Proteolytic response to feeding level in rainbow trout (Oncorhynchus mykiss)

Aquaculture

Volumn 319, Issue 1-2, 2011, Pages 194-204

  Cleveland, Beth M ^a   Burr, Gary S ^b  

^a APPALACHIAN FRUIT RESEARCH STATION   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Atrogin 1; Fish; Protein turnover; Proteolysis; Ration

Indexed keywords

AMINO ACID; ARTIFICIAL DIET; DEGRADATION; FOOD INTAKE; GENE EXPRESSION; GROWTH RATE; LIPID; MOLECULAR ANALYSIS; PROTEIN; SALMONID CULTURE;

ONCORHYNCHUS MYKISS;

EID: 80051586436     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2011.06.043     Document Type: Article

References (82)

1. Alami-Durante H., Medale F., Cluzeaud M., Kaushik S.J. Skeletal muscle growth dynamics and expression of related genes in white and red muscle of rainbow trout fed diets with graded levels of a mixture of plant protein sources as substitutes for fishmeal. Aqua 2010, 303:50-58.
2. Azevedo P.A., van Milgen J., Leeson S., Bureau D.P. Comparing efficiency of metabolizable energy utilization by rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) using factorial and multivariate approaches. J. Anim. Sci. 2005, 83:842-851.
3. Aziz A., Liu Q.C., Dilworth F.J. Regulating a master regulator: establishing tissue-specific gene expression in skeletal muscle. Epigenetics 2010, 5:691-695.
4. Ballard F.J., Johnson R.J., Owens P.C., Francis G.L., Upton F.M., McMurtry J.P., Wallace J.C. Chicken insulin-like growth factor-I: amino acid sequence, radioimmunoassay, and plasma levels between strains and during growth. Gen. Comp. Endocrinol. 1990, 79:459-468.
5. Bar N.S., Sigholt T., Shearer K., Krogdahl A. A dynamic model of nutrient pathways, growth, and body composition in fish. Can. J. Fish. Aquat. Sci. 2007, 64:1669-1682.
6. Barrows F., Hardy R.W. Nutrition and feeding. Fish Hatchery Management 2001, The American Fisheries Society, Bethesda. G. Wedemeyer (Ed.).
7. Bartoli M., Richard I. Calpains in muscle wasting. Int. J. Biochem. Cell Biol. 2005, 37:2115-2133.
8. 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.
9. 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.
10. Brown C., Cameron J. The induction of specific dynamic action in channel catfish by infusion of essential amino acids. Physiol. Zool. 1991, 64.
11. Brown C., Cameron J. The relationship between specific dynamic action (SDA) and protein synthesis rates in the channel catfish. Physiol. Zool. 1991, 64:298-309.
12. Buonomo F.C., Baile C.A. Influence of nutritional deprivation on insulin-like growth factor I, somatotropin, and metabolic hormones in swine. J. Anim. Sci. 1991, 69:755-760.
13. Bureau D.P., Hua K., Cho C.Y. Effect of feeding level on growth and nutrient deposition in rainbow trout (Oncorhynchus mykiss) growing from 150 to 600g. Aquac. Res. 2006, 37:1090-1098.
14. Carter C., Owen S., He Z., Watt P., Scrimgeour C., Houlihan D., Rennie M. Determination of protein synthesis in rainbow trout, Oncorhynchus mykiss, using a stable isotope. J. Exp. Biol. 1994, 189:279-284.
15. Castillo J., Codina M., Martinez M.L., 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. 2004, 286:R935-R941.
16. 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.
17. Cleveland B.M., Evenhuis J.P. Molecular characterization of atrogin-1/F-box protein-32 (FBXO32) and F-box protein-25 (FBXO25) in rainbow trout (Oncorhynchus mykiss): expression across tissues in response to feed deprivation. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 157:248-257.
18. 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.
19. Cleveland B.M., Weber G.M., Blemings K.P., Silverstein J.T. 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. 2009, 297:R1332-R1342.
20. Dedieu S., Poussard S., Mazeres G., Grise F., Dargelos E., Cottin P., Brustis J.J. Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organization. Exp. Cell Res. 2004, 292:187-200.
21. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
22. Diaz M., Vraskou Y., Gutierrez J., Planas J.V. 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 2009, 296:R794-R800.
23. 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 2004, 236:583-594.
24. El-Haroun E.R., Bureau D.P., Cant J.P. A mechanistic model of nutritional control of protein synthesis in animal tissues. J. Theor. Biol. 2010, 262:361-369.
25. Eliason E.J., Higgs D.A., Farrell A.P. Effect of isoenergetic diets with different protein and lipid content on the growth performance and heat increment of rainbow trout. Aqua 2007, 272:723-736.
26. Fauconneau B., Gray C., Houlihan D. Assessment of individual protein turnover in three muscle types of rainbow trout. Comp. Biochem. Physiol. 1995, 111B.
