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 and Cell

Volumn 40, Issue 2, 2008, Pages 143-156

  Andrade, M S R ^a   Hanania, F R ^a   Daci, K ^a   Leme, R J A ^a   Chadi, G ^a  

^a Neuroregeneration Center   (Brazil)

Author keywords

Astrocyte; Microglia; NYU Impactor; Secondary degeneration; Spinal cord injury; Stereological quantification

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CONTUSION; DENSITOMETRY; DISEASE SEVERITY; GLIA CELL; GRAY MATTER; IMAGE ANALYSIS; LAMINECTOMY; MACROGLIA; MALE; MICROGLIA; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NISSL STAINING; NONHUMAN; RAT; SPINAL CORD LESION; WHITE MATTER;

ANIMALIA; RATTUS; WALLERIA;

EID: 39749089312     PISSN: 00408166     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tice.2007.11.002     Document Type: Article

References (68)

1. Abe Y., Yamamoto T., Sugiyama Y., Watanabe T., Saito N., Kayama H., and Kumagai T. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J. Neurotrauma 16 (1999) 945-952
2. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., and Popovich P.G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23 (2006) 635-659
3. Beattie M.S., Bresnahan J.C., Komon J., Tovar C.A., Van M.M., Anderson D.K., Faden A.I., Hsu C.Y., Noble L.J., Salzman S., and Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148 (1997) 453-463
4. Beattie M.S., Farooqui A.A., and Bresnahan J.C. Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 17 (2000) 915-925
5. Blight A.R. Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience 60 (1994) 263-273
6. Brandoli C., Shi B., Pflug B., Andrews P., Wrathall J.R., and Mocchetti I. Dexamethasone reduces the expression of p75 neurotrophin receptor and apoptosis in contused spinal cord. Brain Res. Mol. Brain Res. 87 (2001) 61-70
7. Byrnes K.R., Garay J., Di Giovanni S., De Biase A., Knoblach S.M., Hoffman E.P., Movsesyan V., and Faden A.I. Expression of two temporally distinct microglia-related gene clusters after spinal cord injury. Glia 53 (2006) 420-433
8. Carlson S.L., Parrish M.E., Springer J.E., Doty K., and Dossett L. Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 151 (1998) 77-88
9. Cerutti S.M., and Chadi G. 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
10. Chadi G., Andrade M.S., Leme R.J., and Gomide V.C. Experimental models of partial lesion of rat spinal cord to investigate neurodegeneration, glial activation, and behavior impairments. Int. J. Neurosci. 111 3-4 (2001) 137-165
11. Chadi G., Moller A., Rosen L., Janson A.M., Agnati L.A., Goldstein M., Ogren S.O., Pettersson R.F., and Fuxe K. 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
12. Chadi G., Tinner B., Agnati L.F., and Fuxe K. 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
13. Chu G.K., Yu W., and Fehlings M.G. The p75 neurotrophin receptor is essential for neuronal cell survival and improvement of functional recovery after spinal cord injury. Neuroscience 148 (2007) 668-682
14. Constantini S., and Young W. The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. Neurosurgery 80 (1994) 97-111
15. Do Carmo Cunha J., de Freitas Azevedo Levy B., de Luca B.A., de Andrade M.S., Gomide V.C., and Chadi G. 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
16. Davies S.J., Field P.M., and Raisman G. Regeneration of cut adult axons fails even in the presence of continuous aligned glial pathways. Exp. Neurol. 142 (1996) 203-216
17. Dougherty K.D., Dreyfus C.F., and Black I.B. Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol. Dis. (2000) 574-585
18. Dumont R.J., Okonkwo D.O., Verma S., Hurlbert R.J., Boulos P.T., Ellegala D.B., and Dumont A.S. Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin. Neuropharmacol. 24 (2001) 254-264
19. Dusart I., and Schwab M.E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6 (1994) 712-724
