Journal of Zhejiang University-SCIENCE B

, Volume 19, Issue 11, pp 844–852 | Cite as

Effect of a combination of astaxanthin supplementation, heat stress, and intermittent reloading on satellite cells during disuse muscle atrophy

  • Toshinori YoshiharaEmail author
  • Takao Sugiura
  • Nobuyuki Miyaji
  • Yuki Yamamoto
  • Tsubasa Shibaguchi
  • Ryo Kakigi
  • Hisashi Naito
  • Katsumasa Goto
  • Daijiro Ohmori
  • Toshitada Yoshioka


We examined the effect of a combination of astaxanthin (AX) supplementation, repeated heat stress, and intermittent reloading (IR) on satellite cells in unloaded rat soleus muscles. Forty-nine male Wistar rats (8-week-old) were divided into control, hind-limb unweighting (HU), IR during HU, IR with AX supplementation, IR with repeated heat stress (41.0–41.5 °C for 30 min), and IR with AX supplementation and repeated heat stress groups. After the experimental period, the antigravitational soleus muscle was analyzed using an immunohistochemical technique. Our results revealed that the combination of dietary AX supplementation and heat stress resulted in protection against disuse muscle atrophy in the soleus muscle. This protective effect may be partially due to a higher satellite cell number in the atrophied soleus muscle in the IR/AX/heat stress group compared with the numbers found in the other groups. We concluded that the combination treatment with dietary AX supplementation and repeated heat stress attenuates soleus muscle atrophy, in part by increasing the number of satellite cells.

Key words

Antioxidant astaxanthin Disuse muscle atrophy Heat stress Satellite cell 




探讨透过虾青素摄入、热应激和间歇式再负荷的不同处理方式及其联合处理, 对于尾部悬吊后大鼠比目鱼肌卫星细胞的影响。


利用虾青素摄入、热应激与间歇式再负荷的不同方式, 探讨预防大鼠比目鱼肌废用性肌萎缩的有效处理。


将49只雄性Wistar大鼠分成对照组、吊尾组、间歇式再负荷组、虾青素摄入组、热应激组和虾青素摄入+热应激组。摘取7天尾部悬吊后的大鼠的比目鱼肌, 使用免疫组织化学技术, 分析肌卫星细胞的激活程度。


