Molecular mechanisms of neurodegeneration in spinal muscular atrophy

Journal of Experimental Neuroscience

Volumn 10, Issue 1, 2016, Pages 39-49

  Ahmad, Saif ^a   Bhatia, Kanchan ^a   Kannan, Aannapoorna ^a   Gangwani, Laxman ^a  

^a Paul L Foster School of Medicine   (United States)

Author keywords

JNK; MND; ROCK; SMA; SMN; ZPR1

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4 PHENYLBUTYRIC ACID; ACLARUBICIN; ANTISENSE OLIGONUCLEOTIDE; AURINTRICARBOXYLIC ACID; BUTYRIC ACID; D 156844; FASUDIL; FOLLISTATIN; HISTONE DEACETYLASE INHIBITOR; HYDROXYUREA; LDN 76070; M 344; N METHYL DEXTRO ASPARTIC ACID; PANOBINOSTAT; PROLACTIN; QUERCETIN; QUINAZOLINE DERIVATIVE; RESVERATROL; RG 3039; SELUMETINIB; SMALL INTERFERING RNA; SURVIVAL MOTOR NEURON PROTEIN 1; TRICHOSTATIN A; UBEI 41; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID; VANADATE SODIUM; VORINOSTAT;

ALTERNATIVE RNA SPLICING; ARTICLE; DRUG EFFECT; DRUG TARGETING; GENE EXPRESSION; GENE MUTATION; HUMAN; MOTONEURON; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMN1 GENE; SMN2 GENE; SPINAL MUSCULAR ATROPHY; TRANSCRIPTION REGULATION;

EID: 84962274560     PISSN: None     EISSN: 11790695     Source Type: Journal    
DOI: 10.4137/JEn.s33122     Document Type: Article

References (127)

