Neuronal SH-SY5Y cells use the C-dystrophin promoter coupled with exon 78 skipping and display multiple patterns of alternative splicing including two intronic insertion events

Human Genetics

Volumn 134, Issue 9, 2015, Pages 993-1001

  Nishida, Atsushi ^a   Minegishi, Maki ^a,b   Takeuchi, Atsuko ^b   Awano, Hiroyuki ^c   Niba, Emma Tabe Eko ^a   Matsuo, Masafumi ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; GENOMIC DNA; MESSENGER RNA; RNA SPLICING; TRANSPOSON;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AGAR GEL ELECTROPHORESIS; ARTICLE; BINDING SITE; BRAIN CORTEX; CODON; CONTROLLED STUDY; DNA SEQUENCE; DUCHENNE MUSCULAR DYSTROPHY; EXON; EXON SKIPPING; GENE INSERTION; GENE INSERTION SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; INTRON RETENTION; NERVE CELL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PURKINJE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; ALTERNATIVE RNA SPLICING; GENETICS; GENOMICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RNA SPLICING; TRANSPOSON; TUMOR CELL LINE;

ALTERNATIVE SPLICING; BASE SEQUENCE; CELL LINE, TUMOR; DNA TRANSPOSABLE ELEMENTS; DYSTROPHIN; EXONS; GENOMICS; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RNA SPLICE SITES; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

EID: 84938957480     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-015-1581-2     Document Type: Article

References (54)

