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)

Authors

  • Maryam Vatandoust1* 1. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.
  • Pezhman Motamedi2 2. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.
  • Hamid Rajabi3 3. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.
  • Ata Allah Ghadiri4 4. Dept. of Immunology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.
  • Abdolmahdi Nasirzade5 5. Dept. of Sport Management, School of Physical Education and Sport Sciences, Payame Noor University, Tehran, Iran.
  • Fateme Vatandoust6 6. Dept. of Biology, School of Biosciences, Alzahra University, Tehran, Iran.
  • Enayatoallah Yazdanpanah7 7. Dept. of Biology, Payame Noor University, Tehran, Iran.

DOI:

https://doi.org/10.22100/jkh.v12i4.1818

Keywords:

EAE, Aerobic Swimming, TNF-α, IL-10

Abstract

Introduction: According to importance of complimentary therapies, The aim of this study was to evaluate the effect of four-week aerobic physical activity in water on clinical signs and amount of Tumor Necrosis Factor alpha (TNF- α) and Interleukin 10 (IL-10) in serum levels of animal model of multiple sclerosis (MS) via inducing experimental autoimmune encephalomyelitis (EAE).

Methods: A total number of 80 female Syrian mice from the race of C57BL/6, aging 10 to 12 weeks and weighing 20±2 gram were divided into eight groups of 10, including: control, swimming, MS, MS+swimming, MS+interferon beta (INF- α), MS+interferon beta+swimming, MS+solvent, and MS+solvent+swimming environment. On post-immunization day 9, animals received IFN (150 IU/g) or were subjected to swimming daily for 4 weeks. Weight and clinical score were monitored daily and recorded in all groups. Finally blood samples were taken from the heart and the factors were measured by ELISA. The data were analyzed by one-way ANOVA.

Results: According to clinical signs diagrams, there was seen significant difference between MS+swimming, MS+interferon beta, MS+interferon beta+swimming with MS group (P=0.001). Also, Based on the scores of clinical signs, the severity of injury in MS groups compared to active subjects had a average score of 2 to 3, indicating control and reduction of the progression of demyelin lesions resulting from the effect of exercise in water.

Conclusion: These findings suggest that probably swimming is more effective than IFN to alter clinical signs and the level of TNF- α and IL-10 in the serum of EAE-induced mice. Therefore we conclude that regular moderate exercise could be helpful beside the medical therapies to attenuate the MS disorders.

Author Biographies

  • Maryam Vatandoust1*, 1. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.

    دانشجوی دکتری ، گروه فیزیولوژی ورزشی، دانشکده تربیت بدنی و علوم ورزشی، دانشگاه خوارزمی

  • Pezhman Motamedi2, 2. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.
    استادیار، گروه فیزیولوژی ورزشی، دانشکده تربیت بدنی و علوم ورزشی، دانشگاه خوارزمی
  • Hamid Rajabi3, 3. Dept. of Sport Physiology, School of Physical Education and Sport Sciences, Kharazmi University, Tehran, Iran.
    دانشیار، گروه فیزیولوژی ورزشی، دانشکده تربیت بدنی و علوم ورزشی، دانشگاه خوارزمی
  • Ata Allah Ghadiri4, 4. Dept. of Immunology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.
    استاديار، گروه ايمني شناسي، دانشكده پزشكي، دانشگاه علوم پزشكي جندي شاپور اهواز
  • Abdolmahdi Nasirzade5, 5. Dept. of Sport Management, School of Physical Education and Sport Sciences, Payame Noor University, Tehran, Iran.
    استادیار، گروه مدیریت ورزشی، دانشکده تربیت بدنی و علوم ورزشی، دانشگاه پیام نور
  • Fateme Vatandoust6, 6. Dept. of Biology, School of Biosciences, Alzahra University, Tehran, Iran.
    دانشجوی کارشناسی ارشد، گروه بیولوژی، دانشکده علوم زیستی،  دانشگاه الزهرا
  • Enayatoallah Yazdanpanah7, 7. Dept. of Biology, Payame Noor University, Tehran, Iran.
    استادیار، گروه بیولوژی، دانشگاه پیام نور

References

Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005;23:683-747. doi: 10.1146/annurev.immunol.23.021704.115707

Jana MG, Sofia MK. Prevention of learning disability in the preschool years. Procedia-Social and Behavioral Sciences 2014;146:163-8. doi: 10.1016/j.sbspro.2014.08.105

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

Rombery A, Virtanen A, Ruutiainen J, Aunola S, Karppi SL, Vaara M, et al. Effect of a 6-month exercise program on patient with multiple sclerosis: a randomized study. Neurology 2004;63:48-203.

