Leucine and HMB Differentially Modulate Proteasome System in Skeletal Muscle under Different Sarcopenic Conditions

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Baptista, Igor L ^a   Silva, Willian J ^a   Artioli, Guilherme G ^a   Guilherme, Joao Paulo L F ^a   Leal, Marcelo L ^a   Aoki, Marcelo S ^a   Miyabara, Elen H ^a   Moriscot, Anselmo S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; BETA HYDROXY BETA METHYLBUTYRATE; BUTYRIC ACID DERIVATIVE; DEXAMETHASONE; LEUCINE; MUSCLE RING FINGER 1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN KINASE B; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG MECHANISM; IMMOBILIZATION; MALE; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE TETANIC CONTRACTION; NONHUMAN; PROTEIN EXPRESSION; RAT; SARCOPENIA; SKELETAL MUSCLE; SOLEUS MUSCLE; UBIQUITINATION;

ANIMALS; DIETARY SUPPLEMENTS; HINDLIMB SUSPENSION; LEUCINE; MALE; MUSCLE, SKELETAL; ORGAN SIZE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SARCOPENIA; VALERATES;

EID: 84885068154     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076752     Document Type: Article

References (56)

1. Booth FW, (1982) Effect of limb immobilization on skeletal muscle. J Appl Physiol 52: 1113-1118. PubMed: 7047468.
2. Booth FW, Gollnick PD, (1983) Effects of disuse on the structure and function of skeletal muscle. Med Sci Sports Exerc 15: 415-420. PubMed: 6645872.
3. Bonaldo P, Sandri M, (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model. J Mech 6: 25-39.
4. Vinciguerra M, Musaro A, Rosenthal N, (2010) Regulation of muscle atrophy in aging and disease. Adv Exp Med Biol 694: 211-233. doi:10.1007/978-1-4419-7002-2_15. PubMed: 20886766.
5. Favier FB, Benoit H, Freyssenet D, (2008) Cellular and molecular events controlling skeletal muscle mass in response to altered use. Pflugers Arch 456: 587-600. doi:10.1007/s00424-007-0423-z. PubMed: 18193272.
6. Glass DJ, (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984. doi:10.1016/j.biocel.2005.04.018. PubMed: 16087388.
7. Kandarian SC, Jackman RW, (2006) Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33: 155-165. doi:10.1002/mus.20442. PubMed: 16228971.
8. Zhang P, Chen X, Fan M, (2007) Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses 69: 310-321. doi:10.1016/j.mehy.2006.11.043. PubMed: 17376604.
9. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708. doi:10.1126/science.1065874. PubMed: 11679633.
10. Pattison JS, Folk LC, Madsen RW, Booth FW, (2003) Selected Contribution: identification of differentially expressed genes between young and old rat soleus muscle during recovery from immobilization-induced atrophy. J Appl Physiol 95: 2171-2179. PubMed: 12897032.
11. Urso ML, Clarkson PM, Price TB, (2006) Immobilization effects in young and older adults. Eur J Appl Physiol 96: 564-571. doi:10.1007/s00421-005-0109-1. PubMed: 16369818.
12. Kayali AG, Young VR, Goodman MN, (1987) Sensitivity of myofibrillar proteins to glucocorticoid-induced muscle proteolysis. Am J Physiol 252: E621-E626. PubMed: 3578511.
13. Lecker SH, Solomon V, Price SR, Kwon YT, Mitch WE, et al. (1999) Ubiquitin conjugation by the N-end rule pathway and mRNAs for its components increase in muscles of diabetic rats. J Clin Invest 104: 1411-1420. doi:10.1172/JCI7300. PubMed: 10562303.
14. Tiao G, Fagan JM, Samuels N, James JH, Hudson K, et al. (1994) Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J Clin Invest 94: 2255-2264. doi:10.1172/JCI117588. PubMed: 7989581.
15. Baracos VE, DeVivo C, Hoyle DH, Goldberg AL, (1995) Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol 268: E996-1006. PubMed: 7539218.
16. Price SR, Bailey JL, England BK, (1996) Necessary but not sufficient: the role of glucocorticoids in the acidosis-induced increase in levels of mRNAs encoding proteins of the ATP-dependent proteolytic pathway in rat muscle. Miner Electrolyte Metab 22: 72-75. PubMed: 8676830.
17. Wing SS, Haas AL, Goldberg AL, (1995) Increase in ubiquitin-protein conjugates concomitant with the increase in proteolysis in rat skeletal muscle during starvation and atrophy denervation. Biochem J 307(3):: 639-645. PubMed: 7741691.
