Vitamin D deficiency contributes to overtraining syndrome in excessive trained C57BL/6 mice.

calcitriol muscle strength overtraining protein synthesis rate

Journal

Scandinavian journal of medicine & science in sports
ISSN: 1600-0838
Titre abrégé: Scand J Med Sci Sports
Pays: Denmark
ID NLM: 9111504

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 30 06 2023
received: 15 12 2022
accepted: 04 07 2023
pubmed: 15 7 2023
medline: 15 7 2023
entrez: 15 7 2023
Statut: ppublish

Résumé

Overtraining syndrome is a condition resulting from excessive training load associated with inadequate recovery and poor sleep quality, leading to performance decrements and fatigue. Here we hypothesized that vitamin D (VitD) deficiency is a lead factor in the development of the overtraining syndrome. To test this hypothesis, two groups of 60-week-old C57BL/6 mice followed a 16-week excessive eccentric-based overtraining by excessive downhill running with or without dietary VitD depletion (EX and EX-D

Identifiants

pubmed: 37452567
doi: 10.1111/sms.14449
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2149-2165

Informations de copyright

© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Souberbielle JC, Massart C, Brailly-Tabard S, Cavalier E, Chanson P. Prevalence and determinants of vitamin D deficiency in healthy French adults: the VARIETE study. Endocrine. 2016;53:543-550.
de la Puente YM, Collado Yurrita L, Ciudad Cabañas MJ, Cuadrado Cenzual MA. Role of vitamin D in athletes and their performance: current concepts and new trends. Nutrients. 2020;12:E579.
Close GL, Russell J, Cobley JN, et al. Assessment of vitamin D concentration in non-supplemented professional athletes and healthy adults during the winter months in the UK: implications for skeletal muscle function. J Sports Sci. 2013;31:344-353.
Koundourakis NE, Avgoustinaki PD, Malliaraki N, Margioris AN. Muscular effects of vitamin D in young athletes and non-athletes and in the elderly. Hormones (Athens). 2016;15:471-488.
Barker T, Schneider ED, Dixon BM, Henriksen VT, Weaver LK. Supplemental vitamin D enhances the recovery in peak isometric force shortly after intense exercise. Nutr Metab (Lond). 2013;10:69.
Wyon MA, Koutedakis Y, Wolman R, Nevill AM, Allen N. The influence of winter vitamin D supplementation on muscle function and injury occurrence in elite ballet dancers: a controlled study. J Sci Med Sport. 2014;17:8-12.
Ceglia L, Niramitmahapanya S, da Silva MM, et al. A randomized study on the effect of vitamin D₃ supplementation on skeletal muscle morphology and vitamin D receptor concentration in older women. J Clin Endocrinol Metab. 2013;98:E1927-E1935.
Tanaka M, Kishimoto KN, Okuno H, Saito H, Itoi E. Vitamin D receptor gene silencing effects on differentiation of myogenic cell lines. Muscle Nerve. 2014;49:700-708.
Salles J, Chanet A, Giraudet C, et al. 1,25(OH)2-vitamin D3 enhances the stimulating effect of leucine and insulin on protein synthesis rate through Akt/PKB and mTOR mediated pathways in murine C2C12 skeletal myotubes. Mol Nutr Food Res. 2013;57:2137-2146.
Ruohola JP, Laaksi I, Ylikomi T, et al. Association between serum 25(OH)D concentrations and bone stress fractures in Finnish young men. J Bone Miner Res. 2006;21:1483-1488.
Meeusen R, Duclos M, Foster C, et al. European College of Sport Science, American College of Sports Medicine. Prevention, diagnosis, and treatment of the overtraining syndrome: joint consensus statement of the European College of Sport Science and the American College of Sports Medicine. Med Sci Sports Exerc. 2013;45:186-205.
Kreher JB, Schwartz JB. Overtraining syndrome: a practical guide. Sports Health. 2012;4:128-138.
Rietjens GJWM, Kuipers H, Adam JJ, et al. Physiological, biochemical and psychological markers of strenuous training-induced fatigue. Int J Sports Med. 2005;26:16-26.
Schwellnus M, Soligard T, Alonso JM, et al. How much is too much? (part 2) International Olympic Committee consensus statement on load in sport and risk of illness. Br J Sports Med. 2016;50:1043-1052.
Holick MF, Vitamin D. Deficiency. N Engl J Med. 2007;357:266-281.
Pereira BC, da Rocha AL, Pinto AP, et al. Excessive eccentric exercise-induced overtraining model leads to endoplasmic reticulum stress in mice skeletal muscles. Life Sci. 2016;145:144-151.
