Dietary fish oil alleviates soleus atrophy during immobilization in association with Akt signaling to p70s6k and E3 ubiquitin ligases in rats

Applied Physiology, Nutrition and Metabolism

Volumn 35, Issue 3, 2010, Pages 310-318

  You, Jae Sung ^a   Park, Mi Na ^a   Song, Wook ^a   Lee, Yeon Sook ^a  

^a Seoul National University   (South Korea)

Author keywords

Akt; E3 ubiquitin ligases; Fish oil; Immobilization; Muscle atrophy; Myosin heavy chain; p70 S6 kinase

Indexed keywords

AUTACOID; CORN OIL; FBXO32 PROTEIN, RAT; FISH OIL; INSULIN; MUSCLE PROTEIN; MYOSIN HEAVY CHAIN; PROTEIN KINASE B; RNF28 PROTEIN, RAT; S6 KINASE; UBIQUITIN PROTEIN LIGASE;

ANIMAL; ARTICLE; DIET SUPPLEMENTATION; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMOBILIZATION; MALE; METABOLISM; MUSCLE ATROPHY; ORGAN SIZE; OXIDATIVE STRESS; PATHOLOGY; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; CORN OIL; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FISH OILS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HINDLIMB SUSPENSION; INFLAMMATION MEDIATORS; INSULIN; MALE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSIN HEAVY CHAINS; ORGAN SIZE; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TIME FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 77955128259     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H10-022     Document Type: Article

References (44)

