The Effect of Enriched Environment and Two Types of Forced Exercise on Irisin and BDNF Protein Levels in the Hippocampus of Female Mice with Experimental MS

Asadi, Reza; Kordi, Mohammad reza; Shabkhiz, Fatemeh

doi:10.61186/jsmt.21.25.130

Volume 21, Issue 25 (9-2023) RSMT 2023, 21(25): 130-146 | Back to browse issues page

‎ 10.61186/jsmt.21.25.130

Mendeley

Zotero

RefWorks

Asadi R, Kordi M R, Shabkhiz F. The Effect of Enriched Environment and Two Types of Forced Exercise on Irisin and BDNF Protein Levels in the Hippocampus of Female Mice with Experimental MS. RSMT 2023; 21 (25) :130-146
URL: http://jsmt.khu.ac.ir/article-1-577-en.html

The Effect of Enriched Environment and Two Types of Forced Exercise on Irisin and BDNF Protein Levels in the Hippocampus of Female Mice with Experimental MS

Reza Asadi

, Mohammad reza Kordi

, Fatemeh Shabkhiz

Tehran University , mrkordi@ut.ac.ir

Abstract: (2090 Views)

Neurodegenerative processes play an important role in the progression of MS. Appropriate exercise training and living in an enriched environment (EE) can improve or prevent the progression of the disease through the secretion of some neurodevelopmental factors in the hippocampus, including irisin and the neutrophic factor derived from the mouse. The aim of the present study was to investigate the effect of 4 weeks of aerobic and resistance training and EE on irisin protein and hippocampus BDNF levels in female C57BL6 mice with experimental autoimmune encephalomyelitis (EAE). 50 female mice (age 8 weeks, average weight 18 ± 2 grams) were randomly divided into five equal groups (10 mice in each group): 1- healthy control, 2- control + EAE, 3- resistance activity + EAE, 4- Aerobic activity + EAE and 5- EE + EAE. The first and second weeks of adaptation to the environment and then induction of EAE were performed. The training groups trained 5 days a week for half an hour a day for 4 weeks, and the EE group was transferred to its equipped cage. 48 hours after the last training session, the mice were anesthetized and then dissected and tissue removed. The ELISA method was used to measure the amounts of proteins, and the analysis of variance and Tukey's t-test were used to determine the differences between the research variables. All analyzes were performed at a significance level of 0.05 and with SPSS22 software. Hippocampal BDNF expression was increased in all three training groups compared to the EAE control group. This increase in the EE and resistance training group was significant compared to both the EAE control group and the swimming training group. Also, hippocampal irisin expression increased in all three training groups compared to the EAE control group, and this increase was significant in the EE and resistance training groups. Also, the expression of irisin in the EE group increased more than the two aerobic swimming and resistance training groups, and this increase was proportional to It was meaningful to the swimming aerobic training group. It seems that EE and resistance training can increase the secretion of nerve growth factors such as irisin and BDNF and thus help to improve MS disease.

Keywords: Multiple sclerosis, Voluntary Exercises, Forced Exercises, EE, Hippocampus

Full-Text [PDF 2102 kb] (599 Downloads)

Type of Study: Research | Subject: sport physiology
Received: 2023/05/8 | Accepted: 2023/07/11 | Published: 2023/09/1

References

1. 1. Baltan S, Jawaid SS, Chomyk AM, Kidd GJ, Chen J, Battapady HD, et al. Neuronal hibernation following hippocampal demyelination. Acta neuropathologica communications. 2021;9(1):1-15. [DOI:10.1186/s40478-021-01130-9]

2. Rieckmann P, Centonze D, Elovaara I, Giovannoni G, Havrdová E, Kesselring J, et al. Unmet needs, burden of treatment, and patient engagement in multiple sclerosis: a combined perspective from the MS in the 21st century steering group. Multiple sclerosis and related disorders. 2018;19:153-60. [DOI:10.1016/j.msard.2017.11.013]

3. Petzinger GM, Fisher BE, McEwen S, Beeler JA, Walsh JP, Jakowec MW. Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease. The Lancet Neurology. 2013;12(7):716-26. [DOI:10.1016/S1474-4422(13)70123-6]

4. Andrade LP, Gobbi LT, Coelho FG, Christofoletti G, Costa JLR, Stella F. Benefits of multimodal exercise intervention for postural control and frontal cognitive functions in individuals with Alzheimer's disease: a controlled trial. Journal of the American Geriatrics Society. 2013;11(61):1919-26. [DOI:10.1111/jgs.12531]

5. Motl RW, Pilutti LA, Hubbard EA, Wetter NC, Sosnoff JJ, Sutton BP. Cardiorespiratory fitness and its association with thalamic, hippocampal, and basal ganglia volumes in multiple sclerosis. NeuroImage: Clinical. 2015;7:661-6. [DOI:10.1016/j.nicl.2015.02.017]

6. Smith PJ, Blumenthal JA, Hoffman BM, Cooper H, Strauman TA, Welsh-Bohmer K, et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosomatic medicine. 2010;72(3):239. [DOI:10.1097/PSY.0b013e3181d14633]

7. Leal G, Afonso PM, Salazar IL, Duarte CB. Regulation of hippocampal synaptic plasticity by BDNF. Brain research. 2015;1621:82-101. [DOI:10.1016/j.brainres.2014.10.019]

