Chronic treatment with lithium does not improve neuromuscular phenotype in a mouse model of severe spinal muscular atrophy

Neuroscience

Volumn 250, Issue , 2013, Pages 417-433

  Dachs, E ^a   Piedrafita, L ^a   Hereu, M ^a   Esquerda, J E ^a   Caldero J ^a  

^a Universitat de Lleida Facultat de Medicina Sabadell   (Spain)

Author keywords

GSK 3 ; Lithium; Skeletal muscle; SMN 7 mouse; Spinal cord; Spinal muscular atrophy

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG EFFICACY; FEMALE; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; LOCOMOTION; LONG TERM CARE; MACROGLIA; MALE; MICROGLIA; MOUSE; NEUROMUSCULAR SYNAPSE; NICK END LABELING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPINAL CORD; SPINAL MUSCULAR ATROPHY; SURVIVAL; SYMPTOM; SYNAPSE; WESTERN BLOTTING;

ALS; AMYOTROPHIC LATERAL SCLEROSIS; ANALYSIS OF VARIANCE; ANOVA; CALCITONIN GENE-RELATED PEPTIDE; CGRP; FL; FULL-LENGTH; GFAP; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOGEN SYNTHASE KINASE-3Β; GSK-3Β; IBA1; IONIZED CALCIUM-BINDING ADAPTOR MOLECULE 1; LI; LICL; LITHIUM; LITHIUM CHLORIDE; MN; MOTONEURON; N-METHYL-D-ASPARTATE; NMDA; PB; PBS; PHOSPHATE BUFFER; PHOSPHATE-BUFFERED SALINE; PHOSPHATIDYLINOSITOL 3-KINASE; PI3K; ROOM TEMPERATURE; RT; SKELETAL MUSCLE; SMA; SMN; SMNΔ7 MOUSE; SOD1; SPINAL CORD; SPINAL MUSCULAR ATROPHY; SUPEROXIDE DISMUTASE 1; SURVIVAL MOTOR NEURON; TA; TBST; TERMINAL DEOXYNUCLEOTIDYL TRANSFERASE DUTP NICK-END LABELING; TIBIALIS ANTERIOR; TUNEL; TWEEN 20-TRIS-BUFFERED SALINE; VESICULAR GLUTAMATE TRANSPORTER 1; VGLUT1;

ANIMALS; BLOTTING, WESTERN; CELL COUNT; GLYCOGEN SYNTHASE KINASE 3; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LITHIUM CHLORIDE; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUSCLE, SKELETAL; MUSCULAR ATROPHY, SPINAL; MUTATION; ONCOGENE PROTEIN V-AKT; PHENOTYPE; POSTURAL BALANCE; PSYCHOMOTOR PERFORMANCE; REFLEX; SPINAL CORD; SURVIVAL OF MOTOR NEURON 1 PROTEIN;

EID: 84882653841     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.07.026     Document Type: Article

References (145)

1. Aggarwal S.P., Zinman L., Simpson E., McKinley J., Jackson K.E., Pinto H., Kaufman P., Conwit R.A., Schoenfeld D., Shefner J., Cudkowicz M. Safety and efficacy of lithium in combination with riluzole for treatment of amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled trial. Lancet Neurol 2010, 9:481-488. Northeast and Canadian Amyotrophic Lateral Sclerosis Consortia.
2. Ahmad S., Wang Y., Shaik G.M., Burghes A.H., Gangwani L. The zinc finger protein ZPR1 is a potential modifier of spinal muscular atrophy. Hum Mol Genet 2012, 21:2745-2758.
3. Ahn S.W., Kim J.E., Park K.S., Choi W.J., Hong Y.H., Kim S.M., Kim S.H., Lee K.W., Sung J.J. The neuroprotective effect of the GSK-3β inhibitor and influence on the extrinsic apoptosis in the ALS transgenic mice. J Neurol Sci 2012, 320:1-5.
4. Andreassi C., Angelozzi C., Tiziano F.D., Vitali T., De Vincenzi E., Boninsegna A., Villanova M., Bertini E., Pini A., Neri G., Brahe C. Phenylbutyrate increases SMN expression in vitro: relevance for treatment of spinal muscular atrophy. Eur J Hum Genet 2004, 12:59-65.
5. Avila A.M., Burnett B.G., Taye A.A., Gabanella F., Knight M.A., Hartenstein P., Cizman Z., Di Prospero N.A., Pellizzoni L., Fischbeck K.H., Sumner C.J. Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J Clin Invest 2007, 117:659-671.
6. Azzouz M., Le T., Ralph G.S., Walmsley L., Monani U.R., Lee D.C., Wilkes F., Mitrophanous K.A., Kingsman S.M., Burghes A.H., Mazarakis N.D. Lentivector-mediated SMN replacement in a mouse model of spinal muscular atrophy. J Clin Invest 2004, 114:1726-1731.
