New insights into the pathogenesis of spinal muscular atrophy

Brain and Development

Volumn 33, Issue 4, 2011, Pages 321-331

  Ito, Yasushi ^a   Shibata, Noriyuki ^a   Saito, Kayoko ^a   Kobayashi, Makio ^a   Osawa, Makiko ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Ballooned neuron; Clinicopathological study; Programmed cell death; Spinal muscular atrophy (SMA); Survival motor neuron (SMN)

Indexed keywords

CASPASE 3; NEUROFILAMENT PROTEIN; PROTEIN BAX; PROTEIN BCL 2; SURVIVAL MOTOR NEURON PROTEIN;

ADOLESCENT; ARTICLE; CONTROLLED STUDY; FEMALE; FETUS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INFANT; MALE; MOTONEURON; NERVE CELL DEGENERATION; NISSL SUBSTANCE; PATHOGENESIS; PROTEIN EXPRESSION; SPINAL CORD; SPINAL MUSCULAR ATROPHY;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; FEMALE; FETUS; HUMANS; INFANT; MALE; NEURONS; SMN COMPLEX PROTEINS; SPINAL CORD; SPINAL MUSCULAR ATROPHIES OF CHILDHOOD;

EID: 79952312218     PISSN: 03877604     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.braindev.2010.06.009     Document Type: Article

References (49)

