The effect of serum from calorie-restricted mouse on mTOR signaling in C2C12 myotubes

in Journal of Endocrinology
Authors:
Takanaga Shirai Institute of Health and Sport Sciences, University of Tsukuba, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan
Research Fellow of Japan Society for Promotion Science, Chiyoda-ku, Tokyo, Japan
Department of Human Sciences, Kanagawa University, Rokkakubashi, Kanagawa-ku, Yokohama-shi, Kanagawa, Japan

Search for other papers by Takanaga Shirai in
Current site
Google Scholar
PubMed Close
,
Tomohiro Iwata Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan

Search for other papers by Tomohiro Iwata in
Current site
Google Scholar
PubMed Close
,
Kazuki Uemichi Research Fellow of Japan Society for Promotion Science, Chiyoda-ku, Tokyo, Japan
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan

Search for other papers by Kazuki Uemichi in
Current site
Google Scholar
PubMed Close
,
Riku Tanimura Research Fellow of Japan Society for Promotion Science, Chiyoda-ku, Tokyo, Japan
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan

Search for other papers by Riku Tanimura in
Current site
Google Scholar
PubMed Close
,
Ryoto Iwai Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan

Search for other papers by Ryoto Iwai in
Current site
Google Scholar
PubMed Close
, and
Tohru Takemasa Institute of Health and Sport Sciences, University of Tsukuba, University of Tsukuba, Tennodai, Tsukuba, Ibaraki, Japan

Search for other papers by Tohru Takemasa in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0002-9591-2250

Correspondence should be addressed to T Takemasa: takemasa.tohru.gm@u.tsukuba.ac.jp
DOI:
https://doi.org/10.1530/JOE-23-0111
Volume/Issue:
Volume 259: Issue 2
Article Type:
Research Article
Article ID:
e230111
Online Publication Date:
27 Sep 2023
Copyright:
© the author(s) 2023
Restricted access
Rent on DeepDyve

Sign up for journal news

Graphical abstract

Abstract

Calorie restriction (CR) is a widely recognized dietary approach with beneficial impacts on the entire body, including enhancements in oxidative metabolism and life span extension, while maintaining nutritional balance and calorie intake. However, CR leads to reductions in skeletal muscle and fat mass due to decreased food intake. Consequently, CR significantly modifies the metabolic profile of the entire body and its tissues. The observed benefits in skeletal muscle during CR may be attributed to CR-induced signaling mediators or significant changes in blood profiles associated with CR that regulate homeostasis maintenance. This study aimed to examine the mammalian target of rapamycin signaling and mitochondrial function of skeletal muscle from mice that undergone 8 weeks of CR and cells cultured in their serum to determine whether changes in blood secreted factors during CR affect skeletal muscle cells. C57BL6/J male mice were used. For 8 weeks, these were subjected to ad libitum (AL) or 40% CR. C2C12 myotubes were subsequently treated with media containing 10% mouse serum from AL or CR for 24 h. The results indicated that 8 weeks of CR decreased muscle mass and protein synthesis response compared with the AL group. Interestingly, myotubes conditioned with CR serum exhibited an elevation in the protein synthesis response compared with those treated with AL serum. Furthermore, mitochondrial function was enhanced in both CR mice and cells treated with CR serum. These findings suggest that while CR decreases the protein synthesis response, secretory factors present in the blood during CR can activate protein synthesis and promote mitochondrial function.

Journal of Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 172 143 3
PDF Downloads 160 126 1

 

  • Collapse
  • Expand
Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© the author(s) 2023
Article ID:
e230111
Article Type:
Research Article
Received Date:
04 Apr 2023
Accepted Date:
22 Aug 2023
Print Publication Date:
01 Nov 2023
Online Publication Date:
27 Sep 2023
Keywords:
calorie restriction; mitochondria biogenesis and dynamics; mTOR signaling; oxidative metabolism; skeletal muscle

  • Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, et al.2001 Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nature Cell Biology 3 1014–1019. (https://doi.org/10.1038/ncb1101-1014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Buschemeyer WC 3rd, Klink JC, Mavropoulos JC, Poulton SH, Demark-Wahnefried W, Hursting SD, Cohen P, Hwang D, Johnson TL & & Freedland SJ 2010 Effect of intermittent fasting with or without caloric restriction on prostate cancer growth and survival in SCID mice. Prostate 70 1037–1043. (https://doi.org/10.1002/pros.21136)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cantó C & & Auwerx J 2011 Calorie restriction: is AMPK a key sensor and effector? Physiology (Bethesda) 26 214–224. (https://doi.org/10.1152/physiol.00010.2011)

