Regulation of gene expression in mammalian nervous system through alternative pre-mRNA splicing coupled with RNA quality control mechanisms

Molecular and Cellular Neuroscience

Volumn 56, Issue , 2013, Pages 420-428

  Yap, Karen ^a   Makeyev, Eugene V ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Alternative pre mRNA splicing; Nervous system development and function; Nonsense mediated decay; Nuclear retention and elimination of incompletely spliced transcripts; Post transcriptional regulation of gene expression; RNA quality control

Indexed keywords

APOLIPOPROTEIN E; HEAT SHOCK PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA PRECURSOR; NUCLEAR CAP BINDING PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN; SERINE ARGININE RICH PROTEIN; TAR DNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; AUTONOMIC NERVOUS SYSTEM FUNCTION; BIOLOGICAL FUNCTIONS; BRAIN REGION; CELL JUNCTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE CONTROL; GENE EXPRESSION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MAMMAL CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NONSENSE MUTATION; NUCLEAR PORE COMPLEX; PHYSIOLOGY; PRIORITY JOURNAL; QUALITY CONTROL; REVIEW; RNA METABOLISM; RNA PROCESSING; RNA TRANSCRIPTION; RNA TRANSLATION;

EUKARYOTA; MAMMALIA;

ALTERNATIVE PRE-MRNA SPLICING; NERVOUS SYSTEM DEVELOPMENT AND FUNCTION; NONSENSE-MEDIATED DECAY; NUCLEAR RETENTION AND ELIMINATION OF INCOMPLETELY SPLICED TRANSCRIPTS; POST-TRANSCRIPTIONAL REGULATION OF GENE EXPRESSION; RNA QUALITY CONTROL;

ALTERNATIVE SPLICING; ANIMALS; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; NONSENSE MEDIATED MRNA DECAY; RNA, MESSENGER;

EID: 84884817424     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.01.003     Document Type: Review

References (139)

