Amino acids downregulate the expression of several autophagy-related genes in rainbow trout myoblasts

Autophagy

Volumn 8, Issue 3, 2012, Pages 364-375

  Seiliez, Iban ^a   Gabillard, Jean Charles ^b   Riflade, Marine ^a   Sadoul, Bastien ^a   Dias, Karine ^a   Avérous, Julien ^c   Tesseraud, Sophie ^d   Skiba, Sandrine ^a   Panserat, Stéphane ^a  

^a UR1067 Nutrition Metabolism Aquaculture   (France)

^b Campus de Beaulieu   (France)

^c INRA and University of Auvergne   (France)

^d STATION DE RECHERCHES AVICOLES   (France)

Author keywords

Amino acids; Autophagosome; Fish; Gene expression; Myoblast; Signaling

Indexed keywords

AMINO ACID; MESSENGER RNA; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DEGRADATION; DOWN REGULATION; ENERGY; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; LYSOSOME; MYOBLAST; NONHUMAN; NUTRIENT; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAINBOW TROUT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETORY PATHWAY; SERUM; SIGNAL TRANSDUCTION;

ONCORHYNCHUS MYKISS;

AMINO ACIDS; ANIMALS; AUTOPHAGY; DOWN-REGULATION; FISH PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MYOBLASTS; ONCORHYNCHUS MYKISS; PHAGOSOMES; PHOSPHORYLATION; SERUM; SIGNAL TRANSDUCTION; SIROLIMUS; TIME FACTORS; TOR SERINE-THREONINE KINASES;

EID: 84859141601     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.18863     Document Type: Article

References (58)

