Temporal requirement for high SMN expression in SMA mice

Human Molecular Genetics

Volumn 20, Issue 18, 2011, Pages 3578-3591

  Le, Thanh T ^a   McGovern, Vicki L ^a   Alwine, Isaac E ^a   Wang, Xueyong ^b   Massoni Laporte, Aurelie ^a   Rich, Mark M ^b   Burghes, Arthur H M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; SURVIVAL MOTOR NEURON PROTEIN 1; SURVIVAL MOTOR NEURON PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIRTH RATE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; EMBRYO INDUCTION; EXPERIMENTAL MOUSE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MORPHOLOGY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NEUROMUSCULAR JUNCTION DISORDER; NEUROMUSCULAR SYNAPSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SPINAL MUSCULAR ATROPHY; SURVIVAL TIME; TRANSGENE;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HUMANS; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCULAR ATROPHY, SPINAL; SURVIVAL OF MOTOR NEURON 1 PROTEIN; SURVIVAL OF MOTOR NEURON 2 PROTEIN;

MUS;

EID: 80052219408     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr275     Document Type: Article

References (86)

1. Roberts, D.F., Chavez, J. and Court, S.D. (1970) The genetic component in child mortality. Arch. Dis. Child, 45, 33-38.
2. Crawford, T.O. and Pardo, C.A. (1996) The neurobiology of childhood spinal muscular atrophy. Neurobiol. Dis., 3, 97-110.
3. Lefebvre, S., Burglen, L., Reboullet, S., Clermont, O., Burlet, P., Viollet, L., Benichou, B., Cruaud, C., Millasseau, P., Zeviani, M. et al. (1995)Identification and characterization of a spinal muscular atrophy-determining gene. Cell, 80, 155-165.
4. 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. and Burghes, A.H. (1997) The survival motor neuron protein in spinal muscular atrophy. Hum. Mol. Genet., 6, 1205-1214.
5. Lefebvre, S., Burlet, P., Liu, Q., Bertrandy, S., Clermont, O., Munnich, A., Dreyfuss, G. and Melki, J. (1997) Correlation between severity and SMN protein level in spinal muscular atrophy. Nat. Genet., 16, 265-269.
6. Burghes, A.H. and Beattie, C.E. (2009) Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat. Rev. Neurosci., 10, 597-609.
7. Lorson, C.L., Hahnen, E., Androphy, E.J. and Wirth, B. (1999) A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl Acad. Sci. USA, 96, 6307-6311.
8. Monani, U.R., Lorson, C.L., Parsons, D.W., Prior, T.W., Androphy, E.J., Burghes, A.H. and McPherson, J.D. (1999) A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum. Mol. Genet., 8, 1177-1183.
9. Cartegni, L. and Krainer, A.R. (2002) Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet., 30, 377-384.
10. Kashima, T. and Manley, J.L. (2003) A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet., 34, 460-463.
11. Gennarelli, M., Lucarelli, M., Capon, F., Pizzuti, A., Merlini, L., Angelini, C., Novelli, G. and Dallapiccola, B. (1995) Survival motor neuron gene transcript analysis in muscles from spinal muscular atrophy patients. Biochem. Biophys. Res. Commun., 213, 342-348.
12. Parsons, D.W., McAndrew, P.E., Monani, U.R., Mendell, J.R., Burghes, A.H. and Prior, T.W. (1996) An 11 base pair duplication in exon 6 of the SMN gene produces a type I spinal muscular atrophy (SMA) phenotype: further evidence for SMN as the primary SMA-determining gene. Hum. Mol. Genet., 5, 1727-1732.
13. Lorson, C.L., Strasswimmer, J., Yao, J.M., Baleja, J.D., Hahnen, E., Wirth, B., Le, T., Burghes, A.H. and Androphy, E.J. (1998) SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat. Genet., 19, 63-66.
14. Lorson, C.L. and Androphy, E.J. (2000) An exonic enhancer is required for inclusion of an essential exon in the SMA-determining gene SMN. Hum. Mol. Genet., 9, 259-265.
15. Burnett, B.G., Munoz, E., Tandon, A., Kwon, D.Y., Sumner, C.J. and Fischbeck, K.H. (2009) Regulation of SMN protein stability. Mol. Cell Biol., 29, 1107-1115.
16. McAndrew, P.E., Parsons, D.W., Simard, L.R., Rochette, C., Ray, P.N., Mendell, J.R., Prior, T.W. and Burghes, A.H. (1997) Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number. Am. J. Hum. Genet., 60, 1411-1422.
