Treadmill running protects spinal cord contusion from secondary degeneration

Brain Research

Volumn 1346, Issue , 2010, Pages 266-278

  Andrade, Michele Schultz Ramos ^a   Mendonça, Lúcio Mário ^a   Chadi, Gerson ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Neuroplasticity; Neuroprotection; Physical activity; Spinal cord lesion

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; NEUROMODULIN; CD11B ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; CONTUSION; CONVALESCENCE; CYTOKINE PRODUCTION; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; LOCOMOTION; MACROGLIA; MALE; MICRODENSITOMETRY; MICROGLIA; NERVE CELL; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROPROTECTION; NISSL STAINING; NONHUMAN; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SITTING; SPINAL CORD INJURY; STEREOMETRY; TREADMILL EXERCISE; WOUND HEALING; ANIMAL; COMPLICATION; GLIA; IMAGE PROCESSING; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANTIGENS, CD11B; CELL COUNT; FIBROBLAST GROWTH FACTOR 2; GAP-43 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; NERVE DEGENERATION; NEUROGLIA; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; SPINAL CORD INJURIES;

ANIMALIA; RATTUS;

EID: 77955519057     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.05.070     Document Type: Article

References (71)

1. M.S. Andrade, F.R. Hanania, K. Daci, R.J. Leme, and G. Chadi Contuse lesion of the rat spinal cord of moderate intensity leads to a higher time-dependent secondary neurodegeneration than severe one. An open-window for experimental neuroprotective interventions Tissue Cell 40 2008 143 156
2. E.T. Ang, and F. Gomez-Pinilla Potential therapeutic effects of exercise to the brain Curr. Med. Chem. 14 2007 2564 2571
3. E.T. Ang, P.T. Wong, S. Moochhala, and Y.K. Ng Neuroprotection associated with running: is it a result of increased endogenous neurotrophic factors? Neuroscience 118 2003 335 345
4. K.M. Baldwin, and F. Haddad Skeletal muscle plasticity: cellular and molecular responses to altered physical activity paradigms Am. J. Phys. Med. Rehabil. 81 2002 S40 S51
5. D.M. Basso, M.S. Beattie, and J.C. Bresnahan A sensitive and reliable locomotor rating scale for open field testing in rats J. Neurotrauma 12 1995 1 21
6. D.M. Basso, M.S. Beattie, and J.C. Bresnahan Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection Exp. Neurol. 139 1996 244 256
7. D.M. Basso, M.S. Beattie, and J.C. Bresnahan Descending systems contributing to locomotor recovery after mild or moderate spinal cord injury in rats: experimental evidence and a review of literature Restor. Neurol. Neurosci. 20 2002 189 218
8. M.S. Beattie, G.E. Hermann, R.C. Rogers, and J.C. Bresnahan Cell death in models of spinal cord injury Prog. Brain Res. 137 2002 37 47
9. K.R. Bulsara, B.J. Iskandar, A.T. Villavicencio, and J.H. Skene A new millennium for spinal cord regeneration: growth-associated genes Spine 27 2002 1946 1949 (Phila Pa 1976)
10. K.R. Byrnes, and A.I. Faden Role of cell cycle proteins in CNS injury Neurochem. Res. 32 2007 1799 1807
11. B. Calancie, B. Needham-Shropshire, P. Jacobs, K. Willer, G. Zych, and B.A. Green Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man Brain 117 Pt 5 1994 1143 1159
12. S.L. Carlson, M.E. Parrish, J.E. Springer, K. Doty, and L. Dossett Acute inflammatory response in spinal cord following impact injury Exp. Neurol. 151 1998 77 88
13. S.M. Cerutti, and G. Chadi S100 immunoreactivity is increased in reactive astrocytes of the visual pathways following a mechanical lesion of the rat occipital cortex Cell Biol. Int. 24 2000 35 49