  • Carson BP, Patel B, Amigo-Benavent M, Pauk M, Kumar Gujulla S, Murphy SM, Kiely PA & & Jakeman PM 2018 Regulation of muscle protein synthesis in an in vitro cell model using ex vivo human serum. Experimental Physiology 103 783–789. (https://doi.org/10.1113/EP086860)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cerqueira FM, Brandizzi LI, Cunha FM, Laurindo FR & & Kowaltowski AJ 2012 Serum from calorie-restricted rats activates vascular cell eNOS through enhanced insulin signaling mediated by adiponectin. PLoS One 7 e31155. (https://doi.org/10.1371/journal.pone.0031155)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chung HY, Kim HJ, Kim KW, Choi JS & & Yu BP 2002 Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microscopy Research and Technique 59 264–272. (https://doi.org/10.1002/jemt.10203)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E & CALERIE Pennington Team 2007 Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLOS Medicine 4 e76. (https://doi.org/10.1371/journal.pmed.0040076)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, et al.2009 Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325 201–204. (https://doi.org/10.1126/science.1173635)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Corrick KL, Stec MJ, Merritt EK, Windham ST, Thomas SJ, Cross JM & & Bamman MM 2015 Serum from human burn victims impairs myogenesis and protein synthesis in primary myoblasts. Frontiers in Physiology 6 184. (https://doi.org/10.3389/fphys.2015.00184)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cui M, Yu H, Wang J, Gao J & & Li J 2013 Chronic caloric restriction and exercise improve metabolic conditions of dietary-induced obese mice in autophagy correlated manner without involving AMPK. Journal of Diabetes Research 2013 852754. (https://doi.org/10.1155/2013/852754)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Finley LW, Lee J, Souza A, Desquiret-Dumas V, Bullock K, Rowe GC, Procaccio V, Clish CB, Arany Z & & Haigis MC 2012 Skeletal muscle transcriptional coactivator PGC-1α mediates mitochondrial, but not metabolic, changes during calorie restriction. Proceedings of the National Academy of Sciences of the United States of America 109 2931–2936. (https://doi.org/10.1073/pnas.1115813109)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fontana L, Partridge L & & Longo VD 2010 Extending healthy life span--from yeast to humans. Science 328 321–326. (https://doi.org/10.1126/science.1172539)

  • Hernández-Camacho JD, Fernández-Ayala DJM, Vicente-García C, Navas-Enamorado I, López-Lluch G, Oliva C, Artuch R, Garcia-Villoria J, Ribes A, de Cabo R, et al.2022 Calorie restriction rescues mitochondrial dysfunction in Adck2-deficient skeletal muscle. Frontiers in Physiology 13 898792. (https://doi.org/10.3389/fphys.2022.898792)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Horrillo D, Sierra J, Arribas C, García-San Frutos M, Carrascosa JM, Lauzurica N, Fernández-Agulló T & & Ros M 2011 Age-associated development of inflammation in Wistar rats: effects of caloric restriction. Archives of Physiology and Biochemistry 117 140–150. (https://doi.org/10.3109/13813455.2011.577435)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ikeno Y, Lew CM, Cortez LA, Webb CR, Lee S & & Hubbard GB 2006 Do long-lived mutant and calorie-restricted mice share common anti-aging mechanisms?--a pathological point of view. Age (Dordr) 28 163–171. (https://doi.org/10.1007/s11357-006-9007-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jia WH, Wang NQ, Yin L, Chen X, Hou BY, Qiang GF, Chan CB, Yang XY & & Du GH 2019 Effect of skeletal muscle phenotype and gender on fasting-induced myokine expression in mice. Biochemical and Biophysical Research Communications 514 407–414. (https://doi.org/10.1016/j.bbrc.2019.04.155)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Katsimpardi L, Kuperwasser N, Camus C, Moigneu C, Chiche A, Tolle V, Li H, Kokovay E & & Lledo PM 2020 Systemic GDF11 stimulates the secretion of adiponectin and induces a calorie restriction-like phenotype in aged mice. Aging Cell 19 e13038. (https://doi.org/10.1111/acel.13038)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kitada M, Kume S, Takeda-Watanabe A, Tsuda S, Kanasaki K & & Koya D 2013 Calorie restriction in overweight males ameliorates obesity-related metabolic alterations and cellular adaptations through anti-aging effects, possibly including AMPK and SIRT1 activation. Biochimica et Biophysica Acta 1830 4820–4827. (https://doi.org/10.1016/j.bbagen.2013.06.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kitaoka Y, Nakazato K & & Ogasawara R 2016 Combined effects of resistance training and calorie restriction on mitochondrial fusion and fission proteins in rat skeletal muscle. Journal of Applied Physiology 121 806–810. (https://doi.org/10.1152/japplphysiol.00465.2016)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee C & & Longo V 2016 Dietary restriction with and without caloric restriction for healthy aging. F1000Research 5. (https://doi.org/10.12688/f1000research.7136.1)

