Regular exercise promotes memory function and enhances hippocampal neuroplasticity in experimental autoimmune encephalomyelitis mice

Neuroscience

Volumn 346, Issue , 2017, Pages 173-181

  Kim, Tae Woon ^a   Sung, Yun Hee ^b  

^a Kyung Hee University Hospital   (South Korea)

^b Kyungnam University   (South Korea)

Author keywords

BDNF; exercise; memory; multiple sclerosis

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; CASPASE 3; DOUBLECORTIN; MYELIN BASIC PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRDU ASSAY; C57BL 6 MOUSE; CELL PROLIFERATION; CONTROLLED STUDY; DEMYELINATION; DENTATE GYRUS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HISTOPATHOLOGY; KINESIOTHERAPY; LATENT PERIOD; MEMORY; MEMORY DISORDER; MENTAL PERFORMANCE; MOUSE; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; STEP-DOWN PASSIVE AVOIDANCE TEST; TUNEL ASSAY; WESTERN BLOTTING; ANIMAL; AVOIDANCE BEHAVIOR; C57BL MOUSE; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; METABOLISM; MYELIN SHEATH; PATHOPHYSIOLOGY; PSYCHOLOGY;

ANIMALS; AVOIDANCE LEARNING; CELL DIFFERENTIATION; CELL PROLIFERATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EXERCISE THERAPY; FEMALE; HIPPOCAMPUS; MEMORY; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; MYELIN SHEATH; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL;

EID: 85011585932     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2017.01.016     Document Type: Article

References (45)

