Skip to main content Accessibility help
×
Home

The preventive effect of β-carotene on denervation-induced soleus muscle atrophy in mice

  • Masahiro Ogawa (a1), Yoshihiro Kariya (a1), Tomoya Kitakaze (a1), Ryoichi Yamaji (a1), Naoki Harada (a1), Tatsuji Sakamoto (a1), Keisuke Hosotani (a2), Yoshihisa Nakano (a3) and Hiroshi Inui (a1)...

Abstract

Muscle atrophy increases the production of reactive oxygen species and the expression of atrophy-related genes, which are involved in the ubiquitin–proteasome system. In the present study, we investigated the effects of β-carotene on oxidative stress (100 μm-H2O2)-induced muscle atrophy in murine C2C12 myotubes. β-Carotene (10 μm) restored the H2O2-induced decreased levels of myosin heavy chain and tropomyosin (P< 0·05, n 3) and decreased the H2O2-induced increased levels of ubiquitin conjugates. β-Carotene reduced the H2O2-induced increased expression levels of E3 ubiquitin ligases (Atrogin-1 and MuRF1) and deubiquitinating enzymes (USP14 and USP19) (P< 0·05, n 3) and attenuated the H2O2-induced nuclear localisation of FOXO3a. Furthermore, we determined the effects of β-carotene on denervation-induced muscle atrophy. Male ddY mice (8 weeks old, n 30) were divided into two groups and orally pre-administered micelle with or without β-carotene (0·5 mg once daily) for 2 weeks, followed by denervation in the right hindlimb. β-Carotene was further administered once daily until the end of the experiment. At day 3 after denervation, the ratio of soleus muscle mass in the denervated leg to that in the sham leg was significantly higher in β-carotene-administered mice than in control vehicle-administered ones (P< 0·05, n 5). In the denervated soleus muscle, β-carotene administration significantly decreased the expression levels of Atrogin-1, MuRF1, USP14 and USP19 (P< 0·05, n 5) and the levels of ubiquitin conjugates. These results indicate that β-carotene attenuates soleus muscle loss, perhaps by repressing the expressions of Atrogin-1, MuRF1, USP14 and USP19, at the early stage of soleus muscle atrophy.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      The preventive effect of β-carotene on denervation-induced soleus muscle atrophy in mice
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      The preventive effect of β-carotene on denervation-induced soleus muscle atrophy in mice
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      The preventive effect of β-carotene on denervation-induced soleus muscle atrophy in mice
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Professor R. Yamaji, fax +81 72 254 9921, email yamaji@biochem.osakafu-u.ac.jp

