myosin heavy chain gene of torafugu, MYHM743-2, function in the transcriptional regulation of its expression

Gene

Volumn 489, Issue 1, 2011, Pages 41-54

  Asaduzzaman, Md ^a   Kinoshita, Shigeharu ^a   Siddique, Bhuiyan Sharmin ^a   Asakawa, Shuichi ^a   Watabe, Shugo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cis elements; MYHM743 2; Promoter assay; Torafugu; Transcriptional regulation; Zebrafish

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; MYOCYTE ENHANCER FACTOR 2; MYOSIN HEAVY CHAIN; SERUM RESPONSE FACTOR;

ANIMAL EMBRYO; ANIMAL TISSUE; ARTICLE; BASE PAIRING; BINDING SITE; DNA FLANKING REGION; FACE MUSCLE; FAST MUSCLE FIBER; FISH GENETICS; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; IMMUNOHISTOCHEMISTRY; LARVA; MYOBLAST; NONHUMAN; PECTORAL MUSCLE; PRIORITY JOURNAL; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; TRANSIENT EXPRESSION; ZEBRA FISH;

5' FLANKING REGION; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BINDING SITES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MYOD PROTEIN; MYOGENIC REGULATORY FACTORS; MYOSIN HEAVY CHAINS; PROMOTER REGIONS, GENETIC; SERUM RESPONSE FACTOR; TAKIFUGU; ZEBRAFISH;

DANIO RERIO; TAKIFUGU RUBRIPES;

EID: 80053969207     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2011.08.005     Document Type: Article

References (65)