1. D'Amico A, Mercuri E, Tiziano FD, Bertini E. Spinal muscular atrophy. Orphanet J Rare Dis. 2011;6:71.
2. Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80:155-165.
3. Lorson CL, Hahnen E, Androphy EJ, Wirth B. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A. 1999;96:6307-6311.
4. Monani UR, Lorson CL, Parsons DW, et al. A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum Mol Genet. 1999;8:1177-1183.
5. Cusco I, Barcelo MJ, Rojas-Garcia R, et al. SMN2 copy number predicts acute or chronic spinal muscular atrophy but does not account for intrafamilial variability in siblings. J Neurol. 2006;253:21-25.
6. Lefebvre S, Burlet P, Liu Q, et al. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet. 1997;16:265-269.
7. Prior TW, Krainer AR, Hua Y, et al. A positive modifier of spinal muscular atrophy in the SMN2 gene. Am J Hum Genet. 2009;85:408-413.
8. Crawford TO, Pardo CA. The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis. 1996;3:97-110.
9. Dubowitz V. Muscle disorders in childhood. Major Problems in Clinical Pediatrics. Vol 16. London; Philadelphia: Saunders; 1978:1-282.
10. Dubowitz V. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol. 1999;3:49-51.
11. Foust KD, Wang X, McGovern VL, et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol. 2010;28:271-274.
12. Gogliotti RG, Quinlan KA, Barlow CB, Heier CR, Heckman CJ, Didonato CJ. Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, not a cause, of motor neuron dysfunction. J Neurosci. 2012;32:3818-3829.
13. Hua Y, Sahashi K, Hung G, et al. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev. 2010;24:1634-1644.
14. Passini MA, Bu J, Roskelley EM, et al. CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. J Clin Invest. 2010;120:1253-1264.
15. Wirth B, Brichta L, Schrank B, et al. Mildly affected patients with spinal muscular atrophy are partially protected by an increased SMN2 copy number. Hum Genet. 2006;119:422-428.
16. Germain-Desprez D, Brun T, Rochette C, Semionov A, Rouget R, Simard LR. The SMN genes are subject to transcriptional regulation during cellular differentiation. Gene. 2001;279:109-117.
17. Boda B, Mas C, Giudicelli C, et al. Survival motor neuron SMN1 and SMN2 gene promoters: identical sequences and differential expression in neurons and non-neuronal cells. Eur J Hum Genet. 2004;12:729-737.
18. Echaniz-Laguna A, Miniou P, Bartholdi D, Melki J. The promoters of the survival motor neuron gene (SMN) and its copy (SMNc) share common regulatory elements. Am J Hum Genet. 1999;64:1365-1370.
19. Farooq F, Molina FA, Hadwen J, et al. Prolactin increases SMN expression and survival in a mouse model of severe spinal muscular atrophy via the STAT5 pathway. J Clin Invest. 2011;121:3042-3050.
20. Ting CH, Lin CW, Wen SL, Hsieh-Li HM, Li H. STAT5 constitutive activation rescues defects in spinal muscular atrophy. Hum Mol Genet. 2007;16:499-514.
21. Hsieh-Li HM, Chang JG, Jong YJ, et al. A mouse model for spinal muscular atrophy. Nat Genet. 2000;24:66-70.
22. Monani UR, Sendtner M, Coovert DD, et al. 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.
23. Biondi O, Branchu J, Sanchez G, et al. 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.
24. Branchu J, Biondi O, Chali F, et al. Shift from extracellular signal-regulated kinase to AKT/cAMP response element-binding protein pathway increases survival-motor-neuron expression in spinal-muscular-atrophy-like mice and patient cells. J Neurosci. 2013;33:4280-4294.
25. Biondi O, Branchu J, Ben Salah A, et al. IGF-1R reduction triggers neuroprotective signaling pathways in spinal muscular atrophy mice. J Neurosci. 2015;35:12063-12079.
26. Jarecki J, Chen X, Bernardino A, et al. Diverse small-molecule modulators of SMN expression found by high-throughput compound screening: early leads towards a therapeutic for spinal muscular atrophy. Hum Mol Genet. 2005;14:2003-2018.
27. Liu H, Rodgers ND, Jiao X, Kiledjian M. The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J. 2002;21:4699-4708.
