Hsp90 as a Myokine: Its Association with Systemic Inflammation after Exercise Interventions in Patients with Myositis and Healthy Subjects

. 2022 Sep 28 ; 23 (19) : . [epub] 20220928

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu srovnávací studie, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36232755

Grantová podpora
023728, 16-33542A, 16-33574A, NV18-01-00161A Ministry of Health
SVV 260523, Biobanks and Biomolecular Resources Research Infrastructure Consortium BBMRICZ LM2018125 Ministry of Education Youth and Sports

Compelling evidence supports the health benefits of physical exercise on the immune system, possibly through the molecules secreted by the skeletal muscles known as myokines. Herein, we assessed the impact of exercise interventions on plasma Heat shock protein 90 (Hsp90) levels in 27 patients with idiopathic inflammatory myopathies (IIM) compared with 23 IIM patients treated with standard-of-care immunosuppressive therapy only, and in 18 healthy subjects undergoing strenuous eccentric exercise, and their associations with the traditional serum markers of muscle damage and inflammation. In contrast to IIM patients treated with pharmacotherapy only, in whom we demonstrated a significant decrease in Hsp90 over 24 weeks, the 24-week exercise program resulted in a stabilization of Hsp90 levels. These changes in Hsp90 levels were associated with changes in several inflammatory cytokines/chemokines involved in the pathogenesis of IIM or muscle regeneration in general. Strenuous eccentric exercise in healthy volunteers induced a brief increase in Hsp90 levels with a subsequent return to baseline levels at 14 days after the exercise, with less pronounced correlations to systemic inflammation. In this study, we identified Hsp90 as a potential myokine and mediator for exercise-induced immune response and as a potential biomarker predicting improvement after physiotherapy in muscle endurance in IIM.

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Eckel J. Myokines in Metabolic Homeostasis and Diabetes. Diabetologia. 2019;62:1523–1528. doi: 10.1007/s00125-019-4927-9. PubMed DOI

Severinsen M.C.K., Pedersen B.K. Muscle-Organ Crosstalk: The Emerging Roles of Myokines. Endocr. Rev. 2020;41:bnaa016. doi: 10.1210/endrev/bnaa016. PubMed DOI PMC

Pedersen L., Hojman P. Muscle-to-Organ Cross Talk Mediated by Myokines. Adipocyte. 2012;1:164–167. doi: 10.4161/adip.20344. PubMed DOI PMC

Pedersen B.K. Anti-Inflammatory Effects of Exercise: Role in Diabetes and Cardiovascular Disease. Eur. J. Clin. Investig. 2017;47:600–611. doi: 10.1111/eci.12781. PubMed DOI

Pedersen B.K. Exercise-Induced Myokines and Their Role in Chronic Diseases. Brain Behav. Immun. 2011;25:811–816. doi: 10.1016/j.bbi.2011.02.010. PubMed DOI

Pedersen B.K., Steensberg A., Fischer C., Keller C., Keller P., Plomgaard P., Febbraio M., Saltin B. Searching for the Exercise Factor: Is IL-6 a Candidate? J. Muscle Res. Cell Motil. 2003;24:113–119. doi: 10.1023/A:1026070911202. PubMed DOI

Pedersen B.K. Myokines and Metabolism. In: Ahima R.S., editor. Metabolic Syndrome. Springer International Publishing; Cham, Switzerland: 2016. pp. 541–554.

Pedersen B.K. Muscle as a Secretory Organ. Compr. Physiol. 2013;3:1337–1362. doi: 10.1002/cphy.c120033. PubMed DOI

Chow L.S., Gerszten R.E., Taylor J.M., Pedersen B.K., van Praag H., Trappe S., Febbraio M.A., Galis Z.S., Gao Y., Haus J.M., et al. Exerkines in Health, Resilience and Disease. Nat. Rev. Endocrinol. 2022;18:273–289. doi: 10.1038/s41574-022-00641-2. PubMed DOI PMC

Das D.K., Graham Z.A., Cardozo C.P. Myokines in Skeletal Muscle Physiology and Metabolism: Recent Advances and Future Perspectives. Acta Physiol. 2020;228:e13367. doi: 10.1111/apha.13367. PubMed DOI

Scheffer D.d.L., Latini A. Exercise-Induced Immune System Response: Anti-Inflammatory Status on Peripheral and Central Organs. Biochim. Biophys. Acta Mol. Basis Dis. 2020;1866:165823. doi: 10.1016/j.bbadis.2020.165823. PubMed DOI PMC