1. Osawa M, Shishikura K. Werdnig-Hoffmann disease and variants. In: Vinken PJ, Bruyn GW, Klawans HL, Vianney de Jong JM, editors, Handbook of clinical neurology, vol. 15, Diseases of the Motor System. Amsterdam. New York: Elsevier; 1991. p. 51-80.
2. Munsat T.L., Davies K.E. Meeting report: International SMA consortium meeting, Bonn, 1992. Neuromuscul Disord 1992, 2:423-428.
3. Lefebvre S., Burglen L., Reboullet S., Clermont O., Burlet P., Viollet L., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
4. Monani U.R., Lorson C.L., Parsons D.W., Prior T.W., Androphy E.J., Burghes A.H., 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. Roy N., Mahadevan M.S., McLean M., Shutler G., Yaraghi Z., Farahani R., et al. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 1995, 80:167-178.
6. Burglen L., Seroz T., Miniou P., Lefebvre S., Burlet P., Munnich A., et al. The gene encoding p44, a subunit of the transcription factor TFIIH, is involved in large-scale deletions associated with Werdnig-Hoffmann disease. Am J Hum Genet 1997, 60:72-79.
7. Burlet P., Huber C., Bertrandy S., Ludosky M.A., Zwaenepoel I., Clermont O., et al. The distribution of SMN protein complex in human fetal tissues and its alteration in spinal muscular atrophy. Hum Mol Genet 1998, 7:1927-1933.
8. La Bella V., Cisterni C., Salaun D., Pettmann B. Survival motor neuron (SMN) protein in rat is expressed as different molecular forms and is developmentally regulated. Eur J Neurosci 1998, 10:2913-2923.
9. Lefebvre S., Burlet P., Liu Q., Bertrandy S., Clermont O., Munnich A., et al. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 1997, 16:265-269.
10. Coovert D.D., Le T.T., McAndrew P.E., Strasswimmer J., Crawford T.O., Mendell J.R., et al. The survival motor neuron protein in spinal muscular atrophy. Hum Mol Genet 1997, 6:1205-1214.
11. Campbell L., Potter A., Ignatius J., Dubowitz V., Davies K. Genomic variation and gene conversion in spinal muscular atrophy: implications for disease process and clinical phenotype. Am J Hum Genet 1997, 61:40-50.
12. Araki S., Hayashi M., Tamagawa K., Saito M., Kato S., Komori T., et al. Neuropathological analysis in spinal muscular atrophy type II. Acta Neuropathol (Berl) 2003, 106:441-448.
13. Kuru S., Sakai M., Konagaya M., Yoshida M., Hashizume Y., Saito K. An autopsy case of spinal muscular atrophy type III (Kugelberg-Welander disease). Neuropathology 2009, 29:63-67.
14. Fidzianska A., Rafalowska J. Motoneuron death in normal and spinal muscular atrophy-affected human fetuses. Acta Neuropathol (Berl) 2002, 104:363-368.
15. Soler-Botija C., Ferrer I., Gich I., Baiget M., Tizzano E.F. Neuronal death is enhanced and begins during foetal development in type I spinal muscular atrophy spinal cord. Brain 2002, 125:1624-1634.
16. Simic G., Seso-Simic D., Lucassen P.J., Islam A., Krsnik Z., Cviko A., et al. Ultrastructural analysis and TUNEL demonstrate motor neuron apoptosis in Werdnig-Hoffmann disease. J Neuropathol Exp Neurol 2000, 59:398-407.
17. Liu Q., Dreyfuss G. A novel nuclear structure containing the survival of motor neurons protein. EMBO J 1996, 15:3555-3565.
18. Oppenheim R.W. Cell death during development of the nervous system. Annu Rev Neurosci 1991, 14:453-501.
19. Forger N.G., Breedlove S.M. Motoneuronal death during human fetal development. J Comp Neurol 1987, 264:118-122.
20. Young P.J., Day P.M., Zhou J., Androphy E.J., Morris G.E., Lorson C.L. A direct interaction between the survival motor neuron protein and p53 and its relationship to spinal muscular atrophy. J Biol Chem 2002, 277:2852-2859.
21. Lu J., Moochhala S., Kaur C., Ling E.A. Changes in apoptosis-related protein (p53, Bax, Bcl-2 and Fos) expression with DNA fragmentation in the central nervous system in rats after closed head injury. Neurosci Lett 2000, 290:89-92.
22. Cregan S.P., MacLaurin J.G., Craig C.G., Robertson G.S., Nicholson D.W., Park D.S., et al. Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J Neurosci 1999, 19:7860-7869.
23. Sato N., Sakuma C., Sato Y., Gould T.W., Oppenheim R.W., Yaginuma H. Distinct susceptibility of developing neurons to death following Bax overexpression in the chicken embryo. Cell Death Differ 2006, 13:435-445.
24. Hayashi M., Arai N., Murakami T., Yoshio M., Oda M., Matsuyama H. A study of cell death in Werdnig Hoffmann disease brain. Neurosci Lett 1998, 243:117-120.
25. Pumarola M., Anor S., Majo N., Borras D., Ferrer I. Spinal muscular atrophy in Holstein-Friesian calves. Acta Neuropathol (Berl) 1997, 93:178-183.
