Effects of insulin-like growth factor-I, insulin, and leucine on protein turnover and ubiquitin ligase expression in rainbow trout primary myocytes

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 2, 2010, Pages

  Cleveland, Beth M ^a   Weber, Gregory M ^a  

^a APPALACHIAN FRUIT RESEARCH STATION   (United States)

Author keywords

Atrogin 1; Forkhead box O; Insulin like growth factor I; Protein synthesis

Indexed keywords

F BOX PROTEIN; FOXO4 PROTEIN; INSULIN; LEUCINE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RING FINGER PROTEIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; MUSCLE ATROPHY; MUSCLE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RAINBOW TROUT; SIGNAL TRANSDUCTION; UBIQUITINATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANABOLIC AGENTS; ANIMALS; BLOTTING, WESTERN; CATHEPSIN D; CATHEPSIN L; CELL SEPARATION; CULTURE MEDIA; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; F-BOX PROTEINS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LEUCINE; MONOCYTES; ONCORHYNCHUS MYKISS; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UBIQUITIN-PROTEIN LIGASES;

EID: 75449110001     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00516.2009     Document Type: Article

References (90)

1. Banos N, Baro J, Castejon C, Navarro I, Gutierrez J. Influence of high-carbohydrate enriched diets on plasma insulin levels and insulin and IGF-I receptors in trout. Regul Pept 77: 55-62, 1998.
2. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
3. Burgering BM. A brief introduction to FOXOlogy. Oncogene 27: 2258-2262, 2008.
4. Castillo J, Ammendrup-Johnsen I, Codina M, Navarro I, Gutierrez J. IGF-I and insulin receptor signal transduction in trout muscle cells. Am J Physiol Regul Integr Comp Physiol 290: R1683-R1690, 2006.
5. Castillo J, Codina M, Martinez ML, Navarro I, Gutierrez J. Metabolic and mitogenic effects of IGF-I and insulin on muscle cells of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286: R935-R941, 2004.
6. Castillo J, Le Bail PY, Paboeuf G, Navarro I, Weil C, Fauconneau B, Gutierrez J. IGF-I binding in primary culture of muscle cells of rainbow trout: changes during in vitro development. Am J Physiol Regul Integr Comp Physiol 283: R647-R652, 2002.
7. Cleveland BM, Weber GM, Blemings KP, Silverstein JT. Insulin-like growth factor-I and genetic effects on indices of protein degradation in response to feed deprivation in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 297: R1334-R1342, 2009.
8. Codina M, Garcia de la serrana D, Sanchez-Gurmaches J, Montserrat N, Chistyakova O, Navarro I, Gutierrez J. Metabolic and mitogenic effects of IGF-II in rainbow trout (Oncorhynchus mykiss) myocytes in culture and the role of IGF-II in the PI3K/Akt and MAPK signalling pathways. Gen Comp Endocrinol 157: 116-124, 2008.
9. d'Azzo A, Bongiovanni A, Nastasi T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 6: 429-441, 2005.
10. Dardevet D, Sornet C, Vary T, Grizard J. Phosphatidylinositol 3-kinase and p70 s6 kinase participate in the regulation of protein turnover in skeletal muscle by insulin and insulin-like growth factor I. Endocrinology 137: 4087-4094, 1996.
11. Davis TA, Fiorotto ML, Burrin DG, Vann RC, Reeds PJ, Nguyen HV, Beckett PR, Bush JA. Acute IGF-I infusion stimulates protein synthesis in skeletal muscle and other tissues of neonatal pigs. Am J Physiol Endocrinol Metab 283: E638-E647, 2002.
12. de Blaauw I, Deutz NE, von Meyenfeldt MF. Muscle protein and amino acid turnover in rats in vivo: effects of short-term and prolonged starvation. Clin Sci (Lond) 90: 457-466, 1996.
