Effect of acute and chronic insulin administrations on major factors involved in the control of muscle protein turnover in rainbow trout (Oncorhynchus mykiss)

General and Comparative Endocrinology

Volumn 172, Issue 3, 2011, Pages 363-370

  Seiliez, Iban ^a   Panserat, Stéphane ^a   Skiba Cassy, Sandrine ^a   Polakof, Sergio ^a  

^a UR1067 Nutrition Metabolism Aquaculture   (France)

Author keywords

Fish; Insulin; Muscle; Protein synthesis; Proteolysis; Signaling

Indexed keywords

ALPHA TYPE PROTEASOME C2 SUBUNIT; ALPHA TYPE PROTEASOME C9 SUBUNIT; ATROGIN 1; AUTOPHAGY RELATED 4B; CALPASTATIN; GAMMA AMINOBUTYRIC ACID TYPE A RECEPTOR ASSOCIATED PROTEIN LIKE 1; INSULIN; MICROTUBULE ASSOCIATED LIGHT CHAIN 3B; MUSCLE PROTEIN; UNCLASSIFIED DRUG;

ACUTE DRUG ADMINISTRATION; ARTICLE; ATG 4B GENE; ATROGIN 1 GENE; C2 GENE; C9 GENE; CALPASTATIN GENE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME REGULATION; GABARPL 1 GENE; INSULIN TREATMENT; INTRACELLULAR SIGNALING; LC 3B GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAINBOW TROUT;

EID: 79957789730     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.03.026     Document Type: Article

References (69)

