Lithium prevents excitotoxic cell death of motoneurons in organotypic slice cultures of spinal cord

Neuroscience

Volumn 165, Issue 4, 2010, Pages 1353-1369

  Caldero J ^a   Brunet, N ^a   Tarabal, O ^a   Piedrafita, L ^a   Hereu, M ^a   Ayala, V ^a   Esquerda, J E ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

Author keywords

amyotrophic lateral sclerosis; intracellular calcium; kainate; neuronal death; NMDA

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CALCIUM ION; EXCITOTOXIN; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; KAINIC ACID; LITHIUM; NEUROFILAMENT PROTEIN; RILUZOLE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VACUOLE; CHICK; CONTROLLED STUDY; CYTOPATHOLOGY; DRUG POTENTIATION; DRUG TARGETING; EMBRYO; ENZYME INHIBITION; EXCITOTOXICITY; IMMUNOHISTOCHEMISTRY; MOTONEURON; NERVE CELL NECROSIS; NEUROFILAMENT; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RIBOSOME; ROUGH ENDOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; SPINAL CORD; TISSUE CULTURE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CALCIUM; CELL DEATH; CHICK EMBRYO; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG THERAPY, COMBINATION; EXCITATORY AMINO ACID AGONISTS; GLYCOGEN SYNTHASE KINASE 3; KAINIC ACID; LITHIUM; MOTOR NEURONS; NEUROPROTECTIVE AGENTS; RILUZOLE; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 74149092630     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.11.034     Document Type: Article

References (100)

1. Arai Y., Mentis G.Z., Wu J.-Y., and O'Donovan M.J. Ventrolateral origin of each cycle of rhythmic activity generated by the spinal cord of the chick embryo. PLoS One 2 (2007) e417
2. Ayala V., Casas C., Ribera J., Calderó J., Oppenheim R.W., and Esquerda J.E. Specific association of c-Jun-like immunoreactivity but not c-Jun p39 with normal and induced programmed cell death in the chick embryo. J Neurobiol 38 (1999) 171-190
3. Bendotti C., Tortarolo M., Suchak S.K., Calvaresi N., Carvellim L., Bastone A., Rizzi M., Rattray M., and Mennini T. Transgenic SOD1 G93A mice develop reduced GLT-1 in spinal cord without alterations in cerebrospinal fluid glutamate levels. J Neurochem 79 (2001) 737-746
4. Björkblom B., Ostman N., Hongisto V., Komarovski V., Filén J.J., Nyman T.A., Kallunki T., Courtney M.J., and Coffey E.T. Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 25 (2005) 6350-6361
5. Brandish P.E., Su M., Holder D.J., Hodor P., Szumiloski J., Kleinhanz R.R., Forbes J.E., McWhorter M.E., Duenwald S.J., Parrish M.L., Na S., Liu Y., Phillips R.L., Renger J.J., Sankaranarayanan S., Simon A.J., and Scolnick E.M. Regulation of gene expression by lithium and depletion of inositol in slices of adult rat cortex. Neuron 45 (2005) 861-872
6. 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., and 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
7. Brunet N., Tarabal O., Esquerda J.E., and Calderó J. Excitotoxic motoneuron degeneration induced by glutamate receptor agonists and mitochondrial toxins in organotypic cultures of chick embryo spinal cord. J Comp Neurol 516 (2009) 277-290
8. Brunet N., Tarabal O., Portero-Otín M., Oppenheim R.W., Esquerda J.E., and Calderó J. Survival and death of mature avian motoneurons in organotypic slice culture: trophic requirements for survival and different types of degeneration. J Comp Neurol 501 (2007) 669-690
9. Burek M.J., and Oppenheim R.W. Cellular interactions that regulate programmed cell death in the developing vertebrate nervous system. In: Koliatsos V.E., and Ratan R.R. (Eds). Cell death and diseases of the nervous system (1999), Humana Press, Totowa, NJ 145-179
10. Cade J.F. Lithium salts in the treatment of psychotic excitement. Med J Aust 2 (1949) 349-352
11. Calderó J., Casanovas A., Sorribas A., and Esquerda J.E. Calcitonin gene-related peptide in rat spinal cord motoneurons: subcellular distribution and changes induced by axotomy. Neuroscience 48 (1992) 449-461
12. Calderó J., Ciutat D., Lladó J., Castán E., Oppenheim R.W., and Esquerda J.E. Effects of excitatory amino acids on neuromuscular development in the chick embryo. J Comp Neurol 387 (1997) 73-95
