Molecular, genetic and stem cell-mediated therapeutic strategies for spinal muscular atrophy (SMA)

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 2, 2014, Pages 187-196

  Zanetta, Chiara ^a   Riboldi, Giulietta ^a   Nizzardo, Monica ^a   Simone, Chiara ^a   Faravelli, Irene ^a   Bresolin, Nereo ^a   Comi, Giacomo P ^a   Corti, Stefania ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Antisense oligonucleotides; Gene therapy; Induced pluripotent stem cells; Molecular therapy; Morpholino; Spinal muscular atrophy; Stem cell therapy

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MORPHOLINO OLIGONUCLEOTIDE; SMN1 PROTEIN, HUMAN; SURVIVAL MOTOR NEURON PROTEIN 1;

ANIMAL; ANTISENSE OLIGONUCLEOTIDES; ARTICLE; BIOLOGICAL THERAPY; CYTOLOGY; DISEASE MODEL; GENE THERAPY; GENETICS; HUMAN; INFANT; METABOLISM; METHODOLOGY; MOLECULAR THERAPY; MORPHOLINO; MOTONEURON; MUTATION; PATHOLOGY; PHYSIOLOGY; PLURIPOTENT STEM CELL; SPINAL CORD; SPINAL MUSCULAR ATROPHY; STEM CELL TRANSPLANTATION; STEM-CELL THERAPY;

ANTISENSE OLIGONUCLEOTIDES; GENE THERAPY; INDUCED PLURIPOTENT STEM CELLS; MOLECULAR THERAPY; MORPHOLINO; SPINAL MUSCULAR ATROPHY; STEM-CELL THERAPY;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; DISEASE MODELS, ANIMAL; GENETIC THERAPY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INFANT; MORPHOLINOS; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; MUTATION; OLIGONUCLEOTIDES, ANTISENSE; SPINAL CORD; STEM CELL TRANSPLANTATION; SURVIVAL OF MOTOR NEURON 1 PROTEIN;

EID: 84893677349     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12224     Document Type: Article

References (53)