1. Aharoni, R., Arnon, R., Eilam, R., Neurogenesis and neuroprotection induced by peripheral immunomodulatory treatment of experimental autoimmune encephalomyelitis. J Neurosci 25 (2005), 8217–8228.
2. Bernardes, D., Brambilla, R., Bracchi-Ricard, V., Karmally, S., Dellarole, A., Carvalho-Tavares, J., Bethea, J.R., Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis. J Neurochem 136 (2016), 63–73.
3. Biebl, M., Cooper, C.M., Winkler, J., Kuhn, H.G., Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 8 (2000), 17–20.
4. Biegler, R., McGregor, A., Krebs, J.R., Healy, S.D., A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci U S A 98 (2001), 6941–6944.
5. Bruce, J.M., Hancock, L.M., Arnett, P., Lynch, S., Treatment adherence in multiple sclerosis: association with emotional status, personality, and cognition. J Behav Med 33 (2010), 219–227.
6. Chao, F., Zhang, L., Luo, Y., Xiao, Q., Lv, F., He, Q., Zhou, C., Zhang, Y., Jiang, L., Jiang, R., Gu, H., Tang, Y., Running exercise reduces myelinated fiber loss in the dentate gyrus of the hippocampus in APP/PS1 transgenic mice. Curr Alzheimer Res 12 (2015), 377–383.
7. Chiaravalloti, N.D., Genova, H.M., DeLuca, J., Cognitive rehabilitation in multiple sclerosis: the role of plasticity. Front Neurol 6 (2015), 1–10.
8. Chiaravalloti, N.D., DeLuca, J., Cognitive impairment in multiple sclerosis. Lancet Neurol 7 (2008), 1139–1151.
9. Erickson, K.I., Raji, C.A., Lopez, O.L., Becker, J.T., Rosano, C., Newman, A.B., Gach, H.M., Thompson, P.M., Ho, A.J., Kuller, L.H., Physical activity predicts gray matter volume in late adulthood: the Cardiovascular Health Study. Neurology 75 (2010), 1415–1422.
10. Fuchs, E., Gould, E., Mini-review: in vivo neurogenesis in the adult brain: regulation and functional implications. Eur J Neurosci 12 (2000), 2211–2214.
11. Geurts, J.J., Calabrese, M., Fisher, E., Rudick, R.A., Measurement and clinical effect of grey matter pathology in multiple sclerosis. Lancet Neurol 11 (2012), 1082–1092.
12. Giannakopoulou, A., Grigoriadis, N., Bekiari, C., Lourbopoulos, A., Dori, I., Tsingotjidou, A.S., Michaloudi, H., Papadopoulos, G.C., Acute inflammation alters adult hippocampal neurogenesis in a multiple sclerosis mouse model. J Neurosci Res 91 (2013), 890–900.
13. Grant, I., McDonald, W.I., Trimble, M.R., Smith, E., Reed, R., Deficient learning and memory in early and middle phases of multiple sclerosis. J Neurol Neurosurg Psychiatry 47 (1984), 250–255.
14. Gravel, M., Peterson, J., Yong, V.W., Kottis, V., Trapp, B., Braun, P.E., Overexpression of 2',3'-cyclic nucleotide 3'-phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination. Mol Cell Neurosci 7 (1996), 453–466.
15. Grima, D.T., Torrance, G.W., Francis, G., Rice, G., Rosner, A.J., Lafortune, L., Cost and health related quality of life consequences of multiple sclerosis. Mult Scler 6 (2000), 91–98.
16. Horstmann, L., Schmid, H., Heinen, A.P., Kurschus, F.C., Dick, H.B., Joachim, S.C., Inflammatory demyelination induces glia alterations and ganglion cell loss in the retina of an experimental autoimmune encephalomyelitis model. J Neuroinflammation, 10, 2013, 120.
17. Huehnchen, P., Prozorovski, T., Klaissle, P., Lesemann, A., Ingwersen, J., Wolf, S.A., Kupsch, A., Aktas, O., Steiner, B., Modulation of adult hippocampal neurogenesis during myelin-directed autoimmune neuroinflammation. Glia 59 (2011), 132–142.
18. Jin, J.J., Ko, I.G., Kim, S.E., Shin, M.S., Kim, S.H., Jee, Y.S., Swimming exercise ameliorates multiple sclerosis-induced impairment of short-term memory by suppressing apoptosis in the hippocampus of rats. J Exerc Rehabil 30:10 (2014), 69–74.
19. Kim, D.H., Ko, I.G., Kim, B.K., Kim, T.W., Kim, S.E., Shin, M.S., Kim, C.J., Kim, H., Kim, K.M., Baek, S.S., Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav 101 (2010), 655–660.
20. Kim, T.W., Kim, C.S., Kim, J.Y., Kim, C.J., Seo, J.H., Combined exercise ameliorates ovariectomy-induced cognitive impairment by enhancing cell proliferation and suppressing apoptosis. Menopause 23 (2016), 18–26.
21. Laurin, D., Verreault, R., Lindsay, J., MacPherson, K., Rockwood, K., Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol 58 (2001), 498–504.
22. Leavitt, V.M., Cirnigliaro, C., Cohen, A., Farag, A., Brooks, M., Wecht, J.M., Wylie, G.R., Chiaravalloti, N.D., DeLuca, J., Sumowski, J.F., Aerobic exercise increases hippocampal volume and improves memory in multiple sclerosis: preliminary findings. Neurocase 20 (2014), 695–697.