8. 8 .Barbarulo AM, Lus G, Signoriello E, Trojano L, Grossi D, Esposito M, et al. Integrated cognitive and neuromotor rehabilitation in multiple sclerosis: a pragmatic study. Frontiers in behavioral neuroscience. 2018;12:196. [DOI:10.3389/fnbeh.2018.00196]

9. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481(7382):463-8. [DOI:10.1038/nature10777]

10. Wrann CD, White JP, Salogiannnis J, Laznik-Bogoslavski D, Wu J, Ma D, et al. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell metabolism. 2013;18(5):649-59. [DOI:10.1016/j.cmet.2013.09.008]

11. Hill T, Polk JD. BDNF, endurance activity, and mechanisms underlying the evolution of hominin brains. American journal of physical anthropology. 2019;168:47-62. [DOI:10.1002/ajpa.23762]

12. Di Liegro CM, Schiera G, Proia P, Di Liegro I. Physical activity and brain health. Genes. 2019;10(9):720. [DOI:10.3390/genes10090720]

13. Mähler A, Balogh A, Csizmadia I, Klug L, Kleinewietfeld M, Steiniger J, et al. Metabolic, mental and immunological effects of normoxic and hypoxic training in multiple sclerosis patients: a pilot study. Frontiers in immunology. 2018;9:2819. [DOI:10.3389/fimmu.2018.02819]

14. Houdebine L, Gallelli CA, Rastelli M, Sampathkumar NK, Grenier J. Effect of physical exercise on brain and lipid metabolism in mouse models of multiple sclerosis. Chemistry and physics of lipids. 2017;207:127-34. [DOI:10.1016/j.chemphyslip.2017.06.002]

15. 15 Sampedro-Piquero P, Begega A. Environmental enrichment as a positive behavioral intervention across the lifespan. Current neuropharmacology. 2017;15(4):459-70. [DOI:10.2174/1570159X14666160325115909]

16. Fischer A. Environmental enrichment as a method to improve cognitive function. What can we learn from animal models? Neuroimage. 2016;131:42-7. [DOI:10.1016/j.neuroimage.2015.11.039]

17. Silva BA, Miglietta EA, Ferrari CC. Training the brain: could it improve multiple sclerosis treatment? Reviews in the Neurosciences. 2020;31(7):779-92. [DOI:10.1515/revneuro-2020-0014]

18. Gentile A, Musella A, De Vito F, Rizzo FR, Fresegna D, Bullitta S, et al. Immunomodulatory effects of exercise in experimental multiple sclerosis. Frontiers in immunology. 2019;10:2197. [DOI:10.3389/fimmu.2019.02197]

19. 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:10.1007/s12035-016-0014-0]

20. 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:10.1016/j.jneuroim.2020.577172]

21. 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. Multiple Sclerosis Journal-Experimental, Translational and Clinical. 2020;6(4):2055217320959806. [DOI:10.1177/2055217320959806]

22. 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, behavior, and immunity. 2020;89:314-25. [DOI:10.1016/j.bbi.2020.07.010]

23. Peng J, Wu J. Effects of the FNDC5/Irisin on Elderly Dementia and Cognitive Impairment. Frontiers in Aging Neuroscience. 2022;14. [DOI:10.3389/fnagi.2022.863901]

24. Yu K-W, Wang C-J, Wu Y, Wang Y-Y, Wang N-H, Kuang S-Y, et al. An enriched environment increases the expression of fibronectin type III domain-containing protein 5 and brain-derived neurotrophic factor in the cerebral cortex of the ischemic mouse brain. Neural regeneration research. 2020;15(9):1671. [DOI:10.4103/1673-5374.276339]

25. Cruz Y, García EE, Gálvez JV, Arias-Santiago SV, Carvajal HG, Silva-García R, et al. Release of interleukin-10 and neurotrophic factors in the choroid plexus: possible inductors of neurogenesis following copolymer-1 immunization after cerebral ischemia. Neural regeneration research. 2018;13(10):1743. [DOI:10.4103/1673-5374.238615]

26. Zsuga J, Tajti G, Papp C, Juhasz B, Gesztelyi R. FNDC5/irisin, a molecular target for boosting reward-related learning and motivation. Medical Hypotheses. 2016;90:23-8. [DOI:10.1016/j.mehy.2016.02.020]

27. Kim J-Y, Yi E-S, Lee H, Kim J-S, Jee Y-S, Kim S-E, et al. Swimming exercise ameliorates symptoms of MOG-induced experimental autoimmune encephalomyelitis by inhibiting inflammation and demyelination in rats. International Neurourology Journal. 2020;24(Suppl 1):S39. [DOI:10.5213/inj.2040156.078]

28. Naghibzadeh M, Ranjbar R, Tabandeh MR, Habibi A. Effects of two training programs on transcriptional levels of neurotrophins and glial cells population in hippocampus of experimental multiple sclerosis. International journal of sports medicine. 2018;39(08):604-12. [DOI:10.1055/a-0608-4635]

29. Gelfo F, Petrosini L. Environmental Enrichment Enhances Cerebellar Compensation and Develops Cerebellar Reserve. International Journal of Environmental Research and Public Health. 2022;19(9):5697. [DOI:10.3390/ijerph19095697]

30. Kempermann G, Gast D, Gage FH. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long‐term environmental enrichment. Annals of neurology. 2002;52(2):135-43. [DOI:10.1002/ana.10262]