1. Acharyya, S., Ladner, K.J., Nelsen, L.L., Damrauer, J., Reiser, P.J., Swoap, S., and Guttridge, D.C. 2004. Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J. Clin. Invest. 114(3): 370-378.doi:10.1172/JCI200420174. PMID:15286803.
2. Aoki, M.S., Lima, W.P., Miyabara, E.H., Gouveia, C.H., and Moriscot, A.S. 2004. Deleteriuos effects of immobilization upon rat skeletal muscle: role of creatine supplementation. Clin. Nutr. 23(5): 1176-1183. doi:10.1016/j.clnu.2004.03.004. PMID: 15380911.
3. Babcock, T.A., Kurland, A., Helton, W.S., Rahman, A., Anwar, K.N., and Espat, N.J. 2003. Inhibition of activator protein-1 transcription factor activation by omega-3 fatty acid modulation of mitogen-activated protein kinase signaling kinases. JPEN J. Parenter. Enteral Nutr. 27(3): 176-180, discussion 181. doi:10. 1177/0148607103027003176. PMID:12757110.
4. Baptista, I.L., Leal, M.L., Artioli, G.G., Aoki, M.S., Fiamoncini, J., Turri, A.O., et al. 2010. Leucine attenuates skeletal muscle wasting via inhibition of ubiquitin ligases. Muscle Nerve. In press. doi:10.1002/mus.21578. PMID:20082419.
5. Bar-Shai, M., Carmeli, E., Ljubuncic, P., and Reznick, A.Z. 2008. Exercise and immobilization in aging animals: the involvement of oxidative stress and NF-kappaB activation. Free Radic. Biol. Med. 44(2): 202-214.doi:10.1016/j.freeradbiomed.2007.03.019. PMID:18191756.
6. Clarke, B.A., Drujan, D., Willis, M.S., Murphy, L.O., Corpina, R.A., Burova, E., et al. 2007. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 6(5): 376-385. doi:10.1016/j.cmet.2007.09. 009. PMID:17983583.
7. Cohen, S., Brault, J.J., Gygi, S.P., Glass, D.J., Valenzuela, D.M., Gartner, C., et al. 2009. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J. Cell Biol. 185(6): 1083-1095.doi:10.1083/jcb. 200901052. PMID:19506036.
8. Coutinho, E.L., Gomes, A.R., Franca, C.N., and Salvini, T.F. 2002. A new model for the immobilization of the rat hind limb. Braz. J. Med. Biol. Res. 35(11): 1329-1332. doi:10.1590/S0100-879X2002001100010. PMID:12426632.
9. Dong, F., Hua, Y., Zhao, P., Ren, J., Du, M., and Sreejayan, N. 2009. Chromium supplement inhibits skeletal muscle atrophy in hindlimb-suspended mice. J. Nutr. Biochem. 20(12): 992-999. doi:10.1016/j.jnutbio.2008.09.006. PMID:19071005.
10. Gingras, A.A., White, P.J., Chouinard, P.Y., Julien, P., Davis, T.A., Dombrowski, L., et al. 2007. Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signalling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. J. Physiol. 579(Pt. 1): 269-284. doi:10.1113/ jphysiol.2006.121079. PMID:17158167.
11. Grosset, J.F., and Onambele-Pearson, G. 2008. Effect of foot and ankle immobilization on leg and thigh muscles' volume and morphology: a case study using magnetic resonance imaging. Anat. Rec. (Hoboken), 291(12): 1673-1683. doi:10.1002/ar.20759. PMID:18951503.
12. Haugaard, S.B., Madsbad, S., Høy, C.E., and Vaag, A. 2006. Dietary intervention increases n-3 long-chain polyunsaturated fatty acids in skeletal muscle membrane phospholipids of obese subjects. Implications for insulin sensitivity. Clin. Endocrinol. (Oxf.), 64(2): 169-178. doi:10.1111/j.1365-2265.2006.02444.x.PMID:16430716.
13. Hilder, T.L., Tou, J.C., Grindeland, R.E., Wade, C.E., and Graves, L.M. 2003. Phosphorylation of insulin receptor substrate-1 serine 307 correlates with JNK activity in atrophic skeletal muscle. FEBS Lett. 553(1-2): 63-67. doi:10.1016/S0014-5793(03) 00972-4. PMID:14550547.
14. Hilder, T.L., Baer, L.A., Fuller, P.M., Fuller, C.A., Grindeland, R.E., Wade, C.E., and Graves, L.M. 2005. Insulin-independent pathways mediating glucose uptake in hindlimb-suspended skeletal muscle. J. Appl. Physiol. 99(6): 2181-2188. doi:10.1152/ japplphysiol.00743.2005. PMID:16099889.
15. Hirose, M., Kaneki, M., Sugita, H., Yasuhara, S., and Martyn, J.A. 2000. Immobilization depresses insulin signaling in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279(6): E1235-E1241. PMID:11093909.
16. Hirose, M., Kaneki, M., Sugita, H., Yasuhara, S., Ibebunjo, C., Martyn, J.A., and Iebunjo, C. 2001. Long-term denervation impairs insulin receptor substrate-1-mediated insulin signaling in skeletal muscle. Metabolism, 50(2): 216-222.doi:10.1053/meta. 2001.20169. PMID:11229432.
17. Hornberger, T.A., Chu, W.K., Mak, Y.W., Hsiung, J.W., Huang, S.A., and Chien, S. 2006. The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 103(12): 4741-4746. doi:10.1073/pnas.0600678103. PMID:16537399.
18. Hunter, R.B., Stevenson, E., Koncarevic, A., Mitchell-Felton, H., Essig, D.A., and Kandarian, S.C. 2002. Activation of an alternative NF-kappaB pathway in skeletal muscle during disuse atrophy. FASEB J. 16(6): 529-538. doi:10.1096/fj.01-0866com.PMID:11919155.
19. Ikemoto, M., Nikawa, T., Takeda, S., Watanabe, C., Kitano, T., Baldwin, K.M., et al. 2001. Space shuttle flight (STS-90) enhances degradation of rat myosin heavy chain in association with activation of ubiquitin-proteasome pathway. FASEB J. 15(7): 1279-1281. PMID:11344113.
20. Karakelides, H., and Nair, K.S. 2005. Sarcopenia of aging and its metabolic impact. Curr. Top. Dev. Biol. 68: 123-148. doi:10. 1016/S0070-2153(05)68005-2. PMID:16124998.
21. Kondo, H., Nakagaki, I., Sasaki, S., Hori, S., and Itokawa, Y. 1993. Mechanism of oxidative stress in skeletal muscle atrophied by immobilization. Am. J. Physiol. 265(6 Pt. 1): E839-E844. PMID:8279538.