14. G. Chadi, and K. Fuxe Analysis of trophic responses in lesioned brain: focus on basic fibroblast growth factor mechanisms Braz. J. Med. Biol. Res. 31 1998 231 241
15. G. Chadi, and V.C. Gomide FGF-2 and S100beta immunoreactivities increase in reactive astrocytes, but not in microglia, in ascending dopamine pathways following a striatal 6-OHDA-induced partial lesion of the nigrostriatal system Cell Biol. Int. 28 2004 849 861
16. G. Chadi, A. Moller, L. Rosen, A.M. Janson, L.A. Agnati, M. Goldstein, S.O. Ogren, R.F. Pettersson, and K. Fuxe Protective actions of human recombinant basic fibroblast growth factor on MPTP-lesioned nigrostriatal dopamine neurons after intraventricular infusion Exp. Brain Res. 97 1993 145 158
17. G. Chadi, L. Rosen, A. Cintra, B. Tinner, M. Zoli, R.F. Pettersson, and K. Fuxe Corticosterone increases FGF-2 (bFGF) immunoreactivity in the substantia nigra of the rat NeuroReport 4 1993 783 786
18. G. Chadi, B. Tinner, L.F. Agnati, and K. Fuxe Basic fibroblast growth factor (bFGF, FGF-2) immunoreactivity exists in the noradrenaline, adrenaline and 5-HT nerve cells of the rat brain Neurosci. Lett. 160 1993 171 176
19. G. Chadi, M.S. Andrade, R.J. Leme, and V.C. Gomide Experimental models of partial lesion of rat spinal cord to investigate neurodegeneration, glial activation, and behavior impairments Int. J. Neurosci. 111 2001 137 165
20. A.M. Choo, J. Liu, M. Dvorak, W. Tetzlaff, and T.R. Oxland Secondary pathology following contusion, dislocation, and distraction spinal cord injuries Exp. Neurol. 212 2008 490 506
21. C.W. Cotman, and N.C. Berchtold Exercise: a behavioral intervention to enhance brain health and plasticity Trends Neurosci. 25 2002 295 301
22. R.D. de Leon, J.A. Hodgson, R.R. Roy, and V.R. Edgerton Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats J. Neurophysiol. 79 1998 1329 1340
23. S. Deforges, J. Branchu, O. Biondi, C. Grondard, C. Pariset, S. Lecolle, P. Lopes, P.P. Vidal, C. Chanoine, and F. Charbonnier Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis J. Physiol. 587 2009 3561 3572
24. J. do Carmo Cunha, B. de Freitas Azevedo Levy, B.A. de Luca, M.S. de Andrade, V.C. Gomide, and G. Chadi Responses of reactive astrocytes containing S100beta protein and fibroblast growth factor-2 in the border and in the adjacent preserved tissue after a contusion injury of the spinal cord in rats: implications for wound repair and neuroregeneration Wound Repair Regen. 15 2007 134 146
25. K.D. Dougherty, C.F. Dreyfus, and I.B. Black Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury Neurobiol. Dis. 7 2000 574 585
26. A. Esclarin-De Ruz, M. Alcobendas-Maestro, R. Casado-Lopez, A. Munoz-Gonzalez, M.A. Florido-Sanchez, and E. Gonzalez-Valdizan A robotic system for gait re-education in patients with an incomplete spinal cord injury Rev. Neurol. 49 2009 617 622
27. J.W. Fawcett, and R.A. Asher The glial scar and central nervous system repair Brain Res. Bull. 49 1999 377 391
28. K. Fouad, G.A. Metz, D. Merkler, V. Dietz, and M.E. Schwab Treadmill training in incomplete spinal cord injured rats Behav. Brain Res. 115 2000 107 113
29. G. Garcia-Alias, E. Verdu, J. Fores, R. Lopez-Vales, and X. Navarro Functional and electrophysiological characterization of photochemical graded spinal cord injury in the rat J. Neurotrauma 20 2003 501 510 (Pubitemid 36617952)
30. D. Giulian, K. Vaca, and M. Corpuz Brain glia release factors with opposing actions upon neuronal survival J. Neurosci. 13 1993 29 37
