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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2016, Vol. 10 Issue (3) : 250-257     DOI: 10.1007/s11684-016-0454-y
REVIEW |
Alternative splicing of inner-ear-expressed genes
Yanfei Wang1,Yueyue Liu1,Hongyun Nie1,Xin Ma2,Zhigang Xu1,*()
1. Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Jinan 250100, China
2. School of Control Science and Engineering, Shandong University, Jinan 250061, China
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Abstract  

Alternative splicing plays a fundamental role in the development and physiological function of the inner ear. Inner-ear-specific gene splicing is necessary to establish the identity and maintain the function of the inner ear. For example, exon 68 of Cadherin 23 (Cdh23) gene is subject to inner-ear-specific alternative splicing, and as a result, Cdh23(+68) is only expressed in inner ear hair cells. Alternative splicing along the tonotopic axis of the cochlea contributes to frequency tuning, particularly in lower vertebrates, such as chickens and turtles. Differential splicing of Kcnma1, which encodes for the α subunit of the Ca2+-activated K+ channel (BK channel), has been suggested to affect the channel gating properties and is important for frequency tuning. Consequently, deficits in alternative splicing have been shown to cause hearing loss, as we can observe in Bronx Waltzer (bv) mice and Sfswap mutant mice. Despite the advances in this field, the regulation of alternative splicing in the inner ear remains elusive. Further investigation is also needed to clarify the mechanism of hearing loss caused by alternative splicing deficits.

Keywords alternative splicing      inner ear      hearing loss      hair cells     
Corresponding Authors: Zhigang Xu   
Just Accepted Date: 14 June 2016   Online First Date: 08 July 2016    Issue Date: 30 August 2016
URL:  
http://academic.hep.com.cn/fmd/EN/10.1007/s11684-016-0454-y     OR     http://academic.hep.com.cn/fmd/EN/Y2016/V10/I3/250
Fig.1  Schematic drawing of inner-ear-specific splicing of Cadherin 23 (Cdh23). (A) CDH23 contains a signal peptide (SP), 27 extracellular cadherin (EC) repeats, a transmembrane (TM) domain, and a cytoplasmic segment. Exon 68 encodes for part of the cytoplasmic segment. Alternative splicing of exon 68 produces two splice variants, CDH23(+68) and CDH23(−68). (B) Cdh23(−68) is expressed in multiple tissue, including the inner ear, tongue, eye, testis, cerebrum and cerebellum. By contrast, Cdh23(+68) is only detected in the inner ear.
Gene name Description Characteristics related to alternative splicing Disease caused by gene mutation Hearing-related phenotypes in knockout/mutant mice References
CDH23 Untypical cadherin 23 Exon 68 is subject to inner-ear-specific splicing DFNB12, USH1D Tip-link interruption, hair cell degeneration, and hearing loss [1827]
KCNMA1 Calcium-activated potassium channel, subfamily M α 1 Alternatively spliced along the tonotopic axis in the cochlea Not reported OHC degeneration and progressive hearing loss [3945]
KCNQ4 Voltage-gated potassium channel, subfamily Q member 4 Alternatively spliced along the tonotopic axis in the cochlea DFNA2 OHC degeneration and progressive hearing loss [4649]
SRRM4 Splicing factor, serine/arginine repetitive matrix 4 Alternative splicing factor Not reported IHC degeneration and hearing loss [8,5362]
SFSWAP Splicing factor, suppressor of white-apricot family Alternative splicing factor Not reported OHC and SC loss, ectopic IHC, cochlear shortening, and hearing loss [6369]
Tab.1  Genes involved in or subject to alternative splicing in the inner ear
Fig.2  Schematic drawing of tonotopic alternative splicing of chicken kcnma1 mRNA, which encodes for BK channel a subunit. (A) Proposed membrane topology of BK channel a subunit. There are at least 7 alternative splicing sites in chicken kcnma1 mRNA, and the alternative splicing showed here involves the inclusion of 12 nucleotides, which encodes 4 amino acids (SRKR) [40]. The SRKR insertion site is denoted by an arrow. (B) Chicken Kcnma1 mRNA is subject to alternative splicing along the basilar papilla, which is the avian equivalent of the mammalian organ of Corti. Hair cells are arranged in a tonotopic gradient along the basilar papilla. Low-frequency sounds are detected at the apical end of the basilar papilla, and high-frequency sounds are detected at the basal end of the basilar papilla. The different expression levels of two splice variants (with or without SRKR insertion) of kcnma1 mRNA are observed along the basilar papilla.
