The Effect Of Swimming Aerobic Training On The Levels Of IL-6 And IL-10 In The Brain Tissue Of Female Mice With Experimental Autoimmune Encephalomyelitis

Ahmadi, Elmira; Shahrbanian, Shahnaz; Kordi, Mohamadreza; Gharakhanlou, Reza; Pearcey, Gregory

Volume 22, Issue 27 (8-2024) RSMT 2024, 22(27): 55-74 | Back to browse issues page

Mendeley

Zotero

RefWorks

Ahmadi E, Shahrbanian S, Kordi M, Gharakhanlou R, Pearcey G. The Effect Of Swimming Aerobic Training On The Levels Of IL-6 And IL-10 In The Brain Tissue Of Female Mice With Experimental Autoimmune Encephalomyelitis. RSMT 2024; 22 (27) :55-74
URL: http://jsmt.khu.ac.ir/article-1-605-en.html

The Effect Of Swimming Aerobic Training On The Levels Of IL-6 And IL-10 In The Brain Tissue Of Female Mice With Experimental Autoimmune Encephalomyelitis

Elmira Ahmadi

, Shahnaz Shahrbanian

, Mohamadreza Kordi

, Reza Gharakhanlou

, Gregory Pearcey

Associate professor, Department of Sport Science, Faculty of Humanities, Tarbiat Modares University , sh.shahrbanian@modares.ac.ir

Abstract: (2611 Views)

Fatigue is one of the most common symptoms among individuals with multiple sclerosis (MS). The imbalance of inflammatory cytokines in the brain causes mental fatigue. It is believed that aerobic exercise may moderate the level of inflammation of cytokines and thus reduce mental fatigue. This study was conducted to investigate the effect of swimming aerobic training on pro-inflammatory factors (interleukin 6) and anti-inflammatory factors (interleukin 10) to evaluate mental fatigue in the brains of female mice after EAE induction. In this research, 21 mice (8 weeks old, 18 to 20 grams) were divided into three groups: healthy control, EAE control, and EAE swimming aerobic exercise. The animals in the training group performed moderate-intensity swimming exercises for 4 weeks, with 5 sessions per week, each session lasting 30 minutes. The western blot method was used to analyze the research variables. The results showed no significant difference in the amount of IL-6 between the EAE group and the swimming training group, but the amount of IL-10 in the swimming training group showed a significant increase compared to the EAE group. The ratio of IL-10/IL-6 values between the swimming training group and the EAE group was also not significant. It seems that moderate-intensity swimming aerobic exercises, without changing the pro-inflammatory factor, along with increasing the anti-inflammatory factor IL-10, can lead to an improvement in the balance of the inflammatory index and a reduction in fatigue in the EAE group and the swimming exercise group.

Keywords: Aerobic exercise, Interleukins, Inflammation, MS disease, Cytokines, Mental Fatigue.

Full-Text [PDF 675 kb] (88 Downloads)

Type of Study: Applicable | Subject: sport physiology
Received: 2023/06/6 | Accepted: 2024/01/3 | Published: 2024/08/31

References

1. Reynolds ER, Ashbaugh AD, Hockenberry BJ, McGrew CA. Multiple sclerosis and exercise: a literature review. Current sports medicine reports. 2018;17(1):31-5. (DOI: 10.1249/JSR.0000000000000446) [DOI:10.1249/JSR.0000000000000446]

2. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nature Reviews Immunology. 2015;15(9):545-58. (doi.org/10.1038/nri3871) [DOI:10.1038/nri3871]

3. Schreurs KM, de Ridder DT, Bensing JM. Fatigue in multiple sclerosis: reciprocal relationships with physical disabilities and depression. Journal of psychosomatic research. 2002;53(3):775-81. (doi.org/10.1016/S0022-3999(02)00326-4) [DOI:10.1016/S0022-3999(02)00326-4]

4. Heesen C, Nawrath L, Reich C, Bauer N, Schulz K, Gold S. Fatigue in multiple sclerosis: an example of cytokine mediated sickness behaviour? Journal of Neurology, Neurosurgery & Psychiatry. 2006;77(1):34-9. (doi.org/10.1136/jnnp.2005.065805) [DOI:10.1136/jnnp.2005.065805]

5. Mackworth NH. The breakdown of vigilance during prolonged visual search. Quarterly journal of experimental psychology. 1948;1(1):6-21. (doi.org/10.1080/17470214808416738) [DOI:10.1080/17470214808416738]

