|
Effect of Physical Activity on the Gene Expression of Indoleamine 2, 3-dioxygenase 1 and Arylalkylamine N-acetyltransferase in the Cerebellum of Female Mice with Experimental Autoimmune Encephalomyelitis
|
Samira Emadi1    , Shahnaz Shahrbanian2 , Mohammadreza Kordi3 , Mahdieh Molanouri Shamsi4 |
1- Ph.D Student of Exercise Physiology, Department of Sport Science, Faculty of Humanities, Tarbiat Modares University, Tehran, Iran
2- Associate Professor, Department of Sport Science, Faculty of Humanities, Tarbiat Modares University, Tehran, Iran , sh.shahrbanian@modares.ac.ir
3- Professor, Department of Exercise Physiology, Faculty of Physical Education and Sports Sciences, University of Tehran, Tehran, Iran.
4- Associate Professor, Department of Sport Science, Faculty of Humanities, Tarbiat Modares University, Tehran, Iran. |
|
|
Abstract: (1082 Views) |
Background and Aim: Induction of experimental autoimmune encephalomyelitis (EAE) is associated with an overexpression of indoleamine 2,3-dioxygenase 1 (IDO1) and exacerbation of clinical symptoms. This study aimed to investigate the effect of physical activity on the gene expression of IDO1 and arylalkylamine N-acetyltransferase (AANAT) in the cerebellum of the mice with EAE.
Materials and Methods: 30 C57BL/6 mice were randomly divided into three groups of 10: healthy control, EAE control, and physical activity in the enriched environment. Mice were placed in an enriched environment after induction of EAE with MOG35-55 for 4 weeks and then the cerebellum tissue was dissected and the expression of IDO1 and AANAT genes were measured by real time-PCR method in all three groups. Analysis of variance test was used for data analysis at a significance level of less than 0.05.
Results: The group with physical activity in an enriched environment showed significant reduction in the gene expression of IDO1 (P = 0.02) and AANAT (P = 0.04) genes, and also significantly reduced the clinical score (P = 0.001) compared to the EAE group.
Conclusion: Changing the environment and lifestyle in the enriched environment can prevent the progression of the autoimmune diseases such as MS, through downregulation of the expression of the IDO1 and AANAT genes.
|
|
| Keywords: Indoleamine 2, 3-dioxygenase 1, Arylalkylamine N-acetyltransferase, Multiple sclerosis, Physical activity |
|
|
Full-Text [PDF 598 kb]
(374 Downloads)
|
Type of Study: Original Research |
Subject:
Physical Education
Received: 2023/05/2 | Accepted: 2023/11/15 | Published: 2024/07/10
|
|
|
|
|
|
|
| References |
1. Bert A, Luchicchi A, Schenk GJ, Killestein J, Geurts JJ. Multiple sclerosis and drug discovery: A work of translation. EBioMedicine. 2021;68:103-392. [ DOI:10.1016/j.ebiom.2021.103392] [ PMID] [ ] 2. Khftan P, Vameghi R, Khankeh HR, Fathi M, Arshi M, Gholami Jam F. Exploring therapeutic problems in women with Multiple Sclerosis: A qualitative study. JQRHS. 2020;6(1):13-21. 3. Azami M, YektaKooshali MH, Shohani M, Khorshidi A, Mahmudi L. Epidemiology of multiple sclerosis in Iran: A systematic review and meta-analysis. PloS one. 2019;14(4):e0219466. [ DOI:10.1371/journal.pone.0219466] [ PMID] [ ] 4. Waubant E, Lucas R, Mowry E, Graves J, Olsson T, Alfredsson L, et al. Environmental and genetic risk factors for MS: an integrated review. Ann Clin Transl Neurol. 2019;6(9):1905-22. [ DOI:10.1002/acn3.50862] [ PMID] [ ] 5. Martin R, McFarland HF, Boggs J. Immunological aspects of experimental allergic encephalomyelitis and multiple sclerosis. Crit Rev Clin Lab Sci. 1995;32(2):121-82. [ DOI:10.3109/10408369509084683] [ PMID] 6. Correale J. Immunosuppressive amino-acid catabolizing enzymes in multiple sclerosis. Front Immunol. 2021;11:600428. [ DOI:10.3389/fimmu.2020.600428] [ PMID] [ ] 7. Stone TW, Darlington LG. Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov. 2002;1(8):609-20. [ DOI:10.1038/nrd870] [ PMID] 8. Yan Y, Zhang G-X, Gran B, Fallarino F, Yu S, Li H, et al. IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis. J Immunol. 2010;185(10):5953-61. [ DOI:10.4049/jimmunol.1001628] [ PMID] [ ] 9. Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, et al. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol. 2009;183(4):2475-83. [ DOI:10.4049/jimmunol.0900986] [ PMID] [ ] 10. Heyes MP, Saito K, Chen CY, Proescholdt MG, Nowak Jr TS, Li J, et al. Species heterogeneity between gerbils and rats: quinolinate production by microglia and astrocytes and accumulations in response to ischemic brain injury and systemic immune activation. J Neurochem. 