Proteomic signature of muscle atrophy in rainbow trout

Journal of Proteomics

Volumn 73, Issue 4, 2010, Pages 778-789

  Salem, Mohamed ^a   Kenney, P Brett ^a   Rexroad III, Caird E ^b   Yao, Jianbo ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b NATIONAL CENTER FOR COOL AND COLD WATER AQUACULTURE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESTROGEN RECEPTOR; FOLLISTATIN; GLUTAMATE AMMONIA LIGASE; GROWTH HORMONE; I KAPPA B; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 1; MITOGEN ACTIVATED PROTEIN KINASE; MYOGENIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR JUNB; UNSPECIFIC MONOOXYGENASE;

ARTICLE; GLYCOLYSIS; IMMUNE RESPONSE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEOMICS; RAINBOW TROUT; SIGNAL TRANSDUCTION;

ANAEROBIOSIS; ANIMALS; BIOLOGICAL MARKERS; CHROMATOGRAPHY, LIQUID; FEMALE; FOLLISTATIN; GROWTH HORMONE; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERLEUKIN-1; MASS SPECTROMETRY; MUSCLE PROTEINS; MUSCULAR ATROPHY; NF-KAPPA B; ONCORHYNCHUS MYKISS; PROTEIN BIOSYNTHESIS; PROTEOME; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, ESTROGEN; REPRODUCTION; TRANSCRIPTION FACTORS;

MAMMALIA; ONCORHYNCHUS MYKISS;

EID: 74849108510     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.10.014     Document Type: Article

References (72)