1. Agholme L, Nath S, Domert J, Marcusson J, Kagedal K, Hallbeck M (2014) Proteasome inhibition induces stress kinase dependent transport deficits—Implications for Alzheimer’s disease. Mol Cell Neurosci 58:29–39. doi:10.1016/j.mcn.2013.11.001
2. Ahn AH, Kunkel LM (1993) The structural and functional diversity of dystrophin. Nat Genet 3:283–291. doi:10.1038/ng0493-283
3. Banihani R, Smile S, Yoon G, Dupuis A, Mosleh M, Snider A, McAdam L (2015) Cognitive and neurobehavioral profile in boys with duchenne muscular dystrophy. J Child Neurol. doi:10.1177/0883073815570154(in press)
4. Barry G (2014) Integrating the roles of long and small non-coding RNA in brain function and disease. Mol. Psychiatry 19:410–416. doi:10.1038/mp.2013.196
5. Biedler JL, Helson L, Spengler BA (1973) Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 33:2643–2652
6. Bies RD, Phelps SF, Cortez MD, Roberts R, Caskey CT, Chamberlain JS (1992) Human and murine dystrophin mRNA transcripts are differentially expressed during skeletal muscle, heart, and brain development. Nucleic Acids Res 20:1725–1731. doi:10.1093/nar/20.7.1725
7. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336. doi:10.1146/annurev.biochem.72.121801.161720
8. Bolisetty MT, Beemon KL (2012) Splicing of internal large exons is defined by novel cis-acting sequence elements. Nucleic Acids Res 40:9244–9254. doi:10.1093/nar/gks652
9. Bovolenta M, Erriquez D, Valli E, Brioschi S, Scotton C, Neri M, Falzarano MS, Gherardi S, Fabris M, Rimessi P, Gualandi F, Perini G, Ferlini A (2012) The DMD locus harbours multiple long non-coding RNAs which orchestrate and control transcription of muscle dystrophin mRNA isoforms. PLoS One 7:e45328. doi:10.1371/journal.pone.0045328
10. Castle JC, Zhang C, Shah JK, Kulkarni AV, Kalsotra A, Cooper TA, Johnson JM (2008) Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat Genet 40:1416–1425. doi:10.1038/ng.264
11. Clark BS, Blackshaw S (2014) Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Front Genet 5:164. doi:10.3389/fgene.2014.00164
12. Cyrulnik SE, Fee RJ, De Vivo DC, Goldstein E, Hinton VJ (2007) Delayed developmental language milestones in children with Duchenne’s muscular dystrophy. J Pediatr 150:474–478. doi:10.1016/j.jpeds.2006.12.045
13. Daoud F, Angeard N, Demerre B, Martie I, Benyaou R, Leturcq F, Cossee M, Saillour Y, Tuffery S, Urtizberea A, Toutain A, Echenne B, Frischman M, Mayer M, Desguerre I, Estournet B, Reveillere C, Penisson B, Cuisset JM, Kaplan JC, Heron D, Rivier F, Chelly J (2009) Analysis of Dp71 contribution in the severity of mental retardation through comparison of Duchenne and Becker patients differing by mutation consequences on Dp71 expression. Hum Mol Genet 18:3779–3794. doi:10.1093/hmg/ddp320
14. D’Souza VN, Nguyen TM, Morris GE, Karges W, Pillers DA, Ray PN (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum Mol Genet 4:837–842. doi:10.1093/hmg/4.5.837
15. Emery AEH (1993) Duchenne muscular dystrophy. Oxford University Press, Oxford
16. Feener CA, Koenig M, Kunkel LM (1989) Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 338:509–511. doi:10.1038/338509a0
17. Ge Y, Porse BT (2014) The functional consequences of intron retention: alternative splicing coupled to NMD as a regulator of gene expression. BioEssays 36:236–243. doi:10.1002/bies.201300156
18. Giliberto F, Ferreiro V, Dalamon V, Szijan I (2004) Dystrophin deletions and cognitive impairment in Duchenne/Becker muscular dystrophy. Neurol Res 26:83–87. doi:10.1179/016164104773026589
19. Gorecki DC, Barnard EA (1995) Specific expression of G-dystrophin (Dp71) in the brain. NeuroReport 6:893–896
20. Gorecki DC, Monaco AP, Derry JMJ, Walker AP, Barnard EA, Barnard PJ (1992) Expression of four alternative dystrophin transcripts in brain regions regulated by different promoters. Hum Mol Genet 1:505–510. doi:10.1093/hmg/1.7.505
21. Hawkins JD (1988) A survey on intron and exon lengths. Nucleic Acids Res 16:9893–9908. doi:10.1093/nar/16.21.9893
22. Holder E, Maeda M, Bies RD (1996) Expression and regulation of the dystrophin purkinje promoter in human skeletal muscle, heart, and brain. Hum Genet 97:232–239. doi:10.1007/BF02265272
23. Lannaccone M, Giuberti G, De Vivo G, Caraglia M, Gentile V (2013) Identification of a FXIIIA variant in human neuroblastoma cell lines. Int J Biochem Mol Biol 4:102–107
24. Lidov HG, Selig S, Kunkel LM (1995) Dp140: a novel 140 kDa CNS transcript from the dystrophin locus. Hum Mol Genet 4:329–335. doi:10.1093/hmg/4.3.329
25. Malueka RG, Takaoka Y, Yagi M, Awano H, Lee T, Dwianingsih EK, Nishida A, Takeshima Y, Matsuo M (2012) Categorization of 77 dystrophin exons into 5 groups by a decision tree using indexes of splicing regulatory factors as decision markers. BMC Genet 13:23. doi:10.1186/1471-2156-13-23
26. Matlin AJ, Clark F, Smith CW (2005) Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 6:386–398. doi:10.1038/nrm1645
27. Matsuo M, Masumura T, Nishio H, Nakajima T, Kitoh Y, Takumi T, Koga J, Nakamura H (1991) Exon skipping during splicing of dystrophin mRNA precursor due to an intraexon deletion in the dystrophin gene of Duchenne muscular dystrophy Kobe. J Clin Invest 87:2127–2131. doi:10.1172/JCI115244