1997;69(4):1519-29. [ DOI:10.1046/j.1471-4159.1997.69041519.x] [ PMID] 11. Tosini G, Ye K, Iuvone PM. N-acetylserotonin: neuroprotection, neurogenesis, and the sleepy brain. Neuroscientist. 2012;18(6):645-53. [ DOI:10.1177/1073858412446634] [ PMID] [ ] 12. Mondanelli G, Coletti A, Greco FA, Pallotta MT, Orabona C, Iacono A, et al. Positive allosteric modulation of indoleamine 2, 3-dioxygenase 1 restrains neuroinflammation. Proc Natl Acad Sci U S A. 2020;117(7):3848-57. [ DOI:10.1073/pnas.1918215117] [ PMID] [ ] 13. Uz T, Qu T, Sugaya K, Manev H. Neuronal expression of arylalkylamine N-acetyltransferase (AANAT) mRNA in the rat brain. Neurosci Res. 2002;42(4):309-16. [ DOI:10.1016/S0168-0102(02)00011-1] [ PMID] 14. D'Agostino PM, Gottfried-Blackmore A, Anandasabapathy N, Bulloch K. Acta Neuropatho. 2012;124(5):599-614. [ DOI:10.1007/s00401-012-1018-0] [ PMID] [ ] 15. Terness P, Bauer TM, Röse L, Dufter C, Watzlik A, Simon H, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2, 3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med. 2002;196(4):447-57. [ DOI:10.1084/jem.20020052] [ PMID] [ ] 16. Parmar K, Stadelmann C, Rocca MA, Langdon D, D'Angelo E, D'Souza M, et al. The role of the cerebellum in multiple sclerosis-150 years after Charcot. Neurosci Biobehav Rev. 2018;89:85-98. [ DOI:10.1016/j.neubiorev.2018.02.012] [ PMID] 17. Amiri M. Multiple sclerosis in Iran: An epidemiological update with focus on air pollution debate. J Clin Transl Res. 2021;7(1):49-60. 18. Dorans KS, Massa J, Chitnis T, Ascherio A, Munger KL. Physical activity and the incidence of multiple sclerosis. Neurology. 2016;87(17):1770-6. [ DOI:10.1212/WNL.0000000000003260] [ PMID] [ ] 19. Lozinski BM, Yong VW. Exercise and the brain in multiple sclerosis. Mult Scler. 2022;28(8):1167-72. [ DOI:10.1177/1352458520969099] [ PMID] 20. Quchan AHSK, Kordi MR, Namdari H, Shabkhiz F. Voluntary wheel running stimulates the expression of Nrf-2 and interleukin-10 but suppresses interleukin-17 in experimental autoimmune encephalomyelitis. Neurosci Lett. 2020;738:1353-82. [ DOI:10.1016/j.neulet.2020.135382] [ PMID] 21. Liu W, Sheng H, Xu Y, Liu Y, Lu J, Ni X. Swimming exercise ameliorates depression-like behavior in chronically stressed rats: relevant to proinflammatory cytokines and IDO activation. Behav Brain Res. 2013;242:110-6. [ DOI:10.1016/j.bbr.2012.12.041] [ PMID] 22. Souza PS, Gonçalves ED, Pedroso GS, Farias HR, Junqueira SC, Marcon R, et al. Physical exercise attenuates experimental autoimmune encephalomyelitis by inhibiting peripheral immune response and blood-brain barrier disruption. Mol Neurobiol. 2017;54(6):4723-37. [ DOI:10.1007/s12035-016-0014-0] [ PMID] 23. Silva BA, Ferrari CC. Environmental enrichment as a promising strategy for aiding multiple sclerosis treatment. Neural Regen Res. 2020;15(9):1660-61. [ DOI:10.4103/1673-5374.276334] [ PMID] [ ] 24. Chobineh S, Moham G. The effect of four weeks of physical activity in the enriched environment on inflammatory and anti-inflammatory factors in the dorsal horn of the spinal cord of mice with experimental autoimmune encephalomyelitis. JAHSSP. 2022;9(2):138-48. 25. Segal JP, Bannerman CA, Silva JR, Haird CM, Baharnoori M, Gilron I, et al. Chronic mechanical hypersensitivity in experimental autoimmune encephalomyelitis is regulated by disease severity and neuroinflammation. Brain Behav Immun. 2020;89:314-25. [ DOI:10.1016/j.bbi.2020.07.010] [ PMID] 26. Mangalam A, Shahi SK, Luckey D, Karau M, Marietta E, Luo N, et al. Human gut-derived commensal bacteria suppress CNS inflammatory and demyelinating disease. Cell Rep. 2017;20(6):1269-77. [ DOI:10.1016/j.celrep.2017.07.031] [ PMID] [ ] 27. Samani SA, Moloudi MR, Ramezanzadeh R, Abdi M, Nikkhoo B, Izadpanah E, et al. Oral Administration of Probiotic Enterococcus durans to Ameliorate Experimental Autoimmune Encephalomyelitis in Mice. Basic Clin Neurosci. 2022;13(1):35-46. [ DOI:10.32598/bcn.2021.1955.1] [ PMID] [ ] 28. Shahidi SH, Kordi MR, Rajabi H, Malm C, Shah F, Quchan ASK. Exercise modulates the levels of growth inhibitor genes before and after multiple sclerosis. J Neuroimmunol. 2020;341:577172. [ DOI:10.1016/j.jneuroim.2020.577172] [ PMID] 29. Fournier AP, Baudron E, Wagnon I, Aubert P, Vivien D, Neunlist M, et al. Environmental enrichment alleviates the deleterious effects of stress in experimental autoimmune encephalomyelitis. Mult Scler J Exp Transl Clin. 2020;6(4):2055217320959806.
