Ginsenoside Rg1 prevents starvation‑induced muscle protein degradation via regulation of AKT/mTOR/FoxO signaling in C2C12 myotubes
- Authors:
- Fengyu Li
- Xiaoxue Li
- Xuewei Peng
- Lili Sun
- Shengnan Jia
- Ping Wang
- Shuang Ma
- Hongyan Zhao
- Qingmiao Yu
- Hongliang Huo
-
Affiliations: Laboratory of Molecular and Cellular Physiology, School of Life Science, Northeast Normal University, Changchun, Jilin 130024, P.R. China - Published online on: June 15, 2017 https://doi.org/10.3892/etm.2017.4615
- Pages: 1241-1247
This article is mentioned in:
Abstract
Kawai N, Hirasaka K, Maeda T, Haruna M, Shiota C, Ochi A, Abe T, Kohno S, Ohno A, Teshima-Kondo S, et al: Prevention of skeletal muscle atrophy in vitro using anti-ubiquitination oligopeptide carried by atelocollagen. Biochim Biophy Acta. 1853:873–880. 2015. View Article : Google Scholar | |
Langen RC, Gosker HR, Remels AH and Schols AM: Triggers and mechanisms of skeletal muscle wasting in chronic obstructive pulmonary disease. Int J Biochem Cell Biol. 45:2245–2256. 2013. View Article : Google Scholar : PubMed/NCBI | |
Joassard OR, Durieux AC and Freyssenet DG: β2-Adrenergic agonists and the treatment of skeletal muscle wasting disorders. Int J Biochem Cell Biol. 45:2309–2321. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang DT, Yin Y, Yang YJ, Lv PJ, Shi Y, Lu L and Wei LB: Resveratrol prevents TNF-α-induced muscle atrophy via regulation of Akt/mTOR/FoxO1 signaling in C2C12 myotubes. Int Immunopharmacol. 19:206–213. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE and Goldberg AL: Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18:39–51. 2004. View Article : Google Scholar : PubMed/NCBI | |
Langen RC, Gosker HR, Remels AH and Schols AM: Triggers and mechanisms of skeletal muscle wasting in chronic obstructive pulmonary disease. Int J Biochem Cell Biol. 45:2245–2256. 2013. View Article : Google Scholar : PubMed/NCBI | |
Feng W, Tu JC, Pouliquin P, Cabrales E, Shen X, Dulhunty A, Worley PF, Allen PD and Pessah IN: Dynamic regulation of ryanodine receptor type 1 (RyR1) channel activity by Homer 1. Cell Calcium. 43:307–314. 2008. View Article : Google Scholar : PubMed/NCBI | |
Joassard OR, Amirouche A, Gallot YS, Desgeorges MM, Castells J, Durieux AC, Berthon P and Freyssenet DG: Regulation of Akt-mTOR, ubiquitin-proteasome and autophagy-lysosome pathways in response to formoterol administration in rat skeletal muscle. Int J Biochem Cell Biol. 45:2444–2455. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sandri M: Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome. Int J Biochem Cell Biol. 45:2121–2129. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kawai N, Hirasaka K, Maeda T, Haruna M, Shiota C, Ochi A, Abe T, Kohno S, Ohno A, Teshima-Kondo S, et al: Prevention of skeletal muscle atrophy in vitro using anti-ubiquitination oligopeptide carried by atelocollagen. Biochim Biophys Acta. 1853:873–880. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kazi AA, Hong-Brown L, Lang SM and Lang CH: Deptor knockdown enhances mTOR activity and protein synthesis in myocytes and ameliorates disuse muscle atrophy. Mol Med. 17:925–936. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zheng B, Ohkawa S, Li HY, Roberts-Wilson TK and Price SR: FOXO3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB J. 24:2660–2669. 2010. View Article : Google Scholar : PubMed/NCBI | |
You JS, Lincoln HC, Kim CR, Frey JW, Goodman CA, Zhong XP and Hornberger TA: The role of diacylglycerol kinase ζ and phosphatidic acid in the mechanical activation of mammalian target of rapamycin (mTOR) signaling and skeletal muscle hypertrophy. J Biol Chem. 289:1551–1563. 2014. View Article : Google Scholar : PubMed/NCBI | |
Moylan JS, Smith JD, Chambers MA, McLoughlin TJ and Reid MB: TNF induction of atrogin-1/MAFbx mRNA depends on Foxo4 expression but not AKT-Foxo1/3 signaling. Am J Physiol Cell Physiol. 295:C986–C993. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tisdale MJ: The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting. J Support Oncol. 3:209–217. 2005.PubMed/NCBI | |
