A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis

Brain Research Reviews

Volumn 47, Issue 1-3, 2004, Pages 263-274

  Barbeito, Luis H ^a   Pehar, Mariana ^a,b   Cassina, Patricia ^b   Vargas, Marcelo R ^a   Peluffo, Hugo ^b   Viera, Liliana ^c   Estévez, Alvaro G ^c   Beckman, Joseph S ^d  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d OREGON STATE UNIVERSITY   (United States)

Author keywords

Amyotrophic lateral sclerosis; Astrocytes; Disorders of the nervous system; Motor neurons; Neuromuscular diseases; Nitric oxide; Peroxynitrite

Indexed keywords

CYCLOOXYGENASE 2; FAS LIGAND; GLUTAMATE TRANSPORTER; NERVE GROWTH FACTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; ASTROCYTE; CELL CULTURE; CELL FUNCTION; CELL LOSS; CONFERENCE PAPER; CYTOKINE PRODUCTION; DOWN REGULATION; HUMAN; IMMUNOREACTIVITY; MITOCHONDRIAL TOXICITY; MITOCHONDRION; MOTONEURON; NERVE FIBER TRANSECTION; NERVE INJURY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; ASTROCYTES; CELL COMMUNICATION; GLIOSIS; GLUTAMIC ACID; HUMANS; INFLAMMATION MEDIATORS; MOTOR NEURONS;

EID: 9644255989     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2004.05.003     Document Type: Conference Paper

References (141)

1. Abe K., Pan L.H., Watanabe M., Konno H., Kato T., Itoyama Y. Upregulation of protein tyrosine nitration in the anterior horn cells of amyotrophic lateral sclerosis. Neurol. Res. 19:1997;124-128
2. Alexianu M.E., Kozovska M., Appel S.H. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 57:2001;1282-1289
3. Almer G., Vukosavic S., Romero N., Przedborski S. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 72:1999;2415-2425
4. Ang L.C., Bhaumick B., Juurlink B.H.J. Neurite promoting activity of insulin, insulin-like growth factor I and nerve growth factor on spinal motoneurons is astrocyte dependent. Dev. Brain Res. 74:1993;83-88
5. Anneser J.M., Cookson M.R., Ince P.G., Shaw P.J., Borasio G.D. Glial cells of the spinal cord and subcortical white matter up-regulate neuronal nitric oxide synthase in sporadic amyotrophic lateral sclerosis. Exp. Neurol. 171:2001;418-421
6. Bai G., Lipton S.A. Aberrant RNA splicing in sporadic amyotrophic lateral sclerosis. Neuron. 20:1998;363-366
7. Barrett G.L., Bartlett P.F. The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development. Proc. Natl. Acad. Sci. U. S. A. 91:1994;6501-6505
8. Beal M.F., Ferrante L.J., Browne S.E., Matthews R.T., Kowall N.W., Brown R.H. Jr. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann. Neurol. 42:1997;644-654
9. Becher B., Barker P.A., Owens T., Antel J.P. CD95-CD95L: can the brain learn from the immune system? Trends Neurosci. 21:1998;114-117
10. Beckman J.S., Ischiropoulos H., Zhu L., van der Woerd M., Smith C.D., Chen J., Harrison J., Martin J.C., Tsai M. Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298:1992;438-445
11. Beckman J.S., Chen J., Ischiropoulos H., Crow J.P. Oxidative chemistry of peroxynitrite. Methods Enzymol. 233:1994;229-240
12. Beckman J.S., Estévez A.G., Crow J.P., Barbeito L. Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci. 24:2001;S15-S20
13. Bezzi P., Volterra A. A neuron-glia signalling network in the active brain. Curr. Opin. Neurobiol. 11:2001;387-394
14. Blanc E.M., Keller J.N., Fernandez S., Mattson M.P. 4-hydroxynonenal, a lipid peroxidation product, impairs glutamate transport in cortical astrocytes. Glia. 22:1998;149-160
15. Bolaños J.P., Medina J.M. Induction of NOS inhibits gap junction permeability in cultures rat astrocytes. J. Neurochem. 66:1996;2091-2099
16. Bolaños J.P., Heales S.J.R., Land J.M., Clark J.B. Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurons and astrocytes in primary cultures. J. Neurochem. 64:1995;1965-1972
17. Bracci-Laudiero L., Aloe L., Levi-Montalcini R., Buttinelli C., Schilter D., Gillessen S., Otten U. Multiple sclerosis patients express increased levels of nerve growth factor in cerebrospinal fluid. Neurosci. Lett. 147:1992;9-12
18. Bruijn L.I., Becher M.W., Lee M.K., Anderson K.L., Jenkins N.A., Copeland N.G., Sisodia S.S., Rothstein J.D., Borchelt D.R., Price D.L., Cleveland D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 18:1997;327-338