Bradly, Daroff, Fenichel, Jankovic. Neurology in clinical practice. 4th ed. Philadelphia: Elsevier,2004.

Motl RW, Pilutti LA. The benefits of exercise training in multiple sclerosis. Nat Rev Neurol 2012;8:487-97. doi: 10.1038/nrneurol.2012.136

Coelho FG, Gobbi S, Andreatto CA, Corazza DI, Pedroso RV, Santos-Galduróz RF. Physical exercise modulates peripheral levels of brain-derived neurotrophic factor (BDNF): a systematic review of experimental studies in the elderly. Arch Gerontol Geriatr 2013;56:10-5. doi: 10.1016/j.archger.2012.06.003

White LJ, McCoy SC, Castellano V, Ferguson MA, Hou W, Dressendorfer RH. Effect of resistance training on risk of coronary artery disease in women with multiple sclerosis. Scand J Clin Lab Invest 2006;66:351-5. doi: 10.1080/00365510600727686

Castellano V, Patel D, White LJ. Cytokine responses to acute and chronic exercise in multiple sclerosis. J Appl Physiol 2008;104:1697-702. doi: 10.1152/japplphysiol.00954.2007

Kress-Bennett J, Ehrlich G, Bruno A, Post C, Scott T. Preliminary study: treatment with intramuscular interferon beta-1a results in increased levels of IL- 12Rb2+ and decreased levels of IL23R+ CD4+ T - Lymphocytes in multiple sclerosis. BMC Neurology 2011;11:1-7.

Hayes HA, Gappmaier E, LaStayo PC. Effects of high-intensity resistance training on strength, mobility, balance, and fatigue in individuals with multiple sclerosis: a randomized controlled trial. J Neurol Phys Ther 2011;35:2-10. doi: 10.1097/NPT.0b013e31820b5a9d

Branas P, Jordan R, Fry-Smith A, Burls A, Hyde C. Treatments for fatigue in multiple sclerosis: a rapid and systematic review. Health Technol Assess 2000;4:1-61.

White LJ, Castellano V. Exercise and brain health –implications for multiple sclerosispart 1 – neuronal growth factors. Sports Med 2008;38:91-100.

Mahon BD, Gordon SA, Cruz J, Cosman F, Cantorna T. Cytokine profile in patients with multiple sclerosis following vitamin D supplementation. J Neuroimmunol 2003;134:128-32.

Martin R, Mcfarland HF, Mcfarlin DE. Immunological aspect of demyelinationy disease. Ann Rev Immunol 1992;10:153-87. doi: 10.1146/annurev.iy.10.040192.001101

Mary L, Patricia L, Jessie H, Lorene S, Jeanna V, Daryl K, et al. Impact of Resistance Training on Balance and Gait in Multiple Sclerosis. International Journal of MS Care 2010;12:6-12. doi: 10.7224/1537-2073-12.1.6

McCullagh R, Fitzgerald A, Murphy RP, Cooke G. Long-term benefits of exercising on quality of life and fatigue in multiple sclerosis patients with mild disability : a pilot study. Clin Rehabil 2008;22:206-14. doi: 10.1177/0269215507082283

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. Mult Scler 2002;8:161-8. doi: 10.1191/1352458502ms779oa

Motl R, Dlugonski D, Wo´jcicki T, McAuley E, Mohr D. Internet intervention for increasing physical activity in persons with multiple sclerosis. Mult Scler J 2011;17:116-28. doi: 10.1177/1352458510383148

Ogawa K, Sanada K, Machida S, Okutsu M, Suzuki K. Resistance exercise training-induced muscle hypertrophywas associated with reduction of inflammatory markers in elderly women. Mediators Inflamm 2010;2010:7. doi: 10.1155/2010/171023

Petajan JH, Gappmaier E, White AT, Spencer MK, Mino L, Hicks RW. Impact of aerobic training on fitness and quality of life in multiple sclerosis. Am Neurol 1996;39:432-41. doi: 10.1002/ana.410390405

Ring- Dimit riou, S. Nine months aerobic fitness induced changes on blood lipids and lipoproteins in untrained subjects versus controls. Eur J Appl Physiol 2007;99:291-9. doi: 10.1007/s00421-006-0347-x

Morgado JM, Rama L, Silva I, de Jesus Inácio M, Henriques A, Laranjeira P, et al. Cytokine production by monocytes, neutrophils, and dendritic cells is hampered by long-term intensive training in elite swimmers. European Journal of Applied Physiology 2012;112:471-82. doi: 10.1007/s00421-011-1966-4