7. Baughan T.D., Dickson A., Osman E.Y., Lorson C.L. Delivery of bifunctional RNAs that target an intronic repressor and increase SMN levels in an animal model of spinal muscular atrophy. Hum Mol Genet 2009, 18:1600-1611.
8. Benkhelifa-Ziyyat S., Besse A., Roda M., Duque S., Astord S., Carcenac R., Marais T., Barkats M. Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Mol Ther 2013, 21:282-290.
9. Bhat R.V., Budd Haeberlein S.L., Avila J. Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 2004, 89:1313-1317.
10. Biondi O., Branchu J., Sanchez G., Lancelin C., Deforges S., Lopes P., Pariset C., Lécolle S., CÔté J., Chanoine C., Charbonnier F. In vivo NMDA receptor activation accelerates motor unit maturation, protects spinal motor neurons, and enhances SMN2 gene expression in severe spinal muscular atrophy mice. J Neurosci 2010, 30:11288-11299.
11. Biondi O., Grondard C., Lécolle S., Deforges S., Pariset C., Lopes P., Cifuentes-Diaz C., Li H., della Gaspera B., Chanoine C., Charbonnier F. Exercise-induced activation of NMDA receptor promotes motor unit development and survival in a type 2 spinal muscular atrophy model mouse. J Neurosci 2008, 28:953-962.
12. Bosch-Marcé M., Wee C.D., Martinez T.L., Lipkes C.E., Choe D.W., Kong L., Van Meerbeke J.P., Musarò A., Sumner C.J. Increased IGF-1 in muscle modulates the phenotype of severe SMA mice. Hum Mol Genet 2011, 20:1844-1853.
13. Bowerman M., Beauvais A., Anderson C.L., Kothary R. Rho-kinase inactivation prolongs survival of an intermediate SMA mouse model. Hum Mol Genet 2010, 19:1468-1478.
14. Bowerman M., Murray L.M., Boyer J.G., Anderson C.L., Kothary R. Fasudil improves survival and promotes skeletal muscle development in a mouse model of spinal muscular atrophy. BMC Med 2012, 10:24.
15. Brahe C., Vitali T., Tiziano F.D., Angelozzi C., Pinto A.M., Borgo F., Moscato U., Bertini E., Mercuri E., Neri G. Phenylbutyrate increases SMN gene expression in spinal muscular atrophy patients. Eur J Hum Genet 2005, 13:256-259.
16. Brichta L., Hofmann Y., Hahnen E., Siebzehnrubl F.A., Raschke H., Blumcke I., Eyupoglu I.Y., Wirth B. Valproic acid increases the SMN2 protein level: a well-known drug as a potential therapy for spinal muscular atrophy. Hum Mol Genet 2003, 12:2481-2489.
17. Burghes A.H., Beattie C.E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick?. Nat Rev Neurosci 2009, 10:597-609.
18. Butchbach M.E., Singh J., Thorsteinsdóttir M., Saieva L., Slominski E., Thurmond J., Andrésson T., Zhang J., Edwards J.D., Simard L.R., Pellizzoni L., Jarecki J., Burghes A.H., Gurney M.E. Effects of 2,4-diaminoquinazoline derivatives on SMN expression and phenotype in a mouse model for spinal muscular atrophy. Hum Mol Genet 2010, 19:454-467.
19. Calderó J., Brunet N., Tarabal O., Piedrafita L., Hereu M., Ayala V., Esquerda J.E. Lithium prevents excitotoxic cell death of motoneurons in organotypic slice cultures of spinal cord. Neuroscience 2010, 165:1353-1369.
20. Caspi M., Zilberberg A., Eldar-Finkelman H., Rosin-Arbesfeld R. Nuclear GSK-3beta inhibits the canonical Wnt signalling pathway in a beta-catenin phosphorylation-independent manner. Oncogene 2008, 27:3546-3555.
21. Chalecka-Franaszeck E., 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 USA 1999, 96:8745-8750.
22. Chang J.G., Hsieh-Li H.M., Jong Y.J., Wang N.M., Tsai C.H., Li H. Treatment of spinal muscular atrophy by sodium butyrate. Proc Natl Acad Sci USA 2001, 98:9808-9813.
23. Chen P.C., Gaisina I.N., El-Khodor B.F., Ramboz S., Makhortova N.R., Rubin L.L., Kozikowski A.P. Identification of a maleimide-based glycogen synthase kinase-3 (GSK-3) inhibitor, BIP-135, that prolongs the median survival time of δ7 SMA KO mouse model of spinal muscular atrophy. ACS Chem Neurosci 2012, 3:5-11.
