Differential patterns of inflammatory response, axonal damage and myelin impairment following excitotoxic or ischemic damage to the trigeminal spinal nucleus of adult rats

Brain Research

Volumn 1172, Issue 1, 2007, Pages 130-144

  Dos Santos, C D ^a   Picanco Diniz C W ^a   Gomes Leal, W ^a  

^a Biological Sciences Center   (Brazil)

Author keywords

Brain stem; Endothelin 1; Macrophages; Neutrophils; NMDA; Trigeminal system

Indexed keywords

ENDOTHELIN 1; MYELIN; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; BRAIN ISCHEMIA; BRAIN STEM; CONTROLLED STUDY; EXCITOTOXICITY; GRAY MATTER; HISTOPATHOLOGY; INFLAMMATION; MACROPHAGE; MALE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; TISSUE INJURY; TRIGEMINAL NUCLEUS; WHITE MATTER;

AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; AXONS; BRAIN ISCHEMIA; CELL COUNT; DEMYELINATING DISEASES; ECTODYSPLASINS; ENDOTHELIN-1; INFLAMMATION; MALE; MYELIN BASIC PROTEINS; N-METHYLASPARTATE; NEUROTOXINS; RATS; RATS, WISTAR; TIME FACTORS; TRIGEMINAL NUCLEUS, SPINAL;

RATTUS;

EID: 34548688928     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.07.037     Document Type: Article

References (71)