Wang J., Liu S., Li G., Xiao J. Exercise Regulates the Immune System. Adv. Exp. Med. Biol. 2020;1228:395–408. doi: 10.1007/978-981-15-1792-1_27. PubMed DOI

Bay M.L., Pedersen B.K. Muscle-Organ Crosstalk: Focus on Immunometabolism. Front. Physiol. 2020;11:567881. doi: 10.3389/fphys.2020.567881. PubMed DOI PMC

Isanejad A., Amini H. Physical Exercise and Heat Shock Proteins. In: Asea A.A.A., Kaur P., editors. Chaperokine Activity of Heat Shock Proteins. Volume 16. Springer International Publishing; Cham, Switzerland: 2019. pp. 247–277. Heat Shock Proteins.

McGarr G.W., Fujii N., Schmidt M.D., Muia C.M., Kenny G.P. Heat Shock Protein 90 Modulates Cutaneous Vasodilation during an Exercise-Heat Stress, but Not during Passive Whole-Body Heating in Young Women. Physiol. Rep. 2020;8:e14552. doi: 10.14814/phy2.14552. PubMed DOI PMC

Henstridge D.C., Febbraio M.A., Hargreaves M. Heat Shock Proteins and Exercise Adaptations. Our Knowledge Thus Far and the Road Still Ahead. J. Appl. Physiol. 2016;120:683–691. doi: 10.1152/japplphysiol.00811.2015. PubMed DOI

Krüger K., Reichel T., Zeilinger C. Role of Heat Shock Proteins 70/90 in Exercise Physiology and Exercise Immunology and Their Diagnostic Potential in Sports. J. Appl. Physiol. 2019;126:916–927. doi: 10.1152/japplphysiol.01052.2018. PubMed DOI

Choudhury A., Mandrekar P. Chaperones in Sterile Inflammation and Injury. In: Asea A.A.A., Kaur P., editors. Chaperokine Activity of Heat Shock Proteins. Volume 16. Springer International Publishing; Cham, Switzerland: 2019. pp. 155–177. Heat Shock Proteins.

Storkanova H., Tomcik M. Role of Heat Shock Protein 90 in Autoimmune Inflammatory Rheumatic Diseases. In: Asea A.A.A., Kaur P., editors. Chaperokine Activity of Heat Shock Proteins. Volume 16. Springer International Publishing; Cham, Switzerland: 2019. pp. 105–121. Heat Shock Proteins.

Štorkánová H., Oreská S., Špiritović M., Heřmánková B., Bubová K., Kryštůfková O., Mann H., Komarc M., Slabý K., Pavelka K., et al. Hsp90 Levels in Idiopathic Inflammatory Myopathies and Their Association With Muscle Involvement and Disease Activity: A Cross-Sectional and Longitudinal Study. Front. Immunol. 2022;13:811045. doi: 10.3389/fimmu.2022.811045. PubMed DOI PMC

Miller F.W., Lamb J.A., Schmidt J., Nagaraju K. Risk Factors and Disease Mechanisms in Myositis. Nat. Rev. Rheumatol. 2018;14:255–268. doi: 10.1038/nrrheum.2018.48. PubMed DOI PMC

Lundberg I.E., Fujimoto M., Vencovsky J., Aggarwal R., Holmqvist M., Christopher-Stine L., Mammen A.L., Miller F.W. Idiopathic Inflammatory Myopathies. Nat. Rev. Dis. Primers. 2021;7:86. doi: 10.1038/s41572-021-00321-x. PubMed DOI

Vencovský J., Alexanderson H., Lundberg I.E. Idiopathic Inflammatory Myopathies. Rheum. Dis. Clin. N. Am. 2019;45:569–581. doi: 10.1016/j.rdc.2019.07.006. PubMed DOI

Ashton C., Paramalingam S., Stevenson B., Brusch A., Needham M. Idiopathic Inflammatory Myopathies: A Review. Intern. Med. J. 2021;51:845–852. doi: 10.1111/imj.15358. PubMed DOI

Tsamis K.I., Boutsoras C., Kaltsonoudis E., Pelechas E., Nikas I.P., Simos Y.V., Voulgari P.V., Sarmas I. Clinical Features and Diagnostic Tools in Idiopathic Inflammatory Myopathies. Crit. Rev. Clin. Lab. Sci. 2022;59:219–240. doi: 10.1080/10408363.2021.2000584. PubMed DOI