13. Calderó J., Tarabal O., Casanovas A., Ciutat D., Casas C., Lladó J., and Esquerda J.E. Excitotoxic motoneuron disease in chick embryo evolves with autophagic neurodegeneration and deregulation of neuromuscular innervation. J Neurosci Res 85 (2007) 2726-2740
14. Carriedo S.G., Yin H.Z., and Weiss J.H. Motor neurons are selectively vulnerable to AMPA/KA receptor-mediated injury in vitro. J Neurosci 16 (1996) 4069-4079
15. Casanovas A., Ribera J., Hager G., Kreutzberg G.W., and Esquerda J.E. c-Jun regulation in rat neonatal motoneurons postaxotomy. J Neurosci Res 63 (2001) 469-479
16. Chalecka-Franaszeck E., and Chuang D.M. Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci U S A 96 (1999) 8745-8750
17. Chang L., Jones Y., Ellisman M.H., Goldstein L.S., and Karin M. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4 (2003) 521-533
18. Chen G., Zeng W.Z., Yuan P.X., Huang L.D., Jiang Y.M., Zhao Z.H., and Manji H.K. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 72 (1999) 879-882
19. Chen R.W., and Chuang D.M. Long term lithium treatment suppresses p53 and Bax expression but increases Bcl-2 expression. A prominent role in neuroprotection against excitotoxicity. J Biol Chem 274 (1999) 6039-6042
20. Chen R.W., Qin Z.H., Ren M., Kanai H., Chalecka-Franaszek E., Leeds P., and Chuang D.M. Regulation of c-Jun N-terminal kinase, p38 kinase and AP-1 DNA binding in cultured brain neurons: roles in glutamate excitotoxicity and lithium neuroprotection. J Neurochem 84 (2003) 566-575
21. Chuang D.M., Chen R.W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., Kanai H., Hough C., Hiroi T., and Leeds P. Neuroprotective effects of lithium in cultured cells and animal models of diseases. Bipolar Disord 4 (2002) 129-136
22. Chuang D.M. The antiapoptotic actions of mood stabilizers: molecular mechanisms and therapeutic potentials. Ann N Y Acad Sci 1053 (2005) 195-204
23. Clarke P.G.H., and Oppenheim R.W. Neuron death in vertebrate development: in vivo methods. In: Schwartz L.M., and Osborne B.A. (Eds). Methods in cell biology: cell death Vol. 46 (1995), Academic Press, New York 277-321
24. Cleveland D.W., and Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2 (2001) 806-819
25. Colombo R., Milzani A., Contini P., and Dalle Donne I. Effects of lithium ions on actin polymerization in the presence of magnesium ions. Biochem J 274 (1991) 421-425
26. Cordeiro M.L., Gundersen C.B., and Umbach J.A. Convergent effects of lithium and valproate on the expression of proteins associated with large dense core vesicles in NGF-differentiated PC12 cells. Neuropsychopharmacology 29 (2004) 39-44
27. Cordeiro M.L., Umbach J.A., and Gundersen C.B. Lithium ions up-regulate mRNAs encoding dense-core vesicle proteins in nerve growth factor-differentiated PC12 cells. J Neurochem 75 (2000) 2622-2625
28. Coyle J.T., and Duman R.S. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 38 (2003) 157-160
29. Crespo-Biel N., Canudas A.M., Camins A., and Pallàs M. Kainate induces AKT, ERK and cdk5/GSK3beta pathway deregulation, phosphorylates tau protein in mouse hippocampus. Neurochem Int 50 (2007) 435-442
30. Cross D.A., Culbert A.A., Chalmers K.A., Facci L., Skaper S.D., and Reith A.D. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J Neurochem 77 (2001) 94-102
31. Crowder R.J., and Freeman R.S. Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J Biol Chem 275 (2000) 34266-34271
32. Dixon J.F., Los G.V., and Hokin L.E. Lithium stimulates glutamate "release" and inositol 1,4,5-trisphosphate accumulation via activation of the N-methyl-d-aspartate receptor in monkey and mouse cerebral cortex slices. Proc Natl Acad Sci U S A 91 (1994) 8358-8362
33. Doble A. The pharmacology and mechanism of action of riluzole. Neurology 47 Suppl 4 (1996) S233-S241
34. Dou H., Ellison B., Bradley J., Kasiyanov A., Poluektova L.Y., Xiong H., Maggirwar S., Dewhurst S., Gelbard H.A., and Gendelman H.E. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J Neurosci 25 (2005) 8375-8385
35. Ebstein R.P., Lerer B., Shlaufman M., and Belmaker R.H. The effect of repeated electroconvulsive shock treatment and chronic lithium feeding on the release of norepinephrine from rat cortical vesicular preparations. Cell Mol Neurobiol 3 (1983) 191-201