1. Ogino S, Leonard DG, Rennert H, et al. Genetic risk assessment in carrier testing for spinal muscular atrophy. Am J Med Genet. 2002; 110: 301-7.
2. Prior TW. Spinal muscular atrophy: a time for screening. Curr Opin Pediatr. 2010; 22: 696-702.
3. Brzustowicz LM, Lehner T, Castilla LH, et al. Genetic mapping of chronic childhood-onset spinal muscular atrophy to chromosome 5q11.2-13.3. Nature. 1990; 344: 540-1.
4. Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995; 80: 155-65.
5. Munsat TL, Davies KE. International SMA consortium meeting (26-28 June 1992, Bonn, Germany). Neuromuscul Disord. 1992; 2: 423-8.
6. Wang CH, Finkel RS, Bertini ES, et al. Consensus statement for standard of care in spinal muscular atrophy. J Child Neurol. 2007; 22: 1027-49.
7. D'Amico A, Mercuri E, Tiziano FD, et al. Spinal muscular atrophy. Orphanet J Rare Dis. 2011; 6: 71.
8. Williams JH, Schray RC, Patterson CA, et al. Oligonucleotide mediated survival of motor neuron protein expression in CNS improves phenotype in a mouse model of spinal muscular atrophy. J Neurosci. 2009; 29: 7633-8.
9. 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: 1634-44.
10. Passini MA, Bu J, Richards AM, et al. Antisense oligonucleotides delivered to the mouse CNS ameliorate symptoms of severe spinal muscular atrophy. Sci Transl Med. 2011; 3: 72ra18.
11. Singh NK, Singh NN, Androphy EJ, et al. 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: 1333-46.
12. Hua Y, Vickers TA, Baker BF, et al. Enhancement of SMN2 exon 7 inclusion by antisense oligonucleotides targeting the exon. PLoS Biol. 2007; 5: e73.
13. Hua Y, Vickers TA, Okunola HL, et al. Antisense masking of an hnRNP A1/A2 intronic splicing silencer corrects SMN2 splicing in transgenic mice. Am J Hum Genet. 2008; 82: 834-48.
14. Cartegni L, Krainer AR. Correction of disease-associated exon skipping by synthetic exonspecific activators. Nat Struct Biol. 2003; 10: 120-5.
15. Skordis LA, Dunckley MG, Yue B, et al. Bifunctional antisense oligonucleotides provide a trans-acting splicing enhancer that stimulates SMN2 gene expression in patient fibroblasts. Proc Natl Acad Sci. 2003; 100: 4114-9.
16. Marquis J, Meyer K, Angehrn L, et al. Spinal muscular atrophy: SMN2 premRNA splicing corrected by a U7 snRNA derivative carrying a splicing enhancer sequence. Mol Ther. 2007; 15: 1479-86.
17. Osman EY, Yen PF, Lorson CL. Bifunctional RNAs targeting the intronic splicing silencer N1 increase SMN levels and reduce disease severity in an animal model of spinal muscular atrophy. Mol Ther. 2012; 20: 119-26.
18. Baughan TD, Dickson A, Osman EY, et al. 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: 1600-11.
19. Lim SR, Hertel KJ. Modulation of survival motor neuron pre-mRNA splicing by inhibition of alternative 3' splice site pairing. J Biol Chem. 2001; 276: 45476-83.
20. Madocsai C, Lim SR, Geib T, et al. Correction of SMN2 Pre-mRNA splicing by antisense U7 small nuclear RNAs. Mol Ther. 2005; 12: 1013-22.
21. Mitrpant C, Porensky P, Zhou H, et al. Improved antisense oligonucleotide design to suppress aberrant SMN2 gene transcript processing: towards a treatment for spinal muscular atrophy. PLoS ONE. 2013; 8: e62114.
22. Porensky PN, Mitrpant C, McGovern VL, et al. A single administration of morpholino antisense oligomer rescues spinal muscular atrophy in mouse. Hum Mol Genet. 2012; 21: 1625-38.
23. Singh NN, Shishimorova M, Cao LC, et al. A short antisense oligonucleotide masking a unique intronic motif prevents skipping of a critical exon in spinal muscular atrophy. RNA Biol. 2009; 6: 341-50.
24. Zhou H, Janghra N, Mitrpant C, et al. A novel morpholino oligomer targeting ISSN1 improves rescue of severe SMA transgenic mice. Hum Gene Ther. 2013; 24: 331-42.
25. Bowerman M, Murray LM, Beauvais A, et al. A critical smn threshold in mice dictates onset of an intermediate spinal muscular atrophy phenotype associated with a distinct neuromuscular junction pathology. Neuromuscul Disord. 2012; 22: 263-76.
26. Gavrilina TO, McGovern VL, Workman E, et al. Neuronal SMN expression corrects spinal muscular atrophy in severe SMA mice while muscle-specific SMN expression has no phenotypic effect. Hum Mol Genet. 2008; 17: 1063-75.
27. Passini M. Personal communication. Families of SMA International SMA Research Group Meeting, June 23. Bloomington, MN, 2012.
28. Goemans NM, Tulinius M, van den Akker JT, et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med. 2011; 364: 1513-22.
29. Singh NN, Lawler MN, Ottesen EW, et al. An intronic structure enabled by a long-distance interaction serves as a novel target for splicing correction in spinal muscular atrophy. Nucleic Acids Res. 2013; 41: 8144-65.
30. Muntoni F, Wood MJ. Targeting RNA to treat neuromuscular disease. Nat Rev Drug Discov. 2011; 10: 6216-37.
31. Hua Y, Sahashi K, Rigo F, et al. Peripheral SMN restoration is essential for long-term rescue of a severe spinal muscular atrophy mouse model. Nature. 2011; 478: 123-6.
32. 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: 271-4.
33. 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: 1253-64.
34. Valori CF, Ning K, Wyles M, et al. Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci Transl Med. 2010; 2: 35-42.
35. Dominguez E, Marais T, Chatauret N, et al. Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum Mol Genet. 2011; 20: 681-93.
36. Foust KD, Nurre E, Montgomery CL, et al. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol. 2009; 27: 59-65.
37. Naldini L, Blömer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996; 272: 263-7.
38. McCown TJ. Adeno-associated virus (AAV) vectors in the CNS. Curr Gene Ther. 2005; 5: 333-8.
39. Bartlett JS, Samulski RJ, McCown TJ. Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther. 1998; 9: 1181-6.
40. Mazarakis ND, Azzouz M, Rohll JB, et al. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet. 2001; 10: 2109-21.
41. Azzouz M, Le T, Ralph GS, et al. Lentivector-mediated SMN replacement in a mouse model of spinal muscular atrophy. J Clin Invest. 2004; 1: 1726-31.
42. Federici T, Taub JS, Baum GR, et al. Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Ther. 2012; 19: 852-9.
43. McCarty DM. Self-complementary AAV vectors; advances and applications. Mol Ther. 2008; 16: 1648-56.
44. Glascock JJ, Osman EY, Wetz MJ, et al. Decreasing disease severity in symptomatic, Smn(-/-);SMN2(+/+), spinal muscular atrophy mice following scAAV9-SMN delivery. Hum Gene Ther. 2012; 23: 330-5.
45. Wichterle H, Lieberam I, Porter JA, et al. Directed differentiation of embryonic stem cells into motor neurons. Cell. 2002; 110: 385-97.
46. Shin S, Dalton S, Stice SL. Human motor neuron differentiation from human embryonic stem cells. Stem Cells Dev. 2005; 14: 266-9.
47. Corti S, Locatelli F, Papadimitriou D, et al. Transplanted ALDHhiSSClo neural stem cells generate motor neurons and delay disease progression of nmd mice, an animal model of SMARD1. Hum Mol Genet. 2006; 15: 167-87.
48. Corti S, Nizzardo M, Nardini M, et al. Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J Clin Invest. 2008; 118: 3316-30.
49. Nistor G, Siegenthaler MM, Poirier SN, et al. Derivation of high purity neuronal progenitors from human embryonic stem cells. PLoS ONE. 2011; 6: e20692.
50. Wyatt TJ, Rossi SL, Siegenthaler MM, et al. Human motor neuron progenitor transplantation leads to endogenous neuronal sparing in 3 models of motor neuron loss. Stem Cells Int. 2011; 2011: 207230.
51. Corti S, Nizzardo M, Simone C, et al. Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy. Sci Transl Med. 2012; 4: 165ra162.
52. Le TT, Mc Govern VL, Alwine IE, et al. Temporal requirement for high SMN expression in SMA mice. Hum Mol Genet. 2011; 20: 3578-91.
53. Lutz CM, Kariya S, Patruni S, et al. Postsymptomatic restoration of SMN rescues the disease phenotype in a mouse model of severe spinal muscular atrophy. J Clin Invest. 2011; 121: 3029-41.