19. Cassina P., Peluffo H., Barbeito L. Adaptative responses of spinal astrocytes to oxidative stress. Castellanos B. Glial Cell Function. Prog. Brain Res. vol. 132:2001;413-425 Elsevier, Amsterdam
20. Cassina P., Peluffo H., Pehar M., Martinez-Palma L., Ressia A., Beckman J.S., Estévez A.G., Barbeito L. Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J. Neurosci. Res. 67:2002;21-29
21. Chao C.C., Hu S., Sheng W.S., Bu D., Bukrinsky M.I., Peterson P.K. Cytokine-stimulated astrocytes damage human neurons via a nitric oxide mechanism. Glia. 16:1996;276-284
22. Chiu A.Y., Chen E.W., Loera S. A motor neuron-specific epitope and the low-affinity nerve growth factor receptor display reciprocal patterns of expression during development, axotomy, and regeneration. J. Comp. Neurol. 328:1993;351-363
23. Clement A.M., Nguyen M.D., Roberts E.A., Garcia M.L., Boille S., Rule M., McMahon A.P., Doucette W., Siwek D., Ferrante R.J., Brown R.H., Julien J.P., Goldstein S.S., Cleveland D.W. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science. 302:2003;113-117
24. Cleveland D.W., Liu J. Oxidation versus aggregation - how do SOD1 mutants cause ALS? Nat. Med. 6:2000;1320-1321
25. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev., Neurosci. 2:2001;806-819
26. Cova J.L., Aldskogius H. Effect of axotomy on perineuronal glial cells in the hypoglossal and dorsal motor vagal nuclei of the cat. Exp. Neurol. 93:1986;662-667
27. Crutcher K.A., Scott S.A., Liang S., Everson W.V., Weingartner J. Detection of NGF like activity in human brain tissue: increased levels in Alzheimer's disease. J. Neurosci. 13:1993;2540-2550
28. Cruz-Sanchez F.F., Moral A., Tolosa E., de Belleroche J., Rossi M.L. Evaluation of neuronal loss, astrocytosis and abnormalities of cytoskeletal components of large motor neurons in the human anterior horn in aging. J. Neural Transm. 105:1998;689-701
29. Dawson V.L., Brahmbhatt H.P., Mong J.A., Dawson T.M. Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal glial cortical cultures. Neuropharmacology. 33:1994;1425-1430
30. Drachman D.B., Frank K., Dykes-Hoberg M., Teismann P., Almer G., Przedborski S., Rothstein J.D. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann. Neurol. 52:2002;771-778
31. Dong Y., Benveniste E.N. Immune function of astrocytes. Glia. 36:2001;180-190
32. Eagleson K.L., Raju T.R., Bennett M.R. Motoneurone survival is induced by immature astrocytes from developing avian spinal cord. Dev. Brain Res. 17:1985;95-104
33. Eddleston M., Mucke L. Molecular profile of reactive astrocytes: implications for their role in neurologic disease. Neuroscience. 54:1993;15-36
34. Ernfors P., Henschen A., Olson L., Persson H. Expression of nerve growth factor receptor mRNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons. Neuron. 2:1989;1605-1613
35. Estévez A.G., Spear N., Manuel S.M., Radi R., Henderson C.E., Barbeito L., Beckman J.S. Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18:1998;923-931
36. Estévez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., Beckman J.S. Induction of nitric oxide dependent apoptosis in motor neurons by zinc deficient superoxide dismutase. Science. 286:1999;2498-2500
37. Fahnestock M., Scott S.A., Jetté N., Weingartner J.A., Crutcher K.A. Nerve growth factor mRNA and protein levels measured in the same tissue from normal and Alzheimer's disease parietal cortex. Mol. Brain Res. 4:1996;175-178
38. Fahnestock M., Michalski B., Xu B., Coughlin M.D. The precursor pro nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell. Neurosci. 18:2001;210-220
39. Falsig J., Latta M., Leist M. Defined inflammatory states in astrocyte cultures: correlation with susceptibility towards CD95 driven apoptosis. J. Neurochem. 88:2004;181-193
40. Faulkner K.M., Liochev S.E., Fridovich I. Stable Mn(III) porphyrins mimic superoxide dismutase in vitro and substitute for it in vivo. J. Biol. Chem. 268:1994;23471-23476
41. Fedoroff S., Vernadakis A. Astrocytes: Biochemistry, Physiology, and Pharmacology of Astrocytes. vol. 2:1986;Academic Press, Orlando. 420 pp.