Argiles JA, López-Soriano FJ and Busquets S: Apoptosis signalling is essential and precedes protein degradation in wasting skeletal muscle during catabolic conditions. Int J Biochem Cell Biol. 40:1674–1678. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wray CJ, Mammen JM, Hershko DD and Hasselgren PO: Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol. 35:698–705. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tong JF, Yan X, Zhu MJ and Du M: AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes. J Cell Biochem. 108:458–468. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hershko A and Ciechanover A: The ubiquitin system. Annu Rev Biochem. 67:425–479. 1998. View Article : Google Scholar : PubMed/NCBI | |
Argilés JM, López-Soriano FJ and Busquets S: Apoptosis signalling is essential and precedes protein degradation in wasting skeletal muscle during catabolic conditions. Int J Biochem Cell Biol. 40:1674–1678. 2008. View Article : Google Scholar : PubMed/NCBI | |
Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD and Glass DJ: The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell. 14:395–403. 2004. View Article : Google Scholar : PubMed/NCBI | |
Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH and Goldberg AL: Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 117:399–412. 2004. View Article : Google Scholar : PubMed/NCBI | |
Baviera AM, Zanon NM, Navegantes LC and Kettelhut IC: Involvement of cAMP/Epac/PI3K-dependent pathway in the antiproteolytic effect of epinephrine on rat skeletal muscle. Mol Cell Endocrinol. 315:104–112. 2010. View Article : Google Scholar : PubMed/NCBI | |
Sharp ZD and Bartke A: Evidence for down-regulation of phosphoinositide 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR)-dependent translation regulatory signaling pathways in Ames dwarf mice. J Gerontol A Biol Sci Med Sci. 60:293–300. 2005. View Article : Google Scholar : PubMed/NCBI | |
Goodman CA, Mayhew DL and Hornberger TA: Recent progress toward understanding the molecular mechanisms that regulate skeletal muscle mass. Cell Signal. 23:1896–1906. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kimura K, Cheng XW, Inoue A, Hu LN, Koike T and Kuzuya M: β-Hydroxy-β-methylbutyrate facilitates PI3K/Akt-dependent mammalian target of rapamycin and FoxO1/3a phosphorylations and alleviates tumor necrosis factor α/interferon γ-induced MuRF-1 expression in C2C12 cells. Nutr Res. 34:368–374. 2014. View Article : Google Scholar : PubMed/NCBI | |
Jia L, Li YF, Wu GF, Song ZY, Lu HZ, Song CC, Zhang QL, Zhu JY, Yang GS and Shi XE: MiRNA-199a-3p regulates C2C12 myoblast differentiation through IGF-1/AKT/ mTOR signal pathway. Int J Mol Sci. 15:296–308. 2013. View Article : Google Scholar : PubMed/NCBI | |
Risson V, Mazelin L, Roceri M, Sanchez H, Moncollin V, Corneloup C, Richard-Bulteau H, Vignaud A, Baas D, Defour A, et al: Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol. 187:859–874. 2009. View Article : Google Scholar : PubMed/NCBI | |
Sievenpiper JL, Arnason JT, Leiter LA and Vuksan V: Variable effects of American ginseng: A batch of American ginseng (Panax quinquefolius L.) with a depressed ginsenoside profile does not affect postprandial glycemia. Eur J Clin Nutr. 57:243–248. 2003. View Article : Google Scholar : PubMed/NCBI | |
Um JY, Chung HS, Kim MS, Na HJ, Kwon HJ, Kim JJ, Lee KM, Lee SJ, Lim JP, Do KR, et al: Molecular authentication of Panax ginseng species by RAPD analysis and PCR-RFLP. Biol Pharm Bull. 24:872–875. 2001. View Article : Google Scholar : PubMed/NCBI | |
Hou CW, Lee SD, Kao CL, Cheng IS, Lin YN, Chuang SJ, Chen CY, Ivy JL, Huang CY and Kuo CH: Improved inflammatory balance of human skeletal muscle during exercise after supplementations of the ginseng-based steroid Rg1. PLoS One. 10:e01163872015. View Article : Google Scholar : PubMed/NCBI | |
Yu SH, Huang HY, Korivi M, Hsu MF, Huang CY, Hou CW, Chen CY, Kao CL, Lee RP, Lee SD and Kuo CH: Oral Rg1 supplementation strengthens antioxidant defense system against exercise-induced oxidative stress in rat skeletal muscles. J Int Soc Sport Nutr. 9:232012. View Article : Google Scholar | |
Yang XD, Yang YY, Ouyang DS and Yang GP: A review of biotransformation and pharmacology of ginsenoside compound K. Fitoterapia. 100:208–220. 2015. View Article : Google Scholar : PubMed/NCBI | |