Ernste F.C., Reed A.M. Idiopathic Inflammatory Myopathies: Current Trends in Pathogenesis, Clinical Features, and up-to-Date Treatment Recommendations. Mayo Clin. Proc. 2013;88:83–105. doi: 10.1016/j.mayocp.2012.10.017. PubMed DOI

Metsios G.S., Moe R.H., Kitas G.D. Exercise and Inflammation. Best Pract. Res. Clin. Rheumatol. 2020;34:101504. doi: 10.1016/j.berh.2020.101504. PubMed DOI

Benatti F.B., Pedersen B.K. Exercise as an Anti-Inflammatory Therapy for Rheumatic Diseases-Myokine Regulation. Nat. Rev. Rheumatol. 2015;11:86–97. doi: 10.1038/nrrheum.2014.193. PubMed DOI

Dos Santos A.M., Misse R.G., Borges I.B.P., Perandini L.A.B., Shinjo S.K. Physical Exercise for the Management of Systemic Autoimmune Myopathies: Recent Findings, and Future Perspectives. Curr. Opin. Rheumatol. 2021;33:563–569. doi: 10.1097/BOR.0000000000000829. PubMed DOI

Nader G.A., Lundberg I.E. Exercise as an Anti-Inflammatory Intervention to Combat Inflammatory Diseases of Muscle. Curr. Opin. Rheumatol. 2009;21:599–603. doi: 10.1097/BOR.0b013e3283319d53. PubMed DOI

Špiritović M., Heřmánková B., Oreská S., Štorkánová H., Růžičková O., Vernerová L., Klein M., Kubínová K., Šmucrová H., Rathouská A., et al. The Effect of a 24-Week Training Focused on Activities of Daily Living, Muscle Strengthening, and Stability in Idiopathic Inflammatory Myopathies: A Monocentric Controlled Study with Follow-Up. Arthritis Res. Ther. 2021;23:173. doi: 10.1186/s13075-021-02544-5. PubMed DOI PMC

Hody S., Croisier J.-L., Bury T., Rogister B., Leprince P. Eccentric Muscle Contractions: Risks and Benefits. Front. Physiol. 2019;10:536. doi: 10.3389/fphys.2019.00536. PubMed DOI PMC

De Paepe B., Creus K.K., De Bleecker J.L. Role of Cytokines and Chemokines in Idiopathic Inflammatory Myopathies. Curr. Opin. Rheumatol. 2009;21:610–616. doi: 10.1097/BOR.0b013e3283317b31. PubMed DOI

Cerezo L.A., Vencovský J., Šenolt L. Cytokines and Inflammatory Mediators as Promising Markers of Polymyositis/Dermatomyositis. Curr. Opin. Rheumatol. 2020;32:534–541. doi: 10.1097/BOR.0000000000000744. PubMed DOI

da Silva T.C.P., Silva M.G., Shinjo S.K. Relevance of Serum Angiogenic Cytokines in Adult Patients with Dermatomyositis. Adv. Rheumatol. 2018;58:17. doi: 10.1186/s42358-018-0018-8. PubMed DOI

Oishi K., Matsushita T., Takehara K., Hamaguchi Y. Increased Interleukin-9 Levels in Sera, Muscle and Skin of Patients with Dermatomyositis. J. Dermatol. 2018;45:1023–1025. doi: 10.1111/1346-8138.14518. PubMed DOI

Sugiura T., Kawaguchi Y., Harigai M., Takagi K., Ohta S., Fukasawa C., Hara M., Kamatani N. Increased CD40 Expression on Muscle Cells of Polymyositis and Dermatomyositis: Role of CD40-CD40 Ligand Interaction in IL-6, IL-8, IL-15, and Monocyte Chemoattractant Protein-1 Production. J. Immunol. 2000;164:6593–6600. doi: 10.4049/jimmunol.164.12.6593. PubMed DOI

Liprandi A., Bartoli C., Figarella-Branger D., Pellissier J.F., Lepidi H. Local Expression of Monocyte Chemoattractant Protein-1 (MCP-1) in Idiopathic Inflammatory Myopathies. Acta Neuropathol. 1999;97:642–648. doi: 10.1007/s004010051041. PubMed DOI