26. Kuan C.-Y., Roth K.A., Flavell R.A., Rakic P. Mechanisms of programmed cell death in the developmental brain. Trends Neurosci 2000, 23:291-297.
27. Yuan J., Lipinski M., Degterev A. Diversity in the mechanisms of neuronal cell death. Neuron 2003, 40:401-413.
28. Soler-Botija C., Ferrer I., Alvarez J.L., Baiget M., Tizzano E.F. Downregulation of Bcl-2 proteins in type I spinal muscular atrophy motor neurons during fetal development. J Neuropathol Exp Neurol 2003, 62:420-426.
29. Ikemoto A., Hirano A., Matsumoto S., Akiguchi I., Kimura J. Synaptophysin expression in the anterior horn of Werdnig-Hoffmann disease. J Neurol Sci 1996, 136:94-100.
30. Murayama S., Bouldin T.W., Suzuki K. Immunocytochemical and ultrastructural studies of Werdnig-Hoffmann disease. Acta Neuropathol (Berl) 1991, 81:408-417.
31. Fidzianska A., Rafalowska J., Glinka Z. Ultrastructural study of motoneurons in Werdnig-Hoffmann disease. Clin Neuropathol 1984, 3:260-265.
32. Price D.L., Porter K.R. The response of ventral horn neurons to axonal transection. J Cell Biol 1972, 53:24-37.
33. Gillardon F., Klimaschewski L., Wickert H., Krajewski S., Reed J.C., Zimmermann M. Expression pattern of candidate cell death effector proteins Bax, Bcl-2, Bcl-X, and c-Jun in sensory and motor neurons following sciatic nerve transaction in the rat. Brain Res 1996, 739:244-250.
34. Urbanits S., Budka H. Spinal pathology in spinal muscular atrophy in comparison with amyotrophic lateral sclerosis (in German). Wien Med Wochenschr 1996, 146:199-200.
35. Lippa C.F., Smith T.W. Chromatolytic neurons in Werdnig-Hoffmann disease contain phosphorylated neurofilaments. Acta Neuropathol (Berl) 1988, 77:91-94.
36. Kato S., Hirano A. Ubiquitin and phosphorylated neurofilament epitopes in ballooned neurons of the extraocular muscle nuclei in a case of Werdnig-Hoffmann disease. Acta Neuropathol (Berl) 1990, 80:334-337.
37. Hiraga T., Leipold H.W., Cash W.C., Troyer D.L. Reduced numbers and intense anti-ubiquitin immunostaining of bovine motor neurons affected with spinal muscular atrophy. J Neurol Sci 1993, 118:43-47.
38. Rogers N., Paine S., Bedford L., Layfield R. The ubiquitin-proteasome system: contributions to cell death or survival in neurodegeneration. Neuropathol Appl Neurobiol 2010, 36:113-124.
39. Fan L., Simard L.R. Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development. Hum Mol Genet 2002, 11:1605-1614.
40. Pagliardini S., Giavazzi A., Setola V., Lizier C., Di Luca M., DeBiasi S., et al. Subcellular localization and axonal transport of the survival motor neuron (SMN) protein in the developing rat spinal cord. Hum Mol Genet 2000, 9:47-56.
41. Bechade C., Rostaing P., Cisterni C., Kalisch R., La Bella V., Pettmann B., et al. Subcellular distribution of survival motor neuron (SMN) protein: possible involvement in nucleocytoplasmic and dendritic transport. Eur J Neurosci 1999, 11:293-304.
42. Broccolini A., Engel W.K., Askanas V. Localization of survival motor neuron protein in human apoptotic-like and regenerating muscle fibers, and neuromuscular junctions. Neuroreport 1999, 10:1637-1641.
43. Vyas S., Bechade C., Riveau B., Downward J., Triller A. Involvement of survival motor neuron (SMN) protein in cell death. Hum Mol Genet 2002, 11:2751-2764.
44. Kerr D.A., Nery J.P., Traystman R.J., Chau B.N., Hardwick J.M. Survival motor neuron protein modulates neuron-specific apoptosis. Proc Natl Acad Sci USA 2000, 97:13312-13317.
45. Iwahashi H., Eguchi Y., Yasuhara N., Hanafusa T., Matsuzawa Y., Tsujimoto Y. Synergistic anti-apoptotic activity between Bcl-2 and SMN implicated in spinal muscular atrophy. Nature 1997, 390:413-417.
46. La Bella V., Kallenbach S., Pettmann B. Expression and subcellular localization of two isoforms of the survival motor neuron protein in different cell types. J Neurosci Res 2000, 62:346-356.
47. Coovert D.D., Le T.T., Morris G.E., Man N.T., Kralewski M., Sendtner M., et al. Does the survival motor neuron protein (SMN) interact with Bcl-2?. J Med Genet 2000, 37:536-539.
48. Cifuentes-Diaz C., Nicole S., Velasco M.E., Borra-Cebrian C., Panozzo C., Frugier T., et al. Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum Mol Genet 2002, 11:1439-1447.
49. Frugier T., Tiziano F.D., Cifuentes-Diaz C., Miniou P., Roblot N., Dierich A., et al. Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum Mol Genet 2000, 9:849-858.