28. Singh J, Salcius M, Liu SW, et al. DcpS as a therapeutic target for spinal muscular atrophy. ACS Chem Biol. 2008;3:711-722.
29. Butchbach ME, Singh J, Thorsteinsdottir M, et al. 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.
30. Harris AW, Butchbach ME. The effect of the DcpS inhibitor D156844 on the protective action of follistatin in mice with spinal muscular atrophy. Neuromuscul Disord. 2015;25:699-705.
31. Van Meerbeke JP, Gibbs RM, Plasterer HL, et al. The DcpS inhibitor RG3039 improves motor function in SMA mice. Hum Mol Genet. 2013;22:40744083.
32. Gogliotti RG, Cardona H, Singh J, et al. The DcpS inhibitor RG3039 improves survival, function and motor unit pathologies in two SMA mouse models. Hum Mol Genet. 2013;22:4084-4101.
33. Andreassi C, Angelozzi C, Tiziano FD, et al. Phenylbutyrate increases SMN expression in vitro: relevance for treatment of spinal muscular atrophy. Eur J Hum Genet. 2004;12:59-65.
34. Avila AM, Burnett BG, Taye AA, et al. Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J Clin Invest. 2007;117:659-671.
35. Brichta L, Hofmann Y, Hahnen E, et al. 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.
36. Brichta L, Holker I, Haug K, Klockgether T, Wirth B. In vivo activation of SMN in spinal muscular atrophy carriers and patients treated with valproate. Ann Neurol. 2006;59:970-975.
37. Chang JG, Hsieh-Li HM, Jong YJ, Wang NM, Tsai CH, Li H. Treatment of spinal muscular atrophy by sodium butyrate. Proc Natl Acad Sci U S A. 2001;98:9808-9813.
38. Garbes L, Riessland M, Holker I, et al. LBH589 induces up to 10-fold SMN protein levels by several independent mechanisms and is effective even in cells from SMA patients non-responsive to valproate. Hum Mol Genet. 2009;18:3645-3658.
39. Riessland M, Ackermann B, Forster A, et al. SAHA ameliorates the SMA phenotype in two mouse models for spinal muscular atrophy. Hum Mol Genet. 2010;19:1492-1506.
40. Riessland M, Brichta L, Hahnen E, Wirth B. The benzamide M344, a novel histone deacetylase inhibitor, significantly increases SMN2 RNA/protein levels in spinal muscular atrophy cells. Hum Genet. 2006;120:101-110.
41. Sumner CJ, Huynh TN, Markowitz JA, et al. Valproic acid increases SMN levels in spinal muscular atrophy patient cells. Ann Neurol. 2003;54:647-654.
42. Grzeschik SM, Ganta M, Prior TW, Heavlin WD, Wang CH. Hydroxyurea enhances SMN2 gene expression in spinal muscular atrophy cells. Ann Neurol. 2005;58:194-202.
43. Liang WC, Yuo CY, Chang JG, et al. The effect of hydroxyurea in spinal muscular atrophy cells and patients. J Neurol Sci. 2008;268:87-94.
44. Dayangac-Erden D, Bora G, Ayhan P, et al. Histone deacetylase inhibition activity and molecular docking of (e)-resveratrol: its therapeutic potential in spinal muscular atrophy. Chem Biol Drug Des. 2009;73:355-364.
45. Cherry JJ, Osman EY, Evans MC, et al. Enhancement of SMN protein levels in a mouse model of spinal muscular atrophy using novel drug-like compounds. EMBO Mol Med. 2013;5:1035-1050.
46. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998;19:225-268.
47. Darnell JE Jr, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 1994;264:1415-1421.
48. Digicaylioglu M, Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature. 2001;412:641-647.
49. Li WX. Canonical and non-canonical JAK-STAT signaling. Trends Cell Biol. 2008;18:545-551.
50. Murray PJ. The JAK-STAT signaling pathway: input and output integration. J Immunol. 2007;178:2623-2629.
51. Andreassi C, Jarecki J, Zhou J, et al. Aclarubicin treatment restores SMN levels to cells derived from type I spinal muscular atrophy patients. Hum Mol Genet. 2001;10:2841-2849.
52. Goffin V, Binart N, Clement-Lacroix P, et al. From the molecular biology of prolactin and its receptor to the lessons learned from knockout mice models. Genet Anal. 1999;15:189-201.
53. Dal Mas A, Rogalska ME, Bussani E, Pagani F. Improvement of SMN2 pre-mRNA processing mediated by exon-specific U1 small nuclear RNA. Am J Hum Genet. 2015;96:93-103.
54. Howell MD, Singh NN, Singh RN. Advances in therapeutic development for spinal muscular atrophy. Future Med Chem. 2014;6:1081-1099.
