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

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 157, Issue 3, 2010, Pages 248-257

  Cleveland, Beth M ^a   Evenhuis, Jason P ^a  

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

Author keywords

Atrogin 1; Atrophy; Fish; Protein degradation; Salmonid; Starvation; Ubiquitin ligase

Indexed keywords

ATROGIN 1; F BOX PROTEIN; F BOX PROTEIN 25; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; FISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAST MUSCLE; INTESTINE; KIDNEY; LIVER; MUSCLE ATROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; RAINBOW TROUT; SEQUENCE ALIGNMENT; SLOW MUSCLE; STARVATION; TISSUE DISTRIBUTION; ANIMAL; FOOD DEPRIVATION; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

DANIO RERIO; ONCORHYNCHUS MYKISS; SALMONIDAE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; F-BOX PROTEINS; FISH PROTEINS; FOOD DEPRIVATION; GENE EXPRESSION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; ONCORHYNCHUS MYKISS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SKP CULLIN F-BOX PROTEIN LIGASES; TISSUE DISTRIBUTION;

EID: 77956185742     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.06.010     Document Type: Article

References (65)

1. τ-methylhistidine level. Bull. Jpn. Soc. Sci. Fish 1986, 52:1237-1241.
2. Beaulieu M.A., Guderley H. Changes in qualitative composition of white muscle with nutritional status of Atlantic cod, Gadus morhua. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1998, 121:135-141.
3. Blier P.U., Dutil J.D., Lemieux H., Belanger F., Bitetera L. Phenotypic flexibility of digestive system in Atlantic cod (Gadus morhua). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2007, 146:174-179.
4. 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.
5. 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.
6. Chen Y.W., Gregory C.M., Scarborough M.T., Shi R., Walter G.A., Vandenborne K. Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol. Genomics 2007, 31:510-520.
7. 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.
8. 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.
9. Csibi A., Leibovitch M.P., Cornille K., Tintignac L.A., Leibovitch S.A. MAFbx/Atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J. Biol. Chem. 2009, 284:4413-4421.
10. d'Azzo A., Bongiovanni A., Nastasi T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 2005, 6:429-441.
11. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
12. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
13. Frost R.A., Nystrom G.J., Jefferson L.S., Lang C.H. Hormone, cytokine, and nutritional regulation of sepsis-induced increases in atrogin-1 and MuRF1 in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E501-E512.
14. Furne M., Garcia-Gallego M., Hidalgo M.C., Morales A.E., Domezain A., Domezain J., Sanz A. Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008, 149:420-425.
15. Furuno K., Goodman M.N., Goldberg A.L. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J. Biol. Chem. 1990, 265:8550-8557.
16. Gomes M.D., Lecker S.H., Jagoe R.T., Navon A., Goldberg A.L. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc. Natl Acad. Sci. USA 2001, 98:14440-14445.
17. Guderley H., Lapointe D., Bedard M., Dutil J.D. Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2003, 135:347-356.
18. Hagens O., Minina E., Schweiger S., Ropers H.H., Kalscheuer V. Characterization of FBX25, encoding a novel brain-expressed F-box protein. Biochim. Biophys. Acta 2006, 1760:110-118.
19. Herningtyas E.H., Okimura Y., Handayaningsih A.E., 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 2008, 1780:1115-1120.
20. Higgins A., Silverstein J., Engles J., Wilson M., Rexroad C., Blemings K. Starvation induced alterations in hepatic lysine metabolism in different families of rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 2005, 31:33-44.
21. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B.A., de Castro E., Lachaize C., Langendijk-Genevaux P.S., Sigrist C.J.A. The 20years of PROSITE. Nucleic Acids Res. 2008, 36:D245-D249.
22. Jagoe R.T., Lecker S.H., Gomes M., Goldberg A.L. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J. 2002, 16:1697-1712.
23. Jin J., Cardozo T., Lovering R.C., Elledge S.J., Pagano M., Harper J.W. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 2004, 18:2573-2580.
24. Johansen K.A., Overturf K. Alterations in expression of genes associated with muscle metabolism and growth during nutritional restriction and refeeding in rainbow trout. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2006, 144:119-127.
25. Kieffer J., Tufts B. Effects of food deprivation on white muscle energy reserves in rainbow trout (Oncorhynchus mykiss): the relationships with body size and temperature. Fish Physiol. Biochem. 1998, 19:239-245.
26. Kim S.J., Roy R.R., Kim J.A., Zhong H., Haddad F., Baldwin K.M., Edgerton V.R. Gene expression during inactivity-induced muscle atrophy: effects of brief bouts of a forceful contraction countermeasure. J. Appl. Physiol. 2008, 105:1246-1254.