24. Chen R.W., 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 1999, 274:6039-6042.
25. Chen Y., Guan Y., Liu H., Wu X., Yu L., Wang S., Zhao C., Du H., Wang X. Activation of the Wnt/β-catenin signaling pathway is associated with glial proliferation in the adult spinal cord of ALS transgenic mice. Biochem Biophys Res Commun 2012, 420:397-403.
26. Chen Y., Guan Y., Zhang Z., Liu H., Wang S., Yu L., Wu X., Wang X. Wnt signaling pathway is involved in the pathogenesis of amyotrophic lateral sclerosis in adult transgenic mice. Neurol Res 2012, 34:390-399.
27. Chiò A., Borghero G., Calvo A., Capasso M., Caponnetto C., Corbo M., Giannini F., Logroscino G., Mandrioli J., Marcello N., Mazzini L., Moglia C., Monsurrò M.R., Mora G., Patti F., Perini M., Pietrini V., Pisano F., Pupillo E., Sabatelli M., Salvi F., Silani V., Simone I.L., Sorarù G., Tola M.R., Volanti P., Beghi E. Lithium carbonate in amyotrophic lateral sclerosis: lack of efficacy in a dose-finding trial. Neurology 2010, 75:619-625. LITALS Study Group.
28. Chuang D.M., Chen R.W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., Kanai H., Hough C., Hiroi T., Leeds P. Neuroprotective effects of lithium in cultured cells and animal models of diseases. Bipolar Disord 2002, 4:129-136.
29. Chuang D.M., Manji H.K. In search of the Holy Grail for the treatment of neurodegenerative disorders: has a simple cation been overlooked?. Biol Psychiatry 2007, 62:4-6.
30. Chuang D.M., Wang Z., Chiu C.T. GSK-3 as a target for lithium-induced neuroprotection against excitotoxicity in neuronal cultures and animal models of ischemic stroke. Front Mol Neurosci 2011, 4:15.
31. Cifuentes-Diaz C., Frugier T., Tiziano F.D., Lacène E., Roblot N., Joshi V., Moreau M.H., Melki J. Deletion of murine SMN exon 7 directed to skeletal muscle leads to severe muscular dystrophy. J Cell Biol 2001, 152:1107-1114.
32. Clarke P.G.H., Oppenheim R.W. Neuron death in vertebrate development: in vivo methods. Methods in cell biology 1995, vol. 46:277-321. Academic Press, New York.
33. Coady T.H., Lorson C.L. Trans-splicing-mediated improvement in a severe mouse model of spinal muscular atrophy. J Neurosci 2010, 30:126-130.
34. Coovert D.D., Le T.T., McAndrew P.E., Strasswimmer J., Crawford T.O., Mendell J.R., Coulson S.E., Androphy E.J., Prior T.W., Burghes A.H. The survival motor neuron protein in spinal muscular atrophy. Hum Mol Genet 1997, 6:1205-1214.
35. Corti S., Nizzardo M., Nardini M., Donadoni C., Salani S., Ronchi D., Saladino F., Bordoni A., Fortunato F., Del Bo R., Papadimitriou D., Locatelli F., Menozzi G., Strazzer S., Bresolin N., Comi G.P. Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J Clin Invest 2008, 118:3316-3330.
36. Corti S., Nizzardo M., Nardini M., Donadoni C., Salani S., Ronchi D., Simone C., Falcone M., Papadimitriou D., Locatelli F., Mezzina N., Gianni F., Bresolin N., Comi G.P. Embryonic stem cell-derived neural stem cells improve spinal muscular atrophy phenotype in mice. Brain 2010, 133:465-481.
37. Corti S., Nizzardo M., Simone C., Falcone M., Nardini M., Ronchi D., Donadoni C., Salani S., Riboldi G., Magri F., Menozzi G., Bonaglia C., Rizzo F., Bresolin N., Comi G.P. Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy. Sci Transl Med 2012, 4:165ra162.
38. Coyle J.T., Duman R.S. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 2003, 38:157-160.
39. Dachs E., Hereu M., Piedrafita L., Casanovas A., Calderó J., Esquerda J.E. Defective neuromuscular junction organization and postnatal myogenesis in mice with severe spinal muscular atrophy. J Neuropathol Exp Neurol 2011, 70:444-4461.
40. Diehl J.A., Cheng M., Roussel M.F., Sherr C.J. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998, 12:3499-3511.
41. Dominguez E., Marais T., Chatauret N., Benkhelifa-Ziyyat S., Duque S., Ravassard P., Carcenac R., Astord S., Pereira de Moura A., Voit T., Barkats M. Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum Mol Genet 2011, 20:681-693.