Roberts C K, Won D, Pruthi S, Kurtovic S, Sindhu RK, Vaziri ND, et al. Effect of a short-term diet and exercise intervention on oxidative stress, inflammation, MMP-9, and monocyte chemotactic activity in men with metabolic syndrome factors. J Appl Physiol 2006;100:1657-65. doi: 10.1152/japplphysiol.01292.2005

White LJ, Castellano V, McCoy SC. Cytokine responses to resistance training in people with multiple sclerosis. J Sports Sci 2006;24:911-4. doi: 10.1080/02640410500357036

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. Mult Scler 2013;19:613-21. doi: 10.1177/1352458512458605

Compston A, Coles A. Multiple sclerosis. Lancet 2008;372:1502-17. doi: 10.1016/S0140-6736(08)61620-7

Gandhi R, Laroni A, Weiner HL. Role of the innate immune system in the pathogenesis of multiple sclerosis. J Neuroimmunol 2010;221:7-14. doi: 10.1016/j.jneuroim.2009.10.015

Thewissen K, Nuyts AH, Deckx N, Bart Van Wijmeersch, Guy Nagels, Marie D’hooghe, et al. Circulating dendritic cells of multiple sclerosis patients are proinflammatory and their frequency is correlated with MS-associated genetic risk factors. Multiple Sclerosis Journal 2014;20:548-57.

Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, et al. Position statement. Part one. Immune function and exercise. Exerc Immunol Rev 2011;17:6-63.

Nickel T, Hanssen H, Emslander I, Drexel V, Hertel G, Schmidt-Trucksäss A, et al. Immunomodulatory effects of aerobic training in obesity. Mediators of Inflammation 2011;2011:1-10. doi: 10.1155/2011/308965

Pilutti LA, Platta ME, Motl RW, Latimer- Cheung AE. The safety of exercise training in multiple sclerosis: a systematic review. J Neurol Sci 2014;343:3-7. doi: 10.1016/j.jns.2014.05.016

Vassili P. The pathophysiology of tumor necrosis factor. Annu Rev Immunol 1992;10:411-52. doi: 10.1146/annurev.iy.10.040192.002211

Van der Pol T, Lowry SF. Epinephrine inhibits endotoxin-induced IL-1b production: roles of tumor necrosis factor-a and IL-10. Am J Physiol 1997;273:R1885-90.

Brouckaert P, Fiers W. Tumor necrosis factor and the systemic inflammatory response syndrome. Curr Top Microbiol Immunol 1996;216:167-87.

Walley KR, Lukacs NW, Standiford TJ, Strieter RM, Kunkel SL. Balance of inflammatory cytokines related to severity and mortality of murine sepsis. Infect Immun 1996;64:4733-8.

Stordeur P, Goldman M. Interleukin-10 as a regulatory cytokine induced by cellular stress: molecular aspects. Int Rev Immunol 1998; 16:501-22.

Oswald L, Wynn T, Sher A. Interleukine-10 inhibits microbicidal activity by blocking endogenous production of tumor necrosis factor a required as a costimulatory factor for interferon-g -induced activation. Proc Natl Acad Sci USA 1992;89:8676-80.

Eigler A, Siegmund B, Emmerich U, Baumann KH, Hartmann G, Endres S. Anti-inflammatory activities of cAMP-elevating agents: enhancement of IL-10 synthesis and concurrent suppression of TNF production. J Leukoc Biol 1998;63:101-7.

Foey AD, Parry SL, Williams LM, Feldmann M, Foxwell BMJ, Brennan FM. Regulation of monocyte IL-10 synthesis by endogenous IL-1 and TNF-a : role of the p38 and p42/44 mitogen-activated protein kinases. J Immunol 1998;60:920-8.

Romberg A, Virtanen A, Ruutiainen J, Aunola S, Karppi SL, Vaara M, et al. Effect of a 6-month exercise program on patient with multiple sclerosis : a randomized study. Neurology 2004;63:2034-8.

Stinissen P, Raus J, Zhany J. Autoimmune pathogenesis of multiple sclerosis: role of autoreactive T lymphocyte and new immunotherapeatic strategies. Crit Rev Immunol 1997;17:33-75.

Svensson B, Grdle B, Elert J. Endurance training in patients with multiple sclerosis: Five case studies. Phys Ther 1994;74:1017-26.

Tartibian B, Ghodrat Gharabag Z, Gaeini A, Tolouei-Azar J. Influence of 9 weeks aerobic exercise and multivitamin supplement on inflammation biomarkers as cardiovascular risk factor in non-athletic obese women. Zahedan J Res Med Sci (ZJRMS) 2011;13:20-30.