17. Prior, T.W., Krainer, A.R., Hua, Y., Swoboda, K.J., Snyder, P.C., Bridgeman, S.J., Burghes, A.H. and Kissel, J.T. (2009) A positive modifier of spinal muscular atrophy in the SMN2 gene. Am. J. Hum. Genet., 85, 408-413.
18. Vezain, M., Saugier-Veber, P., Goina, E., Touraine, R., Manel, V., Toutain, A., Fehrenbach, S., Frebourg, T., Pagani, F., Tosi, M. et al. (2010) A rare SMN2 variant in a previously unrecognized composite splicing regulatory element induces exon 7 inclusion and reduces the clinical severity of spinal muscular atrophy. Hum. Mutat., 31, E1110-E1125.
19. Monani, U.R., Pastore, M.T., Gavrilina, T.O., Jablonka, S., Le, T.T., Andreassi, C., DiCocco, J.M., Lorson, C., Androphy, E.J., Sendtner, M. et al. (2003) A transgene carrying an A2G missense mutation in the SMN gene modulates phenotypic severity in mice with severe (type I) spinal muscular atrophy. J. Cell Biol., 160, 41-52.
20. Workman, E., Saieva, L., Carrel, T.L., Crawford, T.O., Liu, D., Lutz, C., Beattie, C.E., Pellizzoni, L. and Burghes, A.H. (2009) A SMN missense mutation complements SMN2 restoring snRNPs and rescuing SMA mice. Hum. Mol. Genet., 18, 2215-2229.
21. Liu, Q. and Dreyfuss, G. (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J., 15, 3555-3565.
22. Meister, G., Buhler, D., Pillai, R., Lottspeich, F. and Fischer, U. (2001) A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs. Nat. Cell. Biol., 3, 945-949.
23. Pellizzoni, L., Yong, J. and Dreyfuss, G. (2002) Essential role for the SMN complex in the specificity of snRNP assembly. Science, 298, 1775-1779.
24. Pellizzoni, L. (2007) Chaperoning ribonucleoprotein biogenesis in health and disease. EMBO Rep., 8, 340-345.
25. Schrank, B., Gotz, R., Gunnersen, J.M., Ure, J.M., Toyka, K.V., Smith, A.G. and Sendtner, M. (1997) Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc. Natl Acad. Sci. USA, 94, 9920-9925.
26. Monani, U.R., Sendtner, M., Coovert, D.D., Parsons, D.W., Andreassi, C., Le, T.T., Jablonka, S., Schrank, B., Rossol, W., Prior, T.W. et al. (2000) 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., 9, 333-339.
27. Hsieh-Li, H.M., Chang, J.G., Jong, Y.J., Wu, M.H., Wang, N.M., Tsai, C.H. and Li, H. (2000) A mouse model for spinal muscular atrophy. Nat. Genet., 24, 66-70.
28. Le, T.T., Pham, L.T., Butchbach, M.E., Zhang, H.L., Monani, U.R., Coovert, D.D., Gavrilina, T.O., Xing, L., Bassell, G.J. and Burghes, A.H. (2005) 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., 14, 845-857.
29. Gabanella, F., Butchbach, M.E., Saieva, L., Carissimi, C., Burghes, A.H. and Pellizzoni, L. (2007) Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS ONE, 2, e921.
30. Zhang, Z., Lotti, F., Dittmar, K., Younis, I., Wan, L., Kasim, M. and Dreyfuss, G. (2008) SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell, 133, 585-600.
31. Baumer, D., Lee, S., Nicholson, G., Davies, J.L., Parkinson, N.J., Murray, L.M., Gillingwater, T.H., Ansorge, O., Davies, K.E. and Talbot, K. (2009) Alternative splicing events are a late feature of pathology in a mouse model of spinal muscular atrophy. PLoS Genet., 5, e1000773.
32. Gavrilina, T.O., McGovern, V.L., Workman, E., Crawford, T.O., Gogliotti, R.G., DiDonato, C.J., Monani, U.R., Morris, G.E. and Burghes, A.H. (2008) Neuronal SMN expression corrects spinal muscular atrophy in severe SMA mice while muscle-specific SMN expression has no phenotypic effect. Hum. Mol. Genet., 17, 1063-1075.
33. Rossoll, W., Jablonka, S., Andreassi, C., Kroning, A.K., Karle, K., Monani, U.R. and Sendtner, M. (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol., 163, 801-812.