55. Hua Y, Vickers TA, Baker BF, Bennett CF, Krainer AR. Enhancement of SMN2 exon 7 inclusion by antisense oligonucleotides targeting the exon. PLoS Biol. 2007;5:e73.
56. Nizzardo M, Simone C, Dametti S, et al. Spinal muscular atrophy phenotype is ameliorated in human motor neurons by SMN increase via different novel RNA therapeutic approaches. Sci Rep. 2015;5:11746.
57. Palacino J, Swalley SE, Song C, et al. SMN2 splice modulators enhance U1-pre-mRNA association and rescue SMA mice. Nat Chem Biol. 2015;11:511-517.
58. Singh NK, Singh NN, Androphy EJ, Singh RN. Splicing of a critical exon of human survival motor neuron is regulated by a unique silencer element located in the last intron. Mol Cell Biol. 2006;26:1333-1346.
59. Singh NN, Shishimorova M, Cao LC, Gangwani L, Singh RN. A short antisense oligonucleotide masking a unique intronic motif prevents skipping of a critical exon in spinal muscular atrophy. RNA Biol. 2009;6:341-350.
60. Zhang Z, Kelemen O, van Santen MA, et al. Synthesis and characterization of pseudocantharidins, novel phosphatase modulators that promote the inclusion of exon 7 into the SMN (survival of motoneuron) pre-mRNA. J Biol Chem. 2011;286:10126-10136.
61. Naryshkin NA, Weetall M, Dakka A, et al. Motor neuron disease. SMN2 splicing modifiers improve motor function and longevity in mice with spinal muscular atrophy. Science. 2014;345:688-693.
62. Porensky PN, Burghes AH. Antisense oligonucleotides for the treatment of spinal muscular atrophy. Hum Gene Ther. 2013;24:489-498.
63. Singh NN, Lee BM, DiDonato CJ, Singh RN. Mechanistic principles of antisense targets for the treatment of spinal muscular atrophy. Future Med Chem. 2015;7:1793-1808.
64. Sivanesan S, Howell MD, Didonato CJ, Singh RN. Antisense oligonucleotide mediated therapy of spinal muscular atrophy. Transl Neurosci. 2013;4:1-7.
65. Faravelli I, Nizzardo M, Comi GP, Corti S. Spinal muscular atrophy-recent therapeutic advances for an old challenge. Nat Rev Neurol. 2015;11:351-359.
66. Burghes AH, Beattie CE. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci. 2009;10:597-609.
67. Monani UR. Spinal muscular atrophy: a deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron. 2005;48:885-896.
68. Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, Dotti CG. RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol. 2003;162:1267-1279.
69. Govek EE, Newey SE, Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 2005;19:1-49.
70. Hall A, Nobes CD. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci. 2000;355:965-970.
71. Hall A. Rho GTPases and the actin cytoskeleton. Science. 1998;279:509-514.
72. Schofield AV, Bernard O. Rho-associated coiled-coil kinase (ROCK) signaling and disease. Crit Rev Biochem Mol Biol. 2013;48:301-316.
73. Giesemann T, Rathke-Hartlieb S, Rothkegel M, et al. A role for polyproline motifs in the spinal muscular atrophy protein SMN. Profilins bind to and colocalize with SMN in nuclear gems. J Biol Chem. 1999;274:37908-37914.
74. Sharma A, Lambrechts A, Hao le T, et al. A role for complexes of survival of motor neurons (SMN) protein with gemins and profilin in neurite-like cytoplasmic extensions of cultured nerve cells. Exp Cell Res. 2005;309:185-197.
75. Bowerman M, Shafey D, Kothary R. SMN depletion alters profilin II expression and leads to upregulation of the RhoA/ROCK pathway and defects in neuronal integrity. J Mol Neurosci. 2007;32:120-131.
76. Nolle A, Zeug A, van Bergeijk J, et al. The spinal muscular atrophy disease protein SMN is linked to the Rho-kinase pathway via profilin. Hum Mol Genet. 2011;20:4865-4878.
77. Coque E, Raoul C, Bowerman M. ROCK inhibition as a therapy for spinal muscular atrophy: understanding the repercussions on multiple cellular targets. Front Neurosci. 2014;8:271.
78. Hensel N, Rademacher S, Claus P. Chatting with the neighbors: crosstalk between Rho-kinase (ROCK) and other signaling pathways for treatment of neurological disorders. Front Neurosci. 2015;9:198.