22. Krawiec, B.J., Frost, R.A., Vary, T.C., Jefferson, L.S., and Lang, C.H. 2005. Hindlimb casting decreases muscle mass in part by proteasome-dependent proteolysis but independent of protein synthesis. Am. J. Physiol. Endocrinol. Metab. 289(6): E969-E980. doi:10.1152/ajpendo.00126.2005. PMID:16046454.
23. Lecker, S.H., Solomon, V., Mitch, W.E., and Goldberg, A.L. 1999. Muscle protein breakdown and the critical role of the ubiquitinproteasome pathway in normal and disease states. J. Nutr. 129(Suppl. 1): 227S-237S. PMID:9915905.
24. Léger, B., Cartoni, R., Praz, M., Lamon, S., Dériaz, O., Crettenand, A., et al. 2006. Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 576(Pt. 3): 923-933.doi:10.1113/jphysiol. 2006.116715. PMID:16916907.
25. Li, H., Malhotra, S., and Kumar, A. 2008. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J. Mol. Med. 86(10): 1113-1126. doi:10.1007/s00109-008-0373-8. PMID:18574572.
26. Munoz, K.A., Satarug, S., and Tischler, M.E. 1993. Time course of the response of myofibrillar and sarcoplasmic protein metabolism to unweighting of the soleus muscle. Metabolism, 42(8): 1006-1012. doi:10.1016/0026-0495(93)90014-F. PMID: 8345803.
27. Niemela, O., Parkkila, S., Worrall, S., Emery, P.W., and Preedy, V.R. 2003. Generation of aldehyde-derived protein modifications in ethanol-exposed heart. Alcohol. Clin. Exp. Res. 27(12): 1987-1992.doi:10.1097/01.ALC.0000099260.58926.F2. PMID: 14691387.
28. Ntambi, J.M., and Bené, H. 2001. Polyunsaturated fatty acid regulation of gene expression. J. Mol. Neurosci. 16(2-3): 273-278, discussion 279-284. doi:10.1385/JMN:16:2-3:273. PMID: 11478382.
29. O'Keefe, M.P., Perez, F.R., Sloniger, J.A., Tischler, M.E., and Henriksen, E.J. 2004. Enhanced insulin action on glucose transport and insulin signaling in 7-day unweighted rat soleus muscle. J. Appl. Physiol. 97(1): 63-71.doi:10.1152/japplphysiol. 01361.2003. PMID:15004002.
30. O'Neil, T.K., Duffy, L.R., Frey, J.W., and Hornberger, T.A. 2009. The role of phosphoinositide 3-kinase and phosphatidic acid in the regulation of mammalian target of rapamycin following eccentric contractions. J. Physiol. 587(Pt 14): 3691-3701. doi:10. 1113/jphysiol.2009.173609. PMID:19470781.
31. Powers, S.K., Kavazis, A.N., and DeRuisseau, K.C. 2005. Mechanisms of disuse muscle atrophy: role of oxidative stress. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288(2): R337-R344. doi:10.1152/ajpregu.00469.2004. PMID:15637170.
32. Rennie, M.J., Selby, A., Atherton, P., Smith, K., Kumar, V., Glover, E.L., and Philips, S.M. 2009. Facts, noise and wishful thinking: muscle protein turnover in aging and human disuse atrophy. Scand. J. Med. Sci. Sports, 20(1): 5-9.doi:10.1111/j. 1600-0838.2009.00967.x. PMID:19558380.
33. Servais, S., Letexier, D., Favier, R., Duchamp, C., and Desplanches, D. 2007. Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic. Biol. Med. 42(5): 627-635. doi:10.1016/j.freeradbiomed.2006.12.001. PMID: 17291986.
34. Smith, H.J., Greenberg, N.A., and Tisdale, M.J. 2004. Effect of eicosapentaenoic acid, protein and amino acids on protein synthesis and degradation in skeletal muscle of cachectic mice. Br. J. Cancer, 91(2): 408-412. doi:10.1038/sj.bjc.6601981. PMID: 15213711.
35. Stitt, T.N., Drujan, D., Clarke, B.A., Panaro, F., Timofeyva, Y., Kline, W.O., et al. 2004. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell, 14(3): 395-403. doi:10.1016/S1097-2765(04)00211-4. PMID:15125842.
36. Storlien, L.H., Jenkins, A.B., Chisholm, D.J., Pascoe, W.S., Khouri, S., and Kraegen, E.W. 1991. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes, 40(2): 280-289. doi:10.2337/diabetes.40.2. 280. PMID:1991575.
37. Taouis, M., Dagou, C., Ster, C., Durand, G., Pinault, M., and Delarue, J. 2002. N-3 polyunsaturated fatty acids prevent the defect of insulin receptor signaling in muscle. Am. J. Physiol. Endocrinol. Metab. 282(3): E664-E671. PMID:11832371.
38. Tisdale, M.J. 1997. Cancer cachexia: metabolic alterations and clinical manifestations. Nutrition, 13(1): 1-7.doi:10.1016/S0899-9007(96)00313-9. PMID:9058439.
39. Tisdale, M.J. 2005. The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting. J. Support. Oncol. 3(3): 209-217. PMID:15915823.
40. von Knethen, A., Callsen, D., and Brune, B. 1999. NF-kappaB and AP-1 activation by nitric oxide attenuated apoptotic cell death in RAW 264.7 macrophages. Mol. Biol. Cell, 10(2): 361-372. PMID:9950682.
41. Whitehouse, A.S., Smith, H.J., Drake, J.L., and Tisdale, M.J. 2001. Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid. Cancer Res. 61(9): 3604-3609. PMID:11325828.
42. You, J.S., Park, M.N., and Lee, Y.S. 2009. Dietary fish oil inhibits the early stage of recovery of atrophied soleus muscle in rats via Akt-p70s6k signaling and PGF2a. J. Nutr. Biochem. [Epub ahead of print.].doi:10.1016/j.jnutbio.2009.07.007. PMID: 19954953.
43. Yuan, Y.V., and Kitts, D.D. 2003. Dietary (n-3) fat and cholesterol alter tissue antioxidant enzymes and susceptibility to oxidation in SHR and WKY rats. J. Nutr. 133(3): 679-688. PMID: 12612137.
44. Zhang, P., Chen, X., and Fan, M. 2007. Signaling mechanisms involved in disuse muscle atrophy. Med. Hypotheses, 69(2): 310-321. doi:10.1016/j.mehy.2006.11.043. PMID:17376604.