Muscle-specific growth hormone receptor (GHR) overexpression induces hyperplasia but not hypertrophy in transgenic zebrafish

Transgenic Research

Volumn 21, Issue 3, 2012, Pages 457-469

  Figueiredo, Marcio Azevedo ^a   Mareco, Edson A ^b   Silva, Maeli Dal Pai ^b   Marins, Luis Fernando ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Growth hormone receptor; Hyperplasia; Insulin like growth factor I; Skeletal muscle; Suppressors of cytokine signaling; Transgenic zebrafish

Indexed keywords

GROWTH HORMONE RECEPTOR; MYOGENIC FACTOR; PHOTOPROTEIN; RED FLUORESCENT PROTEIN; SOCS1 PROTEIN, ZEBRAFISH; SOMATOMEDIN C RECEPTOR; SUPPRESSOR OF CYTOKINE SIGNALING; ZEBRAFISH PROTEIN;

ANIMAL; ANIMAL MODEL; ARTICLE; BODY WEIGHT; GENE EXPRESSION REGULATION; GENE TRANSFER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPERPLASIA; HYPERTROPHY; METABOLISM; PATHOLOGY; PROMOTER REGION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY WEIGHT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TRANSFER TECHNIQUES; HYPERPLASIA; HYPERTROPHY; LUMINESCENT PROTEINS; MODELS, ANIMAL; MUSCLE, SKELETAL; MYOGENIC REGULATORY FACTORS; PROMOTER REGIONS, GENETIC; RECEPTOR, IGF TYPE 1; RECEPTORS, SOMATOTROPIN; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84860883618     PISSN: 09628819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11248-011-9546-2     Document Type: Article

References (75)