1. Aarum J., Sandberg K., Haeberlein S.L., and Persson M.A. Migration and differentiation of neural precursor cells can be directed by microglia. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15983-15988
2. Ayres, M., 2005. Biostat 4.0, 4th edn., Sociedade Civil Mamirauá/MCT/CNPQ. Imprensa Oficial do Estado do Pará, Belém, 65 pp.
3. Backonja M.M. Anticonvulsants (antineuropathics) for neuropathic pain syndromes. Clin. J. Pain 16 (2000) S67-S72
4. Bereiter D.A., and Bereiter D.F. Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to the TMJ region. Pain 85 (2000) 65-77
5. Bereiter D.A., Hirata H., and Hu J.W. Trigeminal subnucleus caudalis: beyond homologies with the spinal dorsal horn. Pain 88 (2000) 221-224
6. Beschorner R., Dietz K., Schauer N., Mittelbronn M., Schluesener H.J., Trautmann K., Meyermann R., and Simon P. Expression of EAAT1 reflects a possible neuroprotective function of reactive astrocytes and activated microglia following human traumatic brain injury. Histol. Histopathol. 22 (2007) 515-526
7. Beschorner R., Simon P., Schauer N., Mittelbronn M., Schluesener H.J., Trautmann K., Dietz K., and Meyermann R. Reactive astrocytes and activated microglial cells express EAAT1, but not EAAT2, reflecting a neuroprotective potential following ischaemia. Histopathology 50 (2007) 897-910
8. 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
9. Boloori A.R., and Stanley G.B. The dynamics of spatiotemporal response integration in the somatosensory cortex of the vibrissa system. J. Neurosci. 26 (2006) 3767-3782
10. Bolton S.J., and Perry V.H. Differential blood-brain barrier breakdown and leucocyte recruitment following excitotoxic lesions in juvenile and adult rats. Exp. Neurol. 154 (1998) 231-240
11. Choi D.W. Excitotoxic cell death. J. Neurobiol. 23 (1992) 1261-1276
12. Dawson D.A., Graham D.I., McCulloch J., and Macrae I.M. Anti-ischaemic efficacy of a nitric oxide synthase inhibitor and a N-methyl-d-aspartate receptor antagonist in models of transient and permanent focal cerebral ischaemia. Br. J. Pharmacol. 113 (1994) 247-253
13. Esiri M.M. The interplay between inflammation and neurodegeneration in CNS disease. J. Neuroimmunol. 184 (2007) 4-16
14. Ferguson B., Matyszak M.K., Esiri M.M., and Perry V.H. Axonal damage in acute multiple sclerosis lesions. Brain 120 Pt 3 (1997) 393-939
15. Frost S.B., Barbay S., Mumert M.L., Stowe A.M., and Nudo R.J. An animal model of capsular infarct: endothelin-1 injections in the rat. Behav. Brain Res. 169 (2006) 206-211
16. Gentleman S.M., Nash M.J., Sweeting C.J., Graham D.I., and Roberts G.W. Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci. Lett. 160 (1993) 139-144
17. Gomes-Leal W., Corkill D.J., Freire M.A., Picanco-Diniz C.W., and Perry V.H. Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp. Neurol. 190 (2004) 456-467
18. 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
19. Graham D.I., Raghupathi R., Saatman K.E., Meaney D., and McIntosh T.K. Tissue tears in the white matter after lateral fluid percussion brain injury in the rat: relevance to human brain injury. Acta Neuropathol. 99 (2000) 117-124
20. Gupta Y.K., Briyal S., Sharma U., Jagannathan N.R., and Gulati A. Effect of endothelin antagonist (TAK-044) on cerebral ischemic volume, oxidative stress markers and neurobehavioral parameters in the middle cerebral artery occlusion model of stroke in rats. Life Sci. 77 (2005) 15-27
21. Hendriks J.J., Teunissen C.E., de Vries H.E., and Dijkstra C.D. Macrophages and neurodegeneration. Brain Res. Rev. 48 (2005) 185-195
22. Hicks C.A., Ward M.A., and O'Neill M.J. Neuroprotective effects of the neuronal Ca(2+) channel blockers, LY042826 and LY393615 in vivo. Eur. J. Pharmacol. 408 (2000) 241-248
23. Hughes P.M., Anthony D.C., Ruddin M., Botham M.S., Rankine E.L., Sablone M., Baumann D., Mir A.K., and Perry V.H. Focal lesions in the rat central nervous system induced by endothelin-1. J. Neuropathol. Exp. Neurol. 62 (2003) 1276-1286
24. Jensen T.S. Anticonvulsants in neuropathic pain: rationale and clinical evidence. Eur. J. Pain 6 Suppl A (2002) 61-68
25. Kanellopoulos G.K., Xu X.M., Hsu C.Y., Lu X., Sundt T.M., and Kouchoukos N.T. White matter injury in spinal cord ischemia: protection by AMPA/kainate glutamate receptor antagonism. Stroke 31 (2000) 1945-1952
26. Lazarov N.E. Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog. Neurobiol. 66 (2002) 19-59
27. Lewis S.B., Finnie J.W., Blumbergs P.C., Scott G., Manavis J., Brown C., Reilly P.L., Jones N.R., and McLean A.J. A head impact model of early axonal injury in the sheep. J. Neurotrauma 13 (1996) 505-514
28. Li G.L., Farooque M., Holtz A., and Olsson Y. Changes of beta-amyloid precursor protein after compression trauma to the spinal cord: an experimental study in the rat using immunohistochemistry. J. Neurotrauma 12 (1995) 269-277
29. Li S., Mealing G.A., Morley P., and Stys P.K. Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport. J. Neurosci. 19 (1999) RC16
30. Li S., Jiang Q., and Stys P.K. Important role of reverse Na(+)-Ca(2+) exchange in spinal cord white matter injury at physiological temperature. J. Neurophysiol. 84 (2000) 1116-1119
31. Lipton S.A. The molecular basis of memantine action in Alzheimer's disease and other neurologic disorders: low-affinity, uncompetitive antagonism. Curr. Alzheimer Res. 2 (2005) 155-165
32. Love S. Oxidative stress in brain ischemia. Brain Pathol. 9 (1999) 119-131
33. Masaki T., and Yanagisawa M. Endothelins. Essays Biochem. 27 (1992) 79-89
34. McKenzie K.J., McLellan D.R., Gentleman S.M., Maxwell W.L., Gennarelli T.A., and Graham D.I. Is beta-APP a marker of axonal damage in short-surviving head injury?. Acta Neuropathol. 92 (1996) 608-613
35. Medana I.M., and Esiri M.M. Axonal damage: a key predictor of outcome in human CNS diseases. Brain 126 (2003) 515-530