79. Hensel N, Stockbrugger I, Rademacher S, et al. Bilateral crosstalk of rho- and extracellular-signal-regulated-kinase (ERK) pathways is confined to an unidirectional mode in spinal muscular atrophy (SMA). Cell Signal. 2014;26:540-548.
80. Bruns AF, van Bergeijk J, Lorbeer C, et al. Fibroblast growth factor-2 regulates the stability of nuclear bodies. Proc Natl Acad Sci U S A. 2009;106:12747-12752.
81. Hensel N, Ratzka A, Brinkmann H, Klimaschewski L, Grothe C, Claus P. Analysis of the fibroblast growth factor system reveals alterations in a mouse model of spinal muscular atrophy. PLoS One. 2012;7:e31202.
82. Li G, Liu L, Shan C, et al. RhoA/ROCK/PTEN signaling is involved in AT-101-mediated apoptosis in human leukemia cells in vitro and in vivo. Cell Death Dis. 2014;5:e998.
83. Hopkins BD, Hodakoski C, Barrows D, Mense SM, Parsons RE. PTEN function: the long and the short of it. Trends Biochem Sci. 2014;39:183-190.
84. Genabai NK, Ahmad S, Zhang Z, Jiang X, Gabaldon CA, Gangwani L. Genetic inhibition of JNK3 ameliorates spinal muscular atrophy. Hum Mol Genet. 2015;24(24):6986-7004.
85. Ning K, Drepper C, Valori CF, et al. PTEN depletion rescues axonal growth defect and improves survival in SMN-deficient motor neurons. Hum Mol Genet. 2010;19:3159-3168.
86. Little D, Valori CF, Mutsaers CA, et al. PTEN depletion decreases disease severity and modestly prolongs survival in a mouse model of spinal muscular atrophy. Mol Ther. 2015;23:270-277.
87. Bowerman M, Beauvais A, Anderson CL, Kothary R. Rho-kinase inactivation prolongs survival of an intermediate SMA mouse model. Hum Mol Genet. 2010;19:1468-1478.
88. Bowerman M, Murray LM, Boyer JG, Anderson CL, Kothary R. Fasudil improves survival and promotes skeletal muscle development in a mouse model of spinal muscular atrophy. BMC Med. 2012;10:24.
89. Hammond SM, Gogliotti RG, Rao V, Beauvais A, Kothary R, DiDonato CJ. Mouse survival motor neuron alleles that mimic SMN2 splicing and are inducible rescue embryonic lethality early in development but not late. PLoS One. 2010;5:e15887.
90. Coffey ET. Nuclear and cytosolic JNK signalling in neurons. Nat Rev Neurosci. 2014;15:285-299.
91. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000;103:239-252.
92. Gupta S, Barrett T, Whitmarsh AJ, et al. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 1996;15:2760-2770.
93. Borsello T, Forloni G. JNK signalling: a possible target to prevent neurodegeneration. Curr Pharm Des. 2007;13:1875-1886.
94. Junyent F, Verdaguer E, Folch J, et al. Role of JNK in neurodegenerative diseases. In: Torrero DM, Haro D, Valles J, eds. Recent Advances in Pharmaceutical Sciences II. Transworld Research Network; 2012:15-28.
95. Xu P, Das M, Reilly J, Davis RJ. JNK regulates FoxO-dependent autophagy in neurons. Genes Dev. 2011;25:310-322.
96. Sunayama J, Tsuruta F, Masuyama N, Gotoh Y. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol. 2005;170:295-304.
97. Tournier C, Dong C, Turner TK, Jones SN, Flavell RA, Davis RJ. MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev. 2001;15:1419-1426.
98. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Genet Dev. 2002;12:1421.
99. Kim EK, Noh KT, Yoon JH, et al. Positive regulation of ASK1-mediated c-Jun NH(2)-terminal kinase signaling pathway by the WD-repeat protein Gemin5. Cell Death Differ. 2007;14:1518-1528.
100. Kelkar N, Gupta S, Dickens M, Davis RJ. Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3. Mol Cell Biol. 2000;20:1030-1043.
101. Hahnen E, Forkert R, Marke C, et al. Molecular analysis of candidate genes on chromosome 5q13 in autosomal recessive spinal muscular atrophy: evidence of homozygous deletions of the SMN gene in unaffected individuals. Hum Mol Genet. 1995;4:1927-1933.
102. McAndrew PE, Parsons DW, Simard LR, et al. Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number. Am J Hum Genet. 1997;60:1411-1422.
103. Oprea GE, Krober S, McWhorter ML, et al. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science. 2008;320:524-527.
104. Ahmad S, Wang Y, Shaik GM, Burghes AH, Gangwani L. The zinc finger protein ZPR1 is a potential modifier of spinal muscular atrophy. Hum Mol Genet. 2012;21:2745-2758.