42. Dou H., Ellison B., Bradley J., Kasiyanov A., Poluektova L.Y., Xiong H., Maggirwar S., Dewhurst S., Gelbard H.A., Gendelman H.E. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J Neurosci 2005, 25:8375-8385.
43. El-Khodor B.F., Edgar N., Chen A., Winberg M.L., Joyce C., Brunner D., Suárez-Fariñas M., Heyes M.P. Identification of a battery of tests for drug candidate evaluation in the SMNδ7 neonate model of spinal muscular atrophy. Exp Neurol 2008, 212:29-43.
44. Feldkötter M., Schwarzer V., Wirth R., Wienker T.F., Wirth B. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet 2002, 70:358-368.
45. Feng H.L., Leng Y., Ma C.H., Zhang J., Ren M., 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 2008, 155:567-572.
46. Ferrucci M., Spalloni A., Bartalucci A., Cantafora E., Fulceri F., Nutini M., Longone P., Paparelli A., Fornai F. A systematic study of brainstem motor nuclei in a mouse model of ALS, the effects of lithium. Neurobiol Dis 2010, 37:370-383.
47. Fidziańska A., Goebel H.H., Warlo I. Acute infantile spinal muscular atrophy. Muscle apoptosis as a proposed pathogenetic mechanism. Brain 1990, 113:433-445.
48. 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., Paparelli A. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2008, 105:2052-2057.
49. Foust K.D., Nurre E., Montgomery C.L., Hernandez A., Chan C.M., Kaspar B.K. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009, 27:59-65.
50. Foust K.D., Wang X., McGovern V.L., Braun L., Bevan A.K., Haidet A.M., Le T.T., Morales P.R., Rich M.M., Burghes A.H., Kaspar B.K. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 2010, 28:271-274.
51. Franke T.F., Yang S.I., Chan T.O., Datta K., Kazlauskas A., Morrison D.K., Kaplan D.R., Tsichlis P.N. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 1995, 81:727-736.
52. Gill A., Kidd J., Vieira F., Thompson K., 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 2009, 4:e6489.
53. Glascock J.J., Shababi M., Wetz M.J., Krogman M.M., Lorson C.L. Direct central nervous system delivery provides enhanced protection following vector mediated gene replacement in a severe model of spinal muscular atrophy. Biochem Biophys Res Commun 2012, 417:376-381.
54. Gogliotti R.G., Quinlan K.A., Barlow C.B., Heier C.R., Heckman C.J., Didonato C.J. Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, no a cause, of motor neuron dysfunction. J Neurosci 2012, 32:3818-3829.
55. Gowing G., Svendsen C.N. Stem cell transplantation for motor neuron disease: current approaches and future perspectives. Neurotherapeutics 2011, 8:591-606.
56. Gregory M.A., Qi Y., Hann S.R. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J Biol Chem 2003, 278:51606-51612.
57. Guettier-Sigrist S., Hugel B., Coupin G., Freyssinet J.M., Poindron P., Warter J.M. Possible pathogenic role of muscle cell dysfunction in motor neuron death in spinal muscular atrophy. Muscle Nerve 2002, 25:700-708.
58. Haddad H., Cifuentes-Diaz C., Miroglio A., Roblot N., Joshi V., Melki J. Riluzole attenuates spinal muscular atrophy disease progression in a mouse model. Muscle Nerve 2003, 28:432-437.
59. Harwood A.J., Agam G. Search for a common mechanism of mood stabilizers. Biochem Pharmacol 2003, 66:179-189.
60. Hashimoto R., Hough C., Nakazawa T., Yamamoto T., Chuang D.M. Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J Neurochem 2002, 80:589-597.
61. Hashimoto R., Takei N., Shimazu K., Christ L., Lu B., Chuang D.M. Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: an essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology 2002, 43:1173-1179.
62. Hayhurst M., Wagner A.K., Cerletti M., Wagers A.J., Rubin L.L. A cell-autonomous defect in skeletal muscle satellite cells expressing low levels of survival of motor neuron protein. Dev Biol 2012, 368:323-334.
63. Hu J.H., Zhang H., Wagey R., Krieger C., Pelech S.L. Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord. J Neurochem 2003, 85:432-442.
64. Hua Y., Sahashi K., Hung G., Rigo F., Passini M.A., Bennett C.F., Krainer A.R. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev 2010, 24:1634-1644.
65. Huo K., Sun Y., Li H., Du X., Wang X., Karlsson N., Zhu C., Blomgren K. Lithium reduced neural progenitor apoptosis in the hippocampus and ameliorated functional deficits after irradiation to the immature mouse brain. Mol Cell Neurosci 2012, 51:32-42.
66. Inestrosa N.C., Arenas E. Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 2010, 11:77-86.
67. Inestrosa N.C., Montecinos-Oliva C., Fuenzalida M. Wnt signaling: role in Alzheimer disease and schizophrenia. J Neuroimmune Pharmacol 2012, 7:788-807.