Adamopoulos S, Parissis J, Kroupis C, Georgiadis M, Karatzas D, Karavolias G, et al. Physical training reduces peripheral markers of inflammation in patients with chronic heart failure. Eur Heart J 2001;22:791-7. doi: 10.1053/euhj.2000.2285

Arastoo AA, Ahmadi A, Zahednejad Sh. The comparision of effect of 8 weeks aerobic and yoga training on physiological cost index in multiple sclerosis patients. Sci Med J;2011;10:153-62.[Persian].

Ashton F. The multiple factors of multiple sclerosis. Journal of Nutritional & Environmental Medicine 2004;14:1-11.

Bjarnadottir OH, Konradsdottir AD, Reynisdottir K, Olafsson E. Multiple sclerosis and brief moderate exercise. Mult Scler 2007;13:776-82. doi: 10.1177/1352458506073780

Brown T, Kraft G. Exercise and rehabilitation for individuals with multiple sclerosis. Phys Med Rehabil Clin N Am 2005;16:513-55. doi: 10.1016/j.pmr.2005.01.005

Fischer D, Epstein J, Klasser G. Multiple sclerosis. Medical Management And Pharmacology Update 2009;108:318-27. doi: 10.1016/j.tripleo.2009.05.047

Golzari Z, Shabkhiz F, Soudi S, Kordi MR, Hashemi SM. Combined exercise training reduces IFN-γ and IL-17 levels in the plasma and the supernatant of peripheral blood mononuclear cells in women with multiple sclerosis. Int Immunopharmacol 2010;10:1415-9. doi: 10.1016/j.intimp.2010.08.008

Haan A, van der Vliet MR, Hendriks JJ, Heijnen DA, Dijkstra CD. Changes in characteristics of rat skeletal muscle after experimental allergic encephalomyelitis. Muscle Nerve 2004;29:369-75. doi: 10.1002/mus.10554

Page C, Ferry A, Rieu M. Effect of muscular exercise on chronic relapsing experimental autoimmune encephalomyelitis. J Appl Physiol 1994;77:2341-7. doi: 10.1152/jappl.1994.77.5.2341

Page C, Bourdoulous S, Beraud E, Couraud PO, Rieu M, Ferry A. Effect of physical exercise on adoptive experimental auto-immune encephalomyelitis in rats. Eur J Appl Physiol Occup Physiol 1996;73:130-5.

Sharief MK. Cytokines in multiple sclerosis: pro-inflammation or proremyelination? Mult Scler 1998;4:169-73. doi: 10.1177/135245859800400315

Yuede CM, Zimmerman SD, Dong H, Kling MJ, Bero AW, Holtzman DM, et al. Effects of voluntary and forced exercise on plaque deposition, hippocampal volume, and behavior in the Tg2576 mouse model of Alzheimer's disease. Neurobiol Dis 2009;35:426-32. doi: 10.1016/j.nbd.2009.06.002

Zivadinov R, Bakshi R. Central nervous system atrophy and clinical status in multiple sclerosis. J Neuroimaging 2004;14:27S-35S. doi: 10.1177/1051228404266266

Poser CM, Brinar VV. Diagnostic criteria for multiple sclerosis: an historical review. Clin Neurol Neurosurg 2004;106:147-58. doi: 10.1016/j.clineuro.2004.02.004

Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000;343:938-52. doi: 10.1056/ NEJM200009283431307

disease transgenic mice. Neuroscience 2006;141:569-84. doi:10.1016/j.neuroscience. 2006.04.013

Bernardes D, Brambilla R, Bracchi‐Ricard V, Karmally S, Dellarole A, Carvalho‐Tavares J, et al. Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis. J Neurochem 2016;136:63-73. doi: 10.1111/jnc.13354

Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000;343:938-52. doi:10.1056/ NEJM200009283431307

Platzer C, Meisel C, Vogt K, Platzer M, Volk HD. Up-regulation of monocytic IL-10 by tumor necrosis factor-alpha and cAMP elevating drugs. Int Immunol 1995;7:517-23.

Wanidworanun C, Strober W. Predominant role of tumor necrosis factoralpha in human monocyte IL-10 synthesis. J Immunol 1993;151:6853-61.

Armstrong L, Millar AB. Relative production of tumour necrosis factor a and interleukin-10 in adult respiratory distress syndrome. Thorax 1997;52:442-6.

Pang T, Stam NC, Nithianantharajah J, Howard ML, Hannan AJ. Differential effects of voluntary physical exercise on behavioral and brainderived neurotrophic factor expression deficits in Huntington's

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2018-03-17

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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). Knowledge and Health in Basic Medical Sciences, 12(4), Page:47-60. https://doi.org/10.22100/jkh.v12i4.1818