Pereira BC, da Rocha AL, Pauli JR, et al. Excessive eccentric exercise leads to transitory hypothalamic inflammation, which may contribute to the low body weight gain and food intake in overtrained mice. Neuroscience. 2015;311:231-242.
Hoppeler H. Moderate load eccentric exercise; a distinct novel training modality. Front Physiol. 2016;7:483.
Choi SJ, Lim JY, Nibaldi EG, et al. Eccentric contraction-induced injury to type I, IIa, and IIa/IIx muscle fibers of elderly adults. Age (Dordr). 2012;34:215-226.
Çakir-Atabek H, Dokumaci B, Aygün C. Strength loss after eccentric exercise is related to oxidative stress but not muscle damage biomarkers. Res Q Exerc Sport. 2019;90:385-394.
Smith LL. Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress? Med Sci Sports Exerc. 2000;32:317-331.
Smith LL. TISSUE TRAUMA: The Underlying Cause of Overtraining Syndrome? 9.
da Rocha AL, Pinto AP, Kohama EB, et al. The proinflammatory effects of chronic excessive exercise. Cytokine. 2019;119:57-61.
Pereira BC, Pauli JR, de Souza CT, et al. Nonfunctional overreaching leads to inflammation and myostatin upregulation in swiss mice. Int J Sports Med. 2014;35:139-146.
Ayachi M, Niel R, Momken I, Billat VL, Mille-Hamard L. Validation of a ramp running protocol for determination of the true VO2max in mice. Front Physiol. 2016;7:372.
Salles J, Chanet A, Berry A, et al. Fast digestive, leucine-rich, soluble milk proteins improve muscle protein anabolism, and mitochondrial function in undernourished old rats. Mol Nutr Food Res. 2017;61. doi:10.1002/mnfr.201700287
Belenchia AM, Johnson SA, Kieschnick AC, Rosenfeld CS, Peterson CA. Time course of Vitamin D depletion and repletion in reproductive-age female C57BL/6 mice. Comp Med. 2017;67:483-490.
Aldekwer S, Desiderio A, Farges MC, et al. Vitamin D supplementation associated with physical exercise promotes a tolerogenic immune environment without effect on mammary tumour growth in C57BL/6 mice. Eur J Nutr. 2021;60:2521-2535.
Chang E. Effects of Vitamin D supplementation on adipose tissue inflammation and NF-κB/AMPK activation in obese mice fed a high-fat diet. Int J Mol Sci. 2022;23:10915.
Li Y, Cook KL, Yu W, et al. Inhibition of antiestrogen-promoted pro-survival autophagy and tamoxifen resistance in breast cancer through Vitamin D receptor. Nutrients. 2021;13:1715.
Julian V, Thivel D, Miguet M, et al. Eccentric cycling is more efficient in reducing fat mass than concentric cycling in adolescents with obesity. Scand J Med Sci Sports. 2019;29:4-15.
Kim HJ, Kim YJ, Seong JK. AMP-activated protein kinase activation in skeletal muscle modulates exercise-induced uncoupled protein 1 expression in brown adipocyte in mouse model. J Physiol. 2022;600:2359-2376.
Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci. 1988;84:275-294.
Nilwik R, Snijders T, Leenders M, et al. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol. 2013;48:492-498.
Deschenes MR, Gaertner JR, O'Reilly S. The effects of sarcopenia on muscles with different recruitment patterns and myofiber profiles. Curr Aging Sci. 2013;6:266-272.
Sayed RKA, de Leonardis EC, Guerrero-Martínez JA, et al. Identification of morphological markers of sarcopenia at early stage of aging in skeletal muscle of mice. Exp Gerontol. 2016;83:22-30.
Chanet A, Salles J, Guillet C, et al. Vitamin D supplementation restores the blunted muscle protein synthesis response in deficient old rats through an impact on ectopic fat deposition. J Nutr Biochem. 2017;46:30-38.
Quinn LS, Anderson BG, Drivdahl RH, Alvarez B, Argilés JM. Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders. Exp Cell Res. 2002;280:55-63.
Kang X, Yang MY, Shi YX, et al. Interleukin-15 facilitates muscle regeneration through modulation of fibro/adipogenic progenitors. Cell Commun Signal. 2018;16:42.
Lacraz G, Rakotoarivelo V, Labbé SM, et al. Deficiency of Interleukin-15 confers resistance to obesity by diminishing inflammation and enhancing the Thermogenic function of adipose tissues (MB Aguila, Ed.). PloS One. 2016;11:e0162995.
Grunwald T, De Luca F. Role of fibroblast growth factor 21 (FGF21) in the regulation of Statural growth. Curr Pediatr Rev. 2015;11:98-105.