68. Jablonka S., Schrank B., Kralewski M., Rossoll W., Sendtner M. Reduced survival motor neuron (Smn) gene dose in mice leads to motor neuron degeneration: an animal model for spinal muscular atrophy type III. Hum Mol Genet 2000, 9:341-346.
69. Kariya S., Park G.H., Maeno-Hikichi Y., Leykekhman O., Lutz C., Arkovitz M.S., Landmesser L.T., Monani U.R. Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet 2008, 17:2552-2569.
70. Kinali M., Mercuri E., Main M., De Biasia F., Karatza A., Higgins R., Banks L.M., Manzur A.Y., Muntoni F. Pilot trial of albuterol in spinal muscular atrophy. Neurology 2002, 59:609-610.
71. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 1996, 93:8455-8459.
72. Koh S.H., Kim Y., Kim H.Y., Hwang S., Lee C.H., Kim S.H. Inhibition of glycogen synthase kinase-3 suppresses the onset of symptoms and disease progression of G93A-SOD1 mouse model of ALS. Exp Neurol 2007, 205:336-346.
73. Koh S.H., Lee Y.B., Kim K.S., Kim H.J., Kim M., Lee Y.J., Kim J., Lee K.W., Kim S.H. Role of GSK-3β activity in motor neuronal cell death induced by G93A or A4V mutant hSOD1 gene. Eur J Neurosci 2005, 22:301-309.
74. Kong L., Wang X., Choe D.W., Polley M., Burnett B.G., Bosch-Marcé M., Griffin J.W., Rich M.M., Sumner C.J. Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 2009, 29:842-851.
75. Lee A.J., Awano T., Park G.H., Monani U.R. Limited phenotypic effects of selectively augmenting the SMN protein in the neurons of a mouse model of severe spinal muscular atrophy. PLoS One 2012, 7:e46353.
76. Lee Y.I., Mikesh M., Smith I., Rimer M., Thompson W. Muscles in a mouse model of spinal muscular atrophy show profound defects in neuromuscular development even in the absence of failure in neuromuscular transmission or loss of motor neurons. Dev Biol 2011, 356:432-444.
77. Lefebvre S., Bürglen L., Reboullet S., Clermont O., Burlet P., Viollet L., Benichou B., Cruaud C., Millasseau P., Zeviani M., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
78. Lefebvre S., Burlet P., Liu Q., Bertrandy S., Clermont O., Munnich A., Dreyfuss G., Melki J. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 1997, 16:265-269.
79. Lesbordes J.C., Cifuentes-Diaz C., Miroglio A., Joshi V., Bordet T., Kahn A., Melki J. Therapeutic benefits of cardiotrophin-1 gene transfer in a mouse model of spinal muscular atrophy. Hum Mol Genet 2003, 12:1233-1239.
80. Ling K.K., Lin M.Y., Zingg B., Feng Z., Ko C.P. Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS One 2010, 5:e15457.
81. Lorson C.L., Rindt H., Shababi M. Spinal muscular atrophy: mechanisms and therapeutic strategies. Hum Mol Genet 2010, 19:R111-118.
82. Lucas J.J., Hernández F., Gómez-Ramos P., Morán M.A., Hen R., Avila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice. EMBO J 2001, 20:27-39.
83. Lunn M.R., Wang C.H. Spinal muscular atrophy. Lancet 2008, 371:2120-2133.
84. Luo J. Lithium-mediated protection against ethanol neurotoxicity. Front Neurosci 2010, 4:41.
85. Lutz C.M., Kariya S., Patruni S., Osborne M.A., Liu D., Henderson C.E., Li D.K., Pellizzoni L., Rojas J., Valenzuela D.M., Murphy A.J., Winberg M.L., Monani U.R. Postsymptomatic restoration of SMN rescues the disease phenotype in a mouse model of severe spinal muscular atrophy. J Clin Invest 2011, 121:3029-3041.
86. Mailman M.D., Heinz J.W., Papp A.C., Snyder P.J., Sedra M.S., Wirth B., Burghes A.H., Prior T.W. Molecular analysis of spinal muscular atrophy and modification of the phenotype by SMN2. Genet Med 2002, 4:20-26.
87. Makhortova N.R., Hayhurst M., Cerqueira A., Sinor-Anderson A.D., Zhao W.N., Heiser P.W., Arvanites A.C., Davidow L.S., Waldon Z.O., Steen J.A., Lam K., Ngo H.D., Rubin L.L. A screen for regulators of survival of motor neuron protein levels. Nat Chem Biol 2011, 7:544-552.