References

Hide All
1Powers, SK, Kavazis, AN & McClung, JM (2007) Oxidative stress and disuse muscle atrophy. J Appl Physiol 102, 23892397.
2Furuno, K, Goodman, MN & Goldberg, AL (1990) Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265, 88508857.
3Lawler, JM, Song, W & Demaree, SR (2003) Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35, 916.
4Servais, S, Letexier, D, Favier, R, et al. (2007) Prevention of unloading-induced atrophy by vitamin E supplementation: links between oxidative stress and soleus muscle proteolysis? Free Radic Biol Med 42, 627635.
5Mukai, R, Nakao, R, Yamamoto, H, et al. (2010) Quercetin prevents unloading-derived disused muscle atrophy by attenuating the induction of ubiquitin ligases in tail-suspension mice. J Nat Prod 73, 17081710.
6Bodine, SC, Latres, E, Baumhueter, S, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 17041708.
7Okamoto, T, Torii, S & Machida, S (2011) Differential gene expression of muscle-specific ubiquitin ligase MAFbx/Atrogin-1 and MuRF1 in response to immobilization-induced atrophy of slow-twitch and fast-twitch muscles. J Physiol Sci 61, 537546.
8Sacheck, JM, Hyatt, JP, Raffaello, A, et al. (2007) Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21, 140155.
9Jagoe, RT, Lecker, SH, Gomes, M, et al. (2002) Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 16, 16971712.
10Sandri, M, Sandri, C, Gilbert, A, et al. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399412.
11Li, YP, Lecker, SH, Chen, Y, et al. (2003) TNF-alpha increases ubiquitin-conjugating activity in skeletal muscle by up-regulating UbcH2/E220k. FASEB J 17, 10481057.
12Brunet, A, Sweeney, LB, Sturgill, JF, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 20112015.
13Clavel, S, Siffroi-Fernandez, S, Coldefy, AS, 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, 470480.
14Komander, D, Clague, MJ & Urbé, S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10, 550563.
15Lecker, SH, Jagoe, RT, Gilbert, A, et al. (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18, 3951.
16Combaret, L, Adegoke, OA, Bedard, N, et al. (2005) USP19 is a ubiquitin-specific protease regulated in rat skeletal muscle during catabolic states. Am J Physiol Endocrinol Metab 288, E693E700.
17Sundaram, P, Pang, Z, Miao, M, et al. (2009) USP19-deubiquitinating enzyme regulates levels of major myofibrillar proteins in L6 muscle cells. Am J Physiol Endocrinol Metab 297, E1283E1290.
18Sies, H & Stahl, W (1995) Vitamins E and C, β-carotene, and other carotenoids as antioxidants. Am J Clin Nutr 62, 1315S1321S.
19Paiva, SA & Russell, RM (1999) β-Carotene and other carotenoids as antioxidants. J Am Coll Nutr 18, 426433.
20Kameji, H, Mochizuki, K, Miyoshi, N, et al. (2010) β-Carotene accumulation in 3T3-L1 adipocytes inhibits the elevation of reactive oxygen species and the suppression of genes related to insulin sensitivity induced by tumor necrosis factor-α. Nutrition 26, 11511156.
21Palozza, P, Serini, S, Di Nicuolo, F, et al. (2003) Prooxidant effects of beta-carotene in cultured cells. Mol Aspects Med 24, 353362.
22Kim, Y, Seo, JH & Kim, H (2011) β-Carotene and lutein inhibit hydrogen peroxide-induced activation of NF-κB and IL-8 expression in gastric epithelial AGS cells. J Nutr Sci Vitaminol (Tokyo) 57, 216223.
23Hashimoto, T, Ozaki, Y, Taminato, M, et al. (2009) The distribution and accumulation of fucoxanthin and its metabolites after oral administration in mice. Br J Nutr 102, 242248.
24Ogawa, M, Yamaji, R, Higashimura, Y, et al. (2011) 17β-Estradiol represses myogenic differentiation by increasing ubiquitin-specific peptidase 19 through estrogen receptor α. J Biol Chem 286, 4145541465.
25Yamaji, R, Fujita, K, Takahashi, S, et al. (2003) Hypoxia up-regulates glyceraldehyde-3-phosphate dehydrogenase in mouse brain capillary endothelial cells: involvement of Na+/Ca2+ exchanger. Biochim Biophys Acta 1593, 269276.
26Yamaji, R, Chatani, E, Harada, N, et al. (2005) Glyceraldehyde-3-phosphate dehydrogenase in the extracellular space inhibits cell spreading. Biochim Biophys Acta 1726, 261271.
27Ohkawa, H, Ohishi, N & Yagi, K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95, 351358.
28Muller, FL, Song, W, Jang, YC, et al. (2007) Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am J Physiol Regul Integr Comp Physiol 293, R1159R1168.
29Dehority, W, Halloran, BP, Bikle, DD, et al. (1999) Bone and hormonal changes induced by skeletal unloading in the mature male rat. Am J Physiol 276, E62E69.
30Brocca, L, Pellegrino, MA, Desaphy, JF, et al. (2010) Is oxidative stress a cause or consequence of disuse muscle atrophy in mice? A proteomic approach in hindlimb-unloaded mice. Exp Physiol 95, 331350.
31Miller, NJ, Sampson, J, Candeias, LP, et al. (1996) Antioxidant activities of carotenes and xanthophylls. FEBS Lett 384, 240242.
32Appell, HJ, Duarte, JA & Soares, JM (1997) Supplementation of vitamin E may attenuate skeletal muscle immobilization atrophy. Int J Sports Med 18, 157160.
33Kondo, H, Miura, M, Nakagaki, I, et al. (1992) Trace element movement and oxidative stress in skeletal muscle atrophied by immobilization. Am J Physiol 262, E583E590.
34Peus, D, Vasa, RA, Beyerle, A, et al. (1999) UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J Invest Dermatol 112, 751756.
35Gaitanaki, C, Papatriantafyllou, M, Stathopoulou, K, et al. (2006) Effects of various oxidants and antioxidants on the p38-MAPK signalling pathway in the perfused amphibian heart. Mol Cell Biochem 291, 107117.
36Dimitrov, NV, Meyer, C, Ullrey, DE, et al. (1988) Bioavailability of beta-carotene in humans. Am J Clin Nutr 48, 298304.
37Albanes, D & Heinonen, (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med 330, 10291035.
38Mech-Nowak, A, Swiderski, A, Kruczek, M, et al. (2012) Content of carotenoids in roots of seventeen cultivars of Daucus carota L. Acta Biochim Pol 59, 139141.
39Surles, RL, Weng, N, Simon, PW, et al. (2004) Carotenoid profiles and consumer sensory evaluation of specialty carrots (Daucus carota L.) of various colors. J Agric Food Chem 52, 34173421.
40Moon, RC & Constantinou, AI (1997) Dietary retinoids and carotenoids in rodent models of mammary tumorigenesis. Breast Cancer Res Treat 46, 181189.
41Marisiddaiah, R & Baskaran, V (2009) Bioefficacy of beta-carotene is improved in rats after solubilized as equimolar dose of beta-carotene and lutein in phospholipid-mixed micelles. Nutr Res 29, 588595.
42Hollander, D & Ruble, PE Jr (1978) Beta-carotene intestinal absorption: bile, fatty acid, pH, and flow rate effects on transport. Am J Physiol 235, E686E691.

Keywords

The preventive effect of β-carotene on denervation-induced soleus muscle atrophy in mice

  • Masahiro Ogawa (a1), Yoshihiro Kariya (a1), Tomoya Kitakaze (a1), Ryoichi Yamaji (a1), Naoki Harada (a1), Tatsuji Sakamoto (a1), Keisuke Hosotani (a2), Yoshihisa Nakano (a3) and Hiroshi Inui (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed