Alternative splicing of the neurofibromatosis type 1 pre-mRNA is regulated by the muscleblind-like proteins and the CUG-BP and ELAV-like factors

BMC Molecular Biology

Volumn 13, Issue , 2012, Pages

  Fleming, Victoria A ^a   Geng, Cuiyu ^a   Ladd, Andrea N ^a,c   Lou, Hua ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Alternative splicing; Complex control; CUG BP and ELAV like family (CELF proteins); Muscleblind like (MBNL) proteins; Neurofibromatosis type I (NF1); Splicing regulation

Indexed keywords

CUG BP AND ELAV LIKE FAMILY PROTEIN; MESSENGER RNA; MUSCLEBLIND LIKE PROTEIN; NEUROFIBROMIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CROSS LINKING; EXON; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; HUMAN; INTRON; NEUROFIBROMATOSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BINDING SITES; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL LINE; EXONS; HELA CELLS; HUMANS; NEUROFIBROMATOSIS 1; RATS; RNA INTERFERENCE; RNA PRECURSORS; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84873291900     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-13-35     Document Type: Article

References (49)

1. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40:1413-1415. 10.1038/ng.259, 18978789.
2. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476. 10.1038/nature07509, 2593745, 18978772.
3. Salz HK. Sex determination in insects: a binary decision based on alternative splicing. Curr Opin Genet Dev 2011, 21:395-400. 10.1016/j.gde.2011.03.001, 3134629, 21474300.
4. Lopez AJ. Alternative splicing of pre-mRNA: developmental consequences and mechanisms of regulation. Annu Rev Genet 1998, 32:279-305. 10.1146/annurev.genet.32.1.279, 9928482.
5. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003, 72:291-336. 10.1146/annurev.biochem.72.121801.161720, 12626338.
6. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463. 10.1038/nature08909, 3443858, 20110989.
7. Faustino NA, Cooper TA. Pre-mRNA splicing and human disease. Genes Dev 2003, 17:419-437. 10.1101/gad.1048803, 12600935.
8. Calarco JA, Zhen M, Blencowe BJ. Networking in a global world: establishing functional connections between neural splicing regulators and their target transcripts. RNA 2011, 17:775-791. 10.1261/rna.2603911, 3078728, 21415141.
9. Kuroyanagi H. Fox-1 family of RNA-binding proteins. Cell Mol Life Sci 2009, 66:3895-3907. 10.1007/s00018-009-0120-5, 2777236, 19688295.
10. Barreau C, Paillard L, Mereau A, Osborne HB. Mammalian CELF/Bruno-like RNA-binding proteins: molecular characteristics and biological functions. Biochimie 2006, 88:515-525. 10.1016/j.biochi.2005.10.011, 16480813.
11. Hinman MN, Lou H. Diverse molecular functions of Hu proteins. Cell Mol Life Sci 2008, 65:3168-3181. 10.1007/s00018-008-8252-6, 2580827, 18581050.
12. Pascual M, Vicente M, Monferrer L, Artero R. The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation 2006, 74:65-80. 10.1111/j.1432-0436.2006.00060.x, 16533306.
13. Long JC, Caceres JF. The SR protein family of splicing factors: master regulators of gene expression. Biochem J 2009, 417:15-27. 10.1042/BJ20081501, 19061484.
14. Li Q, Lee JA, Black DL. Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 2007, 8:819-831. 10.1038/nrn2237, 17895907.
15. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell 2009, 33:591-601. 10.1016/j.molcel.2009.01.025, 2702247, 19285943.
16. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. Regulation of alternative splicing by histone modifications. Science 2010, 327:996-1000. 10.1126/science.1184208, 2913848, 20133523.