1. Allen D.L., Weber J.N., Sycuro L.K., Leinwand L.A. Myocyte enhancer factor-2 and serum response factor binding elements regulate fast myosin heavy chain transcription in vivo. J. Biol. Chem. 2005, 280:17126-17134.
2. Arsenian S., Weinhold B., Oelgeschlager M., Ruther U., Nordheim A. Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J. 1998, 17:6289-6299.
3. Berdougo E., Coleman H., Lee D.H., Stainier D.Y., Yelon D. Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development 2003, 130:6121-6129.
4. Bergstrom D.A., Penn B.H., Strand A., Perry R.L., Rudnicki M.A., Tapscott S.J. Promoter-specific regulation of MyoD binding and signal transduction cooperates to pattern gene expression. Mol. Cell 2002, 9:587-600.
5. Berkes C.A., Tapscott S.J. MyoD and the transcriptional control of myogenesis. Cell Dev. Biol. 2005, 16:585-595.
6. Bryson-Richardson R.J., Daggett D.F., Cortes F., Neyt C., Keenan D.G., Currie P.D. Myosin heavy chain expression in zebrafish and slow muscle composition. Dev. Dyn. 2005, 233:1018-1022.
7. Buckingham M. Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Dev. 2001, 11:440-448.
8. Camoretti-Mercado B., Dulin N.O., Solway J. Serum response factor function and dysfunction in smooth muscle. Respir. Physiol. Neurobiol. 2003, 137:223-235.
9. Chen Y.H., et al. Multiple upstream modules regulate zebrafish myf5 expression. BMC Dev. Biol. 2007, 7:1-14.
10. Crow M.T., Stockdale F.E. Myosin expression and specialization among the earliest muscle fibers of the developing avian limb. Dev. Biol. 1986, 113:238-254.
11. Davis J.L., Long X., Georger M.A., Scott I.C., Rich A., Miano J.M. Expression and comparative genomics of two serum response factor genes in zebrafish. Int. J. Dev. Biol. 2008, 52:389-396.
12. Devoto S.H., Melancon E., Eisen J.S., Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo prior to somite formation. Development 1996, 122:3371-3380.
13. Du S.J., 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 2003, 134:123-134.
14. Du S.J., Rotllant J., Tan X. Muscle-specific expression of the smyd1 gene is controlled by its 5.3-kb promoter and 5'-flanking sequence in zebrafish embryos. Dev. Dyn. 2006, 235:3306-3315.
15. Ennion S., Wilkes D., Gauvry L., Alami-Durante H., Goldspink G. Identification and expression analysis of two developmentally regulated myosin heavy chain gene transcript in carp (Cyprinus carpio). J. Exp. Biol. 1999, 202:1081-1090.
16. Fisher S., et al. Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat. Protoc. 2006, 1:1297-1305.
17. Gauvry L.L., Ennion S., Hansen E., Butterworth P., Goldspink G. The characterization of the 5'-regulatory region of a temperature-induced myosin-heavy-chain gene associated with myotomal muscle growth in the carp. Eur. J. Biochem. 1996, 236:887-894.
18. Harrison B.C., Allen D.L., Leinwand L.A. IIb or not IIb? Regulation of myosin heavy chain gene expression in mice and men. Skeletal Muscle 2011, 1:5.
19. Hautmann M.B., Madsen C.S., Mack C.P., Owens G.K. Substitution of the degenerate smooth muscle (SM)α-actin CC(A/T-rich)6GG elements with c-fos serum response elements results in increased basal expression but relaxed SM cell specificity and reduced angiotensin II inducibility. J. Biol. Chem. 1998, 273:8398-8406.
20. Hernandez L.P., Patterson S.E., Devoto S.H. The development of muscle fiber type identity in zebrafish craniofacial muscles. Anat. Embryol. 2005, 209:323-334.
21. Hinits Y., Osborn D.P.S., Hughes S.M. Differential requirements for myogenic regulatory factors distinguish medial and lateral somatic, craniofacial and fin muscle fiber populations. Development 2009, 136:403-414.
22. Hirayama Y., Watabe S. Structural differences in the crossbridge head of temperature-associated myosin subfragment-1 isoforms from carp fast skeletal muscle. Eur. J. Biochem. 1997, 246:380-387.
23. Ikeda D., et al. Genomic structural analysis of the pufferfish (Takifugu rubripes) skeletal myosin heavy chain genes. Mar. Biotechnol. 2004, 6:S462-S467.
24. Ikeda D., Ono Y., Snell P., Edwards Y.J., Elgar G., Watabe S. Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis. Physiol. Genomics 2007, 32:1-15.
25. Ikeda D., Nihei Y., Ono Y., Watabe S. Three embryonic myosin heavy chain genes encoding different motor domain structures from common carp show distinct expression patterns in craniofacial muscles. Mar. Genomics 2010, 3:1-9.
26. Jin D., Ni T.T., Hou J., Rellinger E., Zhong T.P. Promoter analysis of ventricular myosin heavy chain (vmhc) in zebrafish embryos. Dev. Dyn. 2009, 238:1760-1767.
27. Johnston I.A., Cole N.J., Abercromby M., Vieira V. Embryonic temperature modulates muscle growth characteristics in larval and juvenile herring. J. Exp. Biol. 1998, 201:623-646.
28. Jordan T., Jiang H., Li H., DiMario J.X. Inhibition of ryanodine receptor 1 in fast skeletal muscle fibers induces a fast-to-slow muscle fiber type transition. J. Cell Sci. 2004, 11:6175-6183.
29. Kawakami K., Shima A., Kawakami N. Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11403-11408.
30. Kawakami K., Takeda H., Kawakami N., Kobayashi M., Matsuda N., Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 2004, 7:133-144.