1. Aoyama J. Life History and Evolution of Migration in Catadromous Eels (Genus Anguilla). AquaBioScience Monographs 2009; 2:1-42.
2. Tsukamoto K. Oceanic migration and spawning of anguillid eels. J Fish Biol 2009; 74:1833-52; PMID:20735675; http://dx.doi.org/10.1111/j.1095-8649. 2009.02242.x
3. Miller KM, Schulze AD, Ginther N, Li S, Patterson DA, Farrell AP, et al. Salmon spawning migration: Metabolic shifts and environmental triggers. Comp Biochem Physiol Part D Genomics Proteomics 2009; 4:75-89; PMID:20403740; http://dx.doi.org/10.1016/j.cbd.2008.11.002
4. Ueda H. Physiological mechanisms of salmon imprinting and homing migration. 16th Int Congr of Comp Endocrinol. Hong Kong, China, 2009.
5. Mommsen TP, French CJ, Hochachka PW. Sites and patterns of protein and amino-acid utilization during the spawning migration of salmon. Can J Zool-Rev Can Zool 1980; 58:1785-99; http://dx.doi.org/10.1139/ z80-246
6. French CJ, Hochachka PW, Mommsen TP. Metabolic organization of liver during spawning migration of sockeye salmon. Am J Physiol 1983; 245:R827-30; PMID:6660327
7. 2+- dependent systems. In: Bittar EE, Rivett AJ, eds. Advances in Molecular and Cell Biology. Stamford (USA), 1998:235-66.
8. Jagoe RT, Goldberg AL. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy?. Curr Opin Clin Nutr Metab Care 2001; 4:183-90; PMID:11517350; http://dx.doi.org/10.1097/00075197-200105000- 00003
9. 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 2000; 100:595-602; PMID:11078210; http://dx.doi.org/10.1007/ s004010000229
10. Lecker SH, Jagoe RT, 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 2004; 18:39-51; PMID:14718385; http://dx.doi.org/10. 1096/fj.03-0610com
11. Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 1999; 129:227S-37S; PMID:9915905
12. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, et al. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10:507-15; PMID:19945408; http://dx.doi.org/10.1016/j.cmet.2009.10.008
13. Sandri M. Autophagy in skeletal muscle. FEBS Lett 2010; 584:1411-6; PMID:20132819; http://dx.doi.org/10.1016/j.febslet.2010.01.056
14. Cleveland BM, Evenhuis JP. 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; 157:248-57; PMID:20601059; http://dx.doi.org/10.1016/j.cbpb.2010.06.010
15. Cleveland BM, Weber GM. 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:R341-50; PMID:20007517; http://dx.doi.org/10.1152/ajpregu.00516.2009
16. Cleveland BM, Weber GM, Blemings KP, Silverstein JT. 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: R1332-42; PMID:19726716; http://dx.doi.org/10. 1152/ajpregu.00272.2009
17. 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 2004; 137:75-85; PMID:14720593; http://dx.doi.org/10.1016/j.cbpb.2003.09.002
18. Martin SA, Blaney S, Bowman AS, Houlihan DF. Ubiquitin-proteasome- dependent proteolysis in rainbow trout (Oncorhynchus mykiss): effect of food deprivation. Pflugers Arch 2002; 445:257-66; PMID:12457246; http://dx.doi.org/ 10.1007/s00424-002-0916-8
19. 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 2006; 28:33-45; PMID:16882886; http://dx.doi.org/10.1152/physiolgenomics.00114.2006
20. Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, et al. Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. J Nutr 2008; 138:487-91; PMID:18287354
21. Mommsen TP. Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Comp Biochem Physiol B Biochem Mol Biol 2004; 139:383-400; PMID:15544963; http://dx.doi.org/10.1016/j.cbpc.2004.09.018
22. Seiliez I, Gutierrez J, Salmeron C, Skiba-Cassy S, Chauvin C, Dias K, et al. 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; 157:258-66; PMID:20601058; http://dx.doi.org/10.1016/j.cbpb.2010. 06.011
23. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005; 120:237-48; PMID:15680329; http://dx.doi.org/10.1016/j.cell.2004.11. 046
24. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13:132-41; PMID:21258367; http://dx.doi.org/10.1038/ncb2152
25. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
26. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6:458-71; PMID:18054315; http://dx.doi.org/10.1016/j.cmet.2007.11.001
27. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6:472-83; PMID:18054316; http://dx.doi.org/ 10.1016/j.cmet.2007.11.004
28. Lansard M, Panserat S, Plagnes-Juan E, Dias K, Seiliez I, Skiba-Cassy S. L-leucine, L-methionine, and L-lysine are involved in the regulation of intermediary metabolism-related gene expression in rainbow trout hepatocytes. J Nutr 2011; 141:75-80; PMID:21106925; http://dx.doi.org/10.3945/jn.110.124511
29. Lansard M, Panserat S, Plagnes-Juan E, Seiliez I, Skiba-Cassy S. Integration of insulin and amino acid signals that regulate hepatic metabolism-related gene expression in rainbow trout: role of TOR. Amino Acids 2010; 39:801-10; PMID:20213441; http://dx.doi.org/10.1007/s00726-010-0533-3