27. Krogdahl A., Bakke-McKellep A.M. Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon (Salmo salar L.). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2005, 141:450-460.
28. 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.
29. 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.
30. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., Price S.R., Mitch W.E., Goldberg A.L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 2004, 18:39-51.
31. 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. Invest. 2004, 114:1058-1071.
32. 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. Invest. 2007, 117:3211-3223.
33. Lira E.C., Graca F.A., Goncalves D.A., Zanon N.M., Baviera A.M., Strindberg L., Lonnroth P., Migliorini R.H., Kettelhut I.C., Navegantes L.C. Cyclic adenosine monophosphate-phosphodiesterase inhibitors reduce skeletal muscle protein catabolism in septic rats. Shock 2007, 27:687-694.
34. Manfiolli A.O., Maragno A.L., Baqui M.M., Yokoo S., Teixeira F.R., Oliveira E.B., Gomes M.D. FBXO25-associated nuclear domains: a novel subnuclear structure. Mol. Biol. Cell 2008, 19:1848-1861.
35. Maragno A.L., Baqui M.M., Gomes M.D. FBXO25, an F-box protein homologue of atrogin-1, is not induced in atrophying muscle. Biochim. Biophys. Acta 2006, 1760:966-972.
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. Pfluegers Arch. 2002, 445:257-266.
37. Morata P., Vargas A.M., Sanchez-Medina F., Garcia M., Cardenete G., Zamora S. Evolution of gluconeogenic enzyme activities during starvation in liver and kidney of the rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. B 1982, 71:65-70.
38. Moylan J.S., Smith J.D., Chambers M.A., McLoughlin T.J., Reid M.B. TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am. J. Physiol. Cell Physiol. 2008, 295:C986-C993.
39. 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) 2005, 51:248-253.
40. 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. 2006, 70:2775-2778.
41. Olsson C., Holmgren S. The control of gut motility. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 128:481-503.
42. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
43. 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.
44. Rexroad C.E., Lee Y., Keele J.W., Karamycheva S., Brown G., Koop B., Gahr S.A., Palti Y., Quackenbush J. Sequence analysis of a rainbow trout cDNA library and creation of a gene index. Cytogenet. Genome Res. 2003, 102:347-354.
45. Rios F.S., Moraes G., Oba E.T., Fernandes M.N., Donatti L., Kalinin A.L., Rantin F.T. Mobilization and recovery of energy stores in traira, Hoplias malabaricus Bloch (Teleostei, Erythrinidae) during long-term starvation and after re-feeding. J. Comp. Physiol. B 2006, 176:721-728.
46. 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.
47. Sacheck J.M., Hyatt J.P., Raffaello A., Jagoe R.T., Roy R.R., Edgerton V.R., Lecker S.H., Goldberg A.L. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J. 2007, 21:140-155.
48. 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.
49. 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.
50. Sitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
51. Slem 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.
52. 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. 2007, 117:2468-2476.
53. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
54. Tawa N.E., Odessey R., Goldberg A.L. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 1997, 100:197-203.
55. 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.
56. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
57. Tintignac L.A., Lagirand J., Batonnet S., Sirri V., Leibovitch M.P., Leibovitch S.A. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 2005, 280:2847-2856.
58. 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. 2009, 378:399-403.
59. Toyohara H., Ito K., Hori N., Touhata K., Kinoshita M., Kutoba S., Sato K., Ohtsuki K., Sakaguchi M. Effect of steroid hormone administration on the breakdown of muscle proteins in ayu. Fish. Sci. 1998, 64:419-422.
60. Wang T., Hung C.C., Randall D.J. The comparative physiology of food deprivation: from feast to famine. Annu. Rev. Physiol. 2006, 68:223-251.
61. Wilkinson R.J., Porter M., Woolcott H., Longland R., Carragher J.F. 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. 2006, 145:214-224.
62. Wright P.A., Campbell A., Morgan R.L., Rosenberger A.G., Murray B.W. Dogmas and controversies in the handling of nitrogenous wastes: expression of arginase Type I and II genes in rainbow trout: influence of fasting on liver enzyme activity and mRNA levels in juveniles. J. Exp. Biol. 2004, 207:2033-2042.
63. Zhang P., Chen X., Fan M. Signaling mechanisms involved in disuse muscle atrophy. Med. Hypotheses 2007, 69:310-321.
64. Zhao W., Pan J., Wang X., Wu Y., Bauman W.A., Cardozo C.P. Expression of the muscle atrophy factor muscle atrophy F-box is suppressed by testosterone. Endocrinology 2008, 149:5449-5460.
65. Zuckerkandl E., Pauling L. Molecules as documents of evolutionary history. J. Theor. Biol. 1965, 8:357-366.