1. Ablett R.F., Sinnhuber R.O., Holmes R.M., Selivonchick D.P. The effect of prolonged administration of bovine insulin in rainbow trout (Salmo gairdneri R.). Gen. Comp. Endocrinol. 1981, 43:211-217.
2. Ablett R.F., Sinnhuber R.O., Selivonchick D.P. The effect of bovine insulin on [14C]glucose and [3H]leucine incorporation in fed and fasted rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol. 1981, 44:418-427.
3. Arroba A.I., Wallace D., Mackey A., De la Rosa E.J., Cotter T.G. IGF-I maintains calpastatin expression and attenuates apoptosis in several models of photoreceptor cell death. Eur. J. Neurosci. 2009, 30:975-986.
4. Barnoy S., Kosower N.S. Calpastatin in rat myoblasts: transient diminution and decreased phosphorylation depend on myogenin-directed myoblast differentiation. Int. J. Biochem. Cell Biol. 2007, 39:253-261.
5. Barnoy S., Supino-Rosin L., Kosower N.S. Regulation of calpain and calpastatin in differentiating myoblasts: mRNA levels, protein synthesis and stability. Biochem. J. 2000, 351(Pt 2):413-420.
6. Bodine S.C., Latres E., Baumhueter S., Lai V.K., Nunez L., Clarke B.A., Poueymirou W.T., Panaro F.J., Na E., Dharmarajan K., Pan Z.Q., Valenzuela D.M., DeChiara T.M., Stitt T.N., Yancopoulos G.D., Glass D.J. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294:1704-1708.
7. Bower N.I., de la Serrana D.G., Johnston I.A. Characterisation and differential regulation of MAFbx/Atrogin-1 alpha and beta transcripts in skeletal muscle of Atlantic salmon (Salmo salar). Biochem. Biophys. Res. Commun. 2010, 396:265-271.
8. Brunn G.J., Hudson C.C., Sekulic A., Williams J.M., Hosoi H., Houghton P.J., Lawrence J.C., Abraham R.T. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 1997, 277:99-101.
9. Burnett P.E., Barrow R.K., Cohen N.A., Snyder S.H., Sabatini D.M. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA 1998, 95:1432-1437.
10. 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. 2006, 290:R1683-R1690.
11. Castillo J., Le Bail P.Y., 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. 2002, 283:R647-R652.
12. Chen Y., Cao L., Ye J., Zhu D. Upregulation of myostatin gene expression in streptozotocin-induced type 1 diabetes mice is attenuated by insulin. Biochem. Biophys. Res. Commun. 2009, 388:112-116.
13. Cleveland B.M., Weber G.M. Effects of insulin-like growth factor-I, insulin, and leucine on protein turnover and ubiquitin ligase expression in rainbow trout primary myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R341-R350.
14. Cleveland B.M., Weber G.M., Blemings K.P., Silverstein J.T. Insulin-like growth factor-I and genetic effects on indexes of protein degradation in response to feed deprivation in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R1332-R1342.
15. Dardevet D., Sornet C., Attaix D., Baracos V.E., Grizard J. Insulin-like growth factor-1 and insulin resistance in skeletal muscles of adult and old rats. Endocrinology 1994, 134:1475-1484.
16. Davis T.A., Burrin D.G., Fiorotto M.L., Nguyen H.V. Protein synthesis in skeletal muscle and jejunum is more responsive to feeding in 7-than in 26-day-old pigs. Am. J. Physiol. 1996, 270:E802-E809.
17. Davis T.A., Burrin D.G., Fiorotto M.L., Reeds P.J., Jahoor F. Roles of insulin and amino acids in the regulation of protein synthesis in the neonate. J. Nutr. 1998, 128:347S-350S.
18. DeFronzo R.A., Beckles A.D. Glucose intolerance following chronic metabolic acidosis in man. Am. J. Physiol. 1979, 236:E328-E334.
19. Del Prato S., Leonetti F., Simonson D.C., Sheehan P., Matsuda M., DeFronzo R.A. Effect of sustained physiologic hyperinsulinaemia and hyperglycaemia on insulin secretion and insulin sensitivity in man. Diabetologia 1994, 37:1025-1035.
20. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 2001, 294:1102-1105.
21. E.M. Donaldson, U.H.M. Fagerlund, D.A. Higgs, J.R. McBride, Hormonal enhancement of growth, in: W.S. Hoar, D.J. Randall, J.R. Brett (Eds.), Fish Physiology, Academic Press, 1979, pp. 456.
22. Dupont J., Tesseraud S., Derouet M., Collin A., Rideau N., Crochet S., Godet E., Cailleau-Audouin E., Metayer-Coustard S., Duclos M.J., Gespach C., Porter T.E., Cogburn L.A., Simon J. Insulin immuno-neutralization in chicken: effects on insulin signaling and gene expression in liver and muscle. J. Endocrinol. 2008, 197:531-542.
23. Emdin S.O. Effects of hagfish insulin in the atlantic hagfish, Myxine glutinosa. The in vivo metabolism of [14C]glucose and [14C]leucine and studies on starvation and glucose-loading. Gen. Comp. Endocrinol. 1982, 47:414-425.
24. Fauconneau B., Arnal M. In vivo protein synthesis in different tissues and the whole body of rainbow trout (Salmo gairdnerii R.), influence of environmental temperature. Comp. Biochem. Physiol. A 1985, 82:179-187.
25. Goll D.E., Thompson V.F., Li H., Wei W., Cong J. The calpain system. Physiol. Rev. 2003, 83:731-801.
26. Goll D.E., Thompson V.F., Taylor R.G., Christiansen J.A. Role of the calpain system in muscle growth. Biochimie 1992, 74:225-237.
27. Hasselgren P.O., Warner B.W., James J.H., Takehara H., Fischer J.E. Effect of insulin on amino acid uptake and protein turnover in skeletal muscle from septic rats. Evidence for insulin resistance of protein breakdown. Arch. Surg. 1987, 122:228-233.
28. Huang J., Forsberg N.E. Role of calpain in skeletal-muscle protein degradation. Proc. Natl. Acad. Sci. USA 1998, 95:12100-12105.
29. Ince B.W., Thorpe A. The in vivo metabolism of 14C-glucose and 14C-glycine in insulin-treated northern pike (Esox lucius L.). Gen. Comp. Endocrinol. 1976, 28:481-486.
30. Isotani S., Hara K., Tokunaga C., Inoue H., Avruch J., Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J. Biol. Chem. 1999, 274:34493-34498.
31. Kimball S.R., Jefferson L.S. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. J. Biol. Chem. 2010, 285:29027-29032.
32. Kobayashi S., Maesato K., Moriya H., Ohtake T., Ikeda T. Insulin resistance in patients with chronic kidney disease. Am. J. Kidney Dis. 2005, 45:275-280.