42. Ferrante R.J., Shinobu L.A., Schulz J.B., Mathews R.T., Thomas C.E., Kowall N.W., Gurney M.E., Beal M.F. Increased 3 nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann. Neurol. 42:1997;326-334
43. Ferrante R.J., Browne S.E., Shinobu L.A., Bowling A.C., Baik M.J., MacGarvey U., Kowall N.W., Brown R.H. Jr., Beal M.F. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J. Neurochem. 69:1997;2064-2074
44. Ferrer I., Blanco R., Cutillas B., Ambrosio S. Fas and Fas-L expression in Huntington's disease and Parkinson's disease. Neuropathol. Appl. Neurobiol. 26:2000;424-433
45. Ferrer I., Puig B., Krupinsk J., Carmona M., Blanco R. Fas and Fas ligand expression in Alzheimer's disease. Acta Neuropathol. (Berl.). 102:2001;121-131
46. Ferri C.C., Moore F.A., Bisby M.A. Effects of facial nerve injury on mouse motoneurons lacking the p75 low affinity neurotrophin receptor. J. Neurobiol. 34:1998;1-9
47. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glassa J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185:2004;232-240
48. Frade J.M., Barde Y.A. Genetic evidence for cell death mediated by nerve growth factor and the neurotrophin receptor p75 in the developing mouse retina and spinal cord. Development. 126:1999;683-690
49. Frade J.M., Rodriguez Tebar A., Barde Y.A. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature. 383:1996;166-168
50. Gilmore S.A., Sims T.J., Leiting J.E. Astrocytic reactions in spinal grey matter following sciatic axotomy. Glia. 3:1990;342-349
51. Giulian D., Baker T.J. Peptides released by ameboid microglia regulate astroglial proliferation. J. Cell Biol. 101:1985;2411-2415
52. Gong Y.H., Parsadanian A.S., Andreeva A., Snider W.D., Elliott J.L. Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J. Neurosci. 20:2000;660-665
53. Graeber M.B., Kreutzberg G.W. Delayed astrocyte reaction following facial nerve axotomy. J. Neurocytol. 17:1988;209-220
54. Gurney M.E., Pu H., Chiu A.Y., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science. 264:1994;1772-1775
55. Hall E.D., Oostveen J.A., Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia. 23:1998;249-256
56. Hasan W., Pedchenko T., Krizsan Agbas D., Baum L., Smith P.G. Sympathetic neurons synthesize and secrete pro nerve growth factor protein. J. Neurobiol. 57:2003;38-53
57. Hewett S.J., Csernansky C.A., Choi D.W. Selective potentiation of NMDA induced neuronal injury following induction of astrocytic iNOS. Neuron. 13:1994;487-494
58. Heymach J.V. Jr., Shooter E.M. The biosynthesis of neurotrophin heterodimers by transfected mammalian cells. J. Biol. Chem. 270:1995;12297-12304
59. Hirano A. Neuropathology of ALS: an overview. Neurology. 47:1996;S63-S66
60. Honig L.S., Chambliss D.D., Bigio E.H., Carroll S.L., Elliott J.L. Glutamate transporter EAAT2 splice variants occur not only in ALS, but also in AD and controls. Neurology. 55:2000;1082-1088
61. Hooper D.C., Spitsin S., Kean R.B., Champion J.M., Dickson G.M., Chaudhry I., Koprowski H. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 95:1998;675-680
62. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A. 99:2002;1604-1609
63. Hoyaux D., Alao J., Fuchs J., Kiss R., Keller B., Heizmann C.W., Pochet R., Frermann D. S100A6, a calcium and zinc binding protein, is overexpressed in SOD1 mutant mice, a model for amyotrophic lateral sclerosis. Biochim. Biophys. Acta. 1498:2000;264-272
64. Huber K., Meisinger C., Grothe C. Expression of fibroblast growth factor 2 in hypoglossal motoneurons is stimulated by peripheral nerve injury. J. Comp. Neurol. 382:1997;189-198
65. Huie R.E., Padmaja S. The reaction of NO with superoxide. Free Radic. Res. Commun. 18:1993;195-199
66. Junier M.P., Coulpier M., Le Forestier N., Cadusseau J., Suzuki F., Peschanski M., Dreyfus P.A. Transforming growth factor alpha (TGF alpha) expression in degenerating motoneurons of the murine mutant wobbler: a neuronal signal for astrogliosis? J. Neurosci. 14:1994;4206-4216
67. Kaspar B.K., Llado J., Sherkat N., Rothstein J.D., Gage F.H. Retrograde viral delivery of IGF 1 prolongs survival in a mouse model ALS model. Science. 301:2003;839-842
68. Kato S., Hayashi H., Nakashima K., Nanba E., Kato M., Hirano A., Nakano I., Asayama K., Ohama E. Pathological characterization of astrocytic hyaline inclusions in familial amyotrophic lateral sclerosis. Am. J. Pathol. 151:1997;611-620
69. Koliatsos V.E., Crawford T.O., Price D.L. Axotomy induces nerve growth factor receptor immunoreactivity in spinal motor neurons. Brain Res. 549:1991;297-304
70. Kristensson K., Aldskogius M., Peng Z.C., Olsson T., Aldskogius H., Bentivoglio M. Co induction of neuronal interferon gamma and nitric oxide synthase in rat motor neurons after axotomy: a role in nerve repair or death? J. Neurocytol. 23:1994;453-459
71. Kushner P.D., Stephenson D.I., Wright S. Reactive astrogliosis is widespread in the subcortical white matter of amyotrophic lateral sclerosis brain. J. Neuropathol. Exp. Neurol. 50:1991;263-277
72. Kust B.M., Copray J.C., Brouwer N., Troost D., Boddeke H.W. Elevated levels of neurotrophins in human biceps brachii tissue of amyotrophic lateral sclerosis. Exp. Neurol. 177:2002;419-427
73. Kust B.M., Brouwer N., Mantingh I.J., Boddeke H.W., Copray J.C. Reduced p75NTR expression delays disease onset only in female mice of a transgenic model of familial amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Mot. Neuron Disord. 4:2003;100-105
74. Lauderback C.M., Hackett J.M., Huang F.F., Keller J.N., Szweda L.I., Markesbery W.R., Butterfield D.A. The glial glutamate transporter, GLT 1, is oxidatively modified by 4 hydroxy 2 nonenal in the Alzheimer's disease brain: the role of Abeta1 42. J. Neurochem. 78:2001;413-416
75. Lee C.K., Weindruch R., Prolla T.A. Gene expression profile of the ageing brain in mice. Nat. Genet. 25:2000;294-297
76. Lee R., Kermani P., Teng K.K., Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science. 294:2001;1945-1948