Fig.3  Schematic drawing of the domain architecture of some SR proteins. SRSF1, also called SF2 or ASF, is a prototypical SR protein, which contains two RNA recognition motifs (RRM) and one serine/arginine-rich domain (RS). SRRM4 and SFSWAP are two splicing factors whose mutations cause hearing loss in mice.
1 Blencowe BJ. Alternative splicing: new insights from global analyses. Cell 2006; 126(1): 37–47
doi: 10.1016/j.cell.2006.06.023 pmid: 16839875
2 Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 2009; 10(11): 741–754
pmid: 19773805
3 Lee CJ, Irizarry K. Alternative splicing in the nervous system: an emerging source of diversity and regulation. Biol Psychiatry 2003; 54(8): 771–776
doi: 10.1016/S0006-3223(03)00375-5 pmid: 14550676
4 Black DL, Grabowski PJ. Alternative pre-mRNA splicing and neuronal function. Prog Mol Subcell Biol 2003; 31: 187–216
doi: 10.1007/978-3-662-09728-1_7 pmid: 12494767
5 Li Q, Lee JA, Black DL. Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 2007; 8(11): 819–831
doi: 10.1038/nrn2237 pmid: 17895907
6 Licatalosi DD, Darnell RB. Splicing regulation in neurologic disease. Neuron 2006; 52(1): 93–101
doi: 10.1016/j.neuron.2006.09.017 pmid: 17015229
7 Ranum LP, Cooper TA. RNA-mediated neuromuscular disorders. Annu Rev Neurosci 2006; 29(1): 259–277
doi: 10.1146/annurev.neuro.29.051605.113014 pmid: 16776586
8 Nakano Y, Jahan I, Bonde G, Sun X, Hildebrand MS, Engelhardt JF, Smith RJH, Cornell RA, Fritzsch B, Bánfi B. A mutation in the Srrm4 gene causes alternative splicing defects and deafness in the Bronx waltzer mouse. PLoS Genet 2012; 8(10): e1002966
doi: 10.1371/journal.pgen.1002966 pmid: 23055939
9 Ben Rebeh I, Morinière M, Ayadi L, Benzina Z, Charfedine I, Feki J, Ayadi H, Ghorbel A, Baklouti F, Masmoudi S. Reinforcement of a minor alternative splicing event in MYO7A due to a missense mutation results in a mild form of retinopathy and deafness. Mol Vis 2010; 16: 1898–1906
pmid: 21031134
10 Ouyang XM, Xia XJ, Verpy E, Du LL, Pandya A, Petit C, Balkany T, Nance WE, Liu XZ. Mutations in the alternatively spliced exons of USH1C cause non-syndromic recessive deafness. Hum Genet 2002; 111(1): 26–30
doi: 10.1007/s00439-002-0736-0 pmid: 12136232
11 Riazuddin S, Ahmed ZM, Fanning AS, Lagziel A, Kitajiri S, Ramzan K, Khan SN, Chattaraj P, Friedman PL, Anderson JM, Belyantseva IA, Forge A, Riazuddin S, Friedman TB. Tricellulin is a tight-junction protein necessary for hearing. Am J Hum Genet 2006; 79(6): 1040–1051
doi: 10.1086/510022 pmid: 17186462
12 Nal N, Ahmed ZM, Erkal E, Alper OM, Lüleci G, Dinç O, Waryah AM, Ain Q, Tasneem S, Husnain T, Chattaraj P, Riazuddin S, Boger E, Ghosh M, Kabra M, Riazuddin S, Morell RJ, Friedman TB. Mutational spectrum of MYO15A: the large N-terminal extension of myosin XVA is required for hearing. Hum Mutat 2007; 28(10): 1014–1019
doi: 10.1002/humu.20556 pmid: 17546645