Hu C, Zhang X, Zhang N, et al. Osteocrin attenuates inflammation, oxidative stress, apoptosis, and cardiac dysfunction in doxorubicin-induced cardiotoxicity. Clin Transl Med. 2020;10:e124.
Thomas G, Moffatt P, Salois P, et al. Osteocrin, a novel bone-specific secreted protein that modulates the osteoblast phenotype. J Biol Chem. 2003;278:50563-50571.
Banzet S, Koulmann N, Sanchez H, Serrurier B, Peinnequin A, Bigard AX. Musclin gene expression is strongly related to fast-glycolytic phenotype. Biochem Biophys Res Commun. 2007;353:713-718.
Lips P, Eekhoff M, van Schoor N, et al. Vitamin D and type 2 diabetes. J Steroid Biochem Mol Biol. 2017;173:280-285.
Bennour I, Haroun N, Sicard F, Mounien L, Landrier JF. Vitamin D and obesity/adiposity-a brief overview of recent studies. Nutrients. 2022;14:2049.
Seldeen KL, Berman RN, Pang M, et al. Vitamin D insufficiency reduces grip strength, grip endurance and increases frailty in aged C57Bl/6J mice. Nutrients. 2020;12:E3005.
Domingues-Faria C, Boirie Y, Walrand S. Vitamin D and muscle trophicity. Curr Opin Clin Nutr Metab Care. 2017;20:169-174.
Bischoff-Ferrari HA. Relevance of vitamin D in muscle health. Rev Endocr Metab Disord. 2012;13:71-77.
Houston DK, Cesari M, Ferrucci L, et al. Association between vitamin D status and physical performance: the InCHIANTI study. J Gerontol A Biol Sci Med Sci. 2007;62:440-446.
Minasyan A, Keisala T, Zou J, et al. Vestibular dysfunction in vitamin D receptor mutant mice. J Steroid Biochem Mol Biol. 2009;114:161-166.
Bollen SE, Bass JJ, Fujita S, Wilkinson D, Hewison M, Atherton PJ. The Vitamin D/Vitamin D receptor (VDR) axis in muscle atrophy and sarcopenia. Cell Signal. 2022;96:110355.
Fu L, Chen YH, Chen X, Xu S, Yu Z, Xu DX. Vitamin D deficiency impairs neurobehavioral development in male mice. Physiol Behav. 2017;179:333-339.
Chung Y, Hsiao YT, Huang WC. Physiological and psychological effects of treadmill overtraining implementation. Biology. 2021;10:515.
Pereira BC, Pauli JR, De Souza CT, et al. Eccentric exercise leads to performance decrease and insulin signaling impairment. Med Sci Sports Exerc. 2014;46:686-694.
Carmichael MD, Davis JM, Murphy EA, et al. Recovery of running performance following muscle-damaging exercise: relationship to brain IL-1beta. Brain Behav Immun. 2005;19:445-452.
Charoenngam N, Holick MF. Immunologic effects of Vitamin D on human health and disease. Nutrients. 2020;12:2097.
Bischoff-Ferrari H, Borchers M, Gudat F, Dürmüller U, Stähelin H, Dick W. Vitamin D receptor expression in human muscle tissue decreases with age. J Bone Miner Res. 2004;19:265-269.
Johnson JA, Beckman MJ, Pansini-Porta A, et al. Age and gender effects on 1,25-dihydroxyvitamin D3-regulated gene expression. Exp Gerontol. 1995;30:631-643.
Campolina-Silva GH, Barata MC, Werneck-Gomes H, et al. Altered expression of the vitamin D metabolizing enzymes CYP27B1 and CYP24A1 under the context of prostate aging and pathologies. J Steroid Biochem Mol Biol. 2021;209:105832.
Srikuea R, Hirunsai M, Charoenphandhu N. Regulation of vitamin D system in skeletal muscle and resident myogenic stem cell during development, maturation, and ageing. Sci Rep. 2020;10:8239.

Auteurs

J Talvas (J)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

C Norgieux (C)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

E Burban (E)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

C Giraudet (C)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

V Patrac (V)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

J Salles (J)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

J-P Rigaudière (JP)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

F Capel (F)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

O le Bacquer (O)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

L Ouchchane (L)

CHU Clermont-Ferrand, Biostatistics and Medical Computing Unit, Clermont-Ferrand, France.

R Richard (R)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.

S Walrand (S)

Human Nutrition Unit, UMR 1019 INRAE/UCA, CRNH-Auvergne, Clermont-Ferrand, France.
Department of Clinical Nutrition, Clermont-Ferrand University Hospital Center, Clermont-Ferrand, France.

Classifications MeSH