36. Feng H.L., Leng Y., Ma C.H., Zhang J., Ren M., and Chuang D.M. Combined lithium and valproate treatment delays disease onset, reduces neurological deficits and prolongs survival in an amyotrophic lateral sclerosis mouse model. Neuroscience 155 (2008) 567-572
37. Fornai F., Longone P., Cafaro L., Kastsiuchenka O., Ferrucci M., Manca M.L., Lazzeri G., Spalloni A., Bellio N., Lenzi P., Modugno N., Siciliano G., Isidoro C., Murri L., Ruggieri S., and Paparelli A. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 105 (2008) 2052-2057
38. Fornai F., Longone P., Ferrucci M., Lenzi P., Isidoro C., Ruggieri S., and Paparelli A. Autophagy and amyotrophic lateral sclerosis: the multiple roles of lithium. Autophagy 4 (2008) 527-530
39. Gill A., Kidd J., Vieira F., Thompson K., and Perrin S. No benefit from chronic lithium dosing in a sibling-matched, gender balanced, investigator-blinded trial using a standard mouse model of familial ALS. PLoS One 4 (2009) e6489
40. Goodall E.F., and Morrison K.E. Amyotrophic lateral sclerosis (motor neuron disease): proposed mechanisms and pathways to treatment. Expert Rev Mol Med 8 (2006) 1-22
41. Goodenough S., Conrad S., Skutella T., and Behl C. Inactivation of glycogen synthase kinase-3beta protects against kainic acid-induced neurotoxicity in vivo. Brain Res 1026 (2004) 116-125
42. Hallcher L.M., and Sherman W.R. The effects of lithium ion and other agents on the activity of myo-inositol-1-phosphatase from bovine brain. J Biol Chem 255 (1980) 10896-10901
43. Hamburger V., and Hamilton H.L. A series of normal stages in the development of the chick embryo. J Morphol 88 (1951) 49-52
44. Harwood A.J., and Agam G. Search for a common mechanism of mood stabilizers. Biochem Pharmacol 66 (2003) 179-189
45. Harwood A.J. Lithium and bipolar mood disorder: the inositol-depletion hypothesis revisited. Mol Psychiatry 10 (2005) 117-126
46. Hashimoto R., Hough C., Nakazawa T., Yamamoto T., and Chuang D.M. Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly decreasing NR2B tyrosine phosphorylation. J Neurochem 80 (2002) 589-597
47. Heiseke A., Aguib Y., Riemer C., Baier M., and Schätzl H.M. Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J Neurochem 109 (2009) 25-34
48. Hetman M., Cavanaugh J.E., Kimelman D., and Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20 (2000) 2567-2574
49. Hetz C., Thielen P., Matus S., Nassif M., Court F., Kiffin R., Martinez G., Cuervo A.M., Brown R.H., and Glimcher L.H. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev 23 (2009) 2294-2306
50. Hollander B.A., and Bennett G.S. Lithium chloride alters cytoskeletal organization in growing, but not mature, cultured chick sensory neurons. J Neurosci Res 28 (1991) 332-342
51. Hong J.S., Tilson H.A., and Yoshikawa K. Effects of lithium and haloperidol administration on the rat brain levels of substance P. J Pharmacol Exp Ther 224 (1983) 590-593
52. Hongisto V., Smeds N., Brecht S., Herdegen T., Courtney M.J., and Coffey E.T. Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol Cell Biol 23 (2003) 6027-6036
53. Ikonomov O.C., Petrov T., Soden K., Shisheva A., and Manji H.K. Lithium treatment in ovo: effects on embryonic heart rate, natural death of ciliary ganglion neurons, and brain expression of a highly conserved chicken homolog of human MTG8/ETO. Brain Res Dev Brain Res 123 (2000) 13-24
54. Jaeger P.A., and Wyss-Coray T. All-you-can-eat: autophagy in neurodegeneration and neuroprotection. Mol Neurodegener 4 (2009) 16
55. Kang H.J., Noh J.S., Bae Y.S., and Gwag B.J. Calcium-dependent prevention of neuronal apoptosis by lithium ion: essential role of phosphoinositide 3-kinase and phospholipase Cγ. Mol Pharmacol 64 (2003) 228-234
56. Kashihara Y., Sakaguchi M., and Kuno M. Axonal transport and distribution of endogenous calcitonin gene-related peptide in rat peripheral nerve. J Neurosci 9 (1989) 3796-3802
57. Klein P.S., and Melton D.A. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93 (1996) 8455-8459
