5-(N-ethyl-N-isopropyl)-amiloride enhances SMN2 exon 7 inclusion and protein expression in spinal muscular atrophy cells

Annals of Neurology

Volumn 63, Issue 1, 2008, Pages 26-34

  Yuo, Chung Yee ^a,b   Lin, Hui Hua ^a,b   Chang, Ya Sian ^a,b   Yang, Wen Kuang ^c   Chang, Jan Gowth ^a,b  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; MESSENGER RNA; MESSENGER RNA PRECURSOR; PROTEIN KINASE B; SODIUM PROTON EXCHANGE PROTEIN; SURVIVAL MOTOR NEURON PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL FRACTIONATION; CELL GROWTH; CELL PH; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; EXON; GENE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LYMPHOID CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMN1 GENE; SMN2 GENE; SPINAL MUSCULAR ATROPHY; STATISTICAL ANALYSIS; WESTERN BLOTTING;

ALTERNATIVE SPLICING; AMILORIDE; CELL LINE; CELL SURVIVAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME INHIBITORS; EXONS; HUMANS; HYDROGEN-ION CONCENTRATION; LYMPHOCYTES; MOLECULAR BIOLOGY; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; RNA PRECURSORS; RNA SPLICING; RNA-BINDING PROTEINS; SODIUM-HYDROGEN ANTIPORTER; TRANSCRIPTION, GENETIC;

EID: 39049125699     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.21241     Document Type: Article

References (56)