18. Medina R, Wing SS, Goldberg AL, (1995) Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem J 307(3):: 631-637. PubMed: 7741690.
19. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51. doi:10.1096/fj.03-0610com. PubMed: 14718385.
20. Passmore LA, Barford D, (2004) Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem J 379: 513-525. doi:10.1042/BJ20040198. PubMed: 14998368.
21. Pickart CM, Eddins MJ, (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695: 55-72. doi:10.1016/j.bbamcr.2004.09.019. PubMed: 15571809.
22. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL, (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98: 14440-14445. doi:10.1073/pnas.251541198. PubMed: 11717410.
23. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, et al. (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279: 41114-41123. doi:10.1074/jbc.M400674200. PubMed: 15272020.
24. Mammucari C, Schiaffino S, Sandri M, (2008) Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4: 524-526. PubMed: 18367868.
25. Guterman A, Glickman MH, (2004) Deubiquitinating enzymes are IN/(trinsic to proteasome function). Curr Protein Pept Sci 5: 201-211. doi:10.2174/1389203043379756. PubMed: 15188770.
26. Soares AG, Aoki MS, Miyabara EH, Deluca CV, Ono HY, et al. (2007) Ubiquitin-ligase and deubiquitinating gene expression in stretched rat skeletal muscle. Muscle Nerve 36: 685-693. doi:10.1002/mus.20866. PubMed: 17657803.
27. Stipanuk MH, (2007) Leucine and protein synthesis: mTOR and beyond. Nutr Rev 65: 122-129. doi:10.1111/j.1753-4887.2007.tb00289.x. PubMed: 17425063.
28. Vary TC, Anthony JC, Jefferson LS, Kimball SR, Lynch CJ, (2007) Rapamycin blunts nutrient stimulation of eIF4G, but not PKCepsilon phosphorylation, in skeletal muscle. Am J Physiol Endocrinol Metab 293: E188-E196. doi:10.1152/ajpendo.00037.2007. PubMed: 17389711.
29. Baptista IL, Leal ML, Artioli GG, Aoki MS, Fiamoncini J, et al. (2010) Leucine attenuates skeletal muscle wasting via inhibition of ubiquitin ligases. Muscle Nerve 41: 800-808. doi:10.1002/mus.21578. PubMed: 20082419.
30. Nagasawa T, Kido T, Yoshizawa F, Ito Y, Nishizawa N, (2002) Rapid suppression of protein degradation in skeletal muscle after oral feeding of leucine in rats. J Nutr Biochem 13: 121-127. doi:10.1016/S0955-2863(01)00209-1. PubMed: 11834228.
31. Sugawara T, Ito Y, Nishizawa N, Nagasawa T, (2007) Supplementation with dietary leucine to a protein-deficient diet suppresses myofibrillar protein degradation in rats. J Nutr Sci Vitaminol (Tokyo) 53: 552-555. doi:10.3177/jnsv.53.552. PubMed: 18202546.
32. Sugawara T, Ito Y, Nishizawa N, Nagasawa T, (2008) Regulation of muscle protein degradation, not synthesis, by dietary leucine in rats fed a protein-deficient diet. Amino Acids 34.
33. Zanchi NE, Gerlinger-Romero F, Guimarães-Ferreira L, de Siqueira Filho MA, Felitti V, et al. (2010) HMB supplementation: clinical and athletic performance-related effects and mechanisms of action. Amino Acids 40: 1015-1025. PubMed: 20607321.
34. Gerlinger-Romero F, Guimarães-Ferreira L, Giannocco G, Nunes MT, (2011) Chronic supplementation of beta-hydroxy-beta methylbutyrate (HMbeta) increases the activity of the GH/IGF-I axis and induces hyperinsulinemia in rats. Growth Horm IGF Res 21: 57-62. doi:10.1016/j.ghir.2010.12.006. PubMed: 21237681.
35. Kornasio R, Riederer I, Butler-Browne G, Mouly V, Uni Z, et al. (2009) Beta-hydroxy-beta-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta 1793: 755-763. doi:10.1016/j.bbamcr.2008.12.017. PubMed: 19211028.
36. Kimball SR, Jefferson LS, (2006) Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136: 227S-231S. PubMed: 16365087.
37. Aoki MS, Lima WP, Miyabara EH, Gouveia CH, Moriscot AS, (2004) Deleteriuos effects of immobilization upon rat skeletal muscle: role of creatine supplementation. Clin Nutr 23: 1176-1183. doi:10.1016/j.clnu.2004.03.004. PubMed: 15380911.
38. Ansved T, (1995) Effects of immobilization on the rat soleus muscle in relation to age. Acta Physiol Scand 154: 291-302. doi:10.1111/j.1748-1716.1995.tb09913.x. PubMed: 7572227.
39. Guth L, Samaha FJ, (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. Exp Neurol 25: 138-152. doi:10.1016/0014-4886(69)90077-6. PubMed: 4241609.