58. Leng Y., Liang M.H., Ren M., Marinova Z., Leeds P., and Chuang D.M. Synergistic neuroprotective effects of lithium and valproic acid or other histone deacetylase inhibitors in neurons: roles of glycogen synthase kinase-3 inhibition. J Neurosci 28 (2008) 2576-2588
59. Levine S., Saltzman A., and Kumar A.R. A method for peripheral chromatolysis in neurons of trigeminal and dorsal root ganglia, produced in rats by lithium. J Neurosci Methods 132 (2004) 1-7
60. Li L., Prevette D., Oppenheim R.W., and Milligan C.E. Involvement of specific caspases in motoneuron cell death in vivo and in vitro following trophic factor deprivation. Mol Cell Neurosci 12 (1998) 157-167
61. Lladó J., Calderó J., Ribera J., Tarabal O., Oppenheim R.W., and Esquerda J.E. Opposing effects of excitatory amino acids on chick embryo spinal cord motoneurons: excitotoxic degeneration or prevention of programmed cell death. J Neurosci 19 (1999) 10803-10812
62. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-275
63. Manji H.K., Moore G.J., and Chen G. Lithium at 50: have the neuroprotective effects of this unique cation been overlooked?. Biol Psychiatry 46 (1999) 929-940
64. Martin D., Thompson M.A., and Nadler J.V. The neuroprotective agent riluzole inhibits release of glutamate and aspartate from slices of hippocampal area CA1. Eur J Pharmacol 250 (1993) 473-476
65. Mathé A.A., Jousisto-Hanson J., Stenfors C., and Theodorsson E. Effect of lithium on tachykinins, calcitonin gene-related peptide, and neuropeptide Y in rat brain. J Neurosci Res 26 (1990) 233-237
66. Matteoli M., Haimann C., Torri-Tarelli F., Polak J.M., Ceccarelli B., and De Camilli P. Differential effect of alpha-latrotoxin on exocytosis from small synaptic vesicles and from large dense-core vesicles containing calcitonin gene-related peptide at the frog neuromuscular junction. Proc Natl Acad Sci U S A 85 (1988) 7366-7370
67. Mielke K., and Herdegen T. JNK and p38 stresskinases-degenerative effectors of signal-transduction-cascades in the nervous system. Prog Neurobiol 61 (2000) 45-60
68. Miller R.G., Mitchell J.D., Lyon M., and Moore D.H. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev 1 (2007) CD001447
69. +. Eur J Biochem 266 (1999) 886-891
70. Nakamura R., Kamakura K., and Kwak S. Late onset selective neuronal damage in the rat spinal cord induced by continuous intrathecal administration of AMPA. Brain Res 654 (1994) 279-285
71. Newbern J., Taylor A., Robinson M., Lively M.O., and Milligan C.E. C-Jun N-terminal kinase signaling regulates events associated with both health and degeneration in motoneurons. Neuroscience 147 (2007) 680-692
72. Noble W., Planel E., Zehr C., Olm V., Meyerson J., Suleman F., Gaynor K., Wang L., LaFrancois J., Feinstein B., Burns M., Krishnamurthy P., Wen Y., Bhat R., Lewis J., Dickson D., and Duff K. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci U S A 102 (2005) 6990-6995
73. Nonaka S., Hough C.J., and Chuang D.M. Chronic lithium treatment robustly protects neurons in the central nervous system against excitotoxicity by inhibiting N-methyl-d-aspartate receptor-mediated calcium influx. Proc Natl Acad Sci U S A 95 (1998) 2642-2647
74. Nurcombe V., Wreford N.G., and Bertram J.F. The use of the optical dissector to estimate the total number of the neurons in the developing chick lateral motor column: effects of purified growth factors. Anat Rec 231 (1991) 416-424
75. O'Donovan M.J., Bonnot A., Mentis G.Z., Arai Y., Chub N., Schneider N.A., and Wenner P. Imaging the spatiotemporal organization of neural activity in the developing spinal cord. Dev Neurobiol 68 (2008) 788-803
76. Owen R., and Gordon-Weeks P.R. Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol Cell Neurosci 23 (2003) 626-637
77. Petzold A., Gveric D., Groves M., Schmierer K., Grant D., Chapman M., Keir G., Cuzner L., and Thompson E.J. Phosphorylation and compactness of neurofilaments in multiple sclerosis: indicators of axonal pathology. Exp Neurol 213 (2008) 326-335
78. Phiel C.J., and Klein P.S. Molecular targets of lithium action. Annu Rev Pharmacol Toxicol 41 (2001) 789-813
79. Pizzasegola C., Caron I., Daleno C., Ronchi A., Minoia C., Carrì M.T., and Bendotti C. Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice. Amyotroph Lateral Scler 10 (2009) 221-228