13. Dehoux M, Van Beneden R, Pasko N, Lause P, Verniers J, Underwood L, Ketelslegers JM, Thissen JP. Role of the insulin-like growth factor I decline in the induction of atrogin-1/MAFbx during fasting and diabetes. Endocrinology 145: 4806-4812, 2004.
14. Diaz M, Vraskou Y, Gutierrez J, Planas JV. Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiation and regulation by insulin and IGF-I. Am J Physiol Regul Integr Comp Physiol 296: R794-R800, 2009.
15. Dobly A, Martin SA, Blaney SC, Houlihan DF. Protein growth rate in rainbow trout (Oncorhynchus mykiss) is negatively correlated to liver 20S proteasome activity. Comp Biochem Physiol A Mol Integr Physiol 137: 75-85, 2004.
16. Dyer A, Barlow C, Bransden M, Carter C, Glencross B, Richardson N, Thomas P, Williams K, Carragher J. Correlation of plasma IGF-I concentrations and growth rate in aquacultured finfish: a tool for assessing the potential of new diets. Aquaculture 236: 583-594, 2004.
17. Fauconneau B, Paboeuf G. Effect of fasting and refeeding on in vitro muscle cell proliferation in rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 301: 459-463, 2000.
18. Frost RA, Nystrom GJ, Jefferson LS, Lang CH. Hormone, cytokine, and nutritional regulation of sepsis-induced increases in atrogin-1 and MuRF1 in skeletal muscle. Am J Physiol Endocrinol Metab 292: E501-E512, 2007.
19. Fuller SJ, Mynett JR, Sugden PH. Stimulation of cardiac protein synthesis by insulin-like growth factors. Biochem J 282: 85-90, 1992.
20. Furuno K, Goodman MN, Goldberg AL. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550-8557, 1990.
21. Gallardo M, Castejon C, Navarro I, Blasco J, Gutierrez J, Sanchez J. L-Leucine and L-alanine uptake by trout (Salmo trutta) cardiomyocytes: the effect of IGF-I and insulin. Fish Physiol Biochem 25: 239-248, 2001.
22. Gregorio CC, Perry CN, McElhinny AS. Functional properties of the titin/connectin-associated proteins, the muscle-specific RING finger proteins (MURFs), in striated muscle. J Muscle Res Cell Motil 26: 389-400, 2005.
23. Gulve EA, Dice JF. Regulation of protein synthesis and degradation in L8 myotubes. Effects of serum, insulin and insulin-like growth factors. Biochem J 260: 377-387, 1989.
24. Herningtyas EH, Okimura Y, Handayaningsih AE, Yamamoto D, Maki T, Iida K, Takahashi Y, Kaji H, Chihara K. Branched-chain amino acids and arginine suppress MaFbx/atrogin-1 mRNA expression via mTOR pathway in C2C12 cell line. Biochim Biophys Acta 1780: 1115-1120, 2008.
25. Houlihan D, Hall SJ, Gray C, Noble B. Growth rates and proteiinturnover in cod, Gadus morhua. Can J Fish and Aquat Sci 45: 951-964, 1988.
26. Houlihan D, Laurent P. Effects of excercise training on the performance, growth and protein turnover of rainbow trout (Salmo gairdneri). Can J of Fish Aquat Sci 44: 1614-1621, 1987.
27. Houlihan D, McMillan D, Laurent P. Growth rates, protein synthesis, and protein degradation rates in rainbow trout: effects of body size. Physiol Zool 59: 482-493, 1986.
28. Imae M, Fu Z, Yoshida A, Noguchi T, Kato H. Nutritional and hormonal factors control the gene expression of FoxOs, the mammalian homologues of DAF-16. J Mol Endocrinol 30: 253-262, 2003.
29. Jagoe RT, Lecker SH, Gomes M, Goldberg AL. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 16: 1697-1712, 2002.
30. Kettelhut IC, Pepato MT, Migliorini RH, Medina R, Goldberg AL. Regulation of different proteolytic pathways in skeletal muscle in fasting and diabetes mellitus. Braz J Med Biol Res 27: 981-993, 1994.
31. Kim SJ, Roy RR, Kim JA, Zhong H, Haddad F, Baldwin KM, Edgerton VR. Gene expression during inactivity-induced muscle atrophy: effects of brief bouts of a forceful contraction countermeasure. J Appl Physiol 105: 1246-1254, 2008.
