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Article

Chikungunya and Mayaro Viruses Induce Chronic Skeletal Muscle Atrophy Triggered by Pro-Inflammatory and Oxidative Response

by
Mariana Oliveira Lopes da Silva
1,†,
Camila Menezes Figueiredo
1,†,
Rômulo Leão Silva Neris
1,
Iris Paula Guimarães-Andrade
1,
Daniel Gavino-Leopoldino
1,
Leonardo Linhares Miler-da-Silva
1,
Helber da Maia Valença
2,
Leandro Ladislau
2,
Caroline Victorino Felix de Lima
3,4,
Fernanda Meireles Coccarelli
3,4,
Claudia Farias Benjamim
5 and
Iranaia Assunção-Miranda
1,*
1
Department of Virology, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-902, Brazil
2
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-902, Brazil
3
National Center for Structural Biology and Bioimaging (CENABio), Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-902, Brazil
4
Instituto D’Or de Pesquisa e Ensino, Rio de Janeiro 22281-100, Brazil
5
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-902, Brazil
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2024, 25(16), 8909; https://doi.org/10.3390/ijms25168909
Submission received: 23 February 2024 / Revised: 25 March 2024 / Accepted: 26 March 2024 / Published: 16 August 2024
(This article belongs to the Special Issue Advanced Research on Immune Response to Viral Infection)
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Abstract

Chikungunya (CHIKV) and Mayaro (MAYV) viruses are arthritogenic alphaviruses that promote an incapacitating and long-lasting inflammatory muscle–articular disease. Despite studies pointing out the importance of skeletal muscle (SkM) in viral pathogenesis, the long-term consequences on its physiology and the mechanism of persistence of symptoms are still poorly understood. Combining molecular, morphological, nuclear magnetic resonance imaging, and histological analysis, we conduct a temporal investigation of CHIKV and MAYV replication in a wild-type mice model, focusing on the impact on SkM composition, structure, and repair in the acute and late phases of infection. We found that viral replication and induced inflammation promote a rapid loss of muscle mass and reduction in fiber cross-sectional area by upregulation of muscle-specific E3 ubiquitin ligases MuRF1 and Atrogin-1 expression, both key regulators of SkM fibers atrophy. Despite a reduction in inflammation and clearance of infectious viral particles, SkM atrophy persists until 30 days post-infection. The genomic CHIKV and MAYV RNAs were still detected in SkM in the late phase, along with the upregulation of chemokines and anti-inflammatory cytokine expression. In agreement with the involvement of inflammatory mediators on induced atrophy, the neutralization of TNF and a reduction in oxidative stress using monomethyl fumarate, an agonist of Nrf2, decreases atrogen expression and atrophic fibers while increasing weight gain in treated mice. These data indicate that arthritogenic alphavirus infection could chronically impact body SkM composition and also harm repair machinery, contributing to a better understanding of mechanisms of arthritogenic alphavirus pathogenesis and with a description of potentially new targets of therapeutic intervention.
Keywords: arthritogenic alphavirus; skeletal muscle; chronic atrophy; inflammation; oxidative stress arthritogenic alphavirus; skeletal muscle; chronic atrophy; inflammation; oxidative stress

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MDPI and ACS Style

da Silva, M.O.L.; Figueiredo, C.M.; Neris, R.L.S.; Guimarães-Andrade, I.P.; Gavino-Leopoldino, D.; Miler-da-Silva, L.L.; Valença, H.d.M.; Ladislau, L.; de Lima, C.V.F.; Coccarelli, F.M.; et al. Chikungunya and Mayaro Viruses Induce Chronic Skeletal Muscle Atrophy Triggered by Pro-Inflammatory and Oxidative Response. Int. J. Mol. Sci. 2024, 25, 8909. https://doi.org/10.3390/ijms25168909

AMA Style

da Silva MOL, Figueiredo CM, Neris RLS, Guimarães-Andrade IP, Gavino-Leopoldino D, Miler-da-Silva LL, Valença HdM, Ladislau L, de Lima CVF, Coccarelli FM, et al. Chikungunya and Mayaro Viruses Induce Chronic Skeletal Muscle Atrophy Triggered by Pro-Inflammatory and Oxidative Response. International Journal of Molecular Sciences. 2024; 25(16):8909. https://doi.org/10.3390/ijms25168909

Chicago/Turabian Style

da Silva, Mariana Oliveira Lopes, Camila Menezes Figueiredo, Rômulo Leão Silva Neris, Iris Paula Guimarães-Andrade, Daniel Gavino-Leopoldino, Leonardo Linhares Miler-da-Silva, Helber da Maia Valença, Leandro Ladislau, Caroline Victorino Felix de Lima, Fernanda Meireles Coccarelli, and et al. 2024. "Chikungunya and Mayaro Viruses Induce Chronic Skeletal Muscle Atrophy Triggered by Pro-Inflammatory and Oxidative Response" International Journal of Molecular Sciences 25, no. 16: 8909. https://doi.org/10.3390/ijms25168909

APA Style

da Silva, M. O. L., Figueiredo, C. M., Neris, R. L. S., Guimarães-Andrade, I. P., Gavino-Leopoldino, D., Miler-da-Silva, L. L., Valença, H. d. M., Ladislau, L., de Lima, C. V. F., Coccarelli, F. M., Benjamim, C. F., & Assunção-Miranda, I. (2024). Chikungunya and Mayaro Viruses Induce Chronic Skeletal Muscle Atrophy Triggered by Pro-Inflammatory and Oxidative Response. International Journal of Molecular Sciences, 25(16), 8909. https://doi.org/10.3390/ijms25168909

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