Liu QF, Deng ZY, Ye JM, He AL and Li SS: Ginsenoside Rg1 protects chronic cyclosporin a nephropathy from tubular cell apoptosis by inhibiting endoplasmic reticulum stress in rats. Transplant Proc. 47:pp. 566–569. 2015; View Article : Google Scholar : PubMed/NCBI | |
Kim WK, Song SY, Oh WK, Kaewsuwan S, Tran TL, Kim WS and Sung JH: Wound-healing effect of ginsenoside Rd from leaves of Panax ginseng via cyclic AMP-dependent protein kinase pathway. Eur J Pharmacol. 702:285–293. 2013. View Article : Google Scholar : PubMed/NCBI | |
Qi B, Liu L, Zhang H, Zhou GX, Wang S, Duan XZ, Bai XY, Wang SM and Zhao DQ: Anti-fatigue effects of proteins isolated from Panax quinquefolium. J Ethnopharmacol. 153:430–434. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhuang CL, Mao XY, Liu S, Chen WZ, Huang DD, Zhang CJ, Chen BC, Shen X and Yu Z: Ginsenoside Rb1 improves postoperative fatigue syndrome by reducing skeletal muscle oxidative stress through activation of the PI3K/Akt/Nrf2 pathway in aged rats. Eur J Pharmacol. 740:480–487. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wei HJ, Yang HH, Chen CH, Lin WW, Chen SC, Lai PH, Chang Y and Sung HW: Gelatin microspheres encapsulated with a nonpeptide angiogenic agent, ginsenoside Rg1, for intramyocardial injection in a rat model with infarcted myocardium. J Control Release. 120:27–34. 2007. View Article : Google Scholar : PubMed/NCBI | |
Sato S, Ogura Y and Kumar A: TWEAK/Fn14 signaling axis mediates skeletal muscle atrophy and metabolic dysfunction. Front Immunol. 5:182014. View Article : Google Scholar : PubMed/NCBI | |
Argilés JM, López-Soriano FJ and Busquets S: Apoptosis signalling is essential and precedes protein degradation in wasting skeletal muscle during catabolic conditions. Int J Biochem Cell Biol. 40:1674–1678. 2008. View Article : Google Scholar : PubMed/NCBI | |
Thomas MP, Mills J and Engelbrecht AM: Phosphatidylinositol-3-kinase (PI3K) activity decreases in C2C12 myotubes during acute simulated ischemia at a cost to their survival. Life Sci. 91:44–53. 2012. View Article : Google Scholar : PubMed/NCBI | |
Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA and Kandarian SC: Identification of a molecular signature of sarcopenia. Physiol Genomics. 21:253–263. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kandarian SC and Jackman RW: Intracellular signaling during skeletal muscle atrophy. Muscle Nerve. 33:155–165. 2006. View Article : Google Scholar : PubMed/NCBI | |
Schulze PC, Fang J, Kassik KA, Gannon J, Cupesi M, MacGillivray C, Lee RT and Rosenthal N: Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ Res. 97:418–426. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kim WK, Song SY, Oh WK, Kaewsuwan S, Tran TL, Kim WS and Sung JH: Wound-healing effect of ginsenoside Rd from leaves of Panax ginseng via cyclic AMP-dependent protein kinase pathway. Eur J Pharmacol. 702:285–293. 2013. View Article : Google Scholar : PubMed/NCBI | |
Attele AS, Wu JA and Yuan CS: Ginseng pharmacology: Multiple constituents and multiple actions. Biochem Pharmacol. 58:1685–1693. 1999. View Article : Google Scholar : PubMed/NCBI | |
Chen X: Cardiovascular protection by ginsenosides and their nitric oxide releasing action. Clin Exp Pharmacol Physiol. 23:728–732. 1996. View Article : Google Scholar : PubMed/NCBI | |
Gillis CN: Panax ginseng pharmacology: A nitric oxide link? Biochem Pharmacol. 54:1–8. 1997. View Article : Google Scholar : PubMed/NCBI | |
Nag SA, Qin JJ, Wang W, Wang MH, Wang H and Zhang R: Ginsenosides as anticancer agents: In vitro and in vivo activities, structure-activity relationships and molecular mechanisms of action. Front Pharmacol. 3:252012. View Article : Google Scholar : PubMed/NCBI | |
Xie JT, Mehendale S and Yuan CS: Ginseng and diabetes. Am J Chin Med. 33:397–404. 2005. View Article : Google Scholar : PubMed/NCBI | |