30. Polakof S, Panserat S, Craig PM, Martyres DJ, Plagnes-Juan E, Savari S, et al. The metabolic consequences of hepatic AMP-kinase phosphorylation in rainbow trout. PLoS ONE 2011; 6:e20228; PMID:21625448; http://dx.doi.org/10. 1371/journal.pone.0020228
31. Seiliez I, Gabillard JC, Skiba-Cassy S, Garcia-Serrana D, Gutierrez J, Kaushik S, et al. 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:R329-35; PMID:18434442; http://dx.doi.org/10.1152/ajpregu.00146.2008
32. Seiliez I, Sabin N, Gabillard JC. FoxO1 Is Not a Key Transcription Factor in the Regulation of myostatin (mstn-1a and mstn-1b) Gene Expression in Trout Myotubes. Am J Physiol Regul Integr Comp Physiol 2011; 301:R97-104; PMID:21490365; http://dx.doi.org/10.1152/ajpregu.00828.2010
33. Seiliez I, Panserat S, Skiba-Cassy S, Polakof S. Effect of acute and chronic insulin administrations on major factors involved in the control of muscle protein turnover in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 2011; 172:363-70; PMID:21463630; http://dx.doi.org/10.1016/j.ygcen. 2011.03.026
34. Meijer AJ, Codogno P. Signalling and autophagy regulation in health, aging and disease. Mol Aspects Med 2006; 27:411-25; PMID:16973212; http://dx.doi.org/10.1016/j.mam.2006.08.002
35. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
36. Fass E, Shvets E, Degani I, Hirschberg K, Elazar Z. Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 2006; 281:36303-16; PMID:16963441; http://dx.doi.org/10.1074/jbc.M607031200
37. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001; 2:211-6; PMID:11265251; http://dx.doi.org/10.1038/ 35056522
38. Bruhat A, Cherasse Y, Chaveroux C, Maurin AC, Jousse C, Fafournoux P. Amino acids as regulators of gene expression in mammals: molecular mechanisms. Biofactors 2009; 35:249-57; PMID:19415732; http://dx.doi.org/10.1002/biof.40
39. Herningtyas EH, Okimura Y, Handayaningsih AE, Yamamoto D, Maki T, Iida K, et al. Branched-chain amino acids and arginine suppress MaFbx/atrogin-1 mRNA expression via mTOR pathway in C2C12 cell line. Biochim Biophys Acta 2008; 1780:1115-20.
40. Tesseraud S, Metayer-Coustard S, Boussaid S, Crochet S, Audouin E, Derouet M, et al. Insulin and amino acid availability regulate atrogin-1 in avian QT6 cells. Biochem Biophys Res Commun 2007; 357:181-6; PMID:17418104; http://dx.doi.org/10.1016/j.bbrc.2007.03.131
41. Yecies JL, Manning BD. Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res 2011; 71:2815-20; PMID:21487041; http://dx.doi.org/ 10.1158/0008-5472.CAN-10-4158
42. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025-40; PMID:15657430; http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005
43. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004; 36:2491-502; PMID:15325587; http://dx.doi.org/10.1016/j.biocel.2004.02.005
44. Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 2005; 12:1509-18; PMID:16247498; http://dx.doi.org/10.1038/sj.cdd.4401751
45. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
46. Avruch J, Long X, Ortiz-Vega S, Rapley J, Papageorgiou A, Dai N. Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 2009; 296:E592-602; PMID:18765678; http://dx.doi.org/10.1152/ajpendo.90645.2008
47. Kimball SR, Jefferson LS. New functions for amino acids: effects on gene transcription and translation. Am J Clin Nutr 2006; 83:500S-507S; PMID:16470021
48. Jousse C, Averous J, Bruhat A, Carraro V, Mordier S, Fafournoux P. Amino acids as regulators of gene expression: molecular mechanisms. Biochem Biophys Res Commun 2004; 313:447-52; PMID:14684183; http://dx.doi.org/10.1016/j.bbrc. 2003.07.020
49. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 2008; 8:224-36; PMID:18762023; http://dx.doi.org/10.1016/j. cmet.2008.07.007
50. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21:2861-73; PMID:18006683; http://dx.doi.org/10.1101/gad.1599207
51. Johnston IA, Bower NI, Macqueen DJ. Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 2011; 214:1617-28; PMID:21525308; http://dx.doi.org/10.1242/jeb.038620
52. National-Research-Council, ed. Nutrient requirements of fish. Washington, DC, USA, 1993.
53. Mehrpour M, Esclatine A, Beau I, Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res 2010; 20:748-62; PMID:20548331; http://dx.doi.org/10.1038/cr.2010.82
54. Gabillard JC, Sabin N, Paboeuf G. In vitro characterization of proliferation and differentiation of trout satellite cells. Cell Tissue Res 2010; 342:471-7; PMID:21086139; http://dx.doi.org/10.1007/s00441-010-1071-8
55. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45; PMID:11328886; http://dx.doi.org/10.1093/nar/29.9.e45
56. Pfaffl MW, Horgan GW, 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; PMID:11972351; http://dx.doi.org/10.1093/nar/30.9.e36
57. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-54; PMID:942051; http://dx.doi.org/10.1016/0003- 2697(76)90527-3
58. SIGENAE. Information System of Breeding Animals'Genome. http://www.sigenae.org