13 Khateb S, Zelinger L, Ben-Yosef T, Merin S, Crystal-Shalit O, Gross M, Banin E, Sharon D. Exome sequencing identifies a founder frameshift mutation in an alternative exon of USH1C as the cause of autosomal recessive retinitis pigmentosa with late-onset hearing loss. PLoS ONE 2012; 7(12): e51566
doi: 10.1371/journal.pone.0051566 pmid: 23251578
14 Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA, Olson ENA. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol 1994; 14(3): 1647–1656
doi: 10.1128/MCB.14.3.1647 pmid: 8114702
15 Sebastian S, Faralli H, Yao Z, Rakopoulos P, Palii C, Cao Y, Singh K, Liu QC, Chu A, Aziz A, Brand M, Tapscott SJ, Dilworth FJ. Tissue-specific splicing of a ubiquitously expressed transcription factor is essential for muscle differentiation. Genes Dev 2013; 27(11): 1247–1259
doi: 10.1101/gad.215400.113 pmid: 23723416
16 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(7221): 470–476
doi: 10.1038/nature07509 pmid: 18978772
17 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(12): 1413–1415
doi: 10.1038/ng.259 pmid: 18978789
18 Siemens J, Lillo C, Dumont RA, Reynolds A, Williams DS, Gillespie PG, Müller U. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 2004; 428(6986): 950–955
doi: 10.1038/nature02483 pmid: 15057245
19 Kazmierczak P, Sakaguchi H, Tokita J, Wilson-Kubalek EM, Milligan RA, Müller U, Kachar B. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 2007; 449(7158): 87–91
doi: 10.1038/nature06091 pmid: 17805295
20 Bork JM, Peters LM, Riazuddin S, Bernstein SL, Ahmed ZM, Ness SL, Polomeno R, Ramesh A, Schloss M, Srisailpathy CR, Wayne S, Bellman S, Desmukh D, Ahmed Z, Khan SN, Kaloustian VM, Li XC, Lalwani A, Riazuddin S, Bitner-Glindzicz M, Nance WE, Liu XZ, Wistow G, Smith RJ, Griffith AJ, Wilcox ER, Friedman TB, Morell RJ. Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am J Hum Genet 2001; 68(1): 26–37
doi: 10.1086/316954 pmid: 11090341
21 Di Palma F, Holme RH, Bryda EC, Belyantseva IA, Pellegrino R, Kachar B, Steel KP, Noben-Trauth K. Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat Genet 2001; 27(1): 103–107
doi: 10.1038/83660 pmid: 11138008
22 Bolz H, von Brederlow B, Ramírez A, Bryda EC, Kutsche K, Nothwang HG, Seeliger M, del C-Salcedó Cabrera M, Vila MC, Molina OP, Gal A, Kubisch C. Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 2001; 27(1): 108–112
doi: 10.1038/83667 pmid: 11138009
23 Di Palma F, Pellegrino R, Noben-Trauth K. Genomic structure, alternative splice forms and normal and mutant alleles of cadherin 23 (Cdh23). Gene 2001; 281(1-2): 31–41
doi: 10.1016/S0378-1119(01)00761-2 pmid: 11750125
24 Siemens J, Kazmierczak P, Reynolds A, Sticker M, Littlewood-Evans A, Müller U. The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions. Proc Natl Acad Sci USA 2002; 99(23): 14946–14951
doi: 10.1073/pnas.232579599 pmid: 12407180
25 Xu Z, Peng AW, Oshima K, Heller S. MAGI-1, a candidate stereociliary scaffolding protein, associates with the tip-link component cadherin 23. J Neurosci 2008; 28(44): 11269–11276
