Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis

Journal of Neurochemistry

Volumn 136, Issue , 2016, Pages 63-73

  Bernardes, Danielle ^a,b,c   Brambilla, Roberta ^c   Bracchi Ricard, Valerie ^c,d   Karmally, Shaffiat ^c   Dellarole, Anna ^c   Carvalho Tavares, Juliana ^a   Bethea, John R ^d  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^c UNIVERSITY OF MIAMI   (United States)

^d DREXEL UNIVERSITY   (United States)

Author keywords

axonal damage; demyelination; experimental autoimmune encephalomyelitis (EAE); neuroinflammation; swimming exercise

Indexed keywords

ANIMAL; ANIMAL EXPERIMENT; AXON; C57BL MOUSE; DEMYELINATING AUTOIMMUNE DISEASES, CNS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; MOUSE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SWIMMING; TREATMENT OUTCOME;

ANIMALS; AXONS; DEMYELINATING AUTOIMMUNE DISEASES, CNS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; MICE; MICE, INBRED C57BL; PHYSICAL CONDITIONING, ANIMAL; SWIMMING; TREATMENT OUTCOME;

EID: 84956583567     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13354     Document Type: Article

References (64)

1. Adlard P. A., Perreau V. M., and, Cotman C. W., (2005) The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol. Aging 26, 511-520.
2. Almeida P. W., Gomes-Filho A., Ferreira A. J., et al,. (2009) Swim training suppresses tumor growth in mice. J. Appl. Physiol. 107, 261-265.
3. Bauer J., Bradl M., Hickey W. F., Forss-Petter S., Breitschopf H., Linington C., Wekerle H., and, Lassmann H., (1998) T-cell apoptosis in inflammatory brain lesions destruction of T cells does not depend on antigen recognition. Am. J. Pathol. 153, 715-724.
4. Bernardes D., Oliveira-Lima O. C., Vitarelli-Silva T., et al,. (2013) Differential brain and spinal cord cytokine and BDNF levels in experimental autoimmune encephalomyelitis are modulated by prior and regular exercise. J. Neuroimmunol. 264, 24-34.
5. Brambilla R., Ashbaugh J. J., Magliozzi R., Dellarole A., Karmally S., Szymkowski D. E., and, Bethea J. R., (2011) Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134, 2736-2754.
6. Brambilla R., Morton P. D., Ashbaugh J. J., Karmally S., Lambertsen K. L., and, Bethea J. R., (2014) Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 62, 452-467.
7. Cherry J. D., Olschowka J. A., and, O'Banion M. K., (2014) Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J. Neuroinflammation 11, 98.
8. Cravens P. D., Kieseier B. C., Hussain R., et al,. (2013) The neonatal CNS is not conducive for encephalitogenic Th1 T cells and B cells during experimental autoimmune encephalomyelitis. J. Neuroinflammation 10, 67.
9. Dalgas U., and, Stenager E., (2012) Exercise and disease progression in multiple sclerosis: can exercise slow down the progression of multiple sclerosis? Ther. Adv. Neurol. Disord. 5, 81-95.
10. Deforges S., Branchu J., Biondi O., Grondard C., Pariset C., Lecolle S., Lopes P., Vidal P. P., Chanoine C., and, Charbonnier F., (2009) Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis. J. Physiol. 587, 3561-3572.
11. Di Bello I. C., Dawson M. R., Levine J. M., and, Reynolds R., (1999) Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J. Neurocytol. 4-5, 365-381.
12. Ehninger D., Wang L. P., Klempin F., Römer B., Kettenmann H., and, Kempermann G., (2011) Enriched environment and physical activity reduce microglia and influence the fat e of NG2 cells in the amygdala of adult mice. Cell Tissue Res. 345, 69-86.
13. Evangelista F. S., Brum P. C., and, Krieger J. E., (2003) Duration-controlled swimming exercise training induces cardiac hypertrophy in mice. Braz. J. Med. Biol. Res. 36, 1751-1759.
14. Feinstein A., Magalhaes S., Richard J. F., Audet B., and, Moore C., (2014) The link between multiple sclerosis and depression. Nat. Rev. Neurol. 10, 507-517.
15. Franklin R. J. M., and, Gallo V., (2014) The translational biology of remyelination: past, present, and future. Glia 62, 1905-1915.
16. Garay L. I., Gonzalez Deniselle M. C., Brocca M. E., Lima A., Roig P., and, De Nicola A. F., (2012). Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis. Neuroscience 226, 40-50.
17. Gilgun-Sherki Y., Panet H., Holdengreber V., Mosberg-Galili R., and, Offen D., (2003) Axonal damage is reduced following glatiramer acetate treatment in C57/bl mice with chronic-induced experimental autoimmune encephalomyelitis. Neurosci. Res. 47, 201-207.