34. Jablonka, S., Beck, M., Lechner, B.D., Mayer, C. and Sendtner, M. (2007) Defective Ca2+ channel clustering in axon terminals disturbs excitability in motoneurons in spinal muscular atrophy. J. Cell Biol., 179, 139-149.
35. McWhorter, M.L., Monani, U.R., Burghes, A.H. and Beattie, C.E. (2003) Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J. Cell Biol., 162, 919-932.
36. McGovern, V.L., Gavrilina, T.O., Beattie, C.E. and Burghes, A.H. (2008) Embryonic motor axon development in the severe SMA mouse. Hum. Mol. Genet., 17, 2900-2909.
37. Kariya, S., Park, G.H., Maeno-Hikichi, Y., Leykekhman, O., Lutz, C., Arkovitz, M.S., Landmesser, L.T. and Monani, U.R. (2008) Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum. Mol. Genet., 17, 2552-2569.
38. Kong, L., Wang, X., Choe, D.W., Polley, M., Burnett, B.G., Bosch-Marce, M., Griffin, J.W., Rich, M.M. and Sumner, C.J. (2009) Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J. Neurosci., 29, 842-851.
39. Murray, L.M., Comley, L.H., Thomson, D., Parkinson, N., Talbot, K. and Gillingwater, T.H. (2008) 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., 17, 949-962.
40. Butchbach, M.E., Singh, J., Thorsteinsdottir, M., Saieva, L., Slominski, E., Thurmond, J., Andresson, T., Zhang, J., Edwards, J.D., Simard, L.R. et al. (2010) Effects of 2,4-diaminoquinazoline derivatives on SMNexpression and phenotype in a mouse model for spinal muscular atrophy. Hum. Mol. Genet., 19, 454-467.
41. 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. et al. (2007) Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J. Clin. Invest., 117, 659-671.
42. Narver, H.L., Kong, L., Burnett, B.G., Choe, D.W., Bosch-Marce, M., Taye, A.A., Eckhaus, M.A. and Sumner, C.J. (2008) Sustained improvement of spinal muscular atrophy mice treated with trichostatin A plus nutrition. Ann. Neurol., 64, 465-470.
43. Andreassi, C., Jarecki, J., Zhou, J., Coovert, D.D., Monani, U.R., Chen, X., Whitney, M., Pollok, B., Zhang, M., Androphy, E. et al. (2001) Aclarubicin treatment restores SMN levels to cells derived from type I spinal muscular atrophy patients. Hum. Mol. Genet., 10, 2841-2849.
44. Singh, J., Salcius, M., Liu, S.W., Staker, B.L., Mishra, R., Thurmond, J., Michaud, G., Mattoon, D.R., Printen, J., Christensen, J. et al. (2008) DcpS as a therapeutic target for spinal muscular atrophy. ACS Chem. Biol., 3, 711-722.
45. Riessland, M., Ackermann, B., Forster, A., Jakubik, M., Hauke, J., Garbes, L., Fritzsche, I., Mende, Y., Blumcke, I., Hahnen, E. et al. (2010) SAHA ameliorates the SMA phenotype in two mouse models for spinal muscular atrophy. Hum. Mol. Genet., 19, 1492-1506.
46. Hastings, M.L., Berniac, J., Liu, Y.H., Abato, P., Jodelka, F.M., Barthel, L., Kumar, S., Dudley, C., Nelson, M., Larson, K. et al. (2009) Tetracyclines that promote SMN2 exon 7 splicing as therapeutics for spinal muscular atrophy. Sci. Transl. Med., 1, 5ra12.
47. Mattis, V.B., Ebert, A.D., Fosso, M.Y., Chang, C.W. and Lorson, C.L. (2009) Delivery of a read-through inducing compound, TC007, lessens the severity of a spinal muscular atrophy animal model. Hum. Mol. Genet., 18, 3906-3913.
48. Hua, Y., Sahashi, K., Hung, G., Rigo, F., Passini, M.A., Bennett, C.F. and Krainer, A.R. (2010) Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev., 24, 1634-1644.
49. Singh, N.N., Shishimorova, M., Cao, L.C., Gangwani, L. and Singh, R.N. (2009) A short antisense oligonucleotide masking a unique intronic motif prevents skipping of a critical exon in spinal muscular atrophy. RNA Biol., 6, 341-350.
50. Burghes, A.H. and McGovern, V.L. (2010) Antisense oligonucleotides and spinal muscular atrophy: skipping along. Genes Dev., 24, 1574-1579.