doi: 10.1523/JNEUROSCI.3833-08.2008 pmid: 18971469
26 Yonezawa S, Hanai A, Mutoh N, Moriyama A, Kageyama T. Redox-dependent structural ambivalence of the cytoplasmic domain in the inner ear-specific cadherin 23 isoform. Biochem Biophys Res Commun 2008; 366(1): 92–97
doi: 10.1016/j.bbrc.2007.11.102 pmid: 18053802
27 Xu Z, Oshima K, Heller S. PIST regulates the intracellular trafficking and plasma membrane expression of cadherin 23. BMC Cell Biol 2010; 11(1): 80
doi: 10.1186/1471-2121-11-80 pmid: 20958966
28 Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, Wang H, Clark T, Fraser C, Ruggiu M, Zeeberg BR, Kane D, Weinstein JN, Blume J, Darnell RB. Nova regulates brain-specific splicing to shape the synapse. Nat Genet 2005; 37(8): 844–852
doi: 10.1038/ng1610 pmid: 16041372
29 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(5): 591–601
doi: 10.1016/j.molcel.2009.01.025 pmid: 19285943
30 Warzecha CC, Shen S, Xing Y, Carstens RP. The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events. RNA Biol 2009; 6(5): 546–562
doi: 10.4161/rna.6.5.9606 pmid: 19829082
31 Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, Shen S, Guo W, Xing Y, Carstens RP. An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J 2010; 29(19): 3286–3300
doi: 10.1038/emboj.2010.195 pmid: 20711167
32 Keppetipola N, Sharma S, Li Q, Black DL. Neuronal regulation of pre-mRNA splicing by polypyrimidine tract binding proteins, PTBP1 and PTBP2. Crit Rev Biochem Mol Biol 2012; 47(4): 360–378
doi: 10.3109/10409238.2012.691456 pmid: 22655688
33 Romanelli MG, Diani E, Lievens PM. New insights into functional roles of the polypyrimidine tract-binding protein. Int J Mol Sci 2013; 14(11): 22906–22932
doi: 10.3390/ijms141122906 pmid: 24264039
34 Miranda-Rottmann S, Kozlov AS, Hudspeth AJ. Highly specific alternative splicing of transcripts encoding BK channels in the chicken’s cochlea is a minor determinant of the tonotopic gradient. Mol Cell Biol 2010; 30(14): 3646–3660
doi: 10.1128/MCB.00073-10 pmid: 20479127
35 Mann ZF, Kelley MW. Development of tonotopy in the auditory periphery. Hear Res 2011; 276(1-2): 2–15
doi: 10.1016/j.heares.2011.01.011 pmid: 21276841
36 Crawford AC, Fettiplace R. An electrical tuning mechanism in turtle cochlear hair cells. J Physiol 1981; 312(1): 377–412
doi: 10.1113/jphysiol.1981.sp013634 pmid: 7265000
37 Art JJ, Fettiplace R. Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol 1987; 385(1): 207–242
doi: 10.1113/jphysiol.1987.sp016492 pmid: 2443666
38 Fuchs PA, Nagai T, Evans MG. Electrical tuning in hair cells isolated from the chick cochlea. J Neurosci 1988; 8(7): 2460–2467
pmid: 3249237
39 Navaratnam DS, Bell TJ, Tu TD, Cohen EL, Oberholtzer JC. Differential distribution of Ca2+-activated K+ channel splice variants among hair cells along the tonotopic axis of the chick cochlea. Neuron 1997; 19(5): 1077–1085
doi: 10.1016/S0896-6273(00)80398-0 pmid: 9390520