88. Manji H.K., Moore G.J., Chen G. Lithium at 50: Have the neuroprotective effects of this unique cation been overlooked?. Biol Psychiatry 1999, 46:929-940.
89. Markowitz J.A., Singh P., Darras B.T. Spinal muscular atrophy: a clinical and research update. Pediatr Neurol 2012, 46:1-12.
90. Mattis V.B., Ebert A.D., Fosso M.Y., Chang C.W., Lorson C.L. Delivery of a read-through inducing compound, TC007, lessens the severity of a spinal muscular atrophy animal model. Hum Mol Genet 2009, 18:3906-3913.
91. Mentis G.Z., Blivis D., Liu W., Drobac E., Crowder M.E., Kong L., Alvarez F.J., Sumner C.J., O'Donovan M.J. Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 2011, 69:453-467.
92. Merlini L., Solari A., Vita G., Bertini E., Minetti C., Mongini T., Mazzoni E., Angelini C., Morandi L. Role of gabapentin in spinal muscular atrophy: results of a multicenter, randomized Italian study. J Child Neurol 2003, 18:537-541.
93. Miller R.G., Moore D.H., Dronsky V., Bradley W., Barohn R., Bryan W., Prior T.W., Gelinas D.F., Iannaccone S., Kissel J., Leshner R., Mendell J., Mendoza M., Russman B., Samaha F., Smith S. A placebo-controlled trial of gabapentin in spinal muscular atrophy. J Neurol Sci 2001, 191:127-131. SMA Study Group.
94. Miller R.G., Moore D.H., Forshew D.A., Katz J.S., Barohn R.J., Valan M., Bromberg M.B., Goslin K.L., Graves M.C., McCluskey L.F., McVey A.L., Mozaffar T., Florence J.M., Pestronk A., Ross M., Simpson E.P., Appel S.H. Phase II screening trial of lithium carbonate in amyotrophic lateral sclerosis: examining a more efficient trial design. Neurology 2011, 77:973-979. WALS Study Group.
95. Monani U.R. Spinal muscular atrophy: a deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron 2005, 48:885-896.
96. Monani U.R., Sendtner M., Coovert D.D., Parsons D.W., Andreassi C., Le T.T., Jablonka S., Schrank B., Rossoll W., Prior T.W., Morris G.E., Burghes A.H. The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet 2000, 9:333-339.
97. Morisco C., Seta K., Hardt S.E., Lee Y., Vatner S.F., Sadoshima J. Glycogen synthase kinase 3beta regulates GATA4 in cardiac myocytes. J Biol Chem 2001, 276:28586-28597.
98. 2B/- mouse model of spinal muscular atrophy. Neurobiol Dis 2013, 49:57-67.
99. Murray L.M., Comley L.H., Thomson D., Parkinson N., Talbot K., Gillingwater T.H. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum Mol Genet 2008, 17:949-962.
100. Mutsaers C.A., Wishart T.M., Lamont D.J., Riessland M., Schreml J., Comley L.H., Murray L.M., Parson SH S.H., Lochmüller H., Wirth B., Talbot K., Gillingwater T.H. Reversible molecular pathology of skeletal muscle in spinal muscular atrophy. Hum Mol Genet 2011, 20:4334-4344.
101. Narver H.L., Kong L., Burnett B.G., Choe D.W., Bosch-Marcé M., Taye A.A., Eckhaus M.A., Sumner C.J. Sustained improvement of spinal muscular atrophy mice treated with trichostatin A plus nutrition. Ann Neurol 2008, 64:465-470.
102. Nicole S., Desforges B., Millet G., Lesbordes J., Cifuentes-Diaz C., Vertes D., Cao M.L., De Backer F., Languille L., Roblot N., Joshi V., Gillis J.M., Melki J. Intact satellite cells lead to remarkable protection against Smn gene defect in differentiated skeletal muscle. J Cell Biol 2003, 161:571-582.
103. Nizzardo M., Nardini M., Ronchi D., Salani S., Donadoni C., Fortunato F., Colciago G., Falcone M., Simone C., Riboldi G., Govoni A., Bresolin N., Comi G.P., Corti S. Beta-lactam antibiotic offers neuroprotection in a spinal muscular atrophy model by multiple mechanisms. Exp Neurol 2011, 229:214-225.
104. 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., Duff K. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci USA 2005, 102:6990-6995.
105. Nonaka S., Chuang D.M. Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats. Neuroreport 1998, 9:2081-2084.
106. Nonaka S., Hough C.J., 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 USA 1998, 95:2642-2647.
107. Nonaka S., Katsube N., Chuang D.M. Lithium protects rat cerebellar granule cells against apoptosis induced by anticonvulsants, phenytoin and carbamazepine. J Pharmacol Exp Ther 1998, 286:539-547.