6. Qi P, Ru H, Gao L, Zhang X, Zhou T, Tian Y, et al. Neural mechanisms of mental fatigue revisited: New insights from the brain connectome. Engineering. 2019;5(2):276-86. (doi.org/10.1016/j.eng.2018.11.025) [DOI:10.1016/j.eng.2018.11.025]

7. Gentile A, Fresegna D, Federici M, Musella A, Rizzo FR, Sepman H, et al. Dopaminergic dysfunction is associated with IL-1β-dependent mood alterations in experimental autoimmune encephalomyelitis. Neurobiology of disease. 2015;74:347-58. (doi.org/10.1016/j.nbd.2014.11.022) [DOI:10.1016/j.nbd.2014.11.022]

8. Fassbender K, Schmidt R, Mößner R, Kischka U, Kühnen J, Schwartz A, Hennerici M. Mood disorders and dysfunction of the hypothalamic-pituitary-adrenal axis in multiple sclerosis: association with cerebral inflammation. Archives of neurology. 1998;55(1):66-72. (doi:10.1001/archneur.55.1.66) [DOI:10.1001/archneur.55.1.66]

9. Grasser A, Möller A, Backmund H, Yassouridis A, Holsboer F. Heterogeneity of hypothalamic-pituitary-adrenal system response to a combined dexamethasone-CRH test in multiple sclerosis. Experimental and clinical endocrinology & diabetes. 1996;104(01):31-7.( DOI: 10.1055/s-0029-1211419) [DOI:10.1055/s-0029-1211419]

10. Hanken K, Eling P, Hildebrandt H. The representation of inflammatory signals in the brain-a model for subjective fatigue in multiple sclerosis. Frontiers in neurology. 2014;5:264.( doi.org/10.3389/fneur.2014.00264) [DOI:10.3389/fneur.2014.00264]

11. Kuratsune H, Yamaguti K, Lindh G, Evengård B, Hagberg G, Matsumura K, et al. Brain regions involved in fatigue sensation: reduced acetylcarnitine uptake into the brain. Neuroimage. 2002;17(3):1256-65. (doi.org/10.1006/nimg.2002.1260) [DOI:10.1006/nimg.2002.1260]

12. Siessmeier T, Nix W, Hardt J, Schreckenberger M, Egle U, Bartenstein P. Observer independent analysis of cerebral glucose metabolism in patients with chronic fatigue syndrome. Journal of Neurology, Neurosurgery & Psychiatry. 2003;74(7):922-8. (doi.org/10.1006/nimg.2002.1260) [DOI:10.1136/jnnp.74.7.922]

13. Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Dolan RJ, Critchley HD. Neural origins of human sickness in interoceptive responses to inflammation. Biological psychiatry. 2009;66(5):415-22. (doi.org/10.1016/j.biopsych.2009.03.007) [DOI:10.1016/j.biopsych.2009.03.007]

14. Nishino S. Hypothalamus, hypocretins/orexin, and vigilance control. Handbook of Clinical Neurology. 2011;99:765-82. (doi.org/10.1016/B978-0-444-52007-4.00006-0) [DOI:10.1016/B978-0-444-52007-4.00006-0]

15. Farrokhi M, Masoudifar A, Peykanpour F. Interleukin 17 and 10 in relapsing remitting multiple sclerosis. Journal of the Neurological Sciences. 2017;378:63. (doi.org/10.1016/j.jns.2017.04.044) [DOI:10.1016/j.jns.2017.04.044]

16. Langeskov-Christensen M, Bisson EJ, Finlayson ML, Dalgas U. Potential pathophysiological pathways that can explain the positive effects of exercise on fatigue in multiple sclerosis: a scoping review. Journal of the neurological sciences. 2017;373:307-20. (doi.org/10.1016/j.jns.2017.01.002) [DOI:10.1016/j.jns.2017.01.002]

17. Fan J-X. Mechanism of Farfarae Flos in Qingfei Paidu Decoction against COVID-19 based on network pharmacology and molecular docking. Chinese Traditional and Herbal Drugs. 2020:2317-25.

18. Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nature reviews immunology. 2011;11(9):607-15. (doi.org/10.1038/nri3041) [DOI:10.1038/nri3041]

19. Mee-Inta O, Zhao Z-W, Kuo Y-M. Physical exercise inhibits inflammation and microglial activation. Cells. 2019;8(7):691. (doi.org/10.3390/cells8070691) [DOI:10.3390/cells8070691]

20. White LJ, Castellano V, Mc Coy SC. Cytokine responses to resistance training in people with multiple sclerosis. Journal of sports sciences. 2006;24(8):911-4. (doi. rg/10.1080/02640410500357036) [DOI:10.1080/02640410500357036]