31. Kobiyama A., Hirayama M., Muramatsu-Uno M., Watabe S. Functional analysis on the 5'-flanking region of carp fast skeletal myosin heavy chain genes for their expression at different temperatures. Gene 2006, 372:82-91.
32. Koga A., Suzuki M., Inagaki H., Bessho Y., Hori H. Transposable element in fish. Nature 1996, 383:30.
33. Korzh V. Transposons as tools for enhancer trap screens in vertebrates. Genome Biol. 2007, 8(Suppl. 1):S8.
34. Lakich M.M., Diagana T.T., North D.L., Whalen R.G. MEF-2 and Oct-1 bind to two homologous promoter sequence elements and participate in the expression of a skeletal muscle-specific gene. J. Biol. Chem. 1998, 273:15217-15226.
35. Leung S., Miyamoto N.G. Point mutational analysis of the human c-fos serum responsible factor binding site. Nucl. Acid Res. 1989, 14:1177-1195.
36. Li S., et al. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1082-1087.
37. Liang C.S., et al. Fast skeletal muscle myosin heavy chain gene cluster of medaka Oryzias latipes enrolled in temperature adaptation. Physiol. Genomics 2007, 29:201-214.
38. Liang C.S., et al. Myocyte enhancer factor 2 regulates expression of medaka Oryzias latipes fast skeletal myosin heavy chain genes in a temperature-dependent manner. Gene 2008, 407:42-53.
39. Lin C.-Y., Yung R.-F., Lee H.-C., Chen W.-T., Chen Y.-H., Tsai H.-J. Myogenic regulatory factors Myf5 and Myod function distinctly during craniofacial myogenesis of zebrafish. Dev. Biol. 2006, 299:594-608.
40. Mack C.P., Owens G.K. Regulation of smooth muscle alpha-actin expression in vivo is dependent on CArG elements within the 5' and first intron promoter regions. Circ. Res. 1999, 84:852-861.
41. Mascarello F., Rowlerson A., Radaelli G., Scapolo P.A., Veggetti A. Differentiation and growth of muscle in the fish Sparus aurata (L): I. Myosin expression and organization of fiber types in lateral muscle from hatching to adult. J. Muscle Res. Cell Motil. 1995, 16:213-222.
42. McGuigan K., Phillips P.C., Postlethwait J.H. Evolution of sarcomeric myosin heavy chain genes: evidence from fish. Mol. Biol. Evol. 2004, 21:1042-1056.
43. Miano J.M. Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 2003, 35:577-593.
44. Miano J.M., Carlson M.J., Spencer J.A., Misra R.P. Serum response factor-dependent regulation of the smooth muscle calponin gene. J. Biol. Chem. 2000, 275:9814-9822.
45. Nihei Y., et al. Molecular cloning and mRNA expression analysis of carp embryonic, slow and cardiac myosin heavy chain isoforms. J. Exp. Biol. 2006, 209:188-198.
46. Norman C., Runswick M., Pollock R., Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 1988, 55:989-1003.
47. Ono Y., Liang C., Ikeda D., Watabe S. cDNA cloning of myosin heavy chain genes from medaka Oryzias latipes embryos and larvae and their expression patterns during development. Dev. Dyn. 2006, 235:3092-3101.
48. Ono Y., Kinoshita S., Ikeda D., Watabe S. Early development of medaka Oryzias latipes muscles as revealed by transgenic approaches using embryonic and larval types of myosin heavy chain genes. Dev. Dyn. 2010, 239:1807-1817.
49. Park J.-S., et al. Isolation of a ventricle-specific promoters for the zebrafish ventricular myosin heavy chain (vmhc) gene and its regulation by GATA factors during embryonic heart development. Dev. Dyn. 2009, 238:1574-1581.
50. Patterson S.E., Mook L.B., Devoto S.H. Growth in the larval zebrafish pectoral fin and trunk musculature. Dev. Dyn. 2008, 237:307-315.
51. Pellegrini L., Tan S., Richmond T.J. Structure of serum response factor core bound to DNA. Nature 1995, 376:490-498.
52. Rawls A., Olson E.N. MyoD meets its maker. Cell 1997, 89:5-8.
53. Rescan P.Y., et al. Red and white muscle development in the trout (Oncorhynchus mykiss) as shown by in situ hybridization of fast and slow myosin heavy chain transcripts. J. Exp. Biol. 2001, 204:2097-2101.
54. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
55. Shore P., Sharrocks A.D. The MADS-box family of transcription factors. Eur. J. Biochem. 1995, 229:1-13.
56. Swoap S.J. In vivo analysis of the myosin heavy chain IIB promoter region. Am. J. Physiol. 1998, 274:C681-C687.
57. Thorsen D.H., Hale M.E. Development of zebrafish (Danio rerio) pectoral fin musculature. J. Morphol. 2005, 266:241-255.
58. Wallace K.N., et al. Mutation of smooth muscle myosin causes epithelial invasion and cystic expansion of the zebrafish intestine. Dev. Cell 2005, 8:717-726.
59. Watabe S. Temperature plasticity of contractile proteins in fish muscle. J. Exp. Biol. 2002, 205:2231-2236.
60. Watabe S., Ikeda D. Diversity of the pufferfish Takifugu rubripes fast skeletal myosin heavy chain genes. Comp. Biochem. Physiol. D 2006, 1:28-34.
61. Weiss A., Leinwand L.A. The mammalian myosin heavy chain gene family. Annu. Rev. Cell Dev. Biol. 1996, 12:417-439.
62. Weiss A., et al. Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2958-2963.
63. Westerfield M. The Zebrafish Book 1995, University of Oregon Press, Eugene, OR.
64. Xu Y., He J., Wang X., Lim T.M., Gong Z. Asynchronous activation of 10 muscle specific protein (MSP) genes during zebrafish somitogenesis. Dev. Dyn. 2000, 219:201-215.
65. Yasmin L., et al. A 5'-flanking region of embryonic-type myosin heavy chain gene, MYHM743-2, from torafugu Takifugu rubripes regulates developmental muscle-specific expression. Comp. Biochem. Physiol. D 2011, 6:76-81.