1. Gerrard D.E., and Grant A.L. Principles of Animal Growth and Development (2003), Kendall/Hunt Publishing Co, IA
2. Kandarian S.C., and Jackman R.W. Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33 2 (2006) 155-165
3. Hasselgren P.O., and Fischer J.E. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg 233 1 (2001) 9-17
4. Zhang P., Chen X., and Fan M. Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses 69 2 (2007) 310-321
5. Glass D.J. Molecular mechanisms modulating muscle mass. Trends Mol Med 9 8 (2003) 344-350
6. Byrne K.A., Wang Y.H., Lehnert S.A., Harper G.S., McWilliam S.M., Bruce H.L., et al. Gene expression profiling of muscle tissue in Brahman steers during nutritional restriction. J Anim Sci 83 1 (2005) 1-12
7. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18 1 (2004) 39-51
8. Lecker S.H., Solomon V., Mitch W.E., Goldberg A.L., et al. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 129 1S Suppl (1999) 227S-237S
9. Raffaello A., Laveder P., Romualdi C., Bean C., Toniolo L., Germinario E., et al. Denervation in murine fast-twitch muscle: short-term physiological changes and temporal expression profiling. Physiol Genomics 25 1 (2006) 60-74
10. Batt J., Bain J., Goncalves J., Michalski B., Plant P., Fahnestock M., et al. Differential gene expression profiling of short and long term denervated muscle. FASEB J 20 1 (2006) 115-117
11. Salem M., Kenney P.B., Rexroad C.E., and Yao J. Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout. Comp Biochem Physiol D Genomics Proteomics 1 1 (2006) 227-237
12. Salem M., Kenney P.B., Rexroad III C.E., and Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28 1 (2006) 33-45
13. Thorgaard G.H., Bailey G.S., Williams D., Buhler D.R., Kaattari S.L., Ristow S.S., et al. Status and opportunities for genomics research with rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 133 4 (2002) 609-646
14. Bai Q., McGillivray C., da Costa N., Dornan S., Evans G., Stear M.J., et al. Development of a porcine skeletal muscle cDNA microarray: analysis of differential transcript expression in phenotypically distinct muscles. BMC Genomics 4 1 (2003) 8
15. Kim N.K., Joh J.H., Park H.R., Kim O.H., Park B.Y., and Lee C.S. Differential expression profiling of the proteomes and their mRNAs in porcine white and red skeletal muscles. Proteomics 4 11 (2004) 3422-3428
16. Van den Thillart G. Energy metabolism of swimming trout (Salmo gairdneri). Oxidation rates of palmitate, glucose, lactate, alanine, leucine and glutamate. J Comp Physiol B 156 (1986) 511-520
17. Salem M., Kenney B., Rexroad C.E., and Yao J. Development of a 37 k high-density oligonucleotide microarray: a new tool for functional genome research in rainbow trout. J Fish Biol 72 (2008) 2187-2206
18. Martin S.A., Blaney S., Bowman A.S., and Houlihan D.F. Ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss): Effect of food deprivation. Pflugers Arch 445 (2002) 257-266
19. Mommsen T.P. Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Comp Biochem Physiol B Biochem Mol Biol 139 3 (2004) 383-400
20. Salem M., Kenney P.B., Rexroad C.E., and Yao J. Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout. Comp Biochem Physiol D Genomics Proteomics 1 1 (2006) 227-237
21. Salem M., Levesque H., Moon T.W., Rexroad C.E., and Yao J. Anabolic effects of feeding beta(2)-adrenergic agonists on rainbow trout muscle proteases and proteins. Comp Biochem Physiol A Mol Integr Physiol 144 2 (2006) 145-154
22. Salem M., Yao J., Rexroad C.E., Kenney P.B., Semmens K., Killefer J., et al. Characterization of calpastatin gene in fish: its potential role in muscle growth and fillet quality. Comp Biochem Physiol B Biochem Mol Biol 141 4 (2005) 488-497
23. Rescan P.Y., Montfort J., Ralliere C., Le Cam A., Esquerre D., and Hugot K. Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule. BMC Genomics 8 (2007) 438
24. Miller K.M., Schulze A.D., Ginther N., Li S., Patterson D.A., Farrell A.P., et al. Salmon spawning migration: Metabolic shifts and environmental triggers. Comp Biochem Physiol Part D Genomics Proteomics 4 2 (2009) 75-89
25. Nie L., Wu G., and Zhang W. Correlation of mRNA expression and protein abundance affected by multiple sequence features related to translational efficiency in Desulfovibrio vulgaris: a quantitative analysis. Genetics 174 4 (2006) 2229-2243