40 Rosenblatt KP, Sun ZP, Heller S, Hudspeth AJ. Distribution of Ca2+-activated K+ channel isoforms along the tonotopic gradient of the chicken’s cochlea. Neuron 1997; 19(5): 1061–1075
doi: 10.1016/S0896-6273(00)80397-9 pmid: 9390519
41 Ramanathan K, Michael TH, Jiang GJ, Hiel H, Fuchs PA. A molecular mechanism for electrical tuning of cochlear hair cells. Science 1999; 283(5399): 215–217
doi: 10.1126/science.283.5399.215 pmid: 9880252
42 Jones EM, Gray-Keller M, Art JJ, Fettiplace R. The functional role of alternative splicing of Ca2+-activated K+ channels in auditory hair cells. Ann N Y Acad Sci 1999; 868(1): 379–385
doi: 10.1111/j.1749-6632.1999.tb11299.x pmid: 10414307
43 Jones EM, Gray-Keller M, Fettiplace R. The role of Ca2+-activated K+ channel spliced variants in the tonotopic organization of the turtle cochlea. J Physiol 1999; 518(Pt 3): 653–665
doi: 10.1111/j.1469-7793.1999.0653p.x pmid: 10420004
44 Sakai Y, Harvey M, Sokolowski B. Identification and quantification of full-length BK channel variants in the developing mouse cochlea. J Neurosci Res 2011; 89(11): 1747–1760
doi: 10.1002/jnr.22713 pmid: 21800349
45 Rüttiger L, Sausbier M, Zimmermann U, Winter H, Braig C, Engel J, Knirsch M, Arntz C, Langer P, Hirt B, Müller M, Köpschall I, Pfister M, Münkner S, Rohbock K, Pfaff I, Rüsch A, Ruth P, Knipper M. Deletion of the Ca2+-activated potassium (BK) α-subunit but not the BKbeta1-subunit leads to progressive hearing loss. Proc Natl Acad Sci USA 2004; 101(35): 12922–12927
doi: 10.1073/pnas.0402660101 pmid: 15328414
46 Kubisch C, Schroeder BC, Friedrich T, Lütjohann B, El-Amraoui A, Marlin S, Petit C, Jentsch TJ. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 1999; 96(3): 437–446
doi: 10.1016/S0092-8674(00)80556-5 pmid: 10025409
47 Coucke PJ, Van Hauwe P, Kelley PM, Kunst H, Schatteman I, Van Velzen D, Meyers J, Ensink RJ, Verstreken M, Declau F, Marres H, Kastury K, Bhasin S, McGuirt WT, Smith RJ, Cremers CW, Van de Heyning P, Willems PJ, Smith SD, Van Camp G. Mutations in the KCNQ4 gene are responsible for autosomal dominant deafness in four DFNA2 families. Hum Mol Genet 1999; 8(7): 1321–1328
doi: 10.1093/hmg/8.7.1321 pmid: 10369879
48 Kharkovets T, Dedek K, Maier H, Schweizer M, Khimich D, Nouvian R, Vardanyan V, Leuwer R, Moser T, Jentsch TJ. Mice with altered KCNQ4 K+ channels implicate sensory outer hair cells in human progressive deafness. EMBO J 2006; 25(3): 642–652
doi: 10.1038/sj.emboj.7600951 pmid: 16437162
49 Beisel KW, Rocha-Sanchez SM, Morris KA, Nie L, Feng F, Kachar B, Yamoah EN, Fritzsch B. Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss. J Neurosci 2005; 25(40): 9285–9293
doi: 10.1523/JNEUROSCI.2110-05.2005 pmid: 16207888
50 Scheffer DI, Shen J, Corey DP, Chen ZY. Gene expression by mouse inner ear hair cells during development. J Neurosci 2015; 35(16): 6366–6380
doi: 10.1523/JNEUROSCI.5126-14.2015 pmid: 25904789