33. Kumar V., Atherton P., Smith K., Rennie M.J. Human muscle protein synthesis and breakdown during and after exercise. J. Appl. Physiol. 2009, 106:2026-2039.
34. Lee S.W., Dai G., Hu Z., Wang X., Du J., Mitch W.E. Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin-proteasome systems by phosphatidylinositol 3 kinase. J. Am. Soc. Nephrol. 2004, 15:1537-1545.
35. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., Goldberg A.L., Schiaffino S., Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007, 6:458-471.
36. Martin S.A., Blaney S., Bowman A.S., Houlihan D.F. Ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss): effect of food deprivation. Pflugers Arch. 2002, 445:257-266.
37. Mitch W.E. Robert H Herman memorial award in clinical nutrition lecture, 1997. Mechanisms causing loss of lean body mass in kidney disease. Am. J. Clin. Nutr. 1998, 67:359-366.
38. Mommsen T.P., Plisetskaya E.M. Insulin in fishes and agnathans: history, structure, and metabolic regulation. Rev. Aquat. Sci. 1991, 4:225-259.
39. Moxham C.P., Duronio V., Jacobs S. Insulin-like growth factor I receptor beta-subunit heterogeneity. Evidence for hybrid tetramers composed of insulin-like growth factor I and insulin receptor heterodimers. J. Biol. Chem. 1989, 264:13238-13244.
40. I. Navarro, E. Capilla, J. Castillo, A. Albalat, M. Diaz, M.A. Gallardo, J. Blasco, J.V. Planas, J. Gutiérrez, Insulin metabolic effects in fish tissues, in: M. Reinecke, G. Zaccone, B.G. Kapoor (Eds.), Fish Endocrinology, vol. 1, Enfield: Science Publishers, 2006, pp. 15-48.
41. O'Connor P.M., Bush J.A., Suryawan A., Nguyen H.V., Davis T.A. Insulin and amino acids independently stimulate skeletal muscle protein synthesis in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 2003, 284:E110-E119.
42. Parrizas M., Maestro M.A., 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. 1995, 269:R1370-R1377.
43. Parrizas M., Plisetskaya E.M., Planas J., Gutierrez J. Abundant insulin-like growth factor-1 (IGF-1) receptor binding in fish skeletal muscle. Gen. Comp. Endocrinol. 1995, 98:16-25.
44. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
45. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
46. Plisetskaya E. Physiology of fish endocrine pancreas. Fish Physiol. Biochem. 1989, 7:39-48.
47. Polakof S., Skiba-Cassy S., Choubert G., Panserat S. Insulin-induced hypoglycaemia is co-ordinately regulated by liver and muscle during acute and chronic insulin stimulation in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 2010, 213:1443-1452.
48. Price S.R., Bailey J.L., Wang X., Jurkovitz C., England B.K., Ding X., Phillips L.S., Mitch W.E. Muscle wasting in insulinopenic rats results from activation of the ATP-dependent. Ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription. J. Clin. Invest. 1996, 98:1703-1708.
49. Rawls A., Olson E.N. MyoD meets its maker. Cell 1997, 89:5-8.
50. A. Rowlerson, A. Veggetti, Cellular mechanisms of post-embryonic muscle growth in aquaculture species, in: J. Ian (Ed.), Fish Physiology, vol. 18, Academic Press, 2001, pp. 103-140.
51. Saitoh M., Pullen N., Brennan P., Cantrell D., Dennis P.B., Thomas G. Regulation of an activated S6 kinase 1 variant reveals a novel mammalian target of rapamycin phosphorylation site. J. Biol. Chem. 2002, 277:20104-20112.
52. Salem M., Kenney P.B., Rexroad C.E., Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol. Genomics 2006, 28:33-45.
53. Salem M., Nath J., Rexroad C.E., 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. 2005, 140:63-71.
54. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
55. Seiliez I., Gabillard J.C., 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. 2008, 295:R329-R335.
56. Seiliez I., Gutierrez J., Salmeron C., Skiba-Cassy S., Chauvin C., Dias K., Kaushik S., Tesseraud S., Panserat S. An in vivo and in vitro assessment of autophagy-related gene expression in muscle of rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 157:258-266.
57. SIGENAE, Information System of Breeding Animals' Genome. Available from: http://www.sigenae.org/.
58. Soos M.A., Field C.E., Siddle K. Purified hybrid insulin/insulin-like growth factor-I receptors bind insulin-like growth factor-I, but not insulin, with high affinity. Biochem. J. 1993, 290(Pt. 2):419-426.
59. Soos M.A., Siddle K. Immunological relationships between receptors for insulin and insulin-like growth factor I. Biochem. J. 1989, 263:553-563.
60. Tashima L., Cahill G.F. Effects of insulin in the toadfish, Opsanus tau. Gen. Comp. Endocrinol. 1968, 11:262-271.
61. 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. 2007, 357:181-186.
62. Treadway J.L., Morrison B.D., Goldfine I.D., Pessin J.E. Assembly of insulin/insulin-like growth factor-1 hybrid receptors in vitro. J. Biol. Chem. 1989, 264:21450-21453.
63. Ueno M., Carvalheira J.B., Tambascia R.C., Bezerra R.M., Amaral M.E., Carneiro E.M., Folli F., Franchini K.G., Saad M.J. Regulation of insulin signalling by hyperinsulinaemia: role of IRS-1/2 serine phosphorylation and the mTOR/p70 S6K pathway. Diabetologia 2005, 48:506-518.
64. von Manteuffel S.R., Dennis P.B., Pullen N., Gingras A.C., Sonenberg N., Thomas G. The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70s6k. Mol. Cell. Biol. 1997, 17:5426-5436.
65. von Manteuffel S.R., Gingras A.C., Ming X.F., Sonenberg N., Thomas G. 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 1996, 93:4076-4080.
66. Wang X., Hu Z., Hu J., Du J., Mitch W.E. Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 2006, 147:4160-4168.
67. White M.F. IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E413-E422.
68. Wray-Cahen D., Beckett P.R., Nguyen H.V., Davis T.A. Insulin-stimulated amino acid utilization during glucose and amino acid clamps decreases with development. Am. J. Physiol. 1997, 273:E305-E314.
69. Zhao J., Brault J.J., Schild A., Cao P., Sandri M., Schiaffino S., Lecker S.H., Goldberg A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6:472-483.