105. Lyon AN, Pineda RH, Hao le T, Kudryashova E, Kudryashov DS, Beattie CE. Calcium binding is essential for plastin 3 function in SMN-deficient motoneurons. Hum Mol Genet. 2014;23:1990-2004.
106. Ackermann B, Krober S, Torres-Benito L, et al. Plastin 3 ameliorates spinal muscular atrophy via delayed axon pruning and improves neuromuscular junction functionality. Hum Mol Genet. 2013;22:1328-1347.
107. McGovern VL, Massoni-Laporte A, Wang X, et al. Plastin 3 expression does not modify spinal muscular atrophy severity in the 7 SMA mouse. PLoS One. 2015;10:e0132364.
108. Mishra AK, Gangwani L, Davis RJ, Lambright DG. Structural insights into the interaction of the evolutionarily conserved ZPR1 domain tandem with eukaryotic EF1A, receptors, and SMN complexes. Proc Natl Acad Sci U S A. 2007;104:13930-13935.
109. Galcheva-Gargova Z, Gangwani L, Konstantinov KN, et al. The cytoplasmic zinc finger protein ZPR1 accumulates in the nucleolus of proliferating cells. Mol Biol Cell. 1998;9:2963-2971.
110. Galcheva-Gargova Z, Konstantinov KN I, Wu H, Klier FG, Barrett T, Davis RJ. Binding of zinc finger protein ZPR1 to the epidermal growth factor receptor. Science. 1996;272:1797-1802.
111. Gangwani L, Mikrut M, Galcheva-Gargova Z, Davis RJ. Interaction of ZPR1 with translation elongation factor-1alpha in proliferating cells. J Cell Biol. 1998;143:1471-1484.
112. Gangwani L, Mikrut M, Theroux S, Sharma M, Davis RJ. Spinal muscular atrophy disrupts the interaction of ZPR1 with the SMN protein. Nat Cell Biol. 2001;3:376-383.
113. Helmken C, Hofmann Y, Schoenen F, et al. Evidence for a modifying pathway in SMA discordant families: reduced SMN level decreases the amount of its interacting partners and Htra2-beta1. Hum Genet. 2003;114:11-21.
114. Doran B, Gherbesi N, Hendricks G, Flavell RA, Davis RJ, Gangwani L. Deficiency of the zinc finger protein ZPR1 causes neurodegeneration. Proc Natl Acad Sci U S A. 2006;103:7471-7475.
115. Narayanan U, Ospina JK, Frey MR, Hebert MD, Matera AG. SMN, the spinal muscular atrophy protein, forms a pre-import snRNP complex with snurportin1 and importin beta. Hum Mol Genet. 2002;11:1785-1795.
116. Gangwani L, Flavell RA, Davis RJ. ZPR1 is essential for survival and is required for localization of the survival motor neurons (SMN) protein to Cajal bodies. Mol Cell Biol. 2005;25:27442756.
117. Gubitz AK, Feng W, Dreyfuss G. The SMN complex. Exp Cell Res. 2004;296:51-56.
118. Gangwani L. Deficiency of the zinc finger protein ZPR1 causes defects in transcription and cell cycle progression. J Biol Chem. 2006;281:40330-40340.
119. Wishart TM, Mutsaers CA, Riessland M, et al. Dysregulation of ubiquitin homeostasis and beta-catenin signaling promote spinal muscular atrophy. J Clin Invest. 2014;124:1821-1834.
120. Burnett BG, Munoz E, Tandon A, Kwon DY, Sumner CJ, Fischbeck KH. Regulation of SMN protein stability. Mol Cell Biol. 2009;29:1107-1115.
121. Korhonen L, Lindholm D. The ubiquitin proteasome system in synaptic and axonal degeneration: a new twist to an old cycle. J Cell Biol. 2004;165:27-30.
122. Ramser J, Ahearn ME, Lenski C, et al. Rare missense and synonymous variants in UBE1 are associated with X-linked infantile spinal muscular atrophy. Am J Hum Genet. 2008;82:188-193.
123. Park CH, Chang JY, Hahm ER, Park S, Kim HK, Yang CH. Quercetin, a potent inhibitor against beta-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun. 2005;328:227-234.
124. Chan YB, Miguel-Aliaga I, Franks C, et al. Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum Mol Genet. 2003;12:1367-1376.
125. McWhorter ML, Monani UR, Burghes AH, Beattie CE. Knockdown of the survival motor neuron (SMN) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J Cell Biol. 2003;162:919-931.
126. Hamilton G, Gillingwater TH. Spinal muscular atrophy: going beyond the motor neuron. Trends Mol Med. 2013;19:40-50.
127. Le TT, Pham LT, Butchbach ME, et al. SMNDelta7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum Mol Genet. 2005;14:845-857.