108. Oprea G.E., Kröber S., McWhorter M.L., Rossoll W., Müller S., Krawczak M., Bassell G.J., Beattie C.E., Wirth B. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 2008, 320:524-527.
109. Pane M., Staccioli S., Messina S., D'Amico A., Pelliccioni M., Mazzone E.S., Cuttini M., Alfieri P., Battini R., Main M., Muntoni F., Bertini E., Villanova M., Mercuri E. Daily salbutamol in young patients with SMA type II. Neuromuscul Disord 2008, 18:536-540.
110. Park G.H., Maeno-Hikichi Y., Awano T., Landmesser L.T., Monani U.R. Reduced survival of motor neuron (SMN) protein in motor neuronal progenitors functions cell autonomously to cause spinal muscular atrophy in model mice expressing the human centromeric (SMN2) gene. J Neurosci 2010, 30:12005-12019.
111. Passini M.A., Bu J., Roskelley E.M., Richards A.M., Sardi S.P., O'Riordan C.R., Klinger K.W., Shihabuddin L.S., Cheng S.H. CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. Clin Invest 2010, 120:1253-1264.
112. Passini M.A., Cheng S.H. Prospects for the gene therapy of spinal muscular atrophy. Trends Mol Med 2011, 17:259-265.
113. Pellizzoni L., Kataoka N., Charroux B., Dreyfuss G. A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 1998, 95:615-624.
114. Pizzasegola C., Caron I., Daleno C., Ronchi A., Minoia C., Carrì M.T., Bendotti C. Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice. Amyotroph Lateral Scler 2009, 10:221-228.
115. Pruss R.M., Giraudon-Paoli M., Morozova S., Berna P., Abitbol J.L., Bordet T. Drug discovery and development for spinal muscular atrophy: lessons from screening approaches and future challenges for clinical development. Future Med Chem 2010, 2:1429-1440.
116. Rajendra T.K., Gonsalvez G.B., Walker M.P., Shpargel K.B., Salz H.K., Matera A.G. A Drosophila melanogaster model of spinal muscular atrophy reveals a function for SMN in striated muscle. J Cell Biol 2007, 176:831-841.
117. Ren M., Senatorov V.V., Chen R.W., Chuang D.M. Postinsult treatment with lithium reduces brain damage and facilitates neurological recovery in a rat ischemia/reperfusion model. Proc Natl Acad Sci USA 2003, 100:6210-6215.
118. Riessland M., Ackermann B., Förster A., Jakubik M., Hauke J., Garbes L., Fritzsche I., Mende Y., Blumcke I., Hahnen E., Wirth B. SAHA ameliorates the SMA phenotype in two mouse models for spinal muscular atrophy. Hum Mol Genet 2010, 19:1492-1506.
119. Rigo F., Hua Y., Krainer A.R., Bennett C.F. Antisense-based therapy for the treatment of spinal muscular atrophy. J Cell Biol 2012, 199:21-25.
120. Rose F.F., Mattis V.B., Rindt H., Lorson C.L. Delivery of recombinant follistatin lessens disease severity in a mouse model of spinal muscular atrophy. Hum Mol Genet 2009, 18:997-1005.
121. Ruggiu M., McGovern V.L., Lotti F., Saieva L., Li D.K., Kariya S., Monani U.R., Burghes A.H., Pellizzoni L. A role for SMN exon 7 splicing in the selective vulnerability of motor neurons in spinal muscular atrophy. Mol Cell Biol 2012, 32:126-138.
122. 2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J Neurosci 2010, 30:849-857.
123. Schreml J., Riessland M., Paterno M., Garbes L., Roßbach K., Ackermann B., Krämer J., Somers E., Parson S.H., Heller R., Berkessel A., Sterner-Kock A., Wirth B. Severe SMA mice show organ impairment that cannot be rescued by therapy with the HDACi JNJ-26481585. Eur J Hum Genet 2012, 10.1038/ejhg.2012.222.
124. Shababi M., Glascock J., Lorson C.L. Combination of SMN trans-splicing and a neurotrophic factor increases the life span and body mass in a severe model of spinal muscular atrophy. Hum Gene Ther 2011, 22:135-144.
125. Shin J.H., Cho S.I., Lim H.R., Lee J.K., Lee Y.A., Noh J.S., Joo I.S., Kim K.W., Gwag B.J. Concurrent administration of Neu 2000 and lithium produces marked improvement of motor neuron survival, motor function, and mortality in a mouse model of amyotrophic lateral sclerosis. Mol Pharmacol 2007, 71:965-975.
126. Simon C.M., Jablonka S., Ruiz R., Tabares L., Sendtner M. Ciliary neurotrophic factor-induced sprouting preserves motor function in a mouse model of mild spinal muscular atrophy. Hum Mol Genet 2010, 19:973-986.