51 Shen J, Scheffer DI, Kwan KY, Corey DP. SHIELD: an integrative gene expression database for inner ear research. Database (Oxford) 2015, 2015:bav071
52 Long JC, Caceres JF. The SR protein family of splicing factors: master regulators of gene expression. Biochem J 2009; 417(1): 15–27
doi: 10.1042/BJ20081501 pmid: 19061484
53 Deol MS, Gluecksohn-Waelsch S. The role of inner hair cells in hearing. Nature 1979; 278(5701): 250–252
doi: 10.1038/278250a0 pmid: 423972
54 Deol MS. The inner ear in Bronx waltzer mice. Acta Otolaryngol 1981; 92(3-4): 331–336
doi: 10.3109/00016488109133269 pmid: 7324900
55 Bock GR, Yates GK, Deol MS. Cochlear potentials in the Bronx waltzer mutant mouse. Neurosci Lett 1982; 34(1): 19–25
doi: 10.1016/0304-3940(82)90086-6 pmid: 6298667
56 Horner KC, Lenoir M, Bock GR. Distortion product otoacoustic emissions in hearing-impaired mutant mice. J Acoust Soc Am 1985; 78(5): 1603–1611
doi: 10.1121/1.392798 pmid: 4067076
57 Inagaki M, Kon K, Suzuki S, Kobayashi N, Kaga M, Nanba E. Characteristic findings of auditory brainstem response and otoacoustic emission in the Bronx waltzer mouse. Brain Dev 2006; 28(10): 617–624
doi: 10.1016/j.braindev.2006.04.006 pmid: 16730938
58 Whitlon DS, Gabel C, Zhang X. Cochlear inner hair cells exist transiently in the fetal Bronx Waltzer (bv/bv) mouse. J Comp Neurol 1996; 364(3): 515–522
doi: 10.1002/(SICI)1096-9861(19960115)364:3<515::AID-CNE9>3.0.CO;2-7 pmid: 8820880
59 Sobkowicz HM, Inagaki M, August BK, Slapnick SM. Abortive synaptogenesis as a factor in the inner hair cell degeneration in the Bronx Waltzer (bv) mutant mouse. J Neurocytol 1999; 28(1): 17–38
doi: 10.1023/A:1007059616607 pmid: 10573605
60 Cheong MA, Steel KP. Early development and degeneration of vestibular hair cells in bronx waltzer mutant mice. Hear Res 2002; 164(1-2): 179–189
doi: 10.1016/S0378-5955(01)00429-4 pmid: 11950537
61 Bussoli TJ, Kelly A, Steel KP. Localization of the bronx waltzer (bv) deafness gene to mouse chromosome 5. Mamm Genome 1997; 8(10): 714–717
doi: 10.1007/s003359900552 pmid: 9321462
62 Calarco JA, Superina S, O’Hanlon D, Gabut M, Raj B, Pan Q, Skalska U, Clarke L, Gelinas D, van der Kooy D, Zhen M, Ciruna B, Blencowe BJ. Regulation of vertebrate nervous system alternative splicing and development by an SR-related protein. Cell 2009; 138(5): 898–910
doi: 10.1016/j.cell.2009.06.012 pmid: 19737518
63 Moayedi Y, Basch ML, Pacheco NL, Gao SS, Wang R, Harrison W, Xiao N, Oghalai JS, Overbeek PA, Mardon G, Groves AK. The candidate splicing factor Sfswap regulates growth and patterning of inner ear sensory organs. PLoS Genet 2014; 10(1): e1004055
doi: 10.1371/journal.pgen.1004055 pmid: 24391519
64 Chou TB, Zachar Z, Bingham PM. Developmental expression of a regulatory gene is programmed at the level of splicing. EMBO J 1987; 6(13): 4095–4104
pmid: 2832151
65 Zachar Z, Chou TB, Bingham PM. Evidence that a regulatory gene autoregulates splicing of its transcript. EMBO J 1987; 6(13): 4105–4111
pmid: 3443103