77. Levi Montalcini R. The nerve growth factor 35 years later. Science. 237:1987;1154-1162
78. Levine J.B., Kong J., Nadler M., Xu Z. Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS). Glia. 28:1999;215-224
79. Lin C.L., Bristol L.A., Jin L., Dykes Hoberg M., Crawford T., Clawson L., Rothstein J.D. Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter in amyotrophic lateral sclerosis. Neuron. 20:1998;589-602
80. Lowry K.S., Murray S.S., McLean C.A., Talman P., Mathers S., Lopes E.C., Cheema S.S. A potential role for the p75 low affinity neurotrophin receptor in spinal motor neuron degeneration in murine and human amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Mot. Neuron Disord. 2:2001;127-134
81. Maihofner C., Probst-Cousin S., Bergmann M., Neuhuber W., Neundorfer B., Heuss D. Expression and localization of cyclooxygenase 1 and 2 in human sporadic amyotrophic lateral sclerosis. Eur. J. Neurosci. 18:2003;1527-1534
82. Malhotra S.K., Shnitka T.K. Diversity in reactive astrocytes. De Vellis J. Neuroglia in the Aging Brain. 2002;17-33 Humana Press, New Jersey
83. McGeer P.L., McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve. 26:2002;459-470
84. Merrill J.E., Scolding N.J. Mechanisms of damage to myelin and oligodendrocytes and their relevance to disease. Neuropathol. Appl. Neurobiol. 25:1999;435-458
85. Migheli A., Cordera S., Bendotti C., Atzori C., Piva R., Schiffer D. S 100beta protein is upregulated in astrocytes and motor neurons in the spinal cord of patients with amyotrophic lateral sclerosis. Neurosci. Lett. 261:1999;25-28
86. Nagai M., Aoki M., Miyoshi I., Kato M., Pasinelli P., Kasai N., Brown R.H. Jr., Itoyama Y. Rats expressing human cytosolic copper zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci. 21:2001;9246-9254
87. Nagy D., Kato T., Kushner P.D. Reactive astrocytes are widespread in the cortical gray matter of amyotrophic lateral sclerosis. J. Neurosci. Res. 38:1994;336-347
88. Nguyen M.D., D'Aigle T., Gowing G., Julien J.P., Rivest S. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 24:2004;1340-1349
89. Olsson T., Kristensson K., Ljungdahl A., Maehlen J., Holmdahl R., Klareskog L. Gamma interferon like immunoreactivity in axotomized rat motor neurons. J. Neurosci. 9:1989;3870-3875
90. O'Really S.A., Roedica J., Nagy D., Hallewell R.A., Alderson K., Marklund J.K., Kushner P.D. Motor neuron astrocyte interactions and levels of Cu,Zn superoxide dismutase in sporadic amyotrophic lateral sclerosis. Exp. Neurol. 131:1995;203-210
91. Pedersen W.A., Fu W., Keller J.N., Markesberry W.R., Appel S.A., Smith R.G., Kasarkis E., Mattson M.P. Protein modification by the lipid peroxidation product 4 hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients. Ann. Neurol. 44:1998;819-824
92. M.A. Pehar, M.P. Cassina, M.R. Vargas, R.M. Castellanos, L. Viera, J.S. Beckman, A.G. Estevez, L. Barbeito, Astrocytic production of proNGF and motor neuron apoptosis in ALS, Program No. 96.18. (2003) Abstract. Society for Neuroscience, 2003 Online.
