TY - JOUR
T1 - Intense Acute Swimming Induces Delayed-Onset Muscle Soreness Dependent on Spinal Cord Neuroinflammation
AU - Borghi, Sergio M.
AU - Bussulo, Sylvia K.D.
AU - Pinho-Ribeiro, Felipe A.
AU - Fattori, Victor
AU - Carvalho, Thacyana T.
AU - Rasquel-Oliveira, Fernanda S.
AU - Zaninelli, Tiago H.
AU - Ferraz, Camila R.
AU - Casella, Antônio M.B.
AU - Cunha, Fernando Q.
AU - Cunha, Thiago M.
AU - Casagrande, Rubia
AU - Verri, Waldiceu A.
N1 - Funding Information:
This work was supported by grants from Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, finance code 001), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), São Paulo Research Foundation (grant number 2013/08216-2; Center for Research in Inflammatory Disease–CRID), Programa de Apoio a Grupos de Excelência (PRONEX) grant supported by SETI (Secretaria da Ciência, Tecnologia e Ensino Superior)/Araucária Foundation and MCTI (Ministério da Ciência, Tecnologia e Inovação)/CNPq, and Paraná State Government (agreement 014/2017, protocol 46.843) (Brazil). SMB acknowledges Fundação Nacional de Desenvolvimento do Ensino Superior Particular (FUNADESP; grant number 5301159) research fellowship. FC, TMC, RC, and WV acknowledge the CNPq productivity research fellowship. The confocal microscope was acquired by a project supported by Financiadora de Estudo e Projetos (FINEP)-Apoio à Infraestrutura (CT-INFRA 01/2011; process 01.13.0049.00). During the conduction of the study, SMB received postdoctoral fellowships from CAPES and CNPq.
Funding Information:
This work was supported by grants from Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, finance code 001), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), São Paulo Research Foundation (grant number 2013/08216-2; Center for Research in Inflammatory Disease–CRID), Programa de Apoio a Grupos de Excelência (PRONEX) grant supported by SETI (Secretaria da Ciência, Tecnologia e Ensino Superior)/Araucária Foundation and MCTI (Ministério da Ciência, Tecnologia e Inovação)/CNPq, and Paraná State Government (agreement 014/2017, protocol 46.843) (Brazil). SMB acknowledges Fundação Nacional de Desenvolvimento do Ensino Superior Particular (FUNADESP;
Publisher Copyright:
Copyright © 2022 Borghi, Bussulo, Pinho-Ribeiro, Fattori, Carvalho, Rasquel-Oliveira, Zaninelli, Ferraz, Casella, Cunha, Cunha, Casagrande and Verri.
PY - 2022/1/7
Y1 - 2022/1/7
N2 - Unaccustomed exercise involving eccentric contractions, high intensity, or long duration are recognized to induce delayed-onset muscle soreness (DOMS). Myocyte damage and inflammation in affected peripheral tissues contribute to sensitize muscle nociceptors leading to muscle pain. However, despite the essential role of the spinal cord in the regulation of pain, spinal cord neuroinflammatory mechanisms in intense swimming-induced DOMS remain to be investigated. We hypothesized that spinal cord neuroinflammation contributes to DOMS. C57BL/6 mice swam for 2 h to induce DOMS, and nociceptive spinal cord mechanisms were evaluated. DOMS triggered the activation of astrocytes and microglia in the spinal cord 24 h after exercise compared to the sham group. DOMS and DOMS-induced spinal cord nuclear factor κB (NFκB) activation were reduced by intrathecal treatments with glial inhibitors (fluorocitrate, α-aminoadipate, and minocycline) and NFκB inhibitor [pyrrolidine dithiocarbamate (PDTC)]. Moreover, DOMS was also reduced by intrathecal treatments targeting C-X3-C motif chemokine ligand 1 (CX3CL1), tumor necrosis factor (TNF)-α, and interleukin (IL)-1β or with recombinant IL-10. In agreement, DOMS induced the mRNA and protein expressions of CX3CR1, TNF-α, IL-1β, IL-10, c-Fos, and oxidative stress in the spinal cord. All these immune and cellular alterations triggered by DOMS were amenable by intrathecal treatments with glial and NFκB inhibitors. These results support a role for spinal cord glial cells, via NFκB, cytokines/chemokines, and oxidative stress, in DOMS. Thus, unveiling neuroinflammatory mechanisms by which unaccustomed exercise induces central sensitization and consequently DOMS.
AB - Unaccustomed exercise involving eccentric contractions, high intensity, or long duration are recognized to induce delayed-onset muscle soreness (DOMS). Myocyte damage and inflammation in affected peripheral tissues contribute to sensitize muscle nociceptors leading to muscle pain. However, despite the essential role of the spinal cord in the regulation of pain, spinal cord neuroinflammatory mechanisms in intense swimming-induced DOMS remain to be investigated. We hypothesized that spinal cord neuroinflammation contributes to DOMS. C57BL/6 mice swam for 2 h to induce DOMS, and nociceptive spinal cord mechanisms were evaluated. DOMS triggered the activation of astrocytes and microglia in the spinal cord 24 h after exercise compared to the sham group. DOMS and DOMS-induced spinal cord nuclear factor κB (NFκB) activation were reduced by intrathecal treatments with glial inhibitors (fluorocitrate, α-aminoadipate, and minocycline) and NFκB inhibitor [pyrrolidine dithiocarbamate (PDTC)]. Moreover, DOMS was also reduced by intrathecal treatments targeting C-X3-C motif chemokine ligand 1 (CX3CL1), tumor necrosis factor (TNF)-α, and interleukin (IL)-1β or with recombinant IL-10. In agreement, DOMS induced the mRNA and protein expressions of CX3CR1, TNF-α, IL-1β, IL-10, c-Fos, and oxidative stress in the spinal cord. All these immune and cellular alterations triggered by DOMS were amenable by intrathecal treatments with glial and NFκB inhibitors. These results support a role for spinal cord glial cells, via NFκB, cytokines/chemokines, and oxidative stress, in DOMS. Thus, unveiling neuroinflammatory mechanisms by which unaccustomed exercise induces central sensitization and consequently DOMS.
KW - acute exercise
KW - delayed-onset muscle soreness
KW - glial cells
KW - neuroinflammation
KW - spinal cord
UR - http://www.scopus.com/inward/record.url?scp=85123164187&partnerID=8YFLogxK
U2 - 10.3389/fphar.2021.734091
DO - 10.3389/fphar.2021.734091
M3 - Article
C2 - 35069187
AN - SCOPUS:85123164187
SN - 1663-9812
VL - 12
JO - Frontiers in Pharmacology
JF - Frontiers in Pharmacology
M1 - 734091
ER -