Hwang JT, Kim SH, Lee MS, Kim SH, Yang HJ, Kim MJ, Kim HS, Ha J, Kim MS and Kwon DY: Anti-obesity effects of ginsenoside Rh2 are associated with the activation of AMPK signaling pathway in 3T3-L1 adipocyte. Biochem Biophys Res Commun. 364:1002–1008. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cho WC, Chung WS, Lee SK, Leung AW, Cheng CH and Yue KK: Ginsenoside Re of Panax ginseng possesses significant antioxidant and antihyperlipidemic efficacies in streptozotocin-induced diabetic rats. Eur J Pharmacol. 550:173–179. 2006. View Article : Google Scholar : PubMed/NCBI | |
Shang W, Yang Y, Zhou L, Jiang B, Jin H and Chen M: Ginsenoside Rb1 stimulates glucose uptake through insulin-like signaling pathway in 3T3-L1 adipocytes. J Endocrinol. 198:561–569. 2008. View Article : Google Scholar : PubMed/NCBI | |
Song Z, Moser C, Wu H, Faber V, Kharazmi A and Høiby N: Cytokine modulating effect of ginseng treatment in a mouse model of Pseudomonas aeruginosa lung infection. J Cyst Fibros. 2:112–119. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lee E, Ko E, Lee J, Rho S, Ko S, Shin MK, Min BI, Hong MC, Kim SY and Bae H: Ginsenoside Rg1 enhances CD4(+) T-cell activities and modulates Th1/Th2 differentiation. Int Immunopharmacol. 4:235–244. 2004. View Article : Google Scholar : PubMed/NCBI | |
Foletta VC, White LJ, Larsen AE, Léger B and Russell AP: The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pflugers Arch. 461:325–335. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jagoe RT and Goldberg AL: What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care. 4:183–190. 2001. View Article : Google Scholar : PubMed/NCBI | |
Wray CJ, Mammen JM, Hershko DD and Hasselgren PO: Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol. 35:698–705. 2003. View Article : Google Scholar : PubMed/NCBI | |
Krawiec BJ, Nystrom GJ, Frost RA, Jefferson LS and Lang CH: AMP-activated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells. Am J Physiol Endocrinol Metab. 292:E1555–E1567. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, et al: Identification of ubiquitin ligases required for skeletal muscle atrophy. Science. 294:1704–1708. 2001. View Article : Google Scholar : PubMed/NCBI | |
Baehr LM, Furlow JD and Bodine SC: Muscle sparing in muscle RING finger 1 null mice: Response to synthetic glucocorticoids. J Physiol. 589:4759–4776. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cong H, Sun L, Liu C and Tien P: Inhibition of atrogin-1/MAFbx expression by adenovirus-delivered small hairpin RNAs attenuates muscle atrophy in fasting mice. Hum Gene Ther. 22:313–324. 2011. View Article : Google Scholar : PubMed/NCBI | |
Polge C, Heng AE, Jarzaguet M, Ventadour S, Claustre A, Combaret L, Béchet D, Matondo M, Uttenweiler-Joseph S, Monsarrat B, et al: Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1. FASEB J. 25:3790–3802. 2011. View Article : Google Scholar : PubMed/NCBI | |
Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E and Glass DJ: The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 6:376–385. 2007. View Article : Google Scholar : PubMed/NCBI | |
Fielitz J, Kim MS, Shelton JM, Latif S, Spencer JA, Glass DJ, Richardson JA, Bassel-Duby R and Olson EN: Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3. J Clin Invest. 117:2486–2495. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kedar V, McDonough H, Arya R, Li HH, Rockman HA and Patterson C: Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc Natl Acad Sci USA. 101:pp. 18135–18140. 2004; View Article : Google Scholar : PubMed/NCBI | |
Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E and Goldberg AL: During muscle atrophy, thick, but not thin, filaments components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol. 185:1083–1095. 2009. View Article : Google Scholar : PubMed/NCBI | |
Csibi A, Cornille K, Leibovitch MP, Poupon A, Tintignac LA, Sanchez AM and Leibovitch SA: The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS One. 5:e89942010. View Article : Google Scholar : PubMed/NCBI | |
Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP and Leibovitch SA: Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem. 280:2847–2856. 2005. View Article : Google Scholar : PubMed/NCBI | |
Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR and Mitch WE: Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest. 113:115–123. 2004. View Article : Google Scholar : PubMed/NCBI |