SMN, the product of the spinal muscular atrophy-determining gene, is expressed widely but selectively in the developing human forebrain

Journal of Comparative Neurology

Volumn 497, Issue 5, 2006, Pages 808-816

  Briese, Michael ^a   Richter, Dagmak Ulrike ^b   Sattelle, David B ^a   Ulfig, Norbert ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Anterior horn motor neuron; Basal nucleus of Meynert; Gem; Survival motor neuron; Thalamic reticular

Indexed keywords

MONOCLONAL ANTIBODY; SURVIVAL MOTOR NEURON PROTEIN;

AMYGDALOID NUCLEUS; ANTERIOR HORN CELL; ANTIBODY LABELING; ARTICLE; BRAIN DEVELOPMENT; CELL DENSITY; CELL NUCLEOPLASM; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL ULTRASTRUCTURE; CYTOPLASM; DISEASE SEVERITY; ENTORHINAL CORTEX; FETUS; FOREBRAIN; GENE; GENE FUNCTION; GESTATIONAL AGE; GLOBUS PALLIDUS; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MEYNERT BASAL NUCLEUS; MOTOR NEURON DISEASE; NEURITE; NEUROANATOMY; NEUROPATHOLOGY; NUCLEOLUS; PERIRETICULAR NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETICULAR NUCLEUS; SMN GENE; SPINAL MUSCULAR ATROPHY; THALAMUS;

ANTERIOR HORN CELLS; BASAL NUCLEUS OF MEYNERT; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GLOBUS PALLIDUS; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; NERVE TISSUE PROTEINS; NEURONS; PROSENCEPHALON; REFERENCE VALUES; RNA-BINDING PROTEINS; SPINAL CORD; THALAMUS; TISSUE DISTRIBUTION;

EID: 33745597622     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21010     Document Type: Article

References (47)