66 Zachar Z, Chou TB, Kramer J, Mims IP, Bingham PM. Analysis of autoregulation at the level of pre-mRNA splicing of the suppressor-of-white-apricot gene in Drosophila. Genetics 1994; 137(1): 139–150
pmid: 8056305
67 Denhez F, Lafyatis R. Conservation of regulated alternative splicing and identification of functional domains in vertebrate homologs to the Drosophila splicing regulator, suppressor-of-white-apricot. J Biol Chem 1994; 269(23): 16170–16179
pmid: 8206918
68 Sarkissian M, Winne A, Lafyatis R. The mammalian homolog of suppressor-of-white-apricot regulates alternative mRNA splicing of CD45 exon 4 and fibronectin IIICS. J Biol Chem 1996; 271(49): 31106–31114
doi: 10.1074/jbc.271.49.31106 pmid: 8940107
69 Lemaire R, Winne A, Sarkissian M, Lafyatis R. SF2 and SRp55 regulation of CD45 exon 4 skipping during T cell activation. Eur J Immunol 1999; 29(3): 823–837
doi: 10.1002/(SICI)1521-4141(199903)29:03<823::AID-IMMU823>3.0.CO;2-C pmid: 10092085
70 Kiernan AE, Ahituv N, Fuchs H, Balling R, Avraham KB, Steel KP, Hrabé de Angelis M. The Notch ligand Jagged1 is required for inner ear sensory development. Proc Natl Acad Sci USA 2001; 98(7): 3873–3878
doi: 10.1073/pnas.071496998 pmid: 11259677
71 Tsai H, Hardisty RE, Rhodes C, Kiernan AE, Roby P, Tymowska-Lalanne Z, Mburu P, Rastan S, Hunter AJ, Brown SD, Steel KP. The mouse slalom mutant demonstrates a role for Jagged1 in neuroepithelial patterning in the organ of Corti. Hum Mol Genet 2001; 10(5): 507–512
doi: 10.1093/hmg/10.5.507 pmid: 11181574
72 Brooker R, Hozumi K, Lewis J. Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 2006; 133(7): 1277–1286
doi: 10.1242/dev.02284 pmid: 16495313
73 Kiernan AE, Xu J, Gridley T. The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet 2006; 2(1): 27–38
doi: 10.1371/journal.pgen.0020004 pmid: 16410827
74 Verduci L, Simili M, Rizzo M, Mercatanti A, Evangelista M, Mariani L, Rainaldi G, Pitto L. MicroRNA (miRNA)-mediated interaction between leukemia/lymphoma-related factor (LRF) and alternative splicing factor/splicing factor 2 (ASF/SF2) affects mouse embryonic fibroblast senescence and apoptosis. J Biol Chem 2010; 285(50): 39551–39563
doi: 10.1074/jbc.M110.114736 pmid: 20923760
75 Wu H, Sun S, Tu K, Gao Y, Xie B, Krainer AR, Zhu J. A splicing-independent function of SF2/ASF in microRNA processing. Mol Cell 2010; 38(1): 67–77
doi: 10.1016/j.molcel.2010.02.021 pmid: 20385090
76 Meseguer S, Mudduluru G, Escamilla JM, Allgayer H, Barettino D. MicroRNAs-10a and-10b contribute to retinoic acid-induced differentiation of neuroblastoma cells and target the alternative splicing regulatory factor SFRS1 (SF2/ASF). J Biol Chem 2011; 286(6): 4150–4164
doi: 10.1074/jbc.M110.167817 pmid: 21118818
77 Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 2007; 27(3): 435–448
doi: 10.1016/j.molcel.2007.07.015 pmid: 17679093
78 Boutz PL, Chawla G, Stoilov P, Black DL. MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes Dev 2007; 21(1): 71–84