Wu C.-Y., Li L., Zhang L.-H. Detection of Serum MCP-1 and TGF-Β1 in Polymyositis/Dermatomyositis Patients and Its Significance. Eur. J. Med. Res. 2019;24:12. doi: 10.1186/s40001-019-0368-7. PubMed DOI PMC

Bai J., Wu C., Zhong D., Xu D., Wang Q., Zeng X. Hierarchical Cluster Analysis of Cytokine Profiles Reveals a Cutaneous Vasculitis-Associated Subgroup in Dermatomyositis. Clin. Rheumatol. 2021;40:999–1008. doi: 10.1007/s10067-020-05339-2. PubMed DOI

Fritsch J., Fickers R., Klawitter J., Särchen V., Zingler P., Adam D., Janssen O., Krause E., Schütze S. TNF Induced Cleavage of HSP90 by Cathepsin D Potentiates Apoptotic Cell Death. Oncotarget. 2016;7:75774–75789. doi: 10.18632/oncotarget.12411. PubMed DOI PMC

Stephanou A., Latchman D.S. Transcriptional Regulation of the Heat Shock Protein Genes by STAT Family Transcription Factors. Gene Expr. 1999;7:311–319. PubMed PMC

Stephanou A., Isenberg D.A., Nakajima K., Latchman D.S. Signal Transducer and Activator of Transcription-1 and Heat ShockFactor-1 Interact and Activate the Transcription of the Hsp-70 and Hsp-90b Gene Promoters. J. Biol. Chem. 1999;274:1723–1728. doi: 10.1074/jbc.274.3.1723. PubMed DOI

Prodromou C. Mechanisms of Hsp90 Regulation. Biochem. J. 2016;473:2439–2452. doi: 10.1042/BCJ20160005. PubMed DOI PMC

Tukaj S., Węgrzyn G. Anti-Hsp90 Therapy in Autoimmune and Inflammatory Diseases:A Review of Preclinical Studies. Cell Stress Chaperones. 2016;21:213–218. doi: 10.1007/s12192-016-0670-z. PubMed DOI PMC

Chatterjee S., Burns T.F. Heat Shock Protein 90 Inhibitors in Lung Cancer Therapy. In: Asea A.A.A., Kaur P., editors. Heat Shock Proteins in Signaling Pathways. Springer International Publishing; Cham, Switzerland: 2019. pp. 359–395. Heat Shock Proteins.

Jego G., Hermetet F., Girodon F., Garrido C. Chaperoning STAT3/5 by Heat Shock Proteins: Interest of Their Targeting in Cancer Therapy. Cancers. 2020;12:21. doi: 10.3390/cancers12010021. PubMed DOI PMC

Petersen A.M.W., Pedersen B.K. The Anti-Inflammatory Effect of Exercise. J. Appl. Physiol. 2005;98:1154–1162. doi: 10.1152/japplphysiol.00164.2004. PubMed DOI

Abd El-Kader S.M., Al-Jiffri O.H. Aerobic Exercise Modulates Cytokine Profile and Sleep Quality in Elderly. Afr. Health Sci. 2019;19:2198–2207. doi: 10.4314/ahs.v19i2.45. PubMed DOI PMC

Baturcam E., Abubaker J., Tiss A., Abu-Farha M., Khadir A., Al-Ghimlas F., Al-Khairi I., Cherian P., Elkum N., Hammad M., et al. Physical Exercise Reduces the Expression of RANTES and Its CCR5 Receptor in the Adipose Tissue of Obese Humans. Mediat. Inflamm. 2014;2014:627150. doi: 10.1155/2014/627150. PubMed DOI PMC

Alizaei Yousefabadi H., Niyazi A., Alaee S., Fathi M., Mohammad Rahimi G.R. Anti-Inflammatory Effects of Exercise on Metabolic Syndrome Patients: A Systematic Review and Meta-Analysis. Biol. Res. Nurs. 2021;23:280–292. doi: 10.1177/1099800420958068. PubMed DOI

Zheng G., Qiu P., Xia R., Lin H., Ye B., Tao J., Chen L. Effect of Aerobic Exercise on Inflammatory Markers in Healthy Middle-Aged and Older Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Front. Aging Neurosci. 2019;11:98. doi: 10.3389/fnagi.2019.00098. PubMed DOI PMC