26. Tian Q., Stepaniants S.B., Mao M., Weng L., Feetham M.C., et al. Integrated genomic and proteomic analyses of gene expression in Mammalian cells. Mol Cell Proteomics 3 10 (2004) 960-969
27. Fitzpatrick D.P.G., You J.-S., Bemis K.G., Wery J.-P., Ludwig J.R., and Wang M. Searching for Potential Biomarkers of Cisplatin Resistance in Human Ovarian Cancer Using a Label-free LC/MS-based Protein Quantification Method. Proteomics- Clin Appl 1 (2007) 246-263
28. Higgs R.E., Knierman M.D., Gelfanova V., Butler J.P., and Hale J.E. Comprehensive label-free method for the relative quantification of proteins from biological samples. J Proteome Res 4 4 (2005) 1442-1450
29. Gaoa Y., Zhanga R., Hua X., and Li N. Application of genomic technologies to the improvement of meat quality of farm animals. Meat Sci 77 1 (2007) 36-45
30. AOAC. Official Methods of Analysis. 5th edn. (1990), Association of Official Analytical Chemists, Washington, D.C.
31. Hale J.E., Butler J.P., Gelfanova V., You J.S., and Knierman M.D. A simplified procedure for the reduction and alkylation of cysteine residues in proteins prior to proteolytic digestion and mass spectral analysis. Anal Biochem 333 1 (2004) 174-181
32. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
33. Higgs RE, Knierman MD, Freeman AB, Gelbert LM, Patil ST, Hale JE. Estimating the statistical significance of peptide identifications from shotgun proteomics experiments. 2007;6(5):1758-1767.
34. Bolstad B.M., Irizarry R.A., Astrand M., and Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 2 (2003) 185-193
35. Halseth A.E., Bracy D.P., and Wasserman D.H. Overexpression of hexokinase II increases insulinand exercise-stimulated muscle glucose uptake in vivo. Am J Physiol 276 1 Pt 1 (1999) E70-E77
36. Parker K.C., Kong S.W., Walsh R.J.B., Salajegheh M., Moghadaszadeh B., Amato A.A., et al. Fast-twitch sarcomeric and glycolytic enzyme protein loss in inclusion body myositis. Muscle Nerve 39 6 (2009) 739-753
37. Emery P.W., Edwards R.H., Rennie M.J., Souhami R.L., and Halliday D. Protein synthesis in muscle measured in vivo in cachectic patients with cancer. Br Med J (Clin Res Ed) 289 6445 (1984) 584-586
38. Smith R.W., Houlihan D.F., Nilsson G.E., and Brechin J.G. Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol 271 4 Pt 2 (1996) R897-R904
39. Fraser K.P., Houlihan D.F., Lutz P.L., Leone-Kabler S., Manuel L., and Brechin J.G. Complete suppression of protein synthesis during anoxia with no post-anoxia protein synthesis debt in the red-eared slider turtle Trachemys scripta elegans. J Exp Biol 204 Pt 24 (2001) 4353-4360
40. Sacheck J.M., Hyatt J.P., Raffaello A., Jagoe R.T., Roy R.R., Edgerton V.R., et al. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21 1 (2007) 140-155
41. Powers S.K., Kavazis A.N., and McClung J.M. Oxidative stress and disuse muscle atrophy. J Appl Physiol 102 6 (2007) 2389-2397
42. Martin S.A., Blaney S., Bowman A.S., and Houlihan D.F. Ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss): effect of food deprivation. Pflugers Arch 445 2 (2002) 257-266
43. González B., Negredo P., Hernando R., and Manso R. Protein variants of skeletal muscle regulatory myosin light chain isoforms: prevalence in mammals, generation and transitions during muscle remodelling. Pflugers Arch 443 3 (2002) 377-386
44. Seo Y., Lee K., Park K., Bae K., and Choi I. A proteomic assessment of muscle contractile alterations during unloading and reloading. J Biochem 139 1 (2006) 71-80
45. Falduto M.T., Young A.P., and Hickson R.C. Exercise inhibits glucocorticoid-induced glutamine synthetase expression in red skeletal muscles. Am J Physiol 262 1 Pt 1 (1992) C214-C220
46. Salehian B., Mahabadi V., Bilas J., Taylor W.E., and Ma K. The effect of glutamine on prevention of glucocorticoid-induced skeletal muscle atrophy is associated with myostatin suppression. Metabolism 55 9 (2006) 1239-1247
47. Clowes G.H., Randall H.T., and Cha C.J. Amino acid and energy metabolism in septic and traumatized patients. JPEN J Parenter Enteral Nutr 4 2 (1980) 195-205
48. Hundal H.S., Babij P., Watt P.W., Ward M.R., and Rennie M.J. Glutamine transport and metabolism in denervated rat skeletal muscle. Am J Physiol 259 2 Pt 1 (1990) E148-E154
49. Frost R.A., and Lang C.H. Regulation of muscle growth by pathogen-associated molecules. J Anim Sci 86 14 Suppl (2008) E84-E93
