Identification of a novel transforming growth factor-β (TGF-β6) gene in fish: Regulation in skeletal muscle by nutritional state

BMC Molecular Biology

Volumn 11, Issue , 2010, Pages

  Funkenstein, Bruria ^a   Olekh, Elena ^a   Jakowlew, Sonia B ^b  

^a ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYSTEINE; GROWTH HORMONE; PEPTIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA6; UNCLASSIFIED DRUG; FISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DIET RESTRICTION; EMBRYO; EXON; EYE; FISH; FOOD INTAKE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC CONSERVATION; GROWTH REGULATION; HYPOPHYSIS; INTRON; LARVA; LIVER; MARINE SPECIES; MOLECULAR EVOLUTION; MUSCLE GROWTH; MUSCLE TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITIONAL STATUS; PROTEIN CLEAVAGE; PROTEIN MOTIF; SEA BREAM; SKELETAL MUSCLE; SKIN; ANIMAL; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

ARCHOSARGUS RHOMBOIDALIS; MAMMALIA; SPARUS AURATA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; FISH PROTEINS; GENE EXPRESSION REGULATION; LARVA; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; PHYLOGENY; SEA BREAM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFORMING GROWTH FACTOR BETA;

EID: 77951998003     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-11-37     Document Type: Article

References (77)

1. Massagué J. TGF-β signal transduction. Annu Rev Biochem 1998, 67:753-791. 10.1146/annurev.biochem.67.1.753, 9759503.
2. De Martin R, Haendler B, Hofer-Warbinek R, Guagitsch H, Wrann M, Schlüsener H, Seifert JM, Bodmer S, Fontana A, Hofer E. Complementary DNA for human glioblastoma-derived T cell suppressor factor, a novel member of the transforming growth factor-β gene family. EMBO J 1987, 6:3673-3677. 553836, 3322813.
3. Derynck R, Jarrett JA, Chen EY, Eaton DH, Bell JR, Assoian RK, Roberts AB, Sporn MB, Goeddel DV. Human transforming growth factor-β cDNA sequence and expression in tumor cell lines. Nature 1985, 316:701-705. 10.1038/316701a0, 3861940.
4. Miller DA, Lee A, Matsui Y, Chen EY, Moses HL, Derynck R. Complementary DNA cloning of the murine transforming growth factor-β3 precursor and the comparative expression of TGF- β3 and TGF- β1 mRNA in murine embryos and adult tissues. Mol Endocrinol 1989, 3:1926-1934. 10.1210/mend-3-12-1926, 2628730.
5. Miller DA, Lee A, Pelton RW, Chen EY, Moses HL, Derynck R. Murine transforming growth factor-β2 cDNA sequence and expression in adult tissues and embryos. Mol Endocrinol 1989, 3:1108-1114. 10.1210/mend-3-7-1108, 2797004.
6. ten Dijke P, Hansen P, Iwata KK, Pieler C, Foulkes JG. Identification of another member of the transforming growth factor type β gene family. Proc Natl Acad Sci USA 1988, 85:4715-4719. 10.1073/pnas.85.13.4715, 280506, 3164476.
7. Van Obberghen-Schilling E, Kondaiah P, Ludwig RL, Sporn MB, Baker CC. Complementary deoxyribonucleic acid cloning of bovine transforming growth factor-β1. Mol Endocrinol 1987, 1:693-698. 10.1210/mend-1-10-693, 3153459.
8. Jakowlew SB, Dillard PJ, Kondaiah P, Sporn MB, Roberts AB. Complementary deoxyribonucleic acid cloning of a novel transforming growth factor-β from chick embryo chondrocytes. Mol Endocrinol 1988, 2:747-755. 10.1210/mend-2-8-747, 3211158.
9. Jakowlew SB, Dillard PJ, Sporn MB, Roberts AB. Nucleotide sequence of chicken transforming growth factor-β1 (TGF-β1). Nucleic Acids Res 1988, 16:8730. 10.1093/nar/16.17.8730, 338608, 3166520.
10. Jakowlew SB, Dillard PJ, Sporn MB, Roberts AB. Complementary deoxyribonucleic acid cloning of a messenger ribonucleic acid encoding transforming growth factor β4 from chicken embryo chondrocytes. Mol Endocrinol 1988, 2:1186-1195. 10.1210/mend-2-12-1186, 2464131.