93. Pehar M.A, Cassina M.P., Vargas M.R., Castellanos R.M., Viera L., Beckman J.S., Estevez A.G., Barbeito L. Astrocytic production of nerve growth factor and motor neuron apoptosis: implications for amyotrophic lateral sclerosis. J. Neurochem. 89:2004;464-473
94. Peluffo H., Estévez A., Barbeito L., Stutzmann J.M. Riluzole promotes survival of rat motoneurons in vitro by stimulating trophic activity produced by spinal astrocyte monolayers. Neurosci. Lett. 228:1997;207-211
95. Pilegaard K., Ladefoged O. Total number of astrocytes in the molecular layer of the dentate gyrus of rats at different ages. Anal. Quant. Cytol. Histol. 18:1996;279-285
96. Pramatarova A., Laganiere J., Roussel J., Brisebois K., Rouleau G.A. Neuron specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci. 21:2001;3369-3374
97. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266:1991;4244-4250
98. Rao S.D., Yin H.Z., Weiss J.H. Disruption of glial glutamate transport by reactive oxygen species produced in motor neurons. J. Neurosci. 23:2003;2627-2633
99. Raoul C., Henderson C.E., Pettmann B. Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J. Cell Biol. 147:1999;1049-1062
100. Raoul C., Pettmann B., Henderson C.E. Active killing of neurons during development and following stress: a role for p75(NTR) and Fas? Curr. Opin. Neurobiol. 10:2000;111-117
101. Raoul C., Estevez A.G., Nishimune H., Cleveland D.W., deLapeyriere O., Henderson C.E., Haase G., Pettmann B. Motoneuron death triggered by a specific pathway downstream of Fas. Potentiation by ALS linked SOD1 mutations. Neuron. 35:2002;1067-1083
102. Reisert I., Wildemann G., Grab D., Pilgrim C. The glial reaction in the course of axon regeneration: a stereological study of the rat hypoglossal nucleus. J. Comp. Neurol. 229:1984;121-128
103. Rende M., Giambanco I., Buratta M., Tonali P. Axotomy induces a different modulation of both low affinity nerve growth factor receptor and choline acetyltransferase between adult rat spinal and brainstem motoneurons. J. Comp. Neurol. 363:1995;249-263
104. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20:1997;570-577
105. Rizzi M., Perego C., Aliprandi M., Richichi C., Ravizza T., Colella D., Veliskova J., Moshe S.L., De Simoni M.G., Vezzani A. Glia activation and cytokine increase in rat hippocampus by kainic acid induced status epilepticus during postnatal development. Neurobiol. Dis. 14:2003;494-503
106. Rosen D.R., Siddique T., Patterson D., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 362:1993;59-62
107. Rothstein J.D. Excitotoxicity hypothesis. Neurology. 47:1996;S19-S25
108. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., Kuncl R.W. Selective loss of glial glutamate transporter GLT 1 in amyotrophic lateral sclerosis. Ann. Neurol. 38:1995;73-84
109. Rothwell N.J., Hopkins S.J. Cytokines and the nervous system: II. Actions and mechanisms of action. Trends Neurosci. 18:1995;130-136
110. Rowland L.P., Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 344:2001;1688-1700
111. Rozovsky I., Finch C.E., Morgan T.E. Age related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to down regulation. Neurobiol. Aging. 19:1998;97-103
112. Saez J.C., Spray D.C., Hertzberg E.L. Gap Junctions: biochemical properties and functional regulation under physiological and toxicological conditions. In Vitro Toxicol. 3:1990;69-86
113. Sagara J.I., Miura K., Bannai S. Maintenance of neuronal glutathione by glial cells. J. Neurochem. 61:1993;1672-1676
114. Sasaki S., Komori T., Iwata M. Excitatory amino acid transporter 1 and 2 immunoreactivity in the spinal cord in amyotrophic lateral sclerosis. Acta Neuropathol. (Berl.). 100:2000;138-144
115. Sasaki S., Shibata N., Komori T., Iwata M. iNOS and nitrotyrosine immunoreactivity in amyotrophic lateral sclerosis. Neurosci. Lett. 291:2000;44-48
116. Sasaki S., Warita H., Abe K., Iwata M. Inducible nitric oxide synthase (iNOS) and nitrotyrosine immunoreactivity in the spinal cords of transgenic mice with a G93A mutant SOD1 gene. J. Neuropathol. Exp. Neurol. 60:2001;839-846
117. Sasaki S., Warita H., Abe K., Komori T., Iwata M. EAAT1 and EAAT2 immunoreactivity in transgenic mice with a G93A mutant SOD1 gene. NeuroReport. 12:2001;1359-1362
