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Glutamine supplementation accelerates functional recovery of EDL muscles after injury by modulating the expression of S100 calcium-binding proteins

Histochemistry and Cell Biology volume 160, pages 135–146 (2023)Cite this article

Abstract

The aim of the current study was to investigate the effect of glutamine supplementation on the expression of HSP70 and the calcium-binding proteins from the S100 superfamily in the recovering extensor digitorum longus (EDL) muscle after injury. Two-month-old Wistar rats were subjected to cryolesion of the EDL muscle and then randomly divided into two groups (with or without glutamine supplementation). Starting immediately after the injury, the supplemented group received daily doses of glutamine (1 g/kg/day, via gavage) for 3 and 10 days orally. Then, muscles were subjected to histological, molecular, and functional analysis. Glutamine supplementation induced an increase in myofiber size of regenerating EDL muscles and prevented the decline in maximum tetanic strength of these muscles evaluated 10 days after injury. An accelerated upregulation of myogenin mRNA levels was detected in glutamine-supplemented injured muscles on day 3 post-cryolesion. The HSP70 expression increased only in the injured group supplemented with glutamine for 3 days. The increase in mRNA levels of NF-κB, the pro-inflammatory cytokines IL-1β and TNF-α, and the calcium-binding proteins S100A8 and S100A9 on day 3 post-cryolesion in EDL muscles was attenuated by glutamine supplementation. In contrast, the decrease in S100A1 mRNA levels in the 3-day-injured EDL muscles was minimized by glutamine supplementation. Overall, our results suggest that glutamine supplementation accelerates the recovery of myofiber size and contractile function after injury by modulating the expression of myogenin, HSP70, NF-κB, pro-inflammatory cytokines, and S100 calcium-binding proteins.

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Availability of data and material

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We are thankful to Ajinomoto for providing us with L-glutamine and Bianca R. Baggio (M.S. fellowship from CAPES) for technical assistance.

Funding

This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grants No. 18/24946-4 and No. 20/15351-7) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Fellowship/Grant No. 314857/2021-4). A.R.S. and T.E.K. received Ph.D. fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and FAPESP (Grant No. 17/09069-4), respectively. T.C.S. received an M.S. fellowship from CAPES. A.M.S. and N.C.M. received scientific initiation fellowships from Programa Unificado de Bolsas (PUB) of University of São Paulo. A.M.S. also received scientific initiation fellowship from FAPESP (Grant No. 23/00289-2).

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  1. Department of Anatomy, Institute of Biomedical Sciences, University of Sao Paulo, Av Prof. Lineu Prestes, 2415, Sao Paulo, SP, 05508-000, Brazil

    Audrei R. Santos, Tatiana E. Koike, Alana M. Santana, Natalya C. Miranda, Rodrigo A. Dell Aquila, Thiago C. Silva & Elen H. Miyabara

  2. School of Arts, Sciences and Humanities, University of Sao Paulo, Sao Paulo, SP, 03828-000, Brazil

    Marcelo S. Aoki

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  1. Audrei R. Santos
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MSA and EHM: designed the study; ARS, TEK, AMS, NCM, RADA, TCS, MSA and EHM: performed the experiments and/or analyzed the data; ARS, TEK, AMS, NCM, RADA, TCS, MSA and EHM: interpreted the data; ARS, TEK, AMS, NCM, RADA, TCS, MSA and EHM: wrote or revised the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Elen H. Miyabara.

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Santos, A.R., Koike, T.E., Santana, A.M. et al. Glutamine supplementation accelerates functional recovery of EDL muscles after injury by modulating the expression of S100 calcium-binding proteins. Histochem Cell Biol 160, 135–146 (2023). https://doi.org/10.1007/s00418-023-02194-5

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