31. Y. Goldshmit, M.P. Galea, G. Wise, P.F. Bartlett, and A.M. Turnley Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice J. Neurosci. 24 2004 10064 10073
32. Y. Goldshmit, N. Lythgo, M.P. Galea, and A.M. Turnley Treadmill training after spinal cord hemisection in mice promotes axonal sprouting and synapse formation and improves motor recovery J. Neurotrauma 25 2008 449 465
33. F. Gomez-Pinilla, J.W. Lee, and C.W. Cotman Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transection J. Neurosci. 12 1992 345 355
34. F. Gomez-Pinilla, L. Dao, and V. So Physical exercise induces FGF-2 and its mRNA in the hippocampus Brain Res. 764 1997 1 8
35. F. Gomez-Pinilla, Z. Ying, P. Opazo, R.R. Roy, and V.R. Edgerton Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle Eur. J. Neurosci. 13 2001 1078 1084
36. F. Gomez-Pinilla, Z. Ying, R.R. Roy, R. Molteni, and V.R. Edgerton Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity J. Neurophysiol. 88 2002 2187 2195
37. V.C. Gomide, and G. Chadi The trophic factors S-100beta and basic fibroblast growth factor are increased in the forebrain reactive astrocytes of adult callosotomized rat Brain Res. 835 1999 162 174
38. H.J. Gundersen, T.F. Bendtsen, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, and A. Vesterby, et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis APMIS 96 1988 379 394
39. F.P. Guzen, R.J. de Almeida Leme, M.S. de Andrade, B.A. de Luca, and G. Chadi Glial cell line-derived neurotrophic factor added to a sciatic nerve fragment grafted in a spinal cord gap ameliorates motor impairments in rats and increases local axonal growth Restor. Neurol. Neurosci. 27 2009 1 16
40. Helge, J.W., in press. Arm and leg substrate utilization and muscle adaptation after prolonged low-intensity training. Acta Physiol. (Oxf). doi:10.1111/j.17481716.2010.02123.x.
41. S.M. Hsu, L. Raine, and H. Fanger Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures J. Histochem. Cytochem. 29 1981 577 580
42. K.J. Hutchinson, J.K. Linderman, and D.M. Basso Skeletal muscle adaptations following spinal cord contusion injury in rat and the relationship to locomotor function: a time course study J. Neurotrauma 18 2001 1075 1089
43. K.J. Hutchinson, F. Gomez-Pinilla, M.J. Crowe, Z. Ying, and D.M. Basso Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats Brain 127 2004 1403 1414
44. E. Jankowska, and S. Edgley Interactions between pathways controlling posture and gait at the level of spinal interneurones in the cat Prog. Brain Res. 97 1993 161 171
45. R.J. Leme, and G. Chadi Distant microglial and astroglial activation secondary to experimental spinal cord lesion Arq. Neuropsiquiatr. 59 2001 483 492
46. R.G. Lovely, R.J. Gregor, R.R. Roy, and V.R. Edgerton Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat Exp. Neurol. 92 1986 421 435
47. B. Lu BDNF and activity-dependent synaptic modulation Learn. Mem. 10 2003 86 98
48. F. Madiai, S.R. Hussain, V.M. Goettl, R.W. Burry, R.L. Stephens Jr., and K.V. Hackshaw Upregulation of FGF-2 in reactive spinal cord astrocytes following unilateral lumbar spinal nerve ligation Exp. Brain Res. 148 2003 366 376
49. S.A. Neeper, F. Gomez-Pinilla, J. Choi, and C. Cotman Exercise and brain neurotrophins Nature 373 1995 109
50. S.A. Neeper, F. Gomez-Pinilla, J. Choi, and C.W. Cotman Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain Brain Res. 726 1996 49 56
51. H. Nishimaru, and N. Kudo Formation of the central pattern generator for locomotion in the rat and mouse Brain Res. Bull. 53 2000 661 669