40. Wray CJ, Mammen JM, Hershko DD, Hasselgren PO, (2003) Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol 35: 698-705. doi:10.1016/S1357-2725(02)00341-2. PubMed: 12672461.
41. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, et al. (2007) The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6: 376-385. doi:10.1016/j.cmet.2007.09.009. PubMed: 17983583.
42. Nissen S, Sharp R, Ray M, Rathmacher JA, Rice D, et al. (1996) Effect of leucine metabolite beta-hydroxy-beta-methylbutyrate on muscle metabolism during resistance-exercise training. J Appl Physiol 81: 2095-2104. PubMed: 8941534.
43. Aversa Z, Alamdari N, Castillero E, Muscaritoli M, Rossi Fanelli F, et al. (2012) beta-Hydroxy-beta-methylbutyrate (HMB) prevents dexamethasone-induced myotube atrophy. Biochem Biophys Res Commun 423: 739-743. doi:10.1016/j.bbrc.2012.06.029. PubMed: 22705301.
44. Pinheiro CH, Gerlinger-Romero F, Guimarães-Ferreira L, de Souza AL Jr, Vitzel KF, et al. (2012) Metabolic and functional effects of beta-hydroxy-beta-methylbutyrate (HMB) supplementation in skeletal muscle. Eur J Appl Physiol 112: 2531-2537. doi:10.1007/s00421-011-2224-5. PubMed: 22075640.
45. Hao Y, Jackson JR, Wang Y, Edens N, Pereira SL, et al. (2011) beta-Hydroxy-beta-methylbutyrate reduces myonuclear apoptosis during recovery from hind limb suspension-induced muscle fiber atrophy in aged rats. Am J Physiol Regul Integr Comp Physiol 301: R701-R715. doi:10.1152/ajpregu.00840.2010. PubMed: 21697520.
46. Rowlands DS, Thomson JS, (2009) Effects of beta-hydroxy-beta-methylbutyrate supplementation during resistance training on strength, body composition, and muscle damage in trained and untrained young men: a meta-analysis. J Strength Cond Res 23: 836-846. doi:10.1519/JSC.0b013e3181a00c80. PubMed: 19387395.
47. Eley HL, Russell ST, Baxter JH, Mukerji P, Tisdale MJ, (2007) Signaling pathways initiated by beta-hydroxy-beta-methylbutyrate to attenuate the depression of protein synthesis in skeletal muscle in response to cachectic stimuli. Am J Physiol Endocrinol Metab 293: E923-E931. doi:10.1152/ajpendo.00314.2007. PubMed: 17609254.
48. Smith HJ, Mukerji P, Tisdale MJ, (2005) Attenuation of proteasome-induced proteolysis in skeletal muscle by {beta}-hydroxy-{beta}-methylbutyrate in cancer-induced muscle loss. Cancer Res 65: 277-283. PubMed: 15665304.
49. Gustafsson T, Osterlund T, Flanagan JN, von Waldén F, Trappe TA, et al. (2010) Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 109: 721-727. doi:10.1152/japplphysiol.00110.2009. PubMed: 20538844.
50. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, et al. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471. doi:10.1016/j.cmet.2007.11.001. PubMed: 18054315.
51. Senf SM, Sandesara PB, Reed SA, Judge AR, (2011) p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300: C1490-C1501. doi:10.1152/ajpcell.00255.2010. PubMed: 21389279.
52. Clavel S, Siffroi-Fernandez S, Coldefy AS, Boulukos K, Pisani DF, et al. (2010) Regulation of the intracellular localization of Foxo3a by stress-activated protein kinase signaling pathways in skeletal muscle cells. Mol Cell Biol 30: 470-480. doi:10.1128/MCB.00666-09. PubMed: 19917721.
53. Haegens A, Schols AM, Gorissen SH, van Essen AL, Snepvangers F, et al. (2012) NF-kappaB activation and polyubiquitin conjugation are required for pulmonary inflammation-induced diaphragm atrophy. Am J Physiol Lung Cell Mol Physiol 302: L103-L110. doi:10.1152/ajplung.00084.2011. PubMed: 22003096.
54. Langen RC, Haegens A, Vernooy JH, Wouters EF, de Winther MP, et al. (2012) NF-kappaB activation is required for the transition of pulmonary inflammation to muscle atrophy. Am J Respir Cell Mol Biol 47: 288-297. doi:10.1165/rcmb.2011-0119OC. PubMed: 22538866.
55. Liu C, Guan J, Kang Y, Xiu H, Chen Y, et al. (2010) Inhibition of dehydration-induced water intake by glucocorticoids is associated with activation of hypothalamic natriuretic peptide receptor-A in rat. PLOS ONE 5: e15607. doi:10.1371/journal.pone.0015607. PubMed: 21187974.
56. Anthony JC, Anthony TG, Kimball SR, Jefferson LS, (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr 131: 856S-860S. PubMed: 11238774.