27. Heger J., Patras P., Nitrayova S., Karcol J., Dolesova P. Lysine maintenance requirement and efficiency of its utilisation in young pigs as estimated by comparative slaughter technique. Arch. Anim. Nutr. 2008, 62:182-192.
28. Hirner S., Krohne C., Schuster A., Hoffmann S., Witt S., Erber R., Sticht C., Gasch A., Labeit S., Labeit D. MuRF1-dependent regulation of systemic carbohydrate metabolism as revealed from transgenic mouse studies. J. Mol. Biol. 2008, 379:666-677.
29. Hizuka N., Takano K., Shizume K., Asakawa K., Miyakawa M., Tanaka I., Horikawa R. Insulin-like growth factor I stimulates growth in normal growing rats. Eur. J. Pharmacol. 1986, 125:143-146.
30. Ho M.S., Tsai P.I., Chien C.T. F-box proteins: the key to protein degradation. J. Biomed. Sci. 2006, 13:181-191.
31. Hong D., Forsberg N.E. Effects of serum and insulin-like growth factor I on protein degradation and protease gene expression in rat L8 myotubes. J. Anim. Sci. 1994, 72:2279-2288.
32. Houlihan D., McMillan D., Laurent P. Growth rates, protein synthesis, and protein degradation rates in rainbow trout: effects of body size. Physiol. Zool. 1986, 59:482-493.
33. Houlihan D., Hall S., Gray C. Effects of ration on protein turnover in cod. Aquaculture 1989, 79:103-110.
34. Houlihan D., Carter C., McCarthy I.D. Protein synthesis is fish. Biochemistry and Molecular Biology of Fishes 1995, 191-219. Elsevier Science, Amsterdam. P. Hochachka, T. Mommsen (Eds.).
35. Jogo M., Shiraishi S., Tamura T.A. Identification of MAFbx as a myogenin-engaged F-box protein in SCF ubiquitin ligase. FEBS Lett. 2009, 583:2715-2719.
36. Lagirand-Cantaloube J., Cornille K., Csibi A., Batonnet-Pichon S., Leibovitch M.P., Leibovitch S.A. Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS ONE 2009, 4:e4973.
37. Lagirand-Cantaloube J., Offner N., Csibi A., Leibovitch M.P., Batonnet-Pichon S., Tintignac L.A., Segura C.T., Leibovitch S.A. The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J. 2008, 27:1266-1276.
38. Lankford S.E., 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. 2006, 68:151-159.
39. Latres E., Amini A.R., Amini A.A., Griffiths J., Martin F.J., Wei Y., Lin H.C., Yancopoulos G.D., Glass D.J. 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. 2005, 280:2737-2744.
40. Lee Y., Takahashi T. An improved colorimetric determination of amino acids with the use of ninhydrin. Anal. Biochem. 1966, 14:71-77.
41. Leloup L., Mazeres G., Daury L., Cottin P., Brustis J.J. Involvement of calpains in growth factor-mediated migration. Int. J. Biochem. Cell Biol. 2006, 38:2049-2063.
42. Leloup L., Daury L., Mazeres G., Cottin P., Brustis J.J. Involvement of the ERK/MAP kinase signalling pathway in milli-calpain activation and myogenic cell migration. Int. J. Biochem. Cell Biol. 2007, 39:1177-1189.
43. Li H.H., Kedar V., Zhang C., McDonough H., Arya R., Wang D.Z., Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J. Clin. Investig. 2004, 114:1058-1071.
44. Li H.H., Willis M.S., Lockyer P., Miller N., McDonough H., Glass D.J., Patterson C. Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J. Clin. Investig. 2007, 117:3211-3223.
45. Loughna P.T., Goldspink G. The effects of starvation upon protein turnover in red and white myotomal muscle of rainbow trout, Salmo gairdneri Richardson. J. Fish Biol. 1984, 25:223-230.
46. Masiero E., Agatea L., Mammucari C., Blaauw B., Loro E., Komatsu M., Metzger D., Reggiani C., Schiaffino S., Sandri M. Autophagy is required to maintain muscle mass. Cell Metab. 2009, 10:507-515.
47. McCarthy I.D., Houlihan D., Carter C. Individual variation in protein turnover and growth efficiency in rainbow trout, Oncorhynchus mykiss (Walbaum). Proc. Biol. Sci. 1994, 257:141-147.
48. McCormick S.D., Kelley K.M., Young G., Nishioka R.S., Bern H.A. Stimulation of coho salmon growth by insulin-like growth factor I. Gen. Comp. Endocrinol. 1992, 86:398-406.
49. Mingarro M., Vega-Rubin de Celis S., Astola A., Pendon C., Valdivia M.M., Perez-Sanchez J. Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen. Comp. Endocrinol. 2002, 128:102-111.
50. Moore S. Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J. Biol. Chem. 1968, 243:6281-6283.
51. Moriyama S., Swanson P., Nishii M., Takahashi A., Kawauchi H., Dickhoff W.W., Plisetskaya E.M. Development of a homologous radioimmunoassay for coho salmon insulin-like growth factor-I. Gen. Comp. Endocrinol. 1994, 96:149-161.
52. Norbeck L.A., Kittilson J.D., Sheridan M.A. Resolving the growth-promoting and metabolic effects of growth hormone: differential regulation of GH-IGF-I system components. Gen. Comp. Endocrinol. 2007, 151:332-341.