32. Kumamoto T, Fujimoto S, Ito T, Horinouchi H, Ueyama H, Tsuda T. Proteasome expression in the skeletal muscles of patients with muscular dystrophy. Acta Neuropathol 100: 595-602, 2000.
33. Kwak KS, Zhou X, Solomon V, Baracos VE, Davis J, Bannon AW, Boyle WJ, Lacey DL, Han HQ. Regulation of protein catabolism by muscle-specific and cytokine-inducible ubiquitin ligase E3alpha-II during cancer cachexia. Cancer Res 64: 8193-8198, 2004.
34. Lankford SE, Weber G. Association between plasma growth hormone, insulin-like growth factor-I, and cortisol with stress responsiveness and growth performance in a selective breeding program for rainbow trout. N Am J Aquac 68: 151-159, 2006.
35. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, Glass DJ. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280: 2737-2744, 2005.
36. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51, 2004.
37. Li BG, Hasselgren PO, Fang CH, Warden GD. Insulin-like growth factor-I blocks dexamethasone-induced protein degradation in cultured myotubes by inhibiting multiple proteolytic pathways: 2002 ABA paper. J Burn Care Rehabil 25: 112-118, 2004.
38. Louard RJ, Barrett EJ, Gelfand RA. Overnight branched-chain amino acid infusion causes sustained suppression of muscle proteolysis. Metabolism 44: 424-429, 1995.
39. Loughna PT, Goldspink G. The effects of starvation upon protein turnover in red and white myotomal muscle of rainbow trout, Salmo gairdneri Richardson. J Fish Biol 25: 223-230, 1984.
40. Maragno AL, Baqui MM, Gomes MD. FBXO25, an F-box protein homologue of atrogin-1, is not induced in atrophying muscle. Biochim Biophys Acta 1760: 966-972, 2006.
41. McCarthy ID, Houlihan D, Carter C. Individual variation in protein turnover and growth efficiency in rainbow trout, Oncorhynchus mykiss (Walbaum). Proc Biol Sci 257: 141-147, 1994.
42. McCormick SD, Kelley KM, Young G, Nishioka RS, Bern HA. Stimulation of coho salmon growth by insulin-like growth factor I. Gen Comp Endocrinol 86: 398-406, 1992.
43. McElhinny AS, Perry CN, Witt CC, Labeit S, Gregorio CC. Musclespecific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development. J Cell Sci 117: 3175-3188, 2004.
44. Mendez E, Smith A, Figueiredo-Garutti ML, Planas JV, Navarro I, Gutierrez J. Receptors for insulin-like growth factor-I (IGF-I) predominate over insulin receptors in skeletal muscle throughout the life cycle of brown trout, Salmo trutta. Gen Comp Endocrinol 122: 148-157, 2001.
45. Mingarro M, Vega-Rubin de Celis S, Astola A, Pendon C, Valdivia MM, Perez-Sanchez J. Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 128: 102-111, 2002.
46. Mitchell PJ, Johnson SE, Hannon K. Insulin-like growth factor I stimulates myoblast expansion and myofiber development in the limb. Dev Dyn 223: 12-23, 2002.
47. Montserrat N, Sanchez-Gurmaches J, Garcia de la Serrana D, Navarro MI, Gutierrez J. IGF-I binding and receptor signal transduction in primary cell culture of muscle cells of gilthead sea bream: changes throughout in vitro development. Cell Tissue Res 330: 503-513, 2007.
48. Mulvaney DR, Merkel RA, Bergen WG. Skeletal muscle protein turnover in young male pigs. J Nutr 115: 1057-1064, 1985.
49. Nair KS, Schwartz RG, Welle S. Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. Am J Physiol Endocrinol Metab 263: E928-E934, 1992.
50. Nakae J, Oki M, Cao Y. The FoxO transcription factors and metabolic regulation. FEBS Lett 582: 54-67, 2008.