20. Elkabes S., DiCicco-Bloom E.M., and Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci. 16 (1996) 2508-2521
21. Ferguson I.A., Koide T., and Rush R.A. Stimulation of corticospinal tract regeneration in the chronically injured spinal cord. Eur. J. Neurosci. 13 (2001) 1059-1064
22. Fitch M.T., Doller C., Combs C.K., Landreth G.E., and Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J. Neurosci. 19 (1999) 8182-8198
23. Gale K., Kerasidis H., and Wrathall J.R. Spinal cord contusion in the rat: behavioral analysis of functional neurologic impairment. Exp. Neurol. 88 (1985) 123-134
24. Giulian D., and Baker T.J. Peptides released by ameboid microglia regulate astroglial proliferation. J. Cell Biol. 101 (1985) 2411-2415
25. Giulian D., Vaca K., and Corpuz M. Brain glia release factors with opposing actions upon neuronal survival. J. Neurosci. 13 (1993) 29-37
26. Gomes-Leal W., Corkill D.J., and Picanco-Diniz C.W. Systematic analysis of axonal damage and inflammatory response in different white matter tracts of acutely injured rat spinal cord. Brain Res. 1066 (2005) 57-70
27. Gomide V.C., and Chadi G. 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
28. Gomide V., Bibancos T., and Chadi G. Dopamine cell morphology and glial cell hypertrophy and process branching in the nigrostriatal system after striatal 6-OHDA analyzed by specific sterological tools. Int. J. Neurosci. 115 (2005) 557-582
29. Gomide V.C., and Chadi G. Prenatal ethanol enhances rotational behavior to apomorphine in the 24-month-old rat offspring with small striatal lesion. Neurotoxicol. Teratol. 26 (2004) 417-427
30. Gomide V., and Chadi G. Glial bFGF and S100 immunoreactivities increase in ascending dopamine pathways following striatal 6-OHDA-induced partial lesion of the nigrostriatal system: a sterological analysis. Int. J. Neurosci. 115 (2005) 537-555
31. Grewal R.P., Morgan T.E., and Finch C.E. C1qB and clusterin mRNA increase in association with neurodegeneration in sporadic amyotrophic lateral sclerosis. Neurosci. Lett. 271 (1999) 65-67
32. Grossman S.D., Rosenberg L.J., and Wrathall J.R. Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp. Neurol. 168 (2001) 273-282
33. Gruner J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9 (1992) 123-126
34. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988) 857-881
35. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96 (1988) 379-394
36. Hama A., and Sagen J. Behavioral characterization and effect of clinical drugs in a rat model of pain following spinal cord compression. Brain Res. 1185 (2007) 117-128
37. Hill C.E., Beattie M.S., and Bresnahan J.C. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 171 (2001) 153-169
38. Leme R.J., and Chadi G. Distant microglial and astroglial activation secondary to experimental spinal cord lesion. Arq. Neuropsiquiatr. 59 (2001) 483-492
39. Li Y., and Raisman G. Sprouts from cut corticospinal axons persist in the presence of astrocytic scarring in long-term lesions of the adult rat spinal cord. Exp. Neurol. 134 (1995) 102-111
40. Longbrake E.E., Lai W., Ankeny D.P., and Popovich P.G. Characterization and modeling of monocyte-derived macrophages after spinal cord injury. J. Neurochem. 102 (2007) 1083-1094
41. McMillian M.K., Thai L., Hong J.S., O'Callaghan J.P., and Pennypacker K.R. Brain injury in a dish: a model for reactive gliosis. Trends Neurosci. 17 (1994) 138-142
42. Mueller C.A., Schluesener H.J., Conrad S., Pietsch T., and Schwab J.M. Spinal cord injury-induced expression of the immune-regulatory chemokine interleukin-16 caused by activated microglia/macrophages and CD8+ cells. J. Neurosurg. Spine 4 (2006) 233-240
43. Noble L.J., and Wrathall J.R. Correlative analyses of lesion development and functional status after graded spinal cord contusive injuries in the rat. Exp. Neurol. 103 (1989) 34-40
44. Nystrom B., and Berglund J.E. Spinal cord restitution following compression injuries in rats. Acta Neurol. Scand. 78 (1988) 467-472