Mathers J.L., Farnfield M.M., Garnham A.P., Caldow M.K., Cameron-Smith D., Peake J.M. Early Inflammatory and Myogenic Responses to Resistance Exercise in the Elderly. Muscle Nerve. 2012;46:407–412. doi: 10.1002/mus.23317. PubMed DOI

Ferris D.K., Harel-Bellan A., Morimoto R.I., Welch W.J., Farrar W.L. Mitogen and Lymphokine Stimulation of Heat Shock Proteins in T Lymphocytes. Proc. Natl. Acad. Sci. USA. 1988;85:3850–3854. doi: 10.1073/pnas.85.11.3850. PubMed DOI PMC

Barabutis N., Uddin M.A., Catravas J.D. Hsp90 Inhibitors Suppress P53 Phosphorylation in LPS-Induced Endothelial Inflammation. Cytokine. 2019;113:427–432. doi: 10.1016/j.cyto.2018.10.020. PubMed DOI PMC

Ripley B.J., Stephanou A., Isenberg D.A., Latchman D.S. Interleukin-10 Activates Heat-Shock Protein 90beta Gene Expression. Immunology. 1999;97:226–231. doi: 10.1046/j.1365-2567.1999.00773.x. PubMed DOI PMC

Leers M.P.G., Schepers R., Baumgarten R. Effects of a Long-Distance Run on Cardiac Markers in Healthy Athletes. Clin. Chem. Lab. Med. 2006;44:999–1003. doi: 10.1515/CCLM.2006.179. PubMed DOI

Lippi G., Schena F., Salvagno G.L., Montagnana M., Gelati M., Tarperi C., Banfi G., Guidi G.C. Acute Variation of Biochemical Markers of Muscle Damage Following a 21-Km, Half-Marathon Run. Scand. J. Clin. Lab. Investig. 2008;68:667–672. doi: 10.1080/00365510802126844. PubMed DOI

Lappalainen H., Tiula E., Uotila L., Mänttäri M. Elimination Kinetics of Myoglobin and Creatine Kinase in Rhabdomyolysis: Implications for Follow-Up. Crit. Care Med. 2002;30:2212–2215. doi: 10.1097/00003246-200210000-00006. PubMed DOI

Brancaccio P., Lippi G., Maffulli N. Biochemical Markers of Muscular Damage. Clin. Chem. Lab. Med. 2010;48:757–767. doi: 10.1515/CCLM.2010.179. PubMed DOI

Shastry S., Toft D.O., Joyner M.J. HSP70 and HSP90 Expression in Leucocytes after Exercise in Moderately Trained Humans. Acta Physiol. Scand. 2002;175:139–146. doi: 10.1046/j.1365-201X.2002.00979.x. PubMed DOI

De Paepe B., Creus K.K., Martin J.-J., Weis J., De Bleecker J.L. A Dual Role for HSP90 and HSP70 in the Inflammatory Myopathies: From Muscle Fiber Protection to Active Invasion by Macrophages. Ann. N. Y. Acad. Sci. 2009;1173:463–469. doi: 10.1111/j.1749-6632.2009.04812.x. PubMed DOI

Paepe B.D., Creus K.K., Weis J., Bleecker J.L.D. Heat Shock Protein Families 70 and 90 in Duchenne Muscular Dystrophy and Inflammatory Myopathy: Balancing Muscle Protection and Destruction. Neuromuscul. Disord. 2012;22:26–33. doi: 10.1016/j.nmd.2011.07.007. PubMed DOI

Isaacs A.W., Macaluso F., Smith C., Myburgh K.H. C-Reactive Protein Is Elevated Only in High Creatine Kinase Responders to Muscle Damaging Exercise. Front. Physiol. 2019;10:86. doi: 10.3389/fphys.2019.00086. PubMed DOI PMC

Trøseid M., Lappegård K.T., Claudi T., Damås J.K., Mørkrid L., Brendberg R., Mollnes T.E. Exercise Reduces Plasma Levels of the Chemokines MCP-1 and IL-8 in Subjects with the Metabolic Syndrome. Eur. Heart J. 2004;25:349–355. doi: 10.1016/j.ehj.2003.12.006. PubMed DOI

Kim G.-T., Cho M.-L., Park Y.-E., Yoo W.H., Kim J.-H., Oh H.-J., Kim D.-S., Baek S.-H., Lee S.-H., Lee J.-H., et al. Expression of TLR2, TLR4, and TLR9 in Dermatomyositis and Polymyositis. Clin. Rheumatol. 2010;29:273–279. doi: 10.1007/s10067-009-1316-7. PubMed DOI PMC