1. Dubowitz V. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol 1999;3:49-51.
2. Zerres K, Rudnik-Schoneborn S, Forkert R, Wirth B. Genetic basis of adult-onset spinal muscular atrophy. Lancet 1995;346:1162.
3. Munsat TL, Davies KE. International SMA consortium meeting. Neuromuscul Disord 1992;2:423-428.
4. Iannaccone ST. Spinal muscular atrophy. Semin Neurol 1998;18:19-26.
5. Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995;80:155-165.
6. Wirth B. An update of the mutation spectrum of the survival motor neuron gene (SMN1) in autosomal recessive spinal muscular atrophy (SMA). Hum Mutat 2000;15:228-237.
7. Burglen L, Lefebvre S, Clermont O, et al. Structure and organization of the human survival motor neurone (SMN) gene. Genomics 1996;32:479-482.
8. 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.
9. 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.
10. Lorson CL, Strasswimmer J, Yao JM, et al. SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat Genet 1998;19:63-66.
11. Coovert DD, Le TT, McAndrew PE, et al. The survival motor neuron protein in spinal muscular atrophy. Hum Mol Genet 1997;6:1205-1214.
12. 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.
13. Hsieh-Li HM, Chang JG, Jong YJ, et al. A mouse model for spinal muscular atrophy. Nat Genet 2000;24:66-70.
14. Cartegni L, Krainer AR. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat Genet 2002;30:377-384.
15. Kashima T, Manley JL. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat Genet 2003;34:460-463.
16. Cartegni L, Hastings ML, Calarco JA, et al. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am J Hum Genet 2006;78:63-77.
17. Liu Q, Dreyfuss G. A novel nuclear structure containing the survival of motor neurons protein. Embo J 1996;15:3555-3565.
18. Gubitz AK, Feng W, Dreyfuss G. The SMN complex. Exp Cell Res 2004;296:51-56.
19. Carissimi C, Saieva L, Baccon J, et al. Gemin8 is a novel component of the survival motor neuron complex and functions in small nuclear ribonucleoprotein assembly. J Biol Chem 2006;281:8126-8134.
20. 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.
21. Rossoll W, Jablonka S, Andreassi C, et al. 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 2003;163:801-812.
22. Jablonka S, Schrank B, Kralewski M, et al. Reduced survival motor neuron (Smn) gene dose in mice leads to motor neuron degeneration: an animal model for spinal muscular atrophy type III. Hum Mol Genet 2000;9:341-346.
23. 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.
24. Feldkotter M, Schwarzer V, Wirth R, et al. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet 2002;70:358-368.
25. Borsi L, Balza E, Gaggero B, et al. The alternative splicing pattern of the tenascin-C pre-mRNA is controlled by the extracellular pH. J Biol Chem 1995;270:6243-6245.
26. Borsi L, Allemanni G, Gaggero B, Zardi L. Extracellular pH controls pre-mRNA alternative splicing of tenascin-C in normal, but not in malignantly transformed, cells. Int J Cancer 1996;66:632-635.
27. Putney LK, Denker SP, Barber DL. The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions. Annu Rev Pharmacol Toxicol 2002;42:527-552.
28. Bianchini L, Poussegur J. Molecular structure and regulation of vertebrate Na+/H+ exchangers. J Exp Biol 1994;196:337-345.
29. Chang JG, Hsieh-Li HM, Jong YJ, et al. Treatment of spinal muscular atrophy by sodium butyrate. Proc Natl Acad Sci U S A 2001;98:9808-9813.
30. Rich IN, Brackmann I, Worthington-White D, Dewey MJ. Activation of the sodium/hydrogen exchanger via the fibronectin-integrin pathway results in hematopoietic stimulation. J Cell Physiol 1998;177:109-122.
31. Hofmann Y, Wirth B. hnRNP-G promotes exon 7 inclusion of survival motor neuron (SMN) via direct interaction with Htra2-beta1. Hum Mol Genet 2002;11:2037-2049.
32. Young PJ, DiDonato CJ, Hu D, et al. SRp30c-dependent stimulation of survival motor neuron (SMN) exon 7 inclusion is facilitated by a direct interaction with hTra2 beta 1. Hum Mol Genet 2002;11:577-587.
33. Blaustein M, Pelisch F, Tanos T, et al. Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat Struct Mol Biol 2005;12:1037-1044.
34. Patel NA, Kaneko S, Apostolatos HS, et al. Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CbetaII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J Biol Chem 2005;280:14302-14309.
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. 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.
37. 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.
38. 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.
39. Hahnen E, Eyupoglu IY, Brichta L, et al. In vitro and ex vivo evaluation of second-generation histone deacetylase inhibitors for the treatment of spinal muscular atrophy. J Neurochem 2006;98:193-202.
40. 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.
41. Zhang ML, Lorson CL, Androphy EJ, Zhou J. An in vivo reporter system for measuring increased inclusion of exon 7 in SMN2 mRNA: potential therapy of SMA. Gene Ther 2001;8:1532-1538.
42. Lunn MR, Root DE, Martino AM, et al. Indoprofen upregulates the survival motor neuron protein through a cyclooxygenase-independent mechanism. Chem Biol 2004;11:1489-1493.
43. Wolstencroft EC, Mattis V, Bajer AA, et al. A non-sequence-specific requirement for SMN protein activity: the role of aminoglycosides in inducing elevated SMN protein levels. Hum Mol Genet 2005;14:1199-1210.
44. Grzeschik SM, Ganta M, Prior TW, et al. Hydroxyurea enhances SMN2 gene expression in spinal muscular atrophy cells. Ann Neurol 2005;58:194-202.
45. Brichra L, Holker I, Haug K, et al. In vivo activation of SMN in spinal muscular atrophy carriers and patients treated with valproate. Ann Neurol 2006;59:970-975.
46. Brahe C, Vitali T, Tiziano FD, et al. Phenylbutyrate increases SMN gene expression in spinal muscular atrophy patients. Eur J Hum Genet 2005;13:256-259.
47. Endo H, Matsuda C, Kagawa Y. Exclusion of an alternatively spliced exon in human ATP synthase gamma-subunit pre-mRNA requires de novo protein synthesis. J Biol Chem 1994;269:12488-12493.
48. Rosskopf D, Schroder KJ, Siffert W. Role of sodium-hydrogen exchange in the proliferation of immortalised lymphoblasts from patients with essential hypertension and normotensive subjects. Cardiovasc Res 1995;29:254-259.
49. Hofmann Y, Lorson CL, Stamm S, et al. Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc Natl Acad Sci U S A 2000;97:9618-9623.
50. Singh NN, Androphy EJ, Singh RN. An extended inhibitory context causes skipping of exon 7 of SMN2 in spinal muscular atrophy. Biochem Biophys Res Commun 2004;315:381-388.
51. Miyaso H, Okumura M, Kondo S, et al. An intronic splicing enhancer element in survival motor neuron (SMN) pre-mRNA. J Biol Chem 2003;278:15825-15831.
52. Heinrichs V, Baker BS. The Drosophila SR protein RBP1 contributes to the regulation of doublesex alternative splicing by recognizing RBP1 RNA target sequences. Embo J 1995;14:3987-4000.
53. Galiana-Arnoux D, Lejeune F, Gesnel MC, et al. The CD44 alternative v9 exon contains a splicing enhancer responsive to the SR proteins 9G8, ASF/SF2, and SRp20. J Biol Chem 2003;278:32943-32953.
54. Jumaa H, Nielsen PJ. Regulation of SRp20 exon 4 splicing. Biochim Biophys Acta 2000;1494:137-143.
55. Lou H, Neugebauer KM, Gagel RF, Berget SM. Regulation of alternative polyadenylation by U1 snRNPs and SRp20. Mol Cell Biol 1998;18:4977-4985.
56. Yu Q, Guo J, Zhou J. A minimal length between tau exon 10 and 11 is required for correct splicing of exon 10. J Neurochem 2004;90:164-172.