11. Jakowlew SB, Dillard PJ, Sporn MB, Roberts AB. Complementary deoxyribonucleic acid cloning of an mRNA encoding transforming growth factor-β2 from chicken embryo chondrocytes. Growth Factors 1990, 2:123-133. 10.3109/08977199009071499, 2340183.
12. Kondaiah P, Sands MJ, Smith JM, Fields A, Roberts AB, Sporn MB, Melton DA. Identification of a novel transforming growth factor-β (TGF-β5) mRNA in Xenopus laevis. J Biol Chem 1990, 265:1089-1093.
13. Rebbert ML, Bhatia-Dey N, Dawid IB. The sequence of TGF-β2 from Xenopus laevis. Nucleic Acids Res 1990, 18:2185. 10.1093/nar/18.8.2185, 330711, 2336403.
14. Funkenstein B, Cavari B, Jakowlew S. Cloning and expression of TGF-β during early development of fish [abstract]. Am Zool 1994, 34(5):27A.
15. Funkenstein B, Shemer R, Cavari B, Jakowlew S. Identification of developmentally regulated transcripts related to transforming growth factor β (TGF-β) in fish [abstract]. 1st Meeting of Federation of Israeli Societies for Experimental Biology (F.I.S.E.B.) 1995, P19.
16. Daniels GD, Secombes CJ. Genomic organization of rainbow trout, Oncorhynchus mykiss TGF-β. Dev Comp Immunol 1999, 23:139-147. 10.1016/S0145-305X(98)00051-2, 10227481.
17. Hardie LJ, Laing KJ, Daniels GD, Grabowski PS, Cunningham C, Secombes CJ. Isolation of the first piscine transforming growth factor β gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus myskiss). Cytokine 1998, 10:555-563. 10.1006/cyto.1997.0334, 9722928.
18. Yin Z, Kwang J. Molecular isolation and characterization of carp transforming growth factor β1 from activated leucocytes. Fish Shellfish Immunol 2000, 10:309-318. 10.1006/fsim.1999.0241, 10938741.
19. Harms CA, Kennedy-Stoskopf S, Horne WA, Fuller FJ, Tompkins WAF. Cloning and sequencing hybrid striped bass (Morone saxatilis x M. chrysops) transforming growth factor-β (TGF-β), and development of a reverse transcription quantitative competitive polymerase chain reaction (RT-qcPCR) assay to measure TGF-β mRNA of teleost fish. Fish Shelfish Immuno 2000, 10:61-85.
20. Laing KJ, Cunningham C, Secombes CJ. Genes for three different isoforms of transforming growth factor- β are present in plaice (Pleuronectes platessa) DNA. Fish Shellfish Immunol 2000, 10:261-271. 10.1006/fsim.1999.0255, 10938738.
21. Kohli G, Hu S, Clelland E, Di Muccio T, Rothenstein J, Peng C. Cloning of transforming growth factor-β1 (TGF-β1) and its type II receptor from zebrafish ovary and role of TGF-β1 in oocyte maturation. Endocrinology 2003, 144:1931-1941. 10.1210/en.2002-0126, 12697700.
22. Tafalla C, Aranguren R, Secombes CJ, Castrillo JL, Novoa B, Figueras A. Molecular characterization of sea bream (Sparus aurata) transforming growth factor β1. Fish Shellfish Immunol 2003, 14:405-421. 10.1006/fsim.2002.0444, 12711274.
23. Haddad G, Hanington PC, Wilson EC, Grayfer L, Belosevic M. Molecular and functional characterization of goldfish (Carassius auratus L.) transforming growth factor β. Dev Comp Immunol 2008, 32:654-663. 10.1016/j.dci.2007.10.003, 18036659.
24. Sumathy K, Desai KV, Kondaiah P. Isolation of transforming growth factor-β2 cDNA from a fish, Cyprinus carpio by RT-PCR. Gene 1997, 191:103-107. 10.1016/S0378-1119(97)00048-6, 9210595.
25. Wyatt L, Wadham C, Crocker LA, Lardelli M, Khew-Goodall Y. The protein tyrosine phosphatase Pez regulates TGF β, epithelial-mesenchymal transition, and organ development. J Cell Biol 2007, 178:1223-1235. 10.1083/jcb.200705035, 2064655, 17893246.