18. Girolamo F., Ferrara G., Strippoli M., et al,. (2011) Cerebral cortex demyelination and oligodendrocyte precursor response to experimental autoimmune encephalomyelitis. Neurobiol. Disease. 43, 678-689.
19. Goh J., and, Ladiges W. C., (2014) Exercise enhances wound healing and prevents cancer progression during aging by targeting macrophage polarity. Mech. Ageing Dev. 139, 41-48.
20. Haines J. D., Inglese M., and, Casaccia P., (2011) Axonal damage in multiple sclerosis. Mt Sinai J. Med. 78, 231-243.
21. Hayes K., Sprague S., Guo M., Davis W., Friedman A., Kumar A., Jimenez D. F., and, Ding Y., (2008) Forced, not voluntary, exercise effectively induces neuroprotection in stroke. Acta Neuropathol. 115, 289-296.
22. Keirstead H. S., and, Blakemore W. F., (1997) Identification of postmitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J. Neuropathol. Exp. Neurol. 56 (11), 1191-1201.
23. Kinni H., Guo M., Ding J. Y., Konakondla S., Dornbos D., III, Tran R., Guthikonda M., and, Ding Y., (2011) Cerebral metabolism after forced or voluntary physical exercise. Brain Res. 1388, 48-55.
24. Koenning M., Jackson S., Hay C. M., Faux C., Kilpatrick T. J., Willingham M., and, Emery B., (2012) Myelin gene regulatory factor is required for maintenance of myelin and mature oligodendrocyte identity in the adult CNS. J. Neurosci. 32 (36), 12528-12542.
25. Krüger K., and, Mooren F. C., (2014) Exercise-induced leukocyte apoptosis. Exerc. Immunol. Rev. 20, 117-134.
26. Kutzelnigg A., and, Lassmann H., (2014) Pathology of multiple sclerosis and related inflammatory demyelinating diseases. Handb. Clin. Neurol. 122, 15-58.
27. Le Page C., Ferry A., and, Rieu M., (1994) Effect of muscular exercise on chronic relapsing experimental autoimmune encephalomyelitis. J. Appl. Physiol. 77, 2341-2347.
28. Le Page C., Bourdoulous S., Beraud E., Couraud P. O., Rieu M., and, Ferry A., (1996) Effect of physical exercise on adoptive experimental auto-immune encephalomyelitis in rats. Eur. J. Appl. Physiol. Occup. Physiol. 73, 130-135.
29. Luhder F., Gold R., Flügel A., and, Linker R. A., (2013) Brain-derived neurotrophic factor in neuroimmunology: lessons learned from multiple sclerosis patients and experimental autoimmune encephalomyelitis models. Arch. Immunol. Ther. Exp. (Warsz) 61, 95-105.
30. Mann M. K., Ray A., Basu S., Karp C. L., and, Dittel B. N., (2012) Pathogenic and regulatory roles for B cells in experimental autoimmune encephalomyelitis. Autoimmunity 45, 388-399.
31. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., and, Locati M., (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25 (12), 677-686.
32. McTigue D. M., Horner P. J., Stokes B. T., and, Gage F. H., (1998) Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18, 5354-5365.
33. Moore S. M., Khalaj A. J., Kumar S., Winchester Z., Yoon J. H., Yoo T., Martinez-Torres L., Yasui N., Katzenellenbogen J. N., and, Tiwari-Woodruff S. K., (2014) Multiple functional therapeutic effects of the estrogen receptor β agonist indazole-Cl in a mouse model of multiple sclerosis. PNAS 111 (50), 18061-18066.
34. Motl R. W., and, Pilutti L. A., (2012) The benefits of exercise training in multiple sclerosis. Nat. Rev. Neurol. 8, 487-497.
35. Motl R. W., Arnett P. A., Smith M. M., Barwick F. H., Ahlstrom B., and, Stover E. J., (2008) Worsening of symptoms is associated with lower physical activity levels in individuals with multiple sclerosis. Mult. Scler. 14, 140-142.
36. Nakamura K., Guo X., Harada C., Mitamura Y., Matsumoto Y., and, Harada T., (2010) Expression of NG2-positive cells during optic neuritis. Jpn. J. Ophthalmol. 54, 100-102.
37. Oh-ishi S., Kizaki T., Toshinai K., Haga S., Fukuda K., Nagata N., and, Ohno H., (1996) Swimming training improves brown-adipose-tissue activity in young and old mice. Mech. Ageing Dev. 89, 67-78.
38. Patel D. I., and, White L. J., (2013) Effect of 10-day forced treadmill training on neurotrophic factors in experimental autoimmune encephalomyelitis. Appl. Physiol. Nutr. Metab. 38, 194-199.
39. Payne S., Bartlett C. A., Savigni D. L., Harvey A. R., Dunlop S. A., and, Fitzgerald M., (2013) Early proliferation does not prevent the loss of oligodendrocyte progenitor cells during chronic phase of secondary degeneration in a CNS white mater tract. PLoS ONE 8, e65710.
40. Pence B. D., and, Woods J. A., (2014) Exercise, obesity, and cutaneous wound healing: evidence from rodent and human studies. Adv. Wound Care 3, 71-79.