虾青素摄入、热应激与间歇式再负荷的不同方式的联合处理能减少比目鱼肌废用性肌萎缩, 其部分效果可能是由于肌卫星细胞数量的增加所致。


虾青素 废用性肌萎缩 热应激 肌卫星细胞 

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  1. Arentson-Lantz EJ, English KL, Paddon-Jones D, et al., 2016. Fourteen days of bed rest induces a decline in satellite cell content and robust atrophy of skeletal muscle fibers in middle-aged adults. J Appl Physiol, 120(8):965–975. Scholar
  2. Brooks NE, Myburgh KH, 2014. Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways. Front Physiol, 5:99. Scholar
  3. Brooks NE, Cadena SM, Vannier E, et al., 2010. Effects of resistance exercise combined with essential amino acid supplementation and energy deficit on markers of skeletal muscle atrophy and regeneration during bed rest and active recovery. Muscle Nerve, 42(6):927–935. Scholar
  4. Dose J, Matsugo S, Yokokawa H, et al., 2016. Free radical scavenging and cellular antioxidant properties of astaxanthin. Int J Mol Sci, 17(1):103. Scholar
  5. Dumont NA, Bentzinger CF, Sincennes MC, et al., 2015. Satellite cells and skeletal muscle regeneration. Compr Physiol, 5(3):1027–1059. Scholar
  6. Egner IM, Bruusgaard JC, Gundersen K, 2016. Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development, 143(16):2898–2906. Scholar
  7. Fulle S, Di Donna S, Puglielli C, et al., 2005. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol, 40(3):189–197. Scholar
  8. Gao CQ, Zhao YL, Li HC, et al., 2015. Heat stress inhibits proliferation, promotes growth, and induces apoptosis in cultured lantang swine skeletal muscle satellite cells. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 16(6):549–559. Scholar
  9. Ikeda Y, Tsuji S, Satoh A, et al., 2008. Protective effects of astaxanthin on 6-hydroxydopamine-induced apoptosis in human neuroblastoma SH-SY5Y cells. J Neurochem, 107(6):1730–1740. Scholar
  10. Kojima A, Goto K, Morioka S, et al., 2007. Heat stress facilitates the regeneration of injured skeletal muscle in rats. J Orthop Sci, 12(1):74–82. Scholar
  11. le Grand F, Rudnicki MA, 2007. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol, 19(6):628–633. Scholar
  12. Matsuba Y, Goto K, Morioka S, et al., 2009. Gravitational unloading inhibits the regenerative potential of atrophied soleus muscle in mice. Acta Physiol, 196(3):329–339. Scholar
  13. Naito H, Powers SK, Demirel HA, et al., 2000. Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats. J Appl Physiol, 88(1):359–363. Scholar
  14. Oishi Y, Hayashida M, Tsukiashi S, et al., 2009. Heat stress increases myonuclear number and fiber size via satellite cell activation in rat regenerating soleus fibers. J Appl Physiol, 107(5):1612–1621. Scholar
  15. Powers SK, 2014. Can antioxidants protect against disuse muscle atrophy? Sports Med, 44(S2):155–165. Scholar
  16. Powers SK, Kavazis AN, McClung JM, 2007. Oxidative stress and disuse muscle atrophy. J Appl Physiol, 102(6):2389–2397. Scholar
  17. Renault V, Thornell LE, Butler-Browne G, et al., 2002. Human skeletal muscle satellite cells: aging, oxidative stress and the mitotic clock. Exp Gerontol, 37(10–11): 1229–1236. Scholar
  18. Schiaffino S, Dyar KA, Ciciliot S, et al., 2013. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J, 280(17):4294–4314. Scholar
  19. Schultz E, Darr KC, Macius A, 1994. Acute effects of hindlimb unweighting on satellite cells of growing skeletal muscle. J Appl Physiol, 76(1):266–270. Scholar
  20. Selsby JT, Dodd SL, 2005. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol, 289(1): R134–R139. Scholar
  21. Shefer G, van de Mark DP, Richardson JB, et al., 2006. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol, 294(1):50–66. Scholar
  22. Snijders T, Wall BT, Dirks ML, et al., 2014. Muscle disuse atrophy is not accompanied by changes in skeletal muscle satellite cell content. Clin Sci (Lond), 126(8):557–566. Scholar
  23. Sugiura T, Abe N, Nagano M, et al., 2005. Changes in PKB/Akt and calcineurin signaling during recovery in atrophied soleus muscle induced by unloading. Am J Physiol, 288(5): R1273–R1278. Scholar
  24. Uehara K, Goto K, Kobayashi T, et al., 2004. Heat-stress enhances proliferative potential in rat soleus muscle. Jpn J Physiol, 54(3):263–271. Scholar
  25. Yoshihara T, Sugiura T, Yamamoto Y, et al., 2015. The response of apoptotic and proteolytic systems to repeated heat stress in atrophied rat skeletal muscle. Physiol Rep, 3(10):e12597. Scholar
  26. Yoshihara T, Yamamoto Y, Shibaguchi T, et al., 2017. Dietary astaxanthin supplementation attenuates disuse-induced muscle atrophy and myonuclear apoptosis in the rat soleus muscle. J Physiol Sci, 67(1):181–190. Scholar

Copyright information

© Zhejiang University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Toshinori Yoshihara
    • 1
    Email author
  • Takao Sugiura
    • 2
  • Nobuyuki Miyaji
    • 3
  • Yuki Yamamoto
    • 4
  • Tsubasa Shibaguchi
    • 5
  • Ryo Kakigi
    • 6
  • Hisashi Naito
    • 1
  • Katsumasa Goto
    • 7
  • Daijiro Ohmori
    • 8
  • Toshitada Yoshioka
    • 9
  1. 1.Graduate School of Health and Sports ScienceJuntendo UniversityInzai, ChibaJapan
  2. 2.Faculty of EducationYamaguchi UniversityYamaguchi, YamaguchiJapan
  3. 3.Toyo Koso Kagaku Co. Ltd.Urayasu, ChibaJapan
  4. 4.Institute of Health and Sports ScienceKurume UniversityKurume, FukuokaJapan
  5. 5.Institute of Liberal Arts and ScienceKanazawa UniversityKanazawa, IshikawaJapan
  6. 6.Faculty of MedicineJuntendo UniversityBunkyo-ku, TokyoJapan
  7. 7.Graduate School of Health SciencesToyohashi SOZO UniversityToyohashi, AichiJapan
  8. 8.Department of Chemistry, School of MedicineJuntendo UniversityInzai, ChibaJapan
  9. 9.Hirosaki Gakuin UniversityHirosaki, AomoriJapan

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