  • López-Lluch G & & Navas P 2016 Calorie restriction as an intervention in ageing. Journal of Physiology 594 2043–2060. (https://doi.org/10.1113/JP270543)

  • Margolis LM, Rivas DA, Berrone M, Ezzyat Y, Young AJ, McClung JP, Fielding RA & & Pasiakos SM 2016 Prolonged calorie restriction downregulates skeletal muscle mTORC1 signaling independent of dietary protein intake and associated microRNA expression. Frontiers in Physiology 7 445. (https://doi.org/10.3389/fphys.2016.00445)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miller BF, Robinson MM, Reuland DJ, Drake JC, Peelor FF 3rd, Bruss MD, Hellerstein MK & & Hamilton KL 2013 Calorie restriction does not increase short-term or long-term protein synthesis. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 68 530–538. (https://doi.org/10.1093/gerona/gls219)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miyazaki M & & Esser KA 2009 Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. Journal of Applied Physiology 106 1367–1373. (https://doi.org/10.1152/japplphysiol.91355.2008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miyazaki M, Shimozuru M & & Tsubota T 2022 Supplementing cultured human myotubes with hibernating bear serum results in increased protein content by modulating Akt/FOXO3a signaling. PLoS One 17 e0263085. (https://doi.org/10.1371/journal.pone.0263085)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals 2011 The National Academies collection: reports funded by National Institutes of Health. In Guide for the Care and Use of Laboratory Animals, vol 8. Washington , DC, USA: National Academies Press. (https://doi.org/10.17226/12910)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, et al.2005 Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310 314–317. (https://doi.org/10.1126/science.1117728)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ristow M 2014 Unraveling the truth about antioxidants: mitohormesis explains ROS-induced health benefits. Nature Medicine 20 709–711. (https://doi.org/10.1038/nm.3624)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shirai T, Uemichi K, Hidaka Y, Kitaoka Y & & Takemasa T 2021 Effect of lactate administration on mouse skeletal muscle under calorie restriction. Current Research in Physiology 4 202–208. (https://doi.org/10.1016/j.crphys.2021.09.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sipe LM, Yang C, Ephrem J, Garren E, Hirsh J & & Deppmann CD 2017 Differential sympathetic outflow to adipose depots is required for visceral fat loss in response to calorie restriction. Nutrition and Diabetes 7 e260. (https://doi.org/10.1038/nutd.2017.13)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takeda K, Kitaoka Y, Watanabe K, Miyakawa S, Lindley MR & & Takemasa T 2018 Effects of eicosapentaenoic acid intake on denervation-induced mitochondrial adaptation in mouse skeletal muscle. Journal of Physical Fitness and Sports Medicine 7 261–267. (https://doi.org/10.7600/jpfsm.7.261)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tanimura R, Kobayashi L, Shirai T & & Takemasa T 2022 Effects of exercise intensity on white adipose tissue browning and its regulatory signals in mice. Physiological Reports 10 e15205. (https://doi.org/10.14814/phy2.15205)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Uemichi K, Shirai T, Matsuno R, Iwata T, Tanimura R & & Takemasa T 2023 The role of the mechanistic target of rapamycin complex 1 in the regulation of mitochondrial adaptation during skeletal muscle atrophy under denervation or calorie restriction in mice. Applied Physiology, Nutrition and Metabolism 48 241–255. (https://doi.org/10.1139/apnm-2022-0336)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walford RL, Mock D, Verdery R & & MacCallum T 2002 Calorie restriction in biosphere 2: alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 57 B211–B224. (https://doi.org/10.1093/gerona/57.6.b211)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Weindruch R & & Sohal RS 1997 Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. New England Journal of Medicine 337 986–994. (https://doi.org/10.1056/NEJM199710023371407)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Weiss EP, Albert SG, Reeds DN, Kress KS, Ezekiel UR, McDaniel JL, Patterson BW, Klein S & & Villareal DT 2015 Calorie restriction and matched weight loss from exercise: independent and additive effects on glucoregulation and the incretin system in overweight women and men. Diabetes Care 38 1253–1262. (https://doi.org/10.2337/dc14-2913)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu BP, Masoro EJ & & McMahan CA 1985 Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. Journal of Gerontology 40 657–670. (https://doi.org/10.1093/geronj/40.6.657)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhu J, Liu C, Jia J, Zhang C, Yuan W, Leng H, Xu Y & & Song C 2020 Short-term caloric restriction induced bone loss in both axial and appendicular bones by increasing adiponectin. Annals of the New York Academy of Sciences 1474 47–60. (https://doi.org/10.1111/nyas.14380)

    • PubMed
    • Search Google Scholar
    • Export Citation