26. Laing KJ, Pilstrom L, Cunningham C, Secombes CL. TGF-β3 exists in bony fish. Vet Immunol Immunopathol 1999, 72:45-53. 10.1016/S0165-2427(99)00116-6, 10614492.
27. Cheah FSH, Jabs EW, Chong SS. Genomic, cDNA, and embryonic expression analysis of zebrafish transforming growth factor β3 (tgfβ3). Dev Dyn 2005, 232:1021-1030. 10.1002/dvdy.20282, 15739231.
28. Jakowlew SB, Cimet G, Tuan RS, Sporn MB, Roberts AB. Expression of transforming growth factor-β2 and β3 mRNAs and proteins in the developing chicken embryo. Differentiation 1994, 55:105-118. 10.1046/j.1432-0436.1994.5520105.x, 8143928.
29. Akhurst RJ, Fitzpatrick DR, Gatherer D, Lehnert SA, Millan FA. Transforming growth factor βs in mammalian embryogenesis. Prog Growth Factor Res 1990, 2:153-168. 10.1016/0955-2235(90)90002-2, 2132953.
30. Kollias HD, McDermott JC. Transforming growth factor-β and myostatin signaling in skeletal muscle. J Appl Physiol 2008, 104:579-587. 10.1152/japplphysiol.01091.2007, 18032576.
31. Lafyatis R, Lechleider R, Roberts AB, Sporn MB. Secretion and transcriptional regulation of transforming growth factor-β3 during myogenesis. Mol Cell Biol 1991, 11:3795-3803. 361150, 1710772.
32. Koishi K, Dalzell KGB, McLennan IS. The expression and structure of TGF-β2 transcripts in rat muscles. Biochim Biophys Acta 2000, 1492:311-319.
33. Liu D, Black BL, Derynck R. TGF-β inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev 2001, 15:2950-2966. 10.1101/gad.925901, 312830, 11711431.
34. Schabort EJ, Merwe M, Loos B, Moore FP, Niesler CU. TGF-β's delay skeletal muscle progenitor cell differentiation in an isoform-independent manner. Exp Cell Res 2009, 315:373-384. 10.1016/j.yexcr.2008.10.037, 19038250.
35. Zhu J, Li Y, Shen W, Qiao C, Ambrosio F, Lavasani M, Nozaki M, Branca MF, Huard J. Relationships between TGF-β1, myostatin, and decorin: implications for skeletal fibrosis. J Biol Chem 2007, 282:25852-25863. 10.1074/jbc.M704146200, 17597062.
36. Harms CA, Ottinger CA, Blazer VS, Densmore CL, Pieper LH, Kennedy-Stoskopf S. Quantitative polymerase chain reaction for transforming growth factor-β applied to a field study of fish health in Chesapeake Bay tributaries. Environ Health Perspect 2000, 108:447-452. 10.2307/3454386, 1638039, 10811572.
37. Yang M, Zhou H. Grass carp transforming growth factor-β1 (TGF-β1): molecular cloning, tissue distribution and immunobiological activity in teleost peripheral blood lymphocytes. Mol Immunol 2008, 45:1792-1798. 10.1016/j.molimm.2007.09.027, 17980429.
38. Castillo J, Teles M, Mackenzie S, Tort L. Stress-related hormones modulate cytokine expression in the head kidney of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 2009, 27:493-499. 10.1016/j.fsi.2009.06.021, 19591943.
39. Kohli G, Clelland E, Peng C. Potential targets of transforming growth factor-β1 during inhibition of oocyte maturation in zebrafish. Rep Biol Endocrinol 2005, 3:53-63.
40. Tan Q, Zagrodny A, Bernaudo S, Peng C. Regulation of membrane progestin receptors in the zebrafish ovary by gonadotropin activin TGF-β and BMP-15. Mol Cell Endocrinol 2009, 312:72-79. 10.1016/j.mce.2009.03.011, 19773085.
41. Rowlerson A, Veggetti A. Cellular mechanisms of post-embryonic muscle growth in aquaculture species. Muscle Development and Growth, Fish Physiology 2001, 18:103-140. San Diego: Academic Press, Johnston IA.
42. Funkenstein B, Jakowlew SB. Piscine (Sparus aurata) α subunit of the G-protein transducin is homologous to mammalian cone and rod transducin. Vision Res 1997, 37:2487-2494. 10.1016/S0042-6989(97)00062-X, 9373680.