51. Passini, M.A., Bu, J., Richards, A.M., Kinnecom, C., Sardi, S.P., Stanek, L.M., Hua, Y., Rigo, F., Matson, J., Hung, G. et al. (2011) Antisense oligonucleotides delivered to the mouse CNS ameliorate symptoms of severe spinal muscular atrophy. Sci. Transl. Med., 3, 72ra18.
52. 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. et al. (2010) Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol., 28, 271-274.
53. Passini, M.A., Bu, J., Roskelley, E.M., Richards, A.M., Sardi, S.P., O'Riordan, C.R., Klinger, K.W., Shihabuddin, L.S. and Cheng, S.H. (2010) CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. J. Clin. Invest., 120, 1253-1264.
54. Meyer, K., Marquis, J., Trub, J., Nlend Nlend, R., Verp, S., Ruepp, M.D., Imboden, H., Barde, I., Trono, D. and Schumperli, D. (2009) Rescue of a severe mouse model for spinal muscular atrophy by U7 snRNA-mediated splicing modulation. Hum. Mol. Genet., 18, 546-555.
55. Valori, C.F., Ning, K., Wyles, M., Mead, R.J., Grierson, A.J., Shaw, P.J. and Azzouz, M. (2010) Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci. Transl. Med., 2, 35ra42.
56. Dominguez, E., Marais, T., Chatauret, N., Benkhelifa-Ziyyat, S., Duque, S., Ravassard, P., Carcenac, R., Astord, S., de Moura, A.P., Voit, T. et al. (2010) Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum. Mol. Genet., 20, 681-693.
57. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D. and Kandel, E.R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science, 274, 1678-1683.
58. Belteki, G., Haigh, J., Kabacs, N., Haigh, K., Sison, K., Costantini, F., Whitsett, J., Quaggin, S.E. and Nagy, A. (2005) Conditional and inducible transgene expression in mice through the combinatorial use ofCre-mediated recombination and tetracycline induction. Nucleic Acids Res., 33, e51.
59. Hayashi, S., Lewis, P., Pevny, L. and McMahon, A.P. (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev., 119 (Suppl. 1), S97-S101.
60. Ling, K.K., Lin, M.Y., Zingg, B., Feng, Z. and Ko, C.P. (2010) Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS ONE, 5, e15457.
61. Ruiz, R., Casanas, J.J., Torres-Benito, L., Cano, R. and Tabares, L. (2010) Altered intracellular Ca2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J. Neurosci., 30, 849-857.
62. Murray, L.M., Lee, S., Baumer, D., Parson, S.H., Talbot, K. and Gillingwater, T.H. (2010) Pre-symptomatic development of lower motor neuron connectivity in a mouse model of severe spinal muscular atrophy. Hum. Mol. Genet., 19, 420-433.
63. Frugier, T., Tiziano, F.D., Cifuentes-Diaz, C., Miniou, P., Roblot, N., Dierich, A., Le Meur, M. and Melki, J. (2000) Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum. Mol. Genet., 9, 849-858.
64. Cifuentes-Diaz, C., Frugier, T., Tiziano, F.D., Lacene, E., Roblot, N., Joshi, V., Moreau, M.H. and Melki, J. (2001) Deletion of murine SMN exon 7 directed to skeletal muscle leads to severe muscular dystrophy. J. Cell Biol., 152, 1107-1114.
65. Vitte, J.M., Davoult, B., Roblot, N., Mayer, M., Joshi, V., Courageot, S., Tronche, F., Vadrot, J., Moreau, M.H., Kemeny, F. et al. (2004) Deletion of murine Smn exon 7 directed to liver leads to severe defect of liver development associated with iron overload. Am. J. Pathol., 165, 1731-1741.
66. Naciff, J.M., Behbehani, M.M., Misawa, H. and Dedman, J.R. (1999) Identification and transgenic analysis of a murine promoter that targets cholinergic neuron expression. J. Neurochem., 72, 17-28.
67. Misawa, H., Nakata, K., Toda, K., Matsuura, J., Oda, Y., Inoue, H., Tateno, M. and Takahashi, R. (2003) VAChT-Cre. Fast and VAChT-Cre.Slow: postnatal expression of Cre recombinase in somatomotor neurons with different onset. Genesis, 37, 44-50.
68. Park, G.H., Maeno-Hikichi, Y., Awano, T., Landmesser, L.T. and Monani, U.R. (2010) 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., 30, 12005-12019.
69. Mentis, G.Z., Blivis, D., Liu, W., Drobac, E., Crowder, M.E., Kong, L., Alvarez, F.J., Sumner, C.J. and O'Donovan, M.J. (2011) Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron, 69, 453-467.