53. Owen S., McCarthy I.D., Watt P., Ladero V., Sanchez J., Houlihan D., Rennie M. In vivo rates of proten synthesis in Atlantic salmon (Salmo salar L.) smolts determined using a stable isotope flooding dose technique. Fish Physiol. Biochem. 1999, 20:87-94.
54. Perez-Sanchez J., Marti-Palanca H., Kaushik S.J. Ration size and protein intake affect circulating growth hormone concentration, hepatic growth hormone binding and plasma insulin-like growth factor-I immunoreactivity in a marine teleost, the gilthead sea bream (Sparus aurata). J. Nutr. 1995, 125:546-552.
55. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
56. Pierce A.L., Beckman B.R., Shearer K.D., Larsen D.A., Dickhoff W.W. Effects of ration on somatotropic hormones and growth in coho salmon. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 128:255-264.
57. Pierce A.L., Shimizu M., Beckman B.R., Baker D.M., Dickhoff W.W. Time course of the GH/IGF axis response to fasting and increased ration in chinook salmon (Oncorhynchus tshawytscha). Gen. Comp. Endocrinol. 2005, 140:192-202.
58. Pozios K.C., Ding J., Degger B., Upton Z., Duan C. IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinase-signaling pathways. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R1230-R1239.
59. Refstie S., Korsøen Ø.J., Storebakken T., Baeverfjord G., Lein I., Roem A.J. Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aqua 2000, 190:49-63.
60. Rescan P.Y., 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. BMC Genomics 2007, 8:438.
61. Sacheck J.M., Ohtsuka A., McLary S.C., Goldberg A.L. 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. 2004, 287:E591-E601.
62. Salem M., Silverstein J., Rexroad C.E., Yao J. Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 2007, 8:328.
63. 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.
64. 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.
65. 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. 2008, 138:487-491.
66. 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.
67. Shimizu M., Beckman B.R., Hara A., Dickhoff W.W. Measurement of circulating salmon IGF binding protein-1: assay development, response to feeding ration and temperature, and relation to growth parameters. J. Endocrinol. 2006, 188:101-110.
68. Shimizu M., Swanson P., Fukada H., Hara A., Dickhoff W.W. Comparison of extraction methods and assay validation for salmon insulin-like growth factor-I using commercially available components. Gen. Comp. Endocrinol. 2000, 119:26-36.
69. Smith M. Estimation of growth potential by measurement of protein synthetic rates in feeding and fasting rainbow trout, Salmo gairdneri. J. Fish Biol. 1981, 19:213-220.
70. Stinefelt B.M., Eya J.C., Semmens K.J., Blemings K.P. Effect of diet and strain on growth and performance in hybrid bluegill. N. Am. J. Aquac. 2004, 66:312-318.
71. Storebakken T., Austreng E. Ration level for salmonids, II. Growth, feed intake, protein digestibility, body composition, and feed conversion in rainbow trout weighing 0.5-1.0kg. Aqua 1987, 60:207-221.
72. Tacchi L., Bickerdike R., Secombes C.J., Pooley N.J., Urquhart K.L., Collet B., Martin S.A. Ubiquitin E3 ligase atrogin-1 (Fbox-32) in Atlantic salmon (Salmo salar): sequence analysis, genomic structure and modulation of expression. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 157:364-373.
73. Talbot C. Some aspects of the biology of feeding and growth in fish. Proc. Nutr. Soc. 1993, 52:403-416.
74. Temiz P., Weihl C.C., Pestronk A. Inflammatory myopathies with mitochondrial pathology and protein aggregates. J. Neurol. Sci. 2009, 278:25-29.
75. Tomas F.M., Jones L.M., Pym R.A. 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. 1988, 29:359-370.
76. Tomas F.M., Pym R.A., McMurtry J.P., Francis G.L. Insulin-like growth factor (IGF)-I but not IGF-II promotes lean growth and feed efficiency in broiler chickens. Gen. Comp. Endocrinol. 1998, 110:262-275.
77. 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. 1995, 208:353-359.
78. Wang Y., Kong L., Kai L., Bureau D.P. Effects of feeding frequency and ration level on growth, feed utilization and nitrogen waste output of crunate drum (Nibea miichthioides) reared in net pens. Aqua 2007, 271:350-356.
79. Watanabe T., Takeuchi T., Ogino C. Optimum ratio of protein to lipid in diets of rainbow trout. Bull. Jpn Soc. Sci. Fish. 1978, 44:683-688.
80. Witt S.H., Granzier H., Witt C.C., Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J. Mol. Biol. 2005, 350:713-722.
81. Yuan Y., Yang H., Gong S., Luo Z., Yuan H., Chen X. Effects of feeding levels on growth performance, feed utilizatin, body composition and apparent digestibility coefficients of nutrients for juvenile Chinese sucker, Myxocyprinus asiaticus. Aquac. Res. 2010, 41.
82. 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.