52. L.J. Noble, and J.R. Wrathall Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord Exp. Neurol. 88 1985 135 149
53. A. Parachikova, K.E. Nichol, and C.W. Cotman Short-term exercise in aged Tg2576 mice alters neuroinflammation and improves cognition Neurobiol. Dis. 30 2008 121 129
54. M. Ramsden, N.C. Berchtold, J. Patrick Kesslak, C.W. Cotman, and C.J. Pike Exercise increases the vulnerability of rat hippocampal neurons to kainate lesion Brain Res. 971 2003 239 244
55. G.A. Robinson, and M.E. Goldberger The development and recovery of motor function in spinal cats. II. Pharmacological enhancement of recovery Exp. Brain Res. 62 1986 387 400
56. R.W. Rodrigues, V.C. Gomide, and G. Chadi Astroglial and microglial reaction after a partial nigrostriatal degeneration induced by the striatal injection of different doses of 6-hydroxydopamine Int. J. Neurosci. 109 2001 91 126
57. S. Rojas Vega, T. Abel, R. Lindschulten, W. Hollmann, W. Bloch, and H.K. Struder Impact of exercise on neuroplasticity-related proteins in spinal cord injured humans Neuroscience 153 2008 1064 1070
58. C.R. Rose, R. Blum, K.W. Kafitz, Y. Kovalchuk, and A. Konnerth From modulator to mediator: rapid effects of BDNF on ion channels Bioessays 26 2004 1185 1194
59. H.R. Sandrow-Feinberg, V. Zhukareva, L. Santi, K. Miller, J.S. Shumsky, D.P. Baker, and J.D. Houle PEGylated interferon-beta modulates the acute inflammatory response and recovery when combined with forced exercise following cervical spinal contusion injury Exp. Neurol. 23 2010 439 451
60. K. Satake, Y. Matsuyama, M. Kamiya, H. Kawakami, H. Iwata, K. Adachi, and K. Kiuchi Up-regulation of glial cell line-derived neurotrophic factor (GDNF) following traumatic spinal cord injury NeuroReport 11 2000 3877 3881
61. M.E. Schwab Structural plasticity of the adult CNS. Negative control by neurite growth inhibitory signals Int. J. Dev. Neurosci. 14 1996 379 385
62. J.H. Skene Axonal growth-associated proteins Annu. Rev. Neurosci. 12 1989 127 156
63. J.H. Skene, and M. Willard Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems J. Cell Biol. 89 1981 96 103
64. M. Skup, J. Czarkowska-Bauch, A. Dwornik, M. Macias, D. Sulejczak, and M. Wiater Locomotion induces changes in Trk B receptors in small diameter cells of the spinal cord Acta Neurobiol. Exp. 60 2000 371 (Wars)
65. C. Smith, M. Berry, W.E. Clarke, and A. Logan Differential expression of fibroblast growth factor-2 and fibroblast growth factor receptor 1 in a scarring and nonscarring model of CNS injury in the rat Eur. J. Neurosci. 13 2001 443 456
66. H. Thoenen Neurotrophins and neuronal plasticity Science 270 1995 593 598
67. R.B. Tripathi, and D.M. McTigue Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats J. Comp. Neurol. 510 2008 129 144
68. M.J. West, and H.J. Gundersen Unbiased stereological estimation of the number of neurons in the human hippocampus J. Comp. Neurol. 296 1990 1 22
69. U. Wilhelmsson, L. Li, M. Pekna, C.H. Berthold, S. Blom, C. Eliasson, O. Renner, E. Bushong, M. Ellisman, T.E. Morgan, and M. Pekny Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration J. Neurosci. 24 2004 5016 5021
70. W. Young, J. Kume-Kick, and S. Constantini Glucocorticoid therapy of spinal cord injury Ann. N.Y. Acad. Sci. 743 1994 241 263 discussion 263-5
71. Y. Zhang, S.R. Ji, C.Y. Wu, X.H. Fan, H.J. Zhou, and G.L. Liu Observation of locomotor functional recovery in adult complete spinal rats with BWSTT using semiquantitative and qualitative methods Spinal Cord 45 2007 496 501