50. Mourkioti F., Kratsios P., Luedde T., Song Y.H., Delafontaine P., Adami R., et al. Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration. J Clin Invest 116 11 (2006) 2945-2954
51. Kawai T., and Akira S. Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med 13 11 (2007) 460-469
52. Haddad F., Zaldivar F., Cooper D.M., and Adams G.R. IL-6-induced skeletal muscle atrophy. J Appl Physiol 98 3 (2005) 911-917
53. Calduch-Giner J., Duval H., Chesnel F., Boeuf G., Pérez-Sánchez J., and Boujard D. Fish growth hormone receptor: molecular characterization of two membrane-anchored forms. Endocrinology 142 7 (2001) 3269-3273
54. Katsumata M., Cattaneo D., White P., Burton K.A., and Dauncey M.J. Growth hormone receptor gene expression in porcine skeletal and cardiac muscles is selectively regulated by postnatal undernutrition. J Nutr 130 10 (2000) 2482-2488
55. Giovannini S., Marzetti E., Borst S.E., and Leeuwenburgh C. Modulation of GH/IGF-1 axis: potential strategies to counteract sarcopenia in older adults. Mech Ageing Dev 129 10 (2008) 593-601
56. Shimasaki S., and Ling N. Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1, -2, -3, -4, -5 and -6). Prog Growth Factor Res 3 4 (1991) 243-266
57. Qin X., Strong D.D., Baylink D.J., and Mohan S. Structure-function analysis of the human insulin-like growth factor binding protein-4. J Biol Chem 273 (1998) 23509-23516
58. Rees C., and Clemmons D.R. Inhibition of IGFBP-5 binding to extracellular matrix and IGF-I-stimulated DNA synthesis by a peptide fragment of IGFBP-5. J Cell Biochem 71 (1998) 375-381
59. Jones J.I., Gockerman A., Busby Jr. W.H., Camacho-Hubner C., and Clemmons D.R. Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I. J Cell Biol 121 (1993) 679-687
60. Hobler S.C., Williams A.B., Fischer J.E., and Hasselgren P.O. IGF-I stimulates protein synthesis but does not inhibit protein breakdown in muscle from septic rats. Am J Physiol 274 2 Pt 2 (1998) R571-R576
61. Viñals F., and Ventura F. Myogenin protein stability is decreased by BMP-2 through a mechanism implicating Id1. J Biol Chem 279 44 (2004) 45766-45772
62. Larsen A.E., Tunstall R.J., Carey K.A., Nicholas G., Kambadur R., Crowe T.C., et al. Actions of short-term fasting on human skeletal muscle myogenic and atrogenic gene expression. Ann Nutr Metab 50 5 (2006) 476-481
63. Drummond M.J., Glynn E.L., Lujan H.L., Dicarlo S.E., and Rasmussen B.B. Gene and protein expression associated with protein synthesis and breakdown in paraplegic skeletal muscle. Muscle Nerve 37 4 (2008) 505-513
64. Gilson H., Schakman O., Kalista S., Lause P., Tsuchida K., and Thissen J.P. Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am J Physiol Endocrinol Metab 297 1 (2009) E157-E164
65. Calura E., Cagnin S., Raffaello A., Laveder P., Lanfranchi G., and Romualdi C. Meta-analysis of expression signatures of muscle atrophy: gene interaction networks in early and late stages. BMC Genomics 9 (2008) 630-630
66. Tiidus P.M. Oestrogen and sex influence on muscle damage and inflammation: evidence from animal models. Curr Opin Clin Nutr Metab Care 4 6 (2001) 509-513
67. Maddalozzo G.F., Cardinal B.J., Li F., and Snow C.M. The association between hormone therapy use and changes in strength and body composition in early postmenopausal women. Menopause 11 4 (2004) 438-446
68. Sugiura T., Ito N., Goto K., Naito H., Yoshioka T., and Powers S.K. Estrogen administration attenuates immobilization-induced skeletal muscle atrophy in male rats. J Physiol Sci 56 6 (2006) 393-399
69. Almansa E., Pérez M.J., Cejas J.R., Badía P., Villamandos J.R., and Lorenzo A. Influence of broodstock gilthead seabream (Sparus aurata L.) dietary fatty acids on egg quality and egg fatty acid composition throughout the spawning season. Aquaculture 170 (1999) 323-336
70. Pérez M.J., Rodríguez C., Cejas J.R., Martín M.V., Jerez S., and Lorenzo A. Lipid and fatty acid content in wild white seabream (Diplodus sargus) broodstock at different stages of the reproductive cycle. Comp Biochem Physiol B Biochem Mol Biol 146 2 (2007) 187-196
71. Wade M.G., and Van der Kraak G. Arachidonic acid and prostaglandin E2 stimulate testosterone production by goldfish testis in vitro. Gen Comp Endocrinol 90 1 (1993) 109-118
72. Salem M., Levesque H., Moon T.W., Rexroad C.E., and Yao J. Anabolic effects of feeding beta2-adrenergic agonists on rainbow trout muscle proteases and proteins. Comp Biochem Physiol A Mol Integr Physiol 144 2 (2006) 145-154