21. Frisullo G, Angelucci F, Mirabella M, Caggiula M, Patanella K, Nociti V, et al. Leptin enhances the release of cytokines by peripheral blood mononuclear cells from relapsing multiple sclerosis patients. Journal of clinical immunology. 2004;24:287-93. (doi. rg/10.1023/B:JOCI.0000025450.48267.a5) [DOI:10.1023/B:JOCI.0000025450.48267.a5]

22. Farrar JD, Murphy KM. Type I interferons and T helper development. Immunology today. 2000;21(10):484-9. (doi.org/10.1016/S0167-5699(00)01710-2) [DOI:10.1016/S0167-5699(00)01710-2]

23. Fehrenbach E. Niess AM, Voelker K, Northoff H, Mooren FC. Exercise intensity and duration affect blood soluble HSP72 Int J Sports Med. 2005;26:552-7. (DOI: 10.1055/s-2004-830334) [DOI:10.1055/s-2004-830334]

24. Majdinasab N, Nakhostin-Mortazavi A, Bahadoram M, Pouretezad M, Afraz P. Effect of Aquatic Therapy on Functional Balance in Patients with Multiple Sclerosis: A Randomized Controlled Trial. Iranian Journal of Medical Sciences. 2016:130-6.

25. Deckx N, Wens I, Nuyts AH, Hens N, De Winter BY, Koppen G, et al. 12 weeks of combined endurance and resistance training reduces innate markers of inflammation in a randomized controlled clinical trial in patients with multiple sclerosis. Mediators of inflammation. 2016;2016. (doi.org/10.1155/2016/6789276) [DOI:10.1155/2016/6789276]

26. Mokhtarzade M, Ranjbar R, Majdinasab N, Patel D, Molanouri Shamsi M. Effect of aerobic interval training on serum IL-10, TNFα, and adipokines levels in women with multiple sclerosis: possible relations with fatigue and quality of life. Endocrine. 2017;57:262-71. (doi.org/10.1007/s12020-017-1337-y) [DOI:10.1007/s12020-017-1337-y]

27. Hoseini SM, Falah Mohammadi Z, Talebi V. Preventive effect six weeks of swimming training on the levels of cytokines and brain-derived neurotrophic rat model of EAE. Journal of Sport Biosciences. 2020;12(1):53-65.(doi.org/10.22059/jsb.2019.246687.1223)

28. Lutz SE, Lengfeld J, Agalliu D. Stem cell-based therapies for multiple sclerosis: recent advances in animal models and human clinical trials. Regenerative medicine. 2014;9(2):129-32. (doi.org/10.2217/rme.14.1) [DOI:10.2217/rme.14.1]

29. Jacquet T, Poulin-Charronnat B, Bard P, Perra J, Lepers R. Physical activity and music to counteract mental fatigue. Neuroscience. 2021;478:75-88. (doi.org/10.1016/j.neuroscience.2021.09.019) [DOI:10.1016/j.neuroscience.2021.09.019]

30. Einstein O, Katz A, Ben-Hur T. Physical exercise therapy for autoimmune neuroinflammation: Application of knowledge from animal models to patient care. Autoimmunity Reviews. 2022;21(4):103033. (doi.org/10.1016/j.autrev.2022.103033) [DOI:10.1016/j.autrev.2022.103033]

31. 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. Molecular neurobiology. 2017;54(6):4723-37. (doi.org/10.1007/s12035-016-0014-0) [DOI:10.1007/s12035-016-0014-0]

32. Mostert S, Kesselring J. Effects of a short-term exercise training program on aerobic fitness, fatigue, health perception and activity level of subjects with multiple sclerosis. Multiple Sclerosis Journal. 2002;8(2):161-8. (doi.org/10.1191/1352458502ms779oa) [DOI:10.1191/1352458502ms779oa]

33. Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR, et al. Ageing, fitness and neurocognitive function. Nature. 1999;400(6743):418-9. (doi.org/10.1038/22682) [DOI:10.1038/22682]

34. Motl RW, Snook EM, Schapiro RT. Symptoms and physical activity behavior in individuals with multiple sclerosis. Research in nursing & health. 2008;31(5):466-75. (doi.org/10.1002/nur.20274) [DOI:10.1002/nur.20274]

35. Vatandoust M, Motamedi P, Rajabi H, Ghadiri A, Nasirzadeh A, Vatandoust F, Yazdanpanah E, The Effect Of Four-Week Aerobic Activity In Water On Clinical Signs And TNF-α And IL-10 Cytokines In Animal Model Of Multiple Sclerosis (MS). 2018