45. Oudega M., and Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 818 (1999) 431-438
46. Pineau I., and Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: multiphasic expression pattern and identification of the cell types involved. J. Comp. Neurol. 500 (2007) 267-285
47. Popovich P.G., Guan Z., Wei P., Huitinga I., Rooijen N.V., and Stokes B.T. Depletion of hematogenous macrophages promotes parcial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158 (1999) 351-365
48. Prewitt C.M., Niesman I.R., Kane C.J., and Houle J.D. Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp. Neurol. 148 (1997) 433-443
49. Rabchevsky A.G., Fugaccia I., Fletcher-Turner A., Blades D.A., Mattson M.P., and Scheff S.W. Basic fibroblast growth factor (bFGF) enhances tissue sparing and functional recovery following moderate spinal cord injury. J. Neurotrauma 16 (1999) 817-830
50. Rabchevsky A.G., Fugaccia I., Turner A.F., Blades D.A., Mattson M., and Scheff S.W. Basic fibroblast growth factor (bFGF) enhances functional recovery following severe spinal cord injury to the rat. Exp. Neurol. 164 (2000) 280-291
51. Rabchevsky A.G., Sullivan P.G., and Scheff S.W. Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55 (2007) 831-843
52. Reichert F., and Rotshenker S. Galectin-3/MAC-2 in experimental allergic encephalomyelitis. Exp. Neurol. 160 (1999) 508-514
53. Rodrigues R.W., Gomide V.C., and Chadi G. 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
54. Rosenberg L.J., and Wrathall J.R. Quantitative analysis of acute axonal pathology in experimental spinal cord contusion. J. Neurotrauma 14 (1997) 823-838
55. Rosenberg L.J., Zai L.J., and Wrathall J.R. Chronic alterations in the cellular composition of spinal cord white matter following contusion injury. Glia 49 (2005) 107-120
56. Satake K., Matsuyama Y., Kamiya M., Kawakami H., Iwata H., Adachi K., and Kiuchi K. Up-regulation of glial cell line-derived neurotrophic factor (GDNF) following traumatic spinal cord injury. Neuroreport 11 (2000) 3877-3881
57. Shuman S.L., Bresnahan J.C., and Beattie M.S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50 (1997) 798-808
58. Silva V.A., Gomide V.C., and Chadi G. Fibroblast growth factor-2 immunoreactivity is present in the central and peripheral auditory pathways of adult rats. J. Morphol. 265 (2005) 141-151
59. Stichel C.C., and Muller H.W. The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res. 294 (1998) 1-9
60. Stokes B.T., Noyes D.H., and Behrmann D.L. An electromechanical spinal injury technique with dynamic sensitivity. J. Neurotrauma 9 (1992) 187-195
61. Tian D.S., Xie M.J., Yu Z.Y., Zhang Q., Wang Y.H., Chen B., Chen C., and Wang W. Cell cycle inhibition attenuates microglia induced inflammatory response and alleviates neuronal cell death after spinal cord injury in rats. Brain Res. 1135 (2007) 177-185
62. Von Euler M., Li-Li M., Whittemore S., Seiger A., and Sundström E. No protective effect of the NMDA antagonist memantine in experimental spinal cord injuries. J. Neurotrauma 14 (1997) 53-61
63. Warden P., Bamber N.I., Li H., Esposito A., Ahmad K.A., Hsu C.Y., and Xu X.M. Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp. Neurol. 168 (2001) 213-224
64. West M.J., and Gundersen H.J. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990) 21-22
65. Wilkin G.P., Marriott D.R., and Cholewinski A.J. Astrocyte heterogeneity. Trends Neurosci. 13 (1990) 43-46
66. Widenfalk J., Lipson A., Jubran M., Hofstetter C., Ebendal T., Cao Y., and Olson L. Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 120 (2003) 951-960
67. Wrathall J.R., Pettegrew R.K., and Harvey F. Spinal cord contusion in the rat: production of graded, reproducible, injury groups. Exp. Neurol. 88 (1985) 108-122
68. Young W. Spinal cord contusion models. Prog. Brain Res. 137 (2002) 231-255