1. Argetsinger LS, Campbell GS, Yang X, Witthuhn BA, Silvennoinen O, Ihle JN, Carter-Su C (1993) Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 74: 237-244.
2. Baker BJ, Akhtar LN, Benveniste EN (2009) SOCS1 and SOCS3 in the control of CNS immunity. Trends Immunol 30: 392-400.
3. Bartke A, Chandrashekar V, Bailey B, Zaczek D, Turyn D (2002) Consequences of growth hormone (GH) overexpression and GH resistance. Neuropeptides 36: 201-208.
4. Björnsson BT, Johansson V, Benedet S, Einarsdottir IE, Hildahl J, Agustsson T, Jönsson E (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27: 227-242.
5. Blackwell T, Weintraub H (1990) Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250: 1104-1110.
6. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019.
7. Brooks AJ, Wooh JW, Tunny KA, Waters MJ (2008) Growth hormone receptor; mechanism of action. Int J Biochem Cell Biol 40: 1984-1989.
8. Butler AA, LeRoith DL (2001) Control of growth by the somatotrophic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annu Rev Physiol 63: 141-164.
9. Canosa LF, Chang JP, Peter RE (2007) Neuroendocrine control of growth hormone in fish. Gen Comp Endocrinol 151: 1-26.
10. Clemmons DR (2009) Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab 20(7): 349-356.
11. Cook JT, McNiven MA, Richardson GF, Sutterlin AM (2000) Growth rate, body composition and feed digestibility/conversion of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188: 15-32.
12. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR (1997) The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272(10): 6653-6662.
13. Croker BA, Kiu H, Nicholson SE (2008) SOCS regulation of the JAK/STAT signaling pathway. Semin Cell Dev Biol 19: 414-422.
14. Dahm R, Geisler R (2006) Learning from small fry: the zebrafish as a genetic model organism for aquaculture fish species. Mar Biotechnol 8: 329-345.
15. Daughaday WH (2000) Growth hormone axis overview-somatomedin hypothesis. Pediatr Nephrol 14: 537-540.
16. Devlin RH, Yesaki TY, Biagi CA, Donaldson EM, Swanson P, Chan WK (1994) Extraordinary salmon growth. Nature 371: 209-210.
17. Devlin RH, Biagi CA, Yesaki TY (2004) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236: 607-632.
18. Devlin RH, Sundstro LF, Muir WM (2006) Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends Biotechnol 24: 89-97.
19. DeVol DL, Rotwein P, Sadow JL, Novakofski J, Bechtel PJ (1990) Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am J Physiol 259: E89-E95.
20. Dominici FP, Argentino DP, Muñoz MC, Miquet JG, Sotelo AI, Turyn D (2005) Influence of the crosstalk between growth hormone and insulin signalling on the modulation of insulin sensitivity. Growth Horm IGF Res 15: 324-336.
21. Dunham RA (2004) Aquaculture and fisheries biotechnology: genetic approaches. CABI Publishing, Oxford.
22. Emerson CP (1990) Myogenesis and developmental control genes. Curr Opin Cell Biol 2: 1065-1075.
23. Figueiredo MA, Lanes CFC, Almeida DV, Proietti MC, Marins LF (2007a) The effect of GH overexpression on GHR and IGF-I gene regulation in different genotypes of GH-transgenic zebrafish. Comp Biochem Physiol Part D Genomics Proteomics 2: 228-233.
24. Figueiredo MA, Lanes CFC, Almeida DV, Marins LF (2007b) Improving the production of transgenic fish germline: in vivo mosaicism evaluation by GFP transgene co-injection strategy. Genet Mol Biol 30: 31-36.
25. Funkenstein B, Skopal T, Rapoport B, Rebhan Y, Du SJ, Radaelli G (2007) 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 Part D Genomics Proteomics 2: 187-199.
26. Glass DJ (2003) Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5: 87-90.
27. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984.
28. Greenhalgh CJ, Alexander WS (2004) Suppressors of cytokine signalling and regulation of growth hormone action. Growth Horm IGF Res 14: 200-206.
29. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551.
30. Herbert NA, Armstrong JD, Björnsson BT (2001) Evidence that growth hormone-induced elevation in rotine metabolism of juvenile Atlantic salmon is a result of increased spontaneous activity. J Fish Biol 59: 754-757.
31. Herrington J, Carter-Su C (2001) Signaling pathways activated by the growth hormone receptor. Trends Endocrinol Metab 12(6): 252-257.
32. Himpe E, Kooijman R (2009) Insulin-like growth factor-I receptor signal transduction and the Janus Kinase/Signal Transducer and Activator of Transcription (JAK-STAT) pathway. Biofactors 35(1): 76-81.
33. Ishtiaq Ahmed AS, Xiong F, Pang S-C, He M-D, Waters MJ, Zhu Z-Y, Sun Y-H (2011) Activation of GH signaling and GH-independent stimulation of growth in zebrafish by introduction of a constitutively activated GHR construct. Transgenic Res 20(3): 557-567.
34. Janssen JAMJL (2009) Advantages and disadvantages of GH/IGF-I combination treatment. Rev Endocr Metab Disord 10: 157-162.
35. Johansen KA, Overturf K (2005) Quantitative expression analysis of genes affecting muscle growth during development of rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 7: 576-587.
36. Johnston IA (1999) Muscle development and growth: potential implication for flesh quality in fish. Aquaculture 177: 99-115.
37. Ju B, Chong SW, He J, Wang X, Xu Y, Wan H, Tong Y, Yan T, Korzh V, Gong Z (2003) Recapitulation of fast skeletal muscle development in zebrafish by transgenic expression of GFP under the mylz2 promoter. Dev Dyn 227: 14-26.
38. Kim H, Barton E, Muja N, Yakar S, Pennisi P, LeRoith D (2005) Intact insulin and insulin-like growth factor-I receptor signaling is required for growth hormone effects on skeletal muscle growth and function in vivo. Endocrinology 146(4): 1772-1779.
39. Koumans JTM, Akster HA (1995) Myogenic cells in development and growth of fish. Comp Biochem Physiol A Mol Integr Physiol 110: 3-20.
40. Lassar A, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, Weintraub H (1989) MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58: 823-831.