70. Rossoll, W. and Bassell, G.J. (2009) Spinal muscular atrophy and a model for survival of motor neuron protein function in axonal ribonucleoprotein complexes. Results Probl. Cell. Differ., 48, 289-326.
71. Cheever, T.R., Olson, E.A. and Ervasti, J.M. (2011) Axonal regeneration and neuronal function are preserved in motor neurons lacking ss-actin in vivo. PLoS ONE, 6, e17768.
72. Li, Q., Lee, J.A. and Black, D.L. (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci., 8, 819-831.
73. Foust, K.D., Nurre, E., Montgomery, C.L., Hernandez, A., Chan, C.M. and Kaspar, B.K. (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol., 27, 59-65.
74. Duque, S., Joussemet, B., Riviere, C., Marais, T., Dubreil, L., Douar, A.M., Fyfe, J., Moullier, P., Colle, M.A. and Barkats, M. (2009) Intravenous Administration of Self-complementary AAV9 Enables Transgene Delivery to Adult Motor Neurons. Mol. Ther., 17, 1187-1196.
75. Swoboda, K.J. (2010) Seize the day: Newborn screening for SMA. Am. J. Med. Genet. A, 152A, 1605-1607.
76. Swoboda, K.J., Prior, T.W., Scott, C.B., McNaught, T.P., Wride, M.C., Reyna, S.P. and Bromberg, M.B. (2005) Natural history of denervation in SMA: relation to age, SMN2 copy number, and function. Ann. Neurol., 57, 704-712.
77. Lewelt, A., Krosschell, K.J., Scott, C., Sakonju, A., Kissel, J.T., Crawford, T.O., Acsadi, G., D'Anjou, G., Elsheikh, B., Reyna, S.P. et al. (2010) Compound muscle action potential and motor function in children with spinal muscular atrophy. Muscle Nerve, 42, 703-708.
78. Bevan, A.K., Hutchinson, K.R., Foust, K.D., Braun, L., McGovern, V.L., Schmelzer, L., Ward, J.G., Petruska, J.C., Lucchesi, P.A., Burghes, A.H. et al.. (2010) Early heart failure in the SMN{Delta}7 model of spinal muscular atrophy and correction by postnatal scAAV9-SMN delivery. Hum. Mol. Genet., 19, 3895-3905.
79. Heier, C.R., Satta, R., Lutz, C. and DiDonato, C.J. (2010) Arrhythmia and cardiac defects are a feature of spinal muscular atrophy model mice. Hum. Mol. Genet., 19, 3906-3918.
80. Shababi, M., Habibi, J., Yang, H.T., Vale, S.M., Sewell, W.A. and Lorson, C.L. (2010) Cardiac defects contribute to the pathology of spinal muscular atrophy models. Hum. Mol. Genet., 19, 4059-4071.
81. Le, T.T., Coovert, D.D., Monani, U.R., Morris, G.E. and Burghes, A.H. (2000) The survival motor neuron (SMN) protein: effect of exon loss and mutation on protein localization. Neurogenetics, 3, 7-16.
82. Gogliotti, R.G., Lutz, C., Jorgensen, M., Huebsch, K., Koh, S. and Didonato, C.J. (2011) Characterization of a commonly used mouse model of SMA reveals increased seizure susceptibility and heightened fear response in FVB/N mice. Neurobiol. Dis, 43, 142-151.
83. Heier, C.R., Gogliotti, R.G. and DiDonato, C.J. (2007) SMN transcript stability: could modulation of messenger RNA degradation provide a novel therapy for spinal muscular atrophy? J. Child Neurol., 22, 1013-1018.
84. Wang, X., Engisch, K.L., Li, Y., Pinter, M.J., Cope, T.C. and Rich, M.M. (2004) Decreased synaptic activity shifts the calcium dependence of release at the mammalian neuromuscular junction in vivo. J. Neurosci., 24, 10687-10692.
85. Wang, X., Engisch, K.L., Teichert, R.W., Olivera, B.M., Pinter, M.J. and Rich, M.M. (2006) Prolongation of evoked and spontaneous synaptic currents at the neuromuscular junction after activity blockade is caused by the upregulation of fetal acetylcholine receptors. J. Neurosci., 26, 8983-8987.
86. Wang, X., Pinter, M.J. and Rich, M.M. (2010) Ca2+ dependence of the binomial parameters p and n at the mouse neuromuscular junction. J. Neurophysiol., 103, 659-666.