43. Funkenstein B, Perrot V, Brown CL. Cloning and ontogeny of putative piscine (Sparus aurata) transthyretin: developmental expression and tissue distribution. Mol Cell Endocrinol 1999, 157:67-73. 10.1016/S0303-7207(99)00160-4, 10619398.
44. Funkenstein B, Jakowlew SB. Molecular cloning of fish alcohol dehydrogenase cDNA. Gene 1996, 174:159-164. 10.1016/0378-1119(96)00513-6, 8863743.
45. Funkenstein B, Skopal T, Rapoport B, Rebhan Y, Du SJ, Radaelli G. Characterization and functional analysis of the 5' flanking region of myosin light chain-2 gene expressed in white muscle of the gilthead sea bream (Sparus aurata). Comp Biochem Physiol Genomics and Proteomics Part D 2007, 2:187-199.
46. Altschul SF, Madden TL, Schaeffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
47. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. TheClustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
48. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
49. Hubbard TJP, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, et al. Ensembl 2009. Nucl AcidsRes 2009, 37:D690-D697.
50. Denhez F, Lafyatis R, Kondaiah P, Roberts AB, Sporn MB. Cloning by polymerase chain reaction of a new mouse TGF-β, mTGF-β3. Growth Factors 1990, 3:139-146. 10.3109/08977199009108276, 2206556.
51. Daopin S, Piez KA, Ogawa Y, Davies DR. Crystal structure of transforming growth factor-β2: an unusual fold for the superfamily. Science 1992, 257:369-373. 10.1126/science.1631557, 1631557.
52. Schlunegger MP, Grütter MG. An unusual feature revealed by the crystal structure at 2.2 A resolution of human transforming growth factor-β2. Nature 1992, 358:430-434. 10.1038/358430a0, 1641027.
53. Derynck R, Lindquist DB, Lee A, Wen D, Tamm J, Graycar JL, Rhee L, Mason AJ, Miller DA, Coffey RJ, Moses HL, Chen EY. A new type of transforming growth factor-β, TGF-β3. The EMBO J 1988, 7:3737-3743.
54. Hart PJ, Deep S, Taylor A, Shu Z, Hinck CS, Hinck AP. Crystal structure of the human TβR2 ectodomain-TGF-β3 complex. Nature Struct Biol 2002, 9:203-208.
55. Derynck R, Rhee L, Chen EY, Van Tilburg A. Intron-exon structure of the human transforming growth factor-β precursor gene. Nucleic Acids Res 1987, 15:3188-3189. 10.1093/nar/15.7.3188, 340929, 3470709.
56. Burt DW, Paton IR. Molecular cloning and primary structure of the chicken transforming growth factor-β2 gene. DNA Cell Biol 1991, 10:723-734. 10.1089/dna.1991.10.723, 1683775.
57. Burt DW, Dey BR, Paton IR, Morrice DR, Law AS. The chicken transforming growth factor-β3 gene: genomic structure, transcriptional analysis, and chromosomal location. DNA Cell Biol 1995, 14:111-123. 10.1089/dna.1995.14.111, 7865129.
58. Vempati UD, Kondaiah P. Molecular organization of the gene encoding Xenopus laevis transforming growth factor-β5. Biochem Mol Biol Int 1998, 45:997-1003.
59. Fujii D, Brissenden JE, Derynck R, Francke U. Transforming growth factor β gene maps to human chromosome 19 long arm and to mouse chromosome 7. Somat Cell Mol Genet 1986, 12:281-288. 10.1007/BF01570787, 3459257.
60. Barton DE, Foellmer BE, Du J, Tamm J, Derynck R, Francke U. Chromosomal mapping of genes for transforming growth factors β2 and β3 in man and mouse: dispersion of TGF-β gene family. Oncogene Res 1988, 3:323-331.
61. ten Dijke P, Geurts van Kessel AH, Foulkes JG, Le Beau MM. Transforming growth factor type β3 maps to human chromosome 14, region q23-q24. Oncogene 1988, 3:721-724.
62. Saunders AM, Seldin MF. A molecular genetic linkage map of mouse chromosome 7. Genomics 1990, 8:525-535. 10.1016/0888-7543(90)90040-2, 1981054.