https://doi.org/10.1101/2020.04.10.033662 [ DOI:10.1177/2055217320959806] [ PMID] [ ] 30. Zarzecki MS, Cattelan Souza L, Giacomeli R, Silva MRP, Prigol M, Boeira SP, et al. Involvement of Indoleamine-2, 3-Dioxygenase and Kynurenine Pathway in Experimental Autoimmune Encephalomyelitis in Mice. Neurochem Res. 2020;45(12):2959-77. [ DOI:10.1007/s11064-020-03144-6] [ PMID] 31. da Silva CC, Bichuetti DB, de Azevedo Silva SMC, Ferraz HB, de Oliveira EML, Borges V. Movement disorders in multiple sclerosis and neuromyelitis optica: A clinical marker of neurological disability. Parkinsonism Relat Disord. 2018;51:73-8. [ DOI:10.1016/j.parkreldis.2018.03.001] [ PMID] 32. Mifflin KA, Yousuf MS, Thorburn KC, Huang J, Pérez-Muñoz ME, Tenorio G, et al. Voluntary wheel running reveals sex-specific nociceptive factors in murine experimental autoimmune encephalomyelitis. Pain. 2019;160(4):870-81. [ DOI:10.1097/j.pain.0000000000001465] [ PMID] 33. Rossi S, Furlan R, De Chiara V, Musella A, Giudice TL, Mataluni G, et al. Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol Dis. 2009;36(1):51-9. [ DOI:10.1016/j.nbd.2009.06.013] [ PMID] 34. Souza LC, Jesse CR, Del Fabbro L, de Gomes MG, Goes ATR, Borges Filho C, et al. Swimming exercise prevents behavioural disturbances induced by an intracerebroventricular injection of amyloid-β1-42 peptide through modulation of cytokine/NF-kappaB pathway and indoleamine-2, 3-dioxygenase in mouse brain. ehav Brain Res. 2017;331:1-13. [ DOI:10.1016/j.bbr.2017.05.024] [ PMID] 35. Kwidzinski E, Bechmann I. IDO expression in the brain: a double-edged sword. JJ Mol Med. 2007;85(12):1351-9. [ DOI:10.1007/s00109-007-0229-7] [ PMID] 36. Vécsei L, Szalárdy L, Fülöp F, Toldi J. Kynurenines in the CNS: recent advances and new questions. Nat Rev Drug Discov. 2013;12(1):64-82. [ DOI:10.1038/nrd3793] [ PMID] 37. Dunn AL, Reigle TG, Youngstedt SD, Armstrong RB, Dishman RK. Brain norepinephrine and metabolites after treadmill training and wheel running in rats. Med Sci Sports Exerc. 1996;28(2):204-9. [ DOI:10.1097/00005768-199602000-00008] [ PMID] |
|
| Send email to the article author |
|
|
|
| Add your comments about this article |
|
|
|
|
Ethics code: IR.SSRC.REC.1401.151
emadi S, Shahrbanian S, Kordi M, Molanouri Shamsi M. Effect of Physical Activity on the Gene Expression of Indoleamine 2, 3-dioxygenase 1 and Arylalkylamine N-acetyltransferase in the Cerebellum of Female Mice with Experimental Autoimmune Encephalomyelitis. SJKU 2024; 29 (2) :12-23 URL: http://sjku.muk.ac.ir/article-1-7903-en.html
|