36. Medana I.M., Day N.P., Hien T.T., Mai N.T., Bethell D., Phu N.H., Farrar J., Esiri M.M., White N.J., and Turner G.D. Axonal injury in cerebral malaria. Am. J. Pathol. 160 (2002) 655-666
37. Meldrum B.S. Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr. 130 (2000) 1007S-1015S
38. Mergenthaler P., Dirnagl U., and Meisel A. Pathophysiology of stroke: lessons from animal models. Metab. Brain Dis. 19 (2004) 151-167
39. Minghetti L. Role of inflammation in neurodegenerative diseases. Curr. Opin. Neurol. 18 (2005) 315-321
40. Mitsios N., Gaffney J., Kumar P., Krupinski J., Kumar S., and Slevin M. Pathophysiology of acute ischaemic stroke: an analysis of common signalling mechanisms and identification of new molecular targets. Pathobiology 73 (2006) 159-175
41. Mosinger J.L., Price M.T., Bai H.Y., Xiao H., Wozniak D.F., and Olney J.W. Blockade of both NMDA and non-NMDA receptors is required for optimal protection against ischemic neuronal degeneration in the in vivo adult mammalian retina. Exp. Neurol. 113 (1991) 10-17
42. Motte S., McEntee K., and Naeije R. Endothelin receptor antagonists. Pharmacol. Ther. 110 (2006) 386-414
43. Moyanova S.G., Kortenska L.V., Mitreva R.G., Pashova V.D., Ngomba R.T., and Nicoletti F. Multimodal assessment of neuroprotection applied to the use of MK-801 in the endothelin-1 model of transient focal brain ischemia. Brain Res. 1153 (2007) 58-67
44. Najimi M., Maloteaux J.M., and Hermans E. Pertussis toxin-sensitive modulation of glutamate transport by endothelin-1 type A receptors in glioma cells. Biochim. Biophys. Acta 1668 (2005) 195-202
45. Neumann J., Gunzer M., Gutzeit H.O., Ullrich O., Reymann K.G., and Dinkel K. Microglia provide neuroprotection after ischemia. FASEB J. 20 (2006) 714-716
46. Pantoni L., Garcia J.H., and Gutierrez J.A. Cerebral white matter is highly vulnerable to ischemia. Stroke 27 (1996) 1641-1646
47. Petty M.A., and Wettstein J.G. White matter ischaemia. Brain Res. Rev. 31 (1999) 58-64
48. Popovich P.G., Guan Z., Wei P., Huitinga I., van Rooijen N., and Stokes B.T. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158 (1999) 351-365
49. Popovich P.G., Guan Z., McGaughy V., Fisher L., Hickey W.F., and Basso D.M. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J. Neuropathol. Exp. Neurol. 61 (2002) 623-633
50. Portera-Cailliau C., Price D.L., and Martin L.J. Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J. Comp. Neurol. 378 (1997) 88-104
51. Robinson A.P., White T.M., and Mason D.W. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57 (1986) 239-247
52. Rubanyi G.M., and Polokoff M.A. Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev. 46 (1994) 325-415
53. Schnell L., Fearn S., Klassen H., Schwab M.E., and Perry V.H. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 11 (1999) 3648-3658
54. Schroeter M., Jander S., Witte O.W., and Stoll G. Local immune responses in the rat cerebral cortex after middle cerebral artery occlusion. J. Neuroimmunol. 55 (1994) 195-203
55. Schroeter M., Jander S., Huitinga I., Witte O.W., and Stoll G. Phagocytic response in photochemically induced infarction of rat cerebral cortex. The role of resident microglia. Stroke 28 (1997) 382-386
56. Schwartz M., Butovsky O., Bruck W., and Hanisch U.K. Microglial phenotype: is the commitment reversible?. Trends Neurosci. 29 (2006) 68-74
57. Sims N.R., and Anderson M.F. Mitochondrial contributions to tissue damage in stroke. Neurochem. Int. 40 (2002) 511-526
58. Sripati A.P., Yoshioka T., Denchev P., Hsiao S.S., and Johnson K.O. Spatiotemporal receptive fields of peripheral afferents and cortical area 3b and 1 neurons in the primate somatosensory system. J. Neurosci. 26 (2006) 2101-2114
59. Stokely M.E., Yorio T., and King M.A. Endothelin-1 modulates anterograde fast axonal transport in the central nervous system. J. Neurosci. Res. 79 (2005) 598-607
60. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., and Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338 (1998) 278-285
61. Trapp B.D., Ransohoff R., and Rudick R. Axonal pathology in multiple sclerosis: relationship to neurologic disability. Curr. Opin. Neurol. 12 (1999) 295-302
62. Uziel D., Garcez P., Lent R., Peuckert C., Niehage R., Weth F., and Bolz J. Connecting thalamus and cortex: the role of ephrins. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288 (2006) 135-142
63. Vos B.P., Strassman A.M., and Maciewicz R.J. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J. Neurosci. 14 (1994) 2708-2723
64. Wang Q., Tang X.N., and Yenari M.A. The inflammatory response in stroke. J. Neuroimmunol. 184 (2007) 53-68
65. Windle V., Szymanska A., Granter-Button S., White C., Buist R., Peeling J., and Corbett D. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp. Neurol. 201 (2006) 324-334
66. Yam P.S., Patterson J., Graham D.I., Takasago T., Dewar D., and McCulloch J. Topographical and quantitative assessment of white matter injury following a focal ischaemic lesion in the rat brain. Brain Res. 2 (1998) 315-322
67. Yanagisawa M., and Masaki T. Endothelin, a novel endothelium-derived peptide. Pharmacological activities, regulation and possible roles in cardiovascular control. Biochem. Pharmacol. 38 (1989) 1877-1883
68. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., and Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332 (1988) 411-415
69. Yrjanheikki J., Tikka T., Keinanen R., Goldsteins G., Chan P.H., and Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13496-13500
70. Zhang Z., Krebs C.J., and Guth L. Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143 (1997) 141-152
71. Ziccardi V.B., Braun T.W., and Ochs M.W. Trigeminal neuralgia: review of etiologies and treatments. Compendium 14 1256 (1993) 1258-1262