51. Nakashima K, Komatsu T, Yamazaki M, Abe H. Effects of fasting and refeeding on expression of proteolytic-related genes in skeletal muscle of chicks. J Nutr Sci Vitaminol (Tokyo) 51: 248-253, 2005.
52. Nakashima K, Yakabe Y, Ishida A, Katsumata M. Effects of orally administered glycine on myofibrillar proteolysis and expression of proteolytic-related genes of skeletal muscle in chicks. Amino Acids 35: 451-456, 2008.
53. Nakashima K, Yakabe Y, Yamazaki M, Abe H. Effects of fasting and refeeding on expression of atrogin-1 and Akt/FOXO signaling pathway in skeletal muscle of chicks. Biosci Biotechnol Biochem 70: 2775-2778, 2006.
54. Negatu Z, Meier AH. In vitro incorporation of [14C]glycine into muscle protein of gulf killifish (Fundulus grandis) in response to insulin-like growth factor-I. Gen Comp Endocrinol 98: 193-201, 1995.
55. NRC. Nutrient Requirements of Fish. Washington, DC: National Academy Press, 1993.
56. NRC. Nutrient Requirements of Laboratory Animals. Washington, DC: National Academy Press, 1995.
57. Parrizas M, Maestro MA, Banos N, Navarro I, Planas J, Gutierrez J. Insulin/IGF-I binding ratio in skeletal and cardiac muscles of vertebrates: a phylogenetic approach. Am J Physiol Regul Integr Comp Physiol 269: R1370-R1377, 1995.
58. Parrizas M, Plisetskaya EM, Planas J, Gutierrez J. Abundant insulinlike growth factor-1 (IGF-1) receptor binding in fish skeletal muscle. Gen Comp Endocrinol 98: 16-25, 1995.
59. Peragon J, Barroso JB, Garcia-Salguero L, Aranda F, de la Higuera M, Lupianez JA. Selective changes in the protein-turnover rates and nature of growth induced in trout liver by long-term starvation followed by re-feeding. Mol Cell Biochem 201: 1-10, 1999.
60. Peragon J, Barroso JB, Garcia-Salguero L, de la Higuera M, Lupianez JA. Growth, protein-turnover rates and nucleic-acid concentrations in the white muscle of rainbow trout during development. Int J Biochem Cell Biol 33: 1227-1238, 2001.
61. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
62. Pierce AL, Beckman BR, Shearer KD, Larsen DA, Dickhoff WW. Effects of ration on somatotropic hormones and growth in coho salmon. Comp Biochem Physiol B Biochem Mol Biol 128: 255-264, 2001.
63. Pozios KC, Ding J, Degger B, Upton Z, Duan C. IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinasesignaling pathways. Am J Physiol Regul Integr Comp Physiol 280: R1230-R1239, 2001.
64. Pym RA, Leclercq B, Tomas FM, Tesseraud S. Protein utilisation and turnover in lines of chickens selected for different aspects of body composition. Br Poult Sci 45: 775-786, 2004.
65. Rajapurohitam V, Bedard N, Wing SS. Control of ubiquitination of proteins in rat tissues by ubiquitin conjugating enzymes and isopeptidases. Am J Physiol Endocrinol Metab 282: E739-E745, 2002.
66. Rescan PY, Montfort J, Ralliere C, Le Cam A, Esquerre D, Hugot K. Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule (Abstract). BMC Genomics 8: 438, 2007.
67. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155, 2007.
68. Sacheck JM, Ohtsuka A, McLary SC, Goldberg AL. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am J Physiol Endocrinol Metab 287: E591-E601, 2004.
69. Salem M, Kenney PB, Rexroad CE, 3rd, Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28: 33-45, 2006.
70. Salem M, Nath J, Rexroad CE, Killefer J, Yao J. Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation. Comp Biochem Physiol B Biochem Mol Biol 140: 63-71, 2005.
71. Salem M, Silverstein J, Rexroad CE, Yao J. Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss) (Abstract). BMC Genomics 8: 328, 2007.
72. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412, 2004.