127. Singh J., Salcius M., Liu S.W., Staker B.L., Mishra R., Thurmond J., Michaud G., Mattoon D.R., Printen J., Christensen J., Bjornsson J.M., Pollok B.A., Kiledjian M., Stewart L., Jarecki J., Gurney M.E. DcpS as a therapeutic target for spinal muscular atrophy. ACS Chem Biol 2008, 3:711-722.
128. Sumner C.J. Therapeutics development for spinal muscular atrophy. NeuroRx 2006, 3:235-245.
129. Sumner C.J., Wee C.D., Warsing L.C., Choe D.W., Ng A.S., Lutz C., Wagner K.R. Inhibition of myostatin does not ameliorate disease features of severe spinal muscular atrophy mice. Hum Mol Genet 2009, 18:3145-3152.
130. Tews D.S., Goebel H.H. DNA fragmentation and BCL-2 expression in infantile spinal muscular atrophy. Neuromuscul Disord 1996, 6:265-273.
131. Thurmond J., Butchbach M.E., Palomo M., Pease B., Rao M., Bedell L., Keyvan M., Pai G., Mishra R., Haraldsson M., Andresson T., Bragason G., Thosteinsdottir M., Bjornsson J.M., Coovert D.D., Burghes A.H., Gurney M.E., Singh J. Synthesis and biological evaluation of novel 2,4-diaminoquinazoline derivatives as SMN2 promoter activators for the potential treatment of spinal muscular atrophy. J Med Chem 2008, 51:449-469.
132. Torres-Benito L., Neher M.F., Cano R., Ruiz R., Tabares L. SMN requirement for synaptic vesicle, active zone and microtubule postnatal organization in motor nerve terminals. PLoS One 2011, 6:e26164.
133. Tsai L.K. Therapy development for spinal muscular atrophy in SMN independent targets. Neural Plast 2012, 2012:456478. 10.1155/2012/456478.
134. Tsai L.K., Chen Y.C., Cheng W.C., Ting C.H., Dodge J.C., Hwu W.L., Cheng S.H., Passini M.A. IGF-1 delivery to CNS attenuates motor neuron cell death but does not improve motor function in type III SMA mice. Neurobiol Dis 2012, 45:272-279.
135. Tsai L.K., Tsai M.S., Ting C.H., Li H. Multiple therapeutic effects of valproic acid in spinal muscular atrophy model mice. J Mol Med (Berl) 2008, 86:1243-1254.
136. Valori C.F., Ning K., Wyles M., Mead R.J., Grierson A.J., Shaw P.J., Azzouz M. Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci Transl Med 2010, 2:35ra42.
137. Wada A., Yokoo H., Yanagita T., Kobayashi H. Lithium: potential therapeutics against acute brain injuries and chronic neurodegenerative diseases. J Pharmacol Sci 2005, 99:307-321.
138. Watcharasit P., Bijur G.N., Zmijewski J.W., Song L., Zmijewska A., Chen X., Johnson G.V., Jope R.S. Direct, activating interaction between glycogen synthase kinase-3beta and p53 after DNA damage. Proc Natl Acad Sci USA 2002, 99:7951-7955.
139. Wei H., Qin Z.H., Senatorov V.V., Wei W., Wang Y., Qian Y., Chuang D.M. Lithium suppresses excitotoxicity-induced striatal lesions in a rat model of Huntington's disease. Neuroscience 2001, 106:603-612.
140. Wirth B., Brichta L., Schrank B., Lochmüller H., Blick S., Baasner A., Heller R. Mildly affected patients with spinal muscular atrophy are partially protected by an increased SMN2 copy number. Hum Genet 2006, 119:422-428.
141. Wolstencroft E.C., Mattis V., Bajer A.A., Young P.J., Lorson C.L. A non-sequence-specific requirement for SMN protein activity: the role of aminoglycosides in inducing elevated SMN protein levels. Hum Mol Genet 2005, 14:1199-1210.
142. Wyatt T.J., Keirstead H.S. Stem cell-erived neurotrophic support for the neuromuscular junction in spinal muscular atrophy. Expert Opin Biol Ther 2010, 10:1587-1594.
143. Xu C., Kim N.G., Gumbiner B.M. Regulation of protein stability by GSK3 mediated phosphorylation. Cell Cycle 2009, 8:4032-4039.
144. Yoshioka W., Akagi T., Nishimura N., Shimizu H., Watanabe C., Tohyama C. Severe toxicity and cyclooxygenase (COX)-2 mRNA increase by lithium in the neonatal mouse kidney. J Toxicol Sci 2009, 34:519-525.
145. Zhang F., Phiel C.J., Spece L., Gurvich N., 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 2003, 278:33067-33077.