63. Dickinson ME, Kobrin MS, Silan CM, Kingsley DM, Justice MJ, Miller DA, Ceci JD, Lock LF, Lee A, Buchberg AM, Siracusa LD, Lyons KM, Derynck R, Hogan BLM, Copeland NG, Jenkins NA. Chromosomal localization of seven members of the murine TGF-β superfamily suggests close linkage to several morphogenetic mutant loci. Genomics 1990, 6:505-520. 10.1016/0888-7543(90)90480-I, 1970330.
64. Burt DW, Paton IR. Evolutionary origins of the TGF-β gene family. DNA Cell Biol 1992, 11:497-510. 10.1089/dna.1992.11.497, 1388723.
65. Chauvigné F, Gabillard JC, Weil C, Rescan PY. Effects of refeeding on IGFI, IGFII, IGF receptors, FGF2, FGF6, and myostatin mRNA expression in rainbow trout myotomal muscle. Gen Comp Endocrinol 2003, 132:209-215. 10.1016/S0016-6480(03)00081-9, 12812767.
66. Gabillard JC, Kamangar BB, Monserrat N. Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J Endocrinol 2006, 191:15-24. 10.1677/joe.1.06869, 17065385.
67. Montserrat N, Gabillard JC, Capilla E, Navarro MI, Gutiérrez J. Role of insulin, insulin-like growth factors, and muscle regulatory factors in the compensatory growth of the trout (Oncorhynchus mykiss). Gen Comp Endocrinol 2007, 150:462-472. 10.1016/j.ygcen.2006.11.009, 17196198.
68. Montserrat N, Gómez-Requeni P, Bellini G, Capilla E, Pérez-Sánchez J, Navarro I, Gutiérrez J. Distinct role of insulin and its receptors in white skeletal muscle during the compensatory growth of gilthead sea bream (Sparus aurata). Aquaculture 2007, 267:188-198.
69. Terova G, Bernardini G, Binelli G, Gornati R, Sargolia M. cDNA encoding sequences for myostatin and FGF6 in sea bass (Dicentrarchus labrax, L.) and the effect of fasting and refeeding on their abundance levels. Domest Anim Endocrinol 2006, 30:304-319. 10.1016/j.domaniend.2005.08.003, 16183242.
70. Terova G, Rimoldi S, Chini V, Gornati R, Bernardini G, Sargolia M. Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax, L.) during long-term fasting and refeeding. J Fish Biol 2007, 70(Suppl B):219-233.
71. Jeanplong F, Bass JJ, Smith HK, Kirk SP, Kambadur R, Sharma M, Oldham JM. Prolonged underfeeding of sheep increases myostatin and myogenic regulatory factor Myf-5 in skeletal muscle while IGF-I and myogenin are repressed. J Endocrinol 2003, 176:425-437. 10.1677/joe.0.1760425, 12630927.
72. Fernández AM, Dupont J, Farrat RP, Lee S, Stannard B, LeRoith D. Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J Clin Invest 2002, 109:347-355. 150853, 11827994.
73. Spiller MP, Kambadur R, Jeanplong F, Thomas M, Matyn JK, Bass JJ, Sharma M. The myostatin gene is a downstream target of basic helix-loop-helix transcription facor MyoD. Mol Cell Biol 2002, 22:7066-7082. 10.1128/MCB.22.20.7066-7082.2002, 139803, 12242286.
74. Liu W, Thomas SG, Asa SL, Gonzalez-Cadavid N, Bhasin S, Ezzat S. Myostatin is a skeletal muscle target of growth hormone anabolic action. J Clin Endocrinol Metab 2003, 88:5490-5496. 10.1210/jc.2003-030497, 14602795.
75. Florini JR, Ewton DZ, Coolican SA. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 1996, 17:481-517.
76. Saxena VK, Sundaresan NR, Malik F, Ahmed KA, Saxena M, Kumar S, Nandedkar PV, Singh RV. Temporal expression of transforming growth factor-β2 and myostatin mRNA during embryonic myogenesis in Indian broilers. Res Vet Sci 2007, 82:50-53. 10.1016/j.rvsc.2006.05.005, 16870219.
77. Suryawan A, Frank JW, Nguyen HV, Davis TA. Expression of the TGF-β family of ligands is developmentally regulated in skeletal muscle of neonatal rats. Pediatr Res 2006, 59:175-179. 10.1203/01.pdr.0000196718.47935.6e, 16439574.