28. Mehler MF (2000) Brain dystrophin, neurogenetics and mental retardation. Brain Res Rev 32:277–307. doi:10.1016/S0165-0173(99)00090-9
29. Mikulak J, Negrini S, Klajn A, D’Alessandro R, Mavilio D, Meldolesi J (2012) Dual REST-dependence of L1CAM: from gene expression to alternative splicing governed by Nova2 in neural cells. J Neurochem 120:699–709. doi:10.1111/j.1471-4159.2011.07626.x
30. Mironov AA, Fickett JW, Gelfand MS (1999) Frequent alternative splicing of human genes. Genome Res 9:1288–1293
31. Mount SM (2000) Genomic sequence, splicing, and gene annotation. Am J Hum Genet 67:788–792. doi:10.1086/303098
32. Muntoni F, Torelli S, Ferlini A (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol 2:731–740. doi:10.1016/S1474-4422(03)00585-4
33. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463. doi:10.1038/nature08909
34. Nishida A, Minegishi M, Takeuchi A, Niba E, Awano H, Lee T, Iijima K, Takeshima Y, Matsuo M (2015) Tissue and case-specific retention of intron 40 in mature dystrophin mRNA. J Hum Genet. doi:10.1038/jhg.2015.24(in press)
35. Oltean S, Bates DO (2013) Hallmarks of alternative splicing in cancer. Oncogene. doi:10.1038/onc.2013.533(in press)
36. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415. doi:10.1038/ng.259
37. Reiss J, Rininsland F (1994) An explanation for the constitutive exon 9 cassette splicing of the DMD gene. Hum Mol Genet 3:295–298. doi:10.1093/hmg/3.2.295
38. Roberts RG, Barby TF, Manners E, Bobrow M, Bentley DR (1991) Direct detection of dystrophin gene rearrangements by analysis of dystrophin mRNA in peripheral blood lymphocytes. Am J Hum Genet 49:298–310
39. Roberts RG, Bentley DR, Bobrow M (1993) Infidelity in the structure of ectopic transcripts: a novel exon in lymphocyte dystrophin transcripts. Hum Mutat 2:293–299. doi:10.1002/humu.1380020409
40. Saint Martin A, Aragon J, Depardon-Benitez F, Sanchez-Trujillo A, Mendoza-Hernandez G, Ceja V, Montanez C (2012) Identification of Dp71e, a new dystrophin with a novel carboxy-terminal end. FEBS J 279:66–77. doi:10.1111/j.1742-4658.2011.08399.x
41. Shapiro MB, Senapathy P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15:7155–7174. doi:10.1093/nar/15.17.7155
42. Shkreta L, Bell B, Revil T, Venables JP, Prinos P, Elela SA, Chabot B (2013) Cancer-associated perturbations in alternative pre-messenger RNA splicing. Cancer Treat Res 158:41–94. doi:10.1007/978-3-642-31659-3_3
43. Sironi M, Cagliani R, Pozzoli U, Bardoni A, Comi GP, Giorda R, Bresolin N (2002) The dystrophin gene is alternatively spliced throughout its coding sequence. FEBS Lett 517:163–166. doi:10.1016/S0014-5793(02)02613-3
44. Surono A, Takeshima Y, Wibawa T, Pramono ZA, Matsuo M (1997) Six novel transcripts that remove a huge intron ranging from 250 to 800 kb are produced by alternative splicing of the 5′ region of the dystrophin gene in human skeletal muscle. Biochem Biophys Res Commun 239:895–899. doi:10.1006/bbrc.1997.7579
45. Surono A, Takeshima Y, Wibawa T, Ikezawa M, Nonaka I, Matsuo M (1999) Circular dystrophin RNAs consisting of exons that were skipped by alternative splicing. Hum Mol Genet 8:493–500
46. Taylor PJ, Betts GA, Maroulis S, Gilissen C, Pedersen RL, Mowat DR, Johnston HM, Buckley MF (2010) Dystrophin gene mutation location and the risk of cognitive impairment in Duchenne muscular dystrophy. PLoS One 5:e8803. doi:10.1371/journal.pone.0008803
47. Torelli S, Muntoni F (1996) Alternative splicing of dystrophin exon 4 in normal human muscle. Hum Genet 97:521–523
48. Wang Z, Burge CB (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14:802–813. doi:10.1261/rna.876308
49. Wang Y, Marino-Enriquez A, Bennett RR, Zhu M, Shen Y, Eilers G, Lee JC, Henze J, Fletcher BS, Gu Z, Fox EA, Antonescu CR, Fletcher CD, Guo X, Raut CP, Demetri GD, van de Rijn M, Ordog T, Kunkel LM, Fletcher JA (2014) Dystrophin is a tumor suppressor in human cancers with myogenic programs. Nat Genet 46:601–606. doi:10.1038/ng.2974
50. Wein N, Vulin A, Falzarano MS, Szigyarto CA, Maiti B, Findlay A, Heller KN, Uhlen M, Bakthavachalu B, Messina S, Vita G, Passarelli C, Gualandi F, Wilton SD, Rodino-Klapac LR, Yang L, Dunn DM, Schoenberg DR, Weiss RB, Howard MT, Ferlini A, Flanigan KM (2014) Translation from a DMD exon 5 IRES results in a functional dystrophin isoform that attenuates dystrophinopathy in humans and mice. Nat Med. doi:10.1038/nm.3628
51. Wong JJ, Ritchie W, Ebner OA, Selbach M, Wong JW, Huang Y, Gao D, Pinello N, Gonzalez M, Baidya K, Thoeng A, Khoo TL, Bailey CG, Holst J, Rasko JE (2013) Orchestrated intron retention regulates normal granulocyte differentiation. Cell 154:583–595. doi:10.1016/j.cell.2013.06.052
52. Xie HR, Hu LS, Li GY (2010) SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson’s disease. Chin Med J (Engl) 123:1086–1092
53. Zhang Z, Habara Y, Nishiyama A, Oyazato Y, Yagi M, Takeshima Y, Matsuo M (2007) Identification of seven novel cryptic exons embedded in the dystrophin gene and characterization of 14 cryptic dystrophin exons. J Hum Genet 52:607–617. doi:10.1007/s10038-007-0163-0
54. Zheng L, Calvo-Garrido J, Hallbeck M, Hultenby K, Marcusson J, Cedazo-Minguez A, Terman A (2013) Intracellular localization of amyloid-beta peptide in SH-SY5Y neuroblastoma cells. J Alzheimers Dis 37:713–733. doi:10.3233/JAD-122455