1. Araki S, Hayashi M, Tamagawa K, Saito M, Kato S, Komori T, Sakakihara Y, Mizutani T, Oda M. 2003. Neuropathological analysis in spinal muscular atrophy type II. Acta Neuropathol 106:441-448.
2. Battaglia G, Princivalle A, Forti F, Lizier C, Zeviani M. 1997. Expression of the SMN gene, the spinal muscular atrophy determining gene, in the mammalian central nervous system. Hum Mol Genet 6:1961-1971.
3. Bechade C, Rostaing P, Cisterni C, Kalisch R, La Bella V, Pettmann B, Triller A. 1999. Subcellular distribution of survival motor neuron (SMN) protein: possible involvement in nucleocytoplasmic and dendritic transport. Eur J Neurosci 11:293-304.
4. Briese M, Esmaeili B, Sattelle DB. 2005. Is spinal muscular atrophy the result of defects in motor neuron processes? Bioessays 27:946-957.
5. Burlet P, Huber C, Bertrandy S, Ludosky MA, Zwaenepoel I, Clermont O, Roume J, Delezoide AL, Cartaud J, Munnich A, Lefebvre S. 1998. The distribution of SMN protein complex in human fetal tissues and its alteration in spinal muscular atrophy. Hum Mol Genet 7:1927-1933.
6. Carissimi C, Saieva L, Baccon J, Chiarella P, Maiolica A, Sawyer A, Rappsilber J, Pellizzoni L. 2006. Gemin8 is a novel component of the survival motor neuron complex and functions in snRNP assembly. J Biol Chem 28:826-834.
7. Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M. 1999. The spinal muscular atrophy disease gene product, SMN: a link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 147:715-728.
8. Conner JM, Culberson A, Packowski C, Chiba AA, Tuszynski MH. 2003. Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38:819-829.
9. Coovert DD, Le TT, McAndrew PE, Strasswimmer J, Crawford TO, Mendell JR, Coulson SE, Androphy EJ, Prior TW, Burghes AH. 1997. The survival motor neuron protein in spinal muscular atrophy. Hum Mol Genet 6:1205-1214.
10. Dubowitz V. 1999. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol 3:49-51.
11. Francis JW, Sandrock AW, Bhide PG, Vonsattel JP, Brown RH Jr. 1998. Heterogeneity of subcellular localization and electrophoretic mobility of survival motor neuron (SMN) protein in mammalian neural cells and tissues. Proc Natl Acad Sci U S A 95:6492-6497.
12. Gangwani L, Mikrut M, Theroux S, Sharma M, Davis RJ. 2001. Spinal muscular atrophy disrupts the interaction of ZPR1 with the SMN protein. Nat Cell Biol 3:376-383.
13. Hayashi M, Araki S, Arai N, Kumada S, Itoh M, Tamagawa K, Oda M, Morimatsu Y. 2002. Oxidative stress and disturbed glutamate transport in spinal muscular atrophy. Brain Dev 24:770-775.
14. Ito Y, Kumada S, Uchiyama A, Saito K, Osawa M, Yagishita A, Kurata K, Hayashi M. 2004. Thalamic lesions in a long-surviving child with spinal muscular atrophy type I: MRI and EEG findings. Brain Dev 26:53-56.
15. Jablonka S, Wiese S, Sendtner M. 2004. Axonal defects in mouse models of motoneuron disease. J Neurobiol 58:272-286.
16. Jablonka S, Karle K, Sandner B, Andreassi C, von Au K, Sendtner M. 2006. Distinct and overlapping alterations in motor and sensory neurons in a mouse model of spinal muscular atrophy. Hum Mol Genet 15:511-518.
17. Jones EG. 1975. Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162:285-308.
18. La Bella V, Cisterni C, Salaun D, Pettmann B. 1998. Survival motor neuron (SMN) protein in rat is expressed as different molecular forms and is developmentally regulated. Eur J Neurosci 10:2913-2923.
19. 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.
20. Lefebvre S, Burlet P, Liu Q, Bertrandy S, Clermont O, Munnich A, Dreyfuss G, Melki J. 1997. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 16:265-269.
21. Lippa CF, Smith TW. 1988. Chromatolytic neurons in Werdnig-Hoffmann disease contain phosphorylated neurofilaments. Acta Neuropathol 77:91-94.
22. Liu Q, Dreyfuss G. 1996. A novel nuclear structure containing the survival of motor neurons protein. EMBO J 15:3555-3565.
23. Lorson CL, Androphy EJ. 2000. An exonic enhancer is required for inclusion of an essential exon in the SMA-determining gene SMN. Hum Mol Genet 9:259-265.
24. Lorson CL, Hahnen E, Androphy EJ, Wirth B. 1999. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A 96:6307-6311.
25. Meister G, Buhler D, Laggerbauer B, Zobawa M, Lottspeich F, Fischer U. 2000. Characterization of a nuclear 20S complex containing the survival of motor neurons (SMN) protein and a specific subset of spliceosomal Sm proteins. Hum Mol Genet 9:1977-1986.
26. Meister G, Eggert C, Fischer U. 2002. SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol 12:472-478.
27. Monani UR. 2005. Spinal muscular atrophy: a deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron 48:885-895.
28. Monani UR, Lorson CL, Parsons DW, Prior TW, Androphy EJ, Burghes AH, McPherson JD. 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.
29. Murayama S, Bouldin TW, Suzuki K. 1991. Immunocytochemical and ultrastructural studies of Werdnig-Hoffmann disease. Acta Neuropathol 81:408-417.
30. Narayanan U, Achsel T, Luhrmann R, Matera AG. 2004. Coupled in vitro import of U snRNPs and SMN, the spinal muscular atrophy protein. Mol Cell 16:223-234.
31. Novelli G, Calza L, Amicucci P, Giardino L, Pozza M, Silani V, Pizzuti A, Gennarelli M, Piombo G, Capon F, Dallapiccola B. 1997. Expression study of survival motor neuron gene in human fetal tissues. Biochem Mol Med 61:102-106.
32. Ogino S, Wilson RB. 2004. Spinal muscular atrophy: molecular genetics and diagnostics. Expert Rev Mol Diagn 4:15-29.
33. Pagliardini S, Giavazzi A, Setola V, Lizier C, Di Luca M, DeBiasi S, Battaglia G. 2000. Subcellular localization and axonal transport of the survival motor neuron (SMN) protein in the developing rat spinal cord. Hum Mol Genet 9:47-56.
34. Paushkin S, Gubitz AK, Massenet S, Dreyfuss G. 2002. The SMN complex, an assemblyosome of ribonucleoproteins. Curr Opin Cell Biol 14:305-312.
35. Pellizzoni L, Kataoka N, Charroux B, Dreyfuss G. 1998. A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 95:615-624.
36. Pellizzoni L, Charroux B, Rappsilber J, Mann M, Dreyfuss G. 2001. A functional interaction between the survival motor neuron complex and RNA polymerase II. J Cell Biol 152:75-85.
37. Rossoll W, Kroning AK, Ohndorf UM, Steegborn C, Jablonka S, Sendtner M. 2002. Specific interaction of Smn, the spinal muscular atrophy determining gene product, with hnRNP-R and gry-rbp/hnRNP-Q: a role for Smn in RNA processing in motor axons? Hum Mol Genet 11:93-105.
38. Rossoll W, Jablonka S, Andreassi C, Kroning AK, Karle K, Monani UR, 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.
39. Rudnik-Schoneborn S, Goebel HH, Schlote W, Molaian S, Omran H, Ketelsen U, Korinthenberg R, Wenzel D, Lauffer H, Kreiss-Nachtsheim M, Wirth B, Zerres K. 2003. Classical infantile spinal muscular atrophy with SMN deficiency causes sensory neuronopathy. Neurology 60:983-987.
40. Sharma A, Lambrechts A, Hao le T, Le TT, Sewry CA, Ampe C, Burghes AH, Morris GE. 2005. 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 309:185-197.
41. Soler-Botija C, Cusco I, Caselles L, Lopez E, Baiget M, Tizzano EF. 2005. Implication of fetal SMN2 expression in type I SMA pathogenesis: protection or pathological gain of function? J Neuropathol Exp Neurol 64:215-223.
42. Towfighi J, Young RS, Ward RM. 1985. Is Werdnig-Hoffmann disease a pure lower motor neuron disorder? Acta Neuropathol 65:270-280.
43. Ulfig N. 1989. Configuration of the magnocellular nuclei in the basal forebrain of the human adult. Acta Anat 134:100-105.
44. Ulfig N, Nickel J, Bohl J. 1998. Transient features of the thalamic reticular nucleus in the human foetal brain. Eur J Neurosci 10:3773-3784.
45. Yong J, Wan L, Dreyfuss G. 2004. Why do cells need an assembly machine for RNA-protein complexes? Trends Cell Biol 14:226-232.
46. Zerres K, Davies KE. 1999. 59th ENMC International Workshop: Spinal Muscular Atrophies: recent progress and revised diagnostic criteria 17-19 April 1998, Soestduinen, The Netherlands. Neuromuscul Disord 9:272-278.
47. Zhang HL, Pan F, Hong D, Shenoy SM, Singer RH, Bassell GJ. 2003. Active transport of the survival motor neuron protein and the role of exon-7 in cytoplasmic localization. J Neurosci 23:6627-6637.