41. Popescu B. F., and, Lucchinetti C. F., (2012) Pathology of demyelinating diseases. Annu. Rev. Pathol. 7, 185-217.
42. Recks M. S., Addicks K., and, Kuerten S., (2011) Spinal cord histopathology of MOG peptide 35-55-induced experimental autoimmune encephalomyelitis is time- and score-dependent. Neurosci. Lett. 494, 227-231.
43. Rossi S., Furlan R., De Chiara V., et al,. (2009) Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol. Dis. 36, 51-59.
44. Ruckh J. M., Zhao J. W., Shadrach J. L., van Wijngaarden P., Rao T. N., Wagers A. J., and, Franklin R. J., (2012) Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10, 96-103.
45. Sa M. J., (2012) Physiopathology of symptoms and signs in multiple sclerosis. Arq. Neuropsiquiatr. 70, 733-740.
46. Sánchez A. J., González-Pérez P., Galve-Roperh I., and, García-Merino A., (2006) R-(+)-[2,3-Dihydro-5-methyl-3-(4-morpholinylmethyl)-pyrrolo-[1,2,3-de]-1,4-benzoxazin-6-yl]-1-naphtalenylmethanone (WIN-2) ameliorates experimental autoimmune encephalomyelitis and induces encephalitogenic T cell apoptosis: partial involvement of the CB2 receptor. Biochem. Pharmacol. 72, 1697-1706.
47. Sauer B., Schmalstieg W., and, Howe C., (2013) Axons are injured by antigen-specific CD8 + T cells through a MHC class I-and granzyme B-dependent mechanism. Neurobiol. Dis. 59, 194-205.
48. Shin T., Ahn M., and, Matsumoto Y., (2012) Mechanism of experimental autoimmune encephalomyelitis in Lewis rats: recent insights from macrophages. Anat. Cell Biol. 45, 141-148.
49. Sigwalt A. R., Budde H., Helmich I., et al,. (2011) Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience 192, 661-674.
50. Simon C., Gotz M., and, Dimou L., (2011) Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59, 869-881.
51. Skihar V., Silva C., Chojnacki A., Doring A., Stallcup W. B., Weiss S., and, Yong V. W., (2009) Promoting oligodendrogenesis and myelin repair using the multiple sclerosis medication glatiramer acetate. Proc. Natl Acad. Sci. USA 106, 17992-17997.
52. Sugiura H., Sugiura H., Nishida H., Inaba R., Mirbod S. M., and, Iwata H., (2001) Effects of different durations of exercise on macrophage functions in mice. J. Appl. Physiol. 90, 789-794.
53. Sung C., Chiu C.-Y., Lee E.-J., Bezyak J., Chan F., and, Muller V., (2013) Exercise, diet, and stress management as mediators between functional disability and health-related quality of life in multiple sclerosis. Rehabilitation Counseling Bulletin 56, 85-95.
54. Sypecka J., Sarnowska A., Gadomska-Szabłowska I., Lukomska B., and, Domanska-Janik K., (2013) Differentiation of glia-committed NG2 cells: the role of factors released from hippocampus and spinal cord. Acta Neurobiol. Exp. 73, 116-129.
55. Trapp B. D., Peterson J., Ransohoff R. M., Rudick R., Mork S., and, Bo L., (1998) Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278-285.
56. Wang D., Ayers M. M., Catmull D. V., Hazelwood L. J., Bernard C. C. A., and, Orian J. M., (2005) Astrocyte associated axonal damage in pre onset stages of experimental autoimmune encephalomyelitis. Glia 51, 235-240.
57. Wang J., Song H., Tang X., Yang Y., Vieira V. J., Niu Y., and, Ma Y., (2011) Effect of exercise training intensity on murine T-regulatory cells and vaccination response. Scand. J. Med. Sci. Sports 22, 643-652.
58. Watanabe M., Toyama Y., and, Nishiyama A., (2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J. Neurosci. Res. 69, 826-836.
59. Weigert A., Johann A. M., von Knethen A., Schmidt H., Geisslinger G., and, Brüne B., (2006) Apoptotic cells promote macrophage survival by releasing the antiapoptotic mediator sphingosine-1-phosphate. Blood 108, 1635-1642.
60. Whitacre C. C., Dowdell K., and, Griffin A. C., (1998) Neuroendocrine influences on experimental autoimmune encephalomyelitis. Ann. N. Y. Acad. Sci. 840, 705-716.
61. Zhang F., Wu Y., and, Jia J., (2011a) Exercise preconditioning e brain ischemic tolerance. Neuroscience 177, 170-176.
62. Zhang J., Kramer E. G., Asp L., Dutta D. J., Navrazhina K., Pham T., Mariani J. N., Argaw A. T., Melendez-Vasquez C. V., and, John G. R., (2011b) Promoting myelin repair and return of function in multiple sclerosis. FEBS Lett. 585, 3813-3820.
63. Ziemssen T., and, Ziemssen F., (2005) The role of the humoral immune system in multiple sclerosis (MS) and its animal model experimental autoimmune encephalomyelitis (EAE). Autoimmun. Rev. 4, 460-467.
64. Zipp F., and, Aktas O., (2006) The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci. 29, 518-527.