17. Allemand E, Batsche E, Muchardt C. Splicing, transcription, and chromatin: a menage a trois. Curr Opin Genet Dev 2008, 18:145-151. 10.1016/j.gde.2008.01.006, 18372167.
18. Alexander R, Beggs JD. Cross-talk in transcription, splicing and chromatin: who makes the first call?. Biochem Soc Trans 2010, 38:1251-1256. 10.1042/BST0381251, 20863294.
19. Leroy O, Wang J, Maurage CA, Parent M, Cooper T, Buee L, Sergeant N, Andreadis A, Caillet-Boudin ML. Brain-specific change in alternative splicing of Tau exon 6 in myotonic dystrophy type 1. Biochim Biophys Acta 2006, 1762:460-467. 10.1016/j.bbadis.2005.12.003, 16487687.
20. Ho TH, Charlet BN, Poulos MG, Singh G, Swanson MS, Cooper TA. Muscleblind proteins regulate alternative splicing. EMBO J 2004, 23:3103-3112. 10.1038/sj.emboj.7600300, 514918, 15257297.
21. Kino Y, Washizu C, Oma Y, Onishi H, Nezu Y, Sasagawa N, Nukina N, Ishiura S. MBNL and CELF proteins regulate alternative splicing of the skeletal muscle chloride channel CLCN1. Nucleic Acids Res 2009, 37:6477-6490. 10.1093/nar/gkp681, 2770659, 19720736.
22. Warf MB, Diegel JV, von Hippel PH, Berglund JA. The protein factors MBNL1 and U2AF65 bind alternative RNA structures to regulate splicing. Proc Natl Acad Sci USA 2009, 106:9203-9208. 10.1073/pnas.0900342106, 2695092, 19470458.
23. Kalsotra A, Xiao X, Ward AJ, Castle JC, Johnson JM, Burge CB, Cooper TA. A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci USA 2008, 105:20333-20338. 10.1073/pnas.0809045105, 2629332, 19075228.
24. Larizza L, Gervasini C, Natacci F, Riva P. Developmental abnormalities and cancer predisposition in neurofibromatosis type 1. Curr Mol Med 2009, 9:634-653. 10.2174/156652409788488801, 19601812.
25. Yunoue S, Tokuo H, Fukunaga K, Feng L, Ozawa T, Nishi T, Kikuchi A, Hattori S, Kuratsu J, Saya H, Araki N. Neurofibromatosis type I tumor suppressor neurofibromin regulates neuronal differentiation via its GTPase-activating protein function toward Ras. J Biol Chem 2003, 278:26958-26969. 10.1074/jbc.M209413200, 12730209.
26. Andersen LB, Ballester R, Marchuk DA, Chang E, Gutmann DH, Saulino AM, Camonis J, Wigler M, Collins FS. A conserved alternative splice in the von Recklinghausen neurofibromatosis (NF1) gene produces two neurofibromin isoforms, both of which have GTPase-activating protein activity. Mol Cell Biol 1993, 13:487-495. 358928, 8417346.
27. Barron VA, Zhu H, Hinman MN, Ladd AN, Lou H. The neurofibromatosis type I pre-mRNA is a novel target of CELF protein-mediated splicing regulation. Nucleic Acids Res 2010, 38:253-264. 10.1093/nar/gkp766, 2800208, 19854948.
28. Zhou HL, Hinman MN, Barron VA, Geng C, Zhou G, Luo G, Siegel RE, Lou H. Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner. Proc Natl Acad Sci USA 2011, 108:E627-E625. 10.1073/pnas.1103344108, 3169152, 21808035.
29. Zhu H, Hinman MN, Hasman RA, Mehta P, Lou H. Regulation of neuron-specific alternative splicing of neurofibromatosis type 1 pre-mRNA. Mol Cell Biol 2008, 28:1240-1251. 10.1128/MCB.01509-07, 2258745, 18086893.
30. Huynh DP, Nechiporuk T, Pulst SM. Alternative transcripts in the mouse neurofibromatosis type 2 (NF2) gene are conserved and code for schwannomins with distinct C-terminal domains. Hum Mol Genet 1994, 3:1075-1079. 10.1093/hmg/3.7.1075, 7981675.
31. Gutmann DH, Zhang Y, Hirbe A. Developmental regulation of a neuron-specific neurofibromatosis 1 isoform. Ann Neurol 1999, 46:777-782. 10.1002/1531-8249(199911)46:5<777::AID-ANA15>3.0.CO;2-H, 10553997.
32. Fernandez-Costa JM, Llamusi MB, Garcia-Lopez A, Artero R. Alternative splicing regulation by Muscleblind proteins: from development to disease. Biol Rev Camb Philos Soc 2011, 86:947-958. 10.1111/j.1469-185X.2011.00180.x, 21489124.
33. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS. A muscleblind knockout model for myotonic dystrophy. Science 2003, 302:1978-1980. 10.1126/science.1088583, 14671308.
34. Hao M, Akrami K, Wei K, De Diego C, Che N, Ku JH, Tidball J, Graves MC, Shieh PB, Chen F. Muscleblind-like 2 (Mbnl2) -deficient mice as a model for myotonic dystrophy. Dev Dyn 2008, 237:403-410. 10.1002/dvdy.21428, 18213585.
35. Du H, Cline MS, Osborne RJ, Tuttle DL, Clark TA, Donohue JP, Hall MP, Shiue L, Swanson MS, Thornton CA, Ares M. Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol 2010, 17:187-193. 10.1038/nsmb.1720, 2852634, 20098426.
36. Kanadia RN, Urbinati CR, Crusselle VJ, Luo D, Lee YJ, Harrison JK, Oh SP, Swanson MS. Developmental expression of mouse muscleblind genes Mbnl1, Mbnl2 and Mbnl3. Gene Expr Patterns 2003, 3:459-462. 10.1016/S1567-133X(03)00064-4, 12915312.
37. Hino S, Kondo S, Sekiya H, Saito A, Kanemoto S, Murakami T, Chihara K, Aoki Y, Nakamori M, Takahashi MP, Imaizumi K. Molecular mechanisms responsible for aberrant splicing of SERCA1 in myotonic dystrophy type 1. Hum Mol Genet 2007, 16:2834-2843. 10.1093/hmg/ddm239, 17728322.
38. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, Thornton CA, Swanson MS. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J 2000, 19:4439-4448. 10.1093/emboj/19.17.4439, 302046, 10970838.
39. Kino Y, Mori D, Oma Y, Takeshita Y, Sasagawa N, Ishiura S. Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum Mol Genet 2004, 13:495-507. 10.1093/hmg/ddh056, 14722159.
40. Warf MB, Berglund JA. MBNL binds similar RNA structures in the CUG repeats of myotonic dystrophy and its pre-mRNA substrate cardiac troponin T. RNA 2007, 13:2238-2251. 10.1261/rna.610607, 2080590, 17942744.
41. Yuan Y, Compton SA, Sobczak K, Stenberg MG, Thornton CA, Griffith JD, Swanson MS. Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs. Nucleic Acids Res 2007, 35:5474-5486. 10.1093/nar/gkm601, 2018611, 17702765.
42. Goers ES, Purcell J, Voelker RB, Gates DP, Berglund JA. MBNL1 binds GC motifs embedded in pyrimidines to regulate alternative splicing. Nucleic Acids Res 2010, 38:2467-2484. 10.1093/nar/gkp1209, 2853123, 20071745.
43. Gitler AD, Epstein JA. Regulating heart development: the role of Nf1. Cell Cycle 2003, 2:96-98.
44. Dhaenens CM, Tran H, Frandemiche ML, Carpentier C, Schraen-Maschke S, Sistiaga A, Goicoechea M, Eddarkaoui S, Van Brussels E, Obriot H, et al. Mis-splicing of Tau exon 10 in myotonic dystrophy type 1 is reproduced by overexpression of CELF2 but not by MBNL1 silencing. Biochim Biophys Acta 2011, 1812:732-742. 10.1016/j.bbadis.2011.03.010, 21439371.
45. Ladd AN, Charlet N, Cooper TA. The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol Cell Biol 2001, 21:1285-1296. 10.1128/MCB.21.4.1285-1296.2001, 99581, 11158314.
46. Russo AF, Lanigan TM, Sullivan BE. Neuronal properties of a thyroid C-cell line: partial repression by dexamethasone and retinoic acid. Mol Endocrinol 1992, 6:207-218. 10.1210/me.6.2.207, 1569964.
47. Russo AF, Clark MS, Durham PL. Thyroid parafollicular cells. An accessible model for the study of serotonergic neurons. Mol Neurobiol 1996, 13:257-276. 10.1007/BF02740626, 8989773.
48. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983, 11:1475-1489. 10.1093/nar/11.5.1475, 325809, 6828386.
49. Terenzi F, Ladd AN. Conserved developmental alternative splicing of muscleblind-like (MBNL) transcripts regulates MBNL localization and activity. RNA Biol 2010, 7:43-55. 10.4161/rna.7.1.10401, 20009516.