118. Schiffer D., Cordera S., Cavalla P., Migheli A. Reactive astrogliosis of the spinal cord in amyotrophic lateral sclerosis. J. Neurol. Sci. 139:1996;27-33
119. Schinder A.F., Poo M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23:2000;639-645
120. Schipper H.M. Astrocytes, brain aging, and neurodegeneration. Neurobiol. Aging. 17:1996;467-480
121. trkB mRNA in amyotrophic lateral sclerosis. Brain Res. 621:1993;111-115
122. Selak I., Skaper S.D., Varon S. Pyruvate participation in the low molecular weight trophic activity for central nervous system neurons and glia. J. Neurochem. 5:1985;23-28
123. Sendtner M., Pei G., Beck M., Schweizer U., Wiese S. Developmental motoneuron cell death and neurotrophic factors. Cell Tissue Res. 301:2000;71-84
124. Skaper S.D., Facci L., Leon A. Inflammatory mediator stimulation of astrocytes and meningeal fibroblasts induces neuronal degeneration via the nitridergic pathway. J. Neurochem. 64:1995;266-276
125. Snider W.D. Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell. 77:1994;627-638
126. Stewart V.C., Sharpe M.A., Clark J.B., Heales S.J.R. Astrocyte derived nitric oxide causes both reversible and irreversible damage to the neuronal mitochondrial respiratory chain. J. Neurochem. 75:2000;694-700
127. Stuerenburg H.J., Kunze K. Tissue nerve growth factor concentrations in neuromuscular diseases. Eur. J. Neurol. 5:1998;487-490
128. Szatkowski M., Barbour B., Attwell D. Non vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature. 348:1999;443-446
129. Tetzlaff W., Graeber M.B., Bisby M.A., Kreutzberg G.W. Increased glial fibrillary acidic protein synthesis in astrocytes during retrograde reaction of the rat facial nucleus. Glia. 1:1988;90-95
130. Tortarolo M., Veglianese P., Calvaresi N., Botturi A., Rossi C., Giorgini A., Migheli A., Bendotti C. Persistent activation of p38 mitogen activated protein kinase in a mouse model of familial amyotrophic lateral sclerosis correlates with disease progression. Mol. Cell. Neurosci. 23:2003;180-192
131. Trotti D., Rossi D., Gjesdal O., Levy L.M., Racagni G., Danbolt N.C., Volterra A. Peroxynitrite inhibits glutamate transporter subtypes. J. Biol. Chem. 271:1996;5976-5979
132. Turner B.J., Cheah I.K., Macfarlane K.J., Lopes E.C., Petratos S., Langford S.J., Cheema S.S. Antisense peptide nucleic acid mediated knockdown of the p75 neurotrophin receptor delays motor neuron disease in mutant SOD1 transgenic mice. J. Neurochem. 87:2003;752-763
133. Ugolini G., Raoul C., Ferri A., Haenggeli C., Yamamoto Y., Salaun D., Henderson C.E., Kato A.C., Pettmann B., Hueber A.O. Fas/tumor necrosis factor receptor death signaling is required for axotomy induced death of motoneurons in vivo. J. Neurosci. 23:2003;8526-8531
134. Urschel B.A., Hulsebosch C.E. Distribution and relative density of p75 nerve growth factor receptors in the rat spinal cord as a function of age and treatment with antibodies to nerve growth factor. Dev. Brain Res. 69:1992;261-270
135. Valdo P., Stegagno C., Mazzucco S., Zuliani E., Zanusso G., Moretto G., Raine C.S., Bonetti B. Enhanced expression of NGF receptors in multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 61:2002;91-98
136. Van der Zee C.E., Hagg T. p75NGFR mediates death of cholinergic neurons during postnatal development of the neostriatum in mice. J. Chem. Neuroanat. 14:1998;129-140
137. Volterra A., Trotti D., Tromba C., Floridi S., Racagni G. Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J. Neurosci. 14:1994;2924-2932
138. Wagner A.P., Reck G., Platt D. Evidence that V+ fibronectin, GFAP and S100 beta mRNAs are increased in the hippocampus of aged rats. Exp. Gerontol. 28:1993;135-143
139. Wiese S., Metzger F., Holtmann B., Sendtner M. The role of p75NTR in modulating neurotrophin survival effects in developing motoneurons. Eur. J. Neurosci. 11:1999;1668-1676
140. Wu W. Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: a comparison among c-jun, off affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp. Neurol. 141:1996;190-200
141. Yan Q., Johnson E.M. Jr. An immunohistochemical study of the nerve growth factor receptor in developing rats. J. Neurosci. 8:1988;3481-3498