80. Provine R.R. Neurophysiological aspects of behavior development in the chick embryo. In: Gottieb G. (Ed). Studies on the development of behavior and the nervous system Vol. 1 (1973), Academic Press, New York 77-102
81. Rothstein J.D., Kuncl R., Chaudhry V., Clawson L., Cornblath D.R., Coyle J.T., and Drachman D.B. Excitatory amino acids in amyotrophic lateral sclerosis: an update. Ann Neurol 30 (1991) 224-225
82. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., and Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38 (1995) 73-84
83. Sarkar S., Floto R.A., Berger Z., Imarisio S., Cordenier A., Pasco M., Cook L.J., and Rubinsztein D.C. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170 (2005) 1101-1111
84. Sarkar S., Krishna G., Imarisio S., Saiki S., O'Kane C.J., and Rubinsztein D.C. A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum Mol Genet 17 (2008) 170-178
85. Sarkar S., and Rubinsztein D.C. Huntington's disease: degradation of mutant huntingtin by autophagy. FEBS J 275 (2008) 4263-4270
86. Shin J.H., Cho S.I., Lim H.R., Lee J.K., Lee Y.A., Noh J.S., Joo I.S., Kim K.W., and Gwag B.J. Concurrent administration of Neu2000 and lithium produces marked improvement of motor neuron survival, motor function, and mortality in a mouse model of amyotrophic lateral sclerosis. Mol Pharmacol 71 (2007) 965-975
87. Sun W., Gould T.W., Newbern J., Milligan C., Choi S.Y., Kim H., and Oppenheim R.W. Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J Neurosci 25 (2005) 5595-5603
88. Tarabal O., Calderó J., Casas C., Oppenheim R.W., and Esquerda J.E. Protein retention in the endoplasmic reticulum, blockade of programmed cell death and autophagy selectively occur in spinal cord motoneurons after glutamate receptor-mediated injury. Mol Cell Neurosci 29 (2005) 283-298
89. Tarabal O., Calderó J., Lladó J., Oppenheim R.W., and Esquerda J.E. Long-lasting aberrant tubulovesicular membrane inclusions accumulate in developing motoneurons after a sublethal excitotoxic insult: a possible model for neuronal pathology in neurodegenerative disease. J Neurosci 21 (2001) 8072-8081
90. Treiser S.L., Cascio C.S., O'Donohue T.L., Thoa N.B., Jacobowitz D.M., and Kellar K.J. Lithium increases serotonin release and decreases serotonin receptors in the hippocampus. Science 213 (1981) 1529-1531
91. Tsvyetlynska N.A., Hill R.H., and Grillner S. Role of AMPA receptor desensitization and the side effects of a DMSO vehicle on reticulospinal EPSPs and locomotor activity. J Neurophysiol 94 (2005) 3951-3960
92. Van Den Bosch L., Van Damme P., Bogaert E., and Robberecht W. The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 1762 (2006) 1068-1082
93. Wada A., Yokoo H., Yanagita T., and Kobayashi H. Lithium: potential therapeutics against acute brain injuries and chronic neurodegenerative diseases. J Pharmacol Sci 99 (2005) 307-321
94. Waetzig V., and Herdegen T. Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol Sci 26 (2005) 455-461
95. Waetzig V., Zhao Y., and Herdegen T. The bright side of JNKs-multitalented mediators in neuronal sprouting, brain development and nerve fiber regeneration. Prog Neurobiol 80 (2006) 84-97
96. Wei H., Qin Z.H., Senatorov V.V., Wei W., Wang Y., Qian Y., and Chuang D.M. Lithium suppresses excitotoxicity-induced striatal lesions in a rat model of Huntington's disease. Neuroscience 106 (2001) 603-612
97. Whitmarsh A.J., Kuan C.Y., Kennedy N.J., Kelkar N., Haydar T.F., Mordes J.P., Appel M., Rossini A.A., Jones S.N., Flavell R.A., Rakic P., and Davis R.J. Requirement of the JIP1 scaffold protein for stress-induced JNK activation. Genes Dev 15 (2001) 2421-2432
98. Yang D.D., Kuan C.Y., Whitmarsh A.J., Rincón M., Zheng T.S., Davis R.J., Rakic P., and Flavell R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389 (1997) 865-870
99. Yuan P., Chen G., and Manji H.K. Lithium activates the c-Jun NH2-terminal kinases in vitro and in the CNS in vivo. J Neurochem 73 (1999) 2299-2309
100. Zhang F., Phiel C.J., Spece L., Gurvich N., and Klein P.S. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 278 (2003) 33067-33077