36. Segal JP, Bannerman CA, Silva JR, Haird CM, Baharnoori M, Gilron I, Ghasemlou N. Chronic mechanical hypersensitivity in experimental autoimmune encephalomyelitis is regulated by disease severity and neuroinflammation. Brain, Behavior, and Immunity. 2020;89:314-25. (doi.org/10.1016/j.bbi.2020.07.010) [DOI:10.1016/j.bbi.2020.07.010]

37. 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. Journal of Neuroimmunology. 2020;341:577172. (doi.org/10.1016/j.jneuroim.2020.577172) [DOI:10.1016/j.jneuroim.2020.577172]

38. Xie Y, Li Z, Wang Y, Xue X, Ma W, Zhang Y, Wang J. Effects of moderate-versus high-intensity swimming training on inflammatory and CD4+ T cell subset profiles in experimental autoimmune encephalomyelitis mice. Journal of neuroimmunology. 2019;328:60-7. (doi.org/10.1016/j.jneuroim.2018.12.005) [DOI:10.1016/j.jneuroim.2018.12.005]

39. Bezheh N, Soltani M, Khaleghzade H. Effects of aerobic training in water on IL-6 and IL-10 in patients with Multiple Sclerosis. Evidence Based Care. 2014;4(2):63-72.

40. Martire S, Navone ND, Montarolo F, Perga S, Bertolotto A. A gene expression study denies the ability of 25 candidate biomarkers to predict the interferon-beta treatment response in multiple sclerosis patients. Journal of Neuroimmunology. 2016;292:34-9. (doi.org/10.1016/j.jneuroim.2016.01.010) [DOI:10.1016/j.jneuroim.2016.01.010]

41. Chen Y-C, Chen S-D, Miao L, Liu Z-G, Li W, Zhao Z-X, et al. Serum levels of interleukin (IL)-18, IL-23 and IL-17 in Chinese patients with multiple sclerosis. Journal of neuroimmunology. 2012;243(1-2):56-60. (doi.org/10.1016/j.jneuroim.2011.12.008) [DOI:10.1016/j.jneuroim.2011.12.008]

42. Etesam Z, Nemati M, Jafarzadeh A. The role of T lymphocyte subsets in the pathogenesis of multiple sclerosis. Journal of Rafsanjan University of Medical Sciences. 2016;15(3):257-80.

43. Moseley T, Haudenschild D, Rose L, Reddi A. Interleukin-17 family and IL-17 receptors. Cytokine & growth factor reviews. 2003;14(2):155-74. (doi.org/10.1016/S1359-6101(03)00002-9) [DOI:10.1016/S1359-6101(03)00002-9]

44. Pullen PR, Nagamia SH, Mehta PK, Thompson WR, Benardot D, Hammoud R, et al. Effects of yoga on inflammation and exercise capacity in patients with chronic heart failure. Journal of cardiac failure. 2008;14(5):407-13. (doi.org/10.1016/j.cardfail.2007.12.007) [DOI:10.1016/j.cardfail.2007.12.007]

45. Castellano V, Patel DI, White LJ. Cytokine responses to acute and chronic exercise in multiple sclerosis. Journal of Applied Physiology. 2008;104(6):1697-702. (doi.org/10.1152/japplphysiol.00954.2007) [DOI:10.1152/japplphysiol.00954.2007]

46. Cerqueira É, Marinho DA, Neiva HP, Lourenço O. Inflammatory effects of high and moderate intensity exercise-a systematic review. Frontiers in physiology. 2020;10:1550. (doi.org/10.1152/japplphysiol.00954.2007) [DOI:10.3389/fphys.2019.01550]

47. Schulz K-H, Gold SM, Witte J, Bartsch K, Lang UE, Hellweg R, et al. Impact of aerobic training on immune-endocrine parameters, neurotrophic factors, quality of life and coordinative function in multiple sclerosis. Journal of the neurological sciences. 2004;225(1-2):11-8. (doi.org/10.1016/j.jns.2004.06.009) [DOI:10.1016/j.jns.2004.06.009]

48. Stringer EA, Baker KS, Carroll IR, Montoya JG, Chu L, Maecker HT, Younger JW. Daily cytokine fluctuations, driven by leptin, are associated with fatigue severity in chronic fatigue syndrome: evidence of inflammatory pathology. Journal of translational medicine. 2013;11(1):1-11. (doi.org/10.1186/1479-5876-11-93) [DOI:10.1186/1479-5876-11-93]

49. Lindquist S, Hassinger S, Lindquist JA, Sailer M. The balance of pro-inflammatory and trophic factors in multiple sclerosis patients: effects of acute relapse and immunomodulatory treatment. Multiple Sclerosis Journal. 2011;17(7):851-66. (doi.org/10.1177/1352458511399797) [DOI:10.1177/1352458511399797]