41. LeRoith D, Bondy C, Yakar S, Liu JL, Butler A (2001) The somatomedin hypothesis: 2001. Endocr Rev 22(1): 53-74.
42. McKenzie DJ, Martinez IR, Morales A, Acosta J, Taylor EW, Steffensen JF, Estrada MP (2000) Metabolic rate, exercise performance and hypoxia tolerance of growth hormone transgenic tilapia (Oreochromis sp.). Comp Biochem Physiol 126: S66.
43. McKenzie DJ, Martínez R, Morales A, Acosta J, Morales R, Taylor EW, Steffensen JF, Estrada MP (2003) Effects of growth hormone transgenesis on metabolic rate, exercise performance and hypoxia tolerance in tilapia hybrids. J Fish Biol 63: 398-409.
44. Megeney LA, Rudnicki MA (1995) Determination versus differentiation and the MyoD family of transcription factors. Biochem Cell Biol 73: 723-732.
45. Mori T, Hiraka I, Kurata Y, Kawachi H, Mano N, Devlin RH, Nagoya H, Araki K (2007) Changes in hepatic gene expression related to innate immunity, growth and iron metabolism in GH-transgenic amago salmon (Oncorhynchus masou) by cDNA subtraction and microarray analysis, and serum lysozyme activity. Gen Comp Endocrinol 151: 42-54.
46. Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB (1989) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58: 537-544.
47. Nam YK, Noh JK, Cho YS, Cho HJ, Cho KN, Kim CG, Kim DS (2001) Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach Misgurnus mizolepis. Transgenic Res 10: 353-362.
48. 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: e36.
49. Pitkänen TI, Krasnov A, Teerijoki H, Mölsä H (1999) Transfer of growth hormone (GH) transgenes into Arctic charr (Salvelinus alpinus L.). I. Growth response to various GH constructs. Genet Anal 15: 91-98.
50. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013.
51. Rosa CE, Figueiredo MA, Lanes CFC, Almeida DV, Monserrat JM, Marins LF (2008) Metabolic rate and reactive oxygen species production in different genotypes of GH-transgenic zebrafish. Comp Biochem Physiol B Biochem Mol Biol 149: 209-214.
52. Rosa CE, Kuradomi RY, Almeida DV, Lanes CFC, Figueiredo MA, Dytz AG, Fonseca DB, Marins LF (2010) GH overexpression modifies muscle expression of anti-oxidant enzymes and increases spinal curvature of old zebrafish. Exp Gerontol 45: 449-456.
53. Rosa CE, Figueiredo MA, Lanes CFC, Almeida DV, Marins LF (2011) Genotype-dependent gene expression profile of the antioxidant defense system (ADS) in the liver of a GH-transgenic zebrafish model. Transgenic Res 20: 85-89.
54. Rowlerson A, Veggetti A (2001) Cellular mechanisms of post-embryonic muscle growth in aquaculture species. In: Johnston IA (ed) Muscle development and growth. Academic Press, London, pp 103-140.
55. Rudnicki MA, Jaenish R (1995) The MyoD family of transcription factors and skeletal muscle myogenesis. Bioessays 17: 203-209.
56. Sabourin LA, Rudnicki MA (2000) The molecular regulation of myogenesis. Clin Genet 57: 16-25.
57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
58. Singleton JR, Feldman EL (2001) Insulin-like growth factor-I in muscle metabolism and myotherapies. Neurobiol Dis 8: 541-554.
59. Sjögren K, Jansson J-O, Isaksson OGP, Ohlsson C (2002) A model for tissue-specific inducible insulin-like growth factor-I (IGF-I) inactivation to determine the physiological role of liver-derived IGF-I. Endocrine 19(3): 249-256.
60. Sotiropoulos A, Ohanna M, Kedzia C, Menon RK, Kopchick JJ, Kelly PA, Pende M (2006) Growth hormone promotes skeletal muscle cell fusion independent of insulin-like growth factor 1 up-regulation. Proc Natl Acad Sci USA 103: 7315-7320.
61. Studzinski AL, Almeida DV, Lanes CF, Figueiredo MA, Marins LF (2009) SOCS1 and SOCS3 are the main negative modulators of the somatotrophic axis in liver of homozygous GH-transgenic zebrafish (Danio rerio). Gen Comp Endocrinol 161: 67-72.
62. Valente LMP, Rocha E, Gomes EFS, Silva MW, Oliveira MH, Monteiro RAF, Fauconneau B (1999) Growth dynamics of white and red muscle fibres in fast- and slow-growing strains of rainbow trout. J Fish Biol 55: 675-691.
63. Vanderkuur JA, Wang X, Zhang L, Campbell GS, Allevato G, Billestrup N, Norstedt G, Carter-Su C (1994) Domains of the growth hormone receptor required for association and activation of JAK2 tyrosine kinase. J Biol Chem 269: 21709-21717.
64. Vanderkuur JA, Wang X, Zhang L, Allevato G, Billestrup N, Carter-Su C (1995) Growth hormone-dependent phosphorylation of tyrosine 333 and/or 338 of the growth hormone receptor. J Biol Chem 270: 21738-21744.
65. Velloso CP (2008) Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol 154: 557-568.
66. Vielkind JR (1992) Medaka and zebrafish: ideal as transient and stable transgenic systems. In: Hew CL, Fletcher GL (eds) Transgenic fish. World Scientific, Singapore.
67. Walters TD, Griffiths AM (2009) Mechanisms of growth impairment in pediatric Crohn's disease. Nat Rev Gastroenterol Hepatol 6: 513-523.
68. Watabe S (1999) Myogenic regulatory factors and muscle differentiation during ontogeny in fish. J Fish Biol 55: 1-18.
69. Watabe S (2001) Myogenic regulatory factors. In: Johnston IA (ed) Muscle development and growth. Academic Press, London, pp 19-41.
70. Waters MJ, Hoang HN, Fairlie DP, Pelekanos RA, Brown RJ (2006) New insights into growth hormone action. J Mol Endocrinol 36: 1-7.
71. Weatherly AH, Gill HS (1987) The biology of fish growth. Academic Press, London.
72. Westerfield M (1995) The zebrafish book: a guide for the laboratory use of zebrafish Danio rerio, 3rd edn. University of Oregon Press, Eugene.
73. Xu Y, He J, Tian HL, Chan CH, Liao J, Yan T, Lam TJ, Gong Z (1999) Fast skeletal muscle-specific expression of a zebrafish myosin light chain 2 gene and characterization of its promoter by direct injection into skeletal muscle. DNA Cell Biol 18: 85-95.
74. Zbikowska HM (2003) Fish can be first-advances in fish transgenesis for commercial applications. Transgenic Res 12: 379-389.
75. Zhu T, Goh ELK, Graichen R, Ling L, Lobie PE (2001) Signal transduction via the growth hormone receptor. Cell Signal 13: 599-616.