doi: 10.1101/gad.1500707 pmid: 17210790
79 Weston MD, Pierce ML, Rocha-Sanchez S, Beisel KW, Soukup GA. MicroRNA gene expression in the mouse inner ear. Brain Res 2006; 1111(1): 95–104
doi: 10.1016/j.brainres.2006.07.006 pmid: 16904081
80 Friedman LM, Dror AA, Mor E, Tenne T, Toren G, Satoh T, Biesemeier DJ, Shomron N, Fekete DM, Hornstein E, Avraham KB. MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci USA 2009; 106(19): 7915–7920
doi: 10.1073/pnas.0812446106 pmid: 19416898
81 Lewis MA, Steel KP. MicroRNAs in mouse development and disease. Semin Cell Dev Biol 2010; 21(7): 774–780
doi: 10.1016/j.semcdb.2010.02.004 pmid: 20152923
82 Ushakov K, Rudnicki A, Avraham KB. MicroRNAs in sensorineural diseases of the ear. Front Mol Neurosci 2013; 6: 52
doi: 10.3389/fnmol.2013.00052 pmid: 24391537
83 Moulton VR, Gillooly AR, Tsokos GC. Ubiquitination regulates expression of the serine/arginine-rich splicing factor 1 (SRSF1) in normal and systemic lupus erythematosus (SLE) T cells. J Biol Chem 2014; 289(7): 4126–4134
doi: 10.1074/jbc.M113.518662 pmid: 24368769
84 Venables JP, Dalgliesh C, Paronetto MP, Skitt L, Thornton JK, Saunders PT, Sette C, Jones KT, Elliott DJ. SIAH1 targets the alternative splicing factor T-STAR for degradation by the proteasome. Hum Mol Genet 2004; 13(14): 1525–1534
doi: 10.1093/hmg/ddh165 pmid: 15163637
85 Zhang L, Tran NT, Su H, Wang R, Lu Y, Tang H, Aoyagi S, Guo A, Khodadadi-Jamayran A, Zhou D, Qian K, Hricik T, Côté J, Han X, Zhou W, Laha S, Abdel-Wahab O, Levine RL, Raffel G, Liu Y, Chen D, Li H, Townes T, Wang H, Deng H, Zheng YG, Leslie C, Luo M, Zhao X. Cross-talk between PRMT1-mediated methylation and ubiquitylation on RBM15 controls RNA splicing. eLife 2015; 4: e07938<?Pub Caret?>
doi: 10.7554/eLife.07938 pmid: 26575292
86 Henzl MT, O’Neal J, Killick R, Thalmann I, Thalmann R. OCP1, an F-box protein, co-localizes with OCP2/SKP1 in the cochlear epithelial gap junction region. Hear Res 2001; 157(1-2): 100–111
doi: 10.1016/S0378-5955(01)00285-4 pmid: 11470190
87 Nelson RF, Glenn KA, Zhang Y, Wen H, Knutson T, Gouvion CM, Robinson BK, Zhou Z, Yang B, Smith RJ, Paulson HL. Selective cochlear degeneration in mice lacking the F-box protein, Fbx2, a glycoprotein-specific ubiquitin ligase subunit. J Neurosci 2007; 27(19): 5163–5171
doi: 10.1523/JNEUROSCI.0206-07.2007 pmid: 17494702
88 Narimatsu M, Bose R, Pye M, Zhang L, Miller B, Ching P, Sakuma R, Luga V, Roncari L, Attisano L, Wrana JL. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 2009; 137(2): 295–307
doi: 10.1016/j.cell.2009.02.025 pmid: 19379695
89 Van Campenhout CA, Eitelhuber A, Gloeckner CJ, Giallonardo P, Gegg M, Oller H, Grant SG, Krappmann D, Ueffing M, Lickert H. Dlg3 trafficking and apical tight junction formation is regulated by nedd4 and nedd4-2 e3 ubiquitin ligases. Dev Cell 2011; 21(3): 479–491
doi: 10.1016/j.devcel.2011.08.003 pmid: 21920314
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