Giriş M., Durmuş H., Yetimler B., Taşli H., Parman Y., Tüzün E. Elevated IL-4 and IFN-γ Levels in Muscle Tissue of Patients with Dermatomyositis. In Vivo. 2017;31:657–660. doi: 10.21873/invivo.11108. PubMed DOI PMC

Sag E., Kale G., Haliloglu G., Bilginer Y., Akcoren Z., Orhan D., Gucer S., Topaloglu H., Ozen S., Talim B. Inflammatory Milieu of Muscle Biopsies in Juvenile Dermatomyositis. Rheumatol. Int. 2021;41:77–85. doi: 10.1007/s00296-020-04735-w. PubMed DOI

Paolucci E.M., Loukov D., Bowdish D.M.E., Heisz J.J. Exercise Reduces Depression and Inflammation but Intensity Matters. Biol. Psychol. 2018;133:79–84. doi: 10.1016/j.biopsycho.2018.01.015. PubMed DOI

Pedersen B.K., Hoffman-Goetz L. Exercise and the Immune System: Regulation, Integration, and Adaptation. Physiol. Rev. 2000;80:1055–1081. doi: 10.1152/physrev.2000.80.3.1055. PubMed DOI

Cronin O., Keohane D.M., Molloy M.G., Shanahan F. The Effect of Exercise Interventions on Inflammatory Biomarkers in Healthy, Physically Inactive Subjects: A Systematic Review. QJM. 2017;110:629–637. doi: 10.1093/qjmed/hcx091. PubMed DOI

García J.J., Bote E., Hinchado M.D., Ortega E. A Single Session of Intense Exercise Improves the Inflammatory Response in Healthy Sedentary Women. J. Physiol. Biochem. 2011;67:87–94. doi: 10.1007/s13105-010-0052-4. PubMed DOI

Van Thillo A., Vulsteke J.-B., Van Assche D., Verschueren P., De Langhe E. Physical Therapy in Adult Inflammatory Myopathy Patients: A Systematic Review. Clin. Rheumatol. 2019;38:2039–2051. doi: 10.1007/s10067-019-04571-9. PubMed DOI

Alexanderson H., Boström C. Exercise Therapy in Patients with Idiopathic Inflammatory Myopathies and Systemic Lupus Erythematosus—A Systematic Literature Review. Best Pract. Res. Clin. Rheumatol. 2020;34:101547. doi: 10.1016/j.berh.2020.101547. PubMed DOI

Mattar M.A., Gualano B., Perandini L.A., Shinjo S.K., Lima F.R., Sá-Pinto A.L., Roschel H. Safety and Possible Effects of Low-Intensity Resistance Training Associated with Partial Blood Flow Restriction in Polymyositis and Dermatomyositis. Arthritis Res. Ther. 2014;16:473. doi: 10.1186/s13075-014-0473-5. PubMed DOI PMC

Tiffreau V., Rannou F., Kopciuch F., Hachulla E., Mouthon L., Thoumie P., Sibilia J., Drumez E., Thevenon A. Postrehabilitation Functional Improvements in Patients With Inflammatory Myopathies: The Results of a Randomized Controlled Trial. Arch. Phys. Med. Rehabil. 2017;98:227–234. doi: 10.1016/j.apmr.2016.09.125. PubMed DOI

Luk H.-Y., Levitt D.E., Appell C., Vingren J.L. Sex Dimorphism in Muscle Damage-Induced Inflammation. Med. Sci. Sports Exerc. 2021;53:1595–1605. doi: 10.1249/MSS.0000000000002628. PubMed DOI

De Bleecker J.L., De Paepe B., Vanwalleghem I.E., Schröder J.M. Differential Expression of Chemokines in Inflammatory Myopathies. Neurology. 2002;58:1779–1785. doi: 10.1212/WNL.58.12.1779. PubMed DOI

Peake J.M., Suzuki K., Hordern M., Wilson G., Nosaka K., Coombes J.S. Plasma Cytokine Changes in Relation to Exercise Intensity and Muscle Damage. Eur. J. Appl. Physiol. 2005;95:514–521. doi: 10.1007/s00421-005-0035-2. PubMed DOI

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