23. Lie, D.C., Song, H., Colamarino, S.A., Ming, G.L., Gage, F.H., Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44 (2004), 399–421.
24. Li, L., Tang, B.L., Environmental enrichment and neurodegenerative diseases. Biochem Biophys Res Commun 334 (2005), 293–297.
25. Magalon, K., Cantarella, C., Monti, G., Cayre, M., Durbec, P., Enriched environment promotes adult neural progenitor cell mobilization in mouse demyelination models. Eur J Neurosci 25 (2007), 761–771.
26. Magavi, S.S., Leavitt, B.R., Macklis, J.D., Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000), 951–955.
27. Mitchell, A.J., Benito-León, J., González, J.M., Rivera-Navarro, J., Quality of life and its assessment in multiple sclerosis: integrating physical and psychological components of wellbeing. Lancet Neurol 4 (2005), 556–566.
28. Nagy, H., Bencsik, K., Rajda, C., Benedek, K., Beniczky, S., Kéri, S., Vécsei, L., The effects of reward and punishment contingencies on decision-making in multiple sclerosis. J Int Neuropsychol Soc 12 (2006), 559–565.
29. Pencea, V., Bingaman, K.D., Wiegand, S.J., Luskin, M.B., Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21 (2001), 6706–6717.
30. Pöttgen, J., Dziobek, I., Reh, S., Heesen, C., Gold, S.M., Impaired social cognition in multiple sclerosis. J Neurol Neurosurg Psychiatry 84 (2013), 523–528.
31. Rivers, L.E., Young, K.M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A., Kessaris, N., Richardson, W.D., PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11 (2008), 1392–1401.
32. Roosendaal, S.D., Moraal, B., Pouwels, P.J., Vrenken, H., Castelijns, J.A., Barkhof, F., Geurts, J.J., Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler 15 (2009), 708–714.
33. Rossi, S., Furlan, R., De Chiara, V., Musella, A., Lo Giudice, T., Mataluni, G., Cavasinni, F., Cantarella, C., Bernardi, G., Muzio, L., Martorana, A., Martino, G., Centonze, D., Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol Dis 36 (2009), 51–59.
34. Sajad, M., Chawla, R., Zargan, J., Umar, S., Sadaqat, M., Khan, H.A., Cytokinetics of adult rat SVZ after EAE. Brain Res 1371 (2011), 140–149.
35. Shanshiashvili, L.V., Kalandadze, I.V., Ramsden, J.J., Mikeladze, D.G., Adhesive properties and inflammatory potential of citrullinated myelin basic protein peptide 45–89. Neurochem Res 37 (2012), 1959–1966.
36. Sicotte, N.L., Kern, K.C., Giesser, B.S., Arshanapalli, A., Schultz, A., Montag, M., Wang, H., Bookheimer, S.Y., Regional hippocampal atrophy in multiple sclerosis. Brain 131 (2008), 1134–1141.
37. Sim, Y.J., Kim, H., Kim, J.Y., Yoon, S.J., Kim, S.S., Chang, H.K., Lee, T.H., Lee, H.H., Shin, M.C., Shin, M.S., Kim, C.J., Long-term treadmill exercise overcomes ischemia-induced apoptotic neuronal cell death in gerbils. Physiol Behav 84 (2005), 733–738.
38. Sung, Y.H., Kim, S.C., Hong, H.P., Park, C.Y., Shin, M.S., Kim, C.J., Seo, J.H., Kim, D.Y., Kim, D.J., Cho, H.J., Treadmill exercise ameliorates dopaminergic neuronal loss through suppressing microglial activation in Parkinson's disease mice. Life Sci 91 (2012), 1309–1316.
39. Stys, P.K., Pathoetiology of multiple sclerosis: are we barking up the wrong tree?. F1000Prime Rep, 5, 2013, 20.
40. Tong, L., Shen, H., Perreau, V.M., Balazs, R., Cotman, C.W., Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol Dis 8 (2001), 1046–1056.
41. Vaynman, S., Gomez-Pinilla, F., License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 19 (2005), 283–295.
42. Vercellino, M., Plano, F., Votta, B., Mutani, R., Giordana, M.T., Cavalla, P., Grey matter pathology in multiple sclerosis. J Neuropathol Exp Neurol 64 (2005), 1101–1107.
43. Winkelmann, A., Engel, C., Apel, A., Zettl, U.K., Cognitive impairment in multiple sclerosis. J Neurol 254 (2007), II35–II42.
44. Zhang, R., Xue, Y.Y., Lu, S.D., Wang, Y., Zhang, L.M., Huang, Y.L., Signore, A.P., Chen, J., Sun, F.Y., Bcl-2 enhances neurogenesis and inhibits apoptosis of newborn neurons in adult rat brain following a transient middle cerebral artery occlusion. Neurobiol Dis 24 (2006), 345–356.
45. Ziehn, M.O., Avedisian, A.A., Tiwari-Woodruff, S., Voskuhl, R.R., Hippocampal CA1 atrophy and synaptic loss during experimental autoimmune encephalomyelitis, EAE. Lab Invest 90 (2010), 774–786.