73. Seiliez I, Gabillard JC, Skiba-Cassy S, Garcia-Serrana D, Gutierrez J, Kaushik S, Panserat S, Tesseraud S. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 295: R329-R335, 2008.
74. Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, Tesseraud S. Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. J Nutr 138: 487-491, 2008.
75. Smith M. Estimation of growth potential by measurement of protein synthetic rates in feeding and fasting rainbow trout, Salmo gairdneri. J of Fish Biol 19: 213-220, 1981.
76. Suzuki N, Motohashi N, Uezumi A, Fukada S, Yoshimura T, Itoyama Y, Aoki M, Miyagoe-Suzuki Y, Takeda S. NO production results in suspension-induced muscle atrophy through dislocation of neuronal NOS. J Clin Invest 117: 2468-2476, 2007.
77. Szewczyk NJ, Jacobson LA. Signal-transduction networks and the regulation of muscle protein degradation. Int J Biochem Cell Biol 37: 1997-2011, 2005.
78. Tesseraud S, Chagneau AM, Grizard J. Muscle protein turnover during early development in chickens divergently selected for growth rate. Poult Sci 79: 1465-1471, 2000.
79. Tesseraud S, Larbier M, Chagneau AM, Geraert PA. Effect of dietary lysine on muscle protein turnover in growing chickens. Reprod Nutr Dev 32: 163-171, 1992.
80. Tesseraud S, Metayer-Coustard S, Boussaid S, Crochet S, Audouin E, Derouet M, Seiliez I. Insulin and amino acid availability regulate atrogin-1 in avian QT6 cells. Biochem Biophys Res Commun 357: 181-186, 2007.
81. Tobimatsu K, Noguchi T, Hosooka T, Sakai M, Inagaki K, Matsuki Y, Hiramatsu R, Kasuga M. Overexpression of the transcriptional coregulator Cited2 protects against glucocorticoid-induced atrophy of C2C12 myotubes. Biochem Biophys Res Commun 378: 399-403, 2009.
82. Tomas FM, Jones LM, Pym RA. Rates of muscle protein breakdown in chickens selected for increased growth rate, food consumption or efficiency of food utilisation as assessed by N tau-methylhistidine excretion. Br Poult Sci 29: 359-370, 1988.
83. Tomas FM, Pym RA, Johnson RJ. Muscle protein turnover in chickens selected for increased growth rate, food consumption or efficiency of food utilisation: effects of genotype and relationship to plasma IGF-I and growth hormone. Br Poult Sci 32: 363-376, 1991.
84. Tomas FM, Pym RA, McMurtry JP, Francis GL. Insulin-like growth factor (IGF)-I but not IGF-II promotes lean growth and feed efficiency in broiler chickens. Gen Comp Endocrinol 110: 262-275, 1998.
85. Tsujinaka T, Ebisui C, Fujita J, Morimoto T, Ogawa A, Ishidoh K, Kominami E, Yano M, Shiozaki H, Monden M. Autocatalytic inactivation of lysosomal cathepsins is associated with inhibition of protein breakdown by insulin-like growth factor-1 (IGF-1) in myotubes. Biochem Biophys Res Commun 208: 353-359, 1995.
86. Wang X, Hu Z, Hu J, Du J, Mitch WE. Insulin resistance accelerates muscle protein degradation: Activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147: 4160-4168, 2006.
87. Weber GM, Sullivan CV. In vitro hormone induction of final oocyte maturation in striped bass (Morone saxatilis) follicles is inhibited by blockers of phosphatidylinositol 3-kinase activity. Comp Biochem Physiol B Biochem Mol Biol 129: 467-473, 2001.
88. Wilkinson RJ, Porter M, Woolcott H, Longland R, Carragher JF. Effects of aquaculture related stressors and nutritional restriction on circulating growth factors (GH, IGF-I and IGF-II) in Atlantic salmon and rainbow trout. Comp Biochem Physiol A Mol Integr Physiol 145: 214-224, 2006.
89. Witt SH, Granzier H, Witt CC, Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 350: 713-722, 2005.
90. Wood AW, Duan C, Bern HA. Insulin-like growth factor signaling in fish. Int Rev Cytol 243: 215-285, 2005.