50. Hooshmandi, Z., Koushki -Jahromi, M. Effect of Aerobic Exercise on Anti Inflammatory Cytokine)Interlukin- 10), Free Radical)Nitric Oxide), Fatigue and Quality of Life in Multiple Sclerosis Patients. Journal of Applied Exercise Physiology, 2017; 13(25): 51-62. doi: 10.22080/jaep.2017.1587

51. Heesen C, Gold SM, Hartmann S, Mladek M, Reer R, Braumann K-M, et al. Endocrine and cytokine responses to standardized physical stress in multiple sclerosis. Brain, behavior, and immunity. 2003;17(6):473-81. (doi. rg/10.1016/S0889-1591(03)00077-1 [DOI:10.1016/S0889-1591(03)00077-1]

52. Kargarfard M, Etemadifar M, Baker P, Mehrabi M, Hayatbakhsh R. Effect of aquatic exercise training on fatigue and health-related quality of life in patients with multiple sclerosis. Archives of physical medicine and rehabilitation. 2012;93(10):1701-8. (doi. rg/10.1016/j.apmr.2012.05.006 [DOI:10.1016/j.apmr.2012.05.006]

53. Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiological reviews. 2000. (doi.org/10.1152/physrev.2000.80.3.1055) [DOI:10.1152/physrev.2000.80.3.1055]

54. Avandi SM, Zahedi M. The effects of eight weeks' yoga training on serum levels of IL-17 in women with multiple sclerosis. Journal of Sport and Exercise Physiology. 2019;12(2):81-92. (10.52547/JOEPPA.12.2.81) [DOI:10.52547/joeppa.12.2.81]

55. Hannestad J, Subramanyam K, DellaGioia N, Planeta-Wilson B, Weinzimmer D, Pittman B, Carson RE. Glucose metabolism in the insula and cingulate is affected by systemic inflammation in humans. Journal of Nuclear Medicine. 2012;53(4):601-7. (doi.org/10.2967/jnumed.111.097014) [DOI:10.2967/jnumed.111.097014]

56. Lim S-Y, Constantinescu CS. TNF-α: A paradigm of paradox and complexity in multiple sclerosis and its animal models. The open autoimmunity journal. 2010;2(1). (10. 174/1876894601002010160)

57. Abtahi Froushani SM, Delerezh N, Hobbenaghi R, Mosayebi G. The Effects of Atorvastatin on the Treatment of Experimental Autoimmune Encephalomyelitis and its Role in the Response ofT-Helper Lymphocytes. Journal of Isfahan Medical School. 2012;30(188.

58. Bansi J, Bloch W, Gamper U, Kesselring J. Training in MS: influence of two different endurance training protocols (aquatic versus overland) on cytokine and neurotrophin concentrations during three week randomized controlled trial. Multiple Sclerosis Journal. 2013;19(5):613-21. (doi.org/10.1177/1352458512458605) [DOI:10.1177/1352458512458605]

59. Gervasoni E, Cattaneo D, Jonsdottir J. Effect of treadmill training on fatigue in multiple sclerosis: a pilot study. International journal of rehabilitation research. 2014;37(1):54-60. (DOI: 10.1097/MRR.0000000000000034) [DOI:10.1097/MRR.0000000000000034]

60. Shamsi MM, Chekachak S, Soudi S, Quinn L, Ranjbar K, Chenari J, et al. Combined effect of aerobic interval training and selenium nanoparticles on expression of IL-15 and IL-10/TNF-α ratio in skeletal muscle of 4T1 breast cancer mice with cachexia. Cytokine. 2017;90:100-8. (doi.org/10.1016/j.cyto.2016.11.005) [DOI:10.1016/j.cyto.2016.11.005]

61. Vatandoust M, Zare-Banaadkouki A. The Effect of 4 Weeks of Voluntary Aerobic Activity along with Interferon Beta on Serum Levels of Tumor Necrosis Factor Alpha (TNF-α) and Interleukin 10 (IL-10) in Mice Model of Multiple Sclerosis. Journal of Isfahan Medical School. 2022;39(651):906-13. (10.22122/JIMS.V39I651.14035)

62. Buc M. Role of regulatory T cells in pathogenesis and biological therapy of multiple sclerosis. Mediators of inflammation. 2013;2013. (doi.org/10.1155/2013/963748) [DOI:10.1155/2013/963748]

63. 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. Journal of Applied Health Studies in Sport Physiology. 2022;9(2):138-48. (10.22049/JAHSSP.2022.27886.1481)