1. Adibhatla R.M., Hatcher J.F. Altered lipid metabolism in brain injury and disorders. Subcell. Biochem. 2008, 49:241-268.
2. Ameur A., Zaghlool A., Halvardson J., Wetterbom A., Gyllensten U., Cavelier L., Feuk L. Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain. Nat. Struct. Mol. Biol. 2011, 18:1435-1440.
3. Andreassi C., Riccio A. To localize or not to localize: mRNA fate is in 3'UTR ends. Trends Cell Biol. 2009, 19:465-474.
4. Anko M.L., Morales L., Henry I., Beyer A., Neugebauer K.M. Global analysis reveals SRp20- and SRp75-specific mRNPs in cycling and neural cells. Nat. Struct. Mol. Biol. 2010, 17:962-970.
5. Anko M.L., Muller-McNicoll M., Brandl H., Curk T., Gorup C., Henry I., Ule J., Neugebauer K.M. The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol. 2012, 13:R17.
6. Avendano-Vazquez S.E., Dhir A., Bembich S., Buratti E., Proudfoot N., Baralle F.E. Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev. 2012, 26:1679-1684.
7. Averbeck N., Sunder S., Sample N., Wise J.A., Leatherwood J. Negative control contributes to an extensive program of meiotic splicing in fission yeast. Mol. Cell 2005, 18:491-498.
8. Ayala Y.M., De Conti L., Avendano-Vazquez S.E., Dhir A., Romano M., D'Ambrogio A., Tollervey J., Ule J., Baralle M., Buratti E., Baralle F.E. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 2011, 30:277-288.
9. Baek D., Green P. Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12813-12818.
10. Barash Y., Calarco J.A., Gao W., Pan Q., Wang X., Shai O., Blencowe B.J., Frey B.J. Deciphering the splicing code. Nature 2010, 465:53-59.
11. Barrett L.W., Fletcher S., Wilton S.D. Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol. Life Sci. 2012, 69:3613-3634.
12. Berg Michael G., Singh Larry N., Younis I., Liu Q., Pinto Anna M., Kaida D., Zhang Z., Cho S., Sherrill-Mix S., Wan L., Dreyfuss G. U1 snRNP determines mRNA length and regulates isoform expression. Cell 2012, 150:53-64.
13. Bicknell A.A., Cenik C., Chua H.N., Roth F.P., Moore M.J. Introns in UTRs: why we should stop ignoring them. Bioessays 2012, 34:1025-1034.
14. Black D.L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 2003, 72:291-336.
15. Boutz P.L., Stoilov P., Li Q., Lin C.H., Chawla G., Ostrow K., Shiue L., Ares M., Black D.L. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev. 2007, 21:1636-1652.
16. Bruno I.G., Karam R., Huang L., Bhardwaj A., Lou C.H., Shum E.Y., Song H.W., Corbett M.A., Gifford W.D., Gecz J., Pfaff S.L., Wilkinson M.F. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol. Cell 2011, 42:500-510.
17. Calarco J.A., 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 B.J. Regulation of vertebrate nervous system alternative splicing and development by an SR-related protein. Cell 2009, 138:898-910.
18. Calarco J.A., Zhen M., Blencowe B.J. Networking in a global world: establishing functional connections between neural splicing regulators and their target transcripts. RNA 2011, 17:775-791.
19. Chang D.D., Sharp P.A. Regulation by HIV Rev depends upon recognition of splice sites. Cell 1989, 59:789-795.
20. Chang Y.F., Imam J.S., Wilkinson M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 2007, 76:51-74.
21. Chen M., Manley J.L. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 2009, 10:741-754.
22. Chen L.L., DeCerbo J.N., Carmichael G.G. Alu element-mediated gene silencing. EMBO J. 2008, 27:1694-1705.
23. Coyle J.H., Bor Y.-C., Rekosh D., Hammarskjold M.-L. The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA 2011, 17:1344-1356.
24. Cremona N., Potter K., Wise J.A. A meiotic gene regulatory cascade driven by alternative fates for newly synthesized transcripts. Mol. Biol. Cell 2011, 22:66-77.
25. Cuccurese M., Russo G., Russo A., Pietropaolo C. Alternative splicing and nonsense-mediated mRNA decay regulate mammalian ribosomal gene expression. Nucleic Acids Res. 2005, 33:5965-5977.
26. Cullen B.R. Nuclear mRNA export: insights from virology. Trends Biochem. Sci. 2003, 28:419-424.
27. Dai W., Zhang G., Makeyev E.V. RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res. 2012, 40:787-800.
28. Damianov A., Black D.L. Autoregulation of Fox protein expression to produce dominant negative splicing factors. RNA 2010, 16:405-416.
29. de Lima Morais D.A., Harrison P.M. Large-scale evidence for conservation of NMD candidature across mammals. PLoS One 2010, 5:e11695.
30. Doma M.K., Parker R. RNA quality control in eukaryotes. Cell 2007, 131:660-668.
31. Dredge B.K., Jensen K.B. NeuN/Rbfox3 nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS One 2011, 6:e21585.
32. Egecioglu D.E., Chanfreau G. Proofreading and spellchecking: a two-tier strategy for pre-mRNA splicing quality control. RNA 2011, 17:383-389.
33. Fasken M.B., Corbett A.H. Mechanisms of nuclear mRNA quality control. RNA Biol. 2009, 6:237-241.
34. Galante P.A., Sakabe N.J., Kirschbaum-Slager N., de Souza S.J. Detection and evaluation of intron retention events in the human transcriptome. RNA 2004, 10:757-765.
35. Galy V., Gadal O., Fromont-Racine M., Romano A., Jacquier A., Nehrbass U. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 2004, 116:63-73.
36. Gehman L.T., Stoilov P., Maguire J., Damianov A., Lin C.H., Shiue L., Ares M., Mody I., Black D.L. The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat. Genet. 2011, 43:706-711.
37. Gehman L.T., Meera P., Stoilov P., Shiue L., O'Brien J.E., Meisler M.H., Ares M., Otis T.S., Black D.L. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev. 2012, 26:445-460.
38. Giorgi C., Yeo G.W., Stone M.E., Katz D.B., Burge C., Turrigiano G., Moore M.J. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 2007, 130:179-191.
39. Girard C., Will C.L., Peng J., Makarov E.M., Kastner B., Lemm I., Urlaub H., Hartmuth K., Lührmann R. Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat. Commun. 2012, 3:994.
40. Gong C., Maquat L.E. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3'UTRs via Alu elements. Nature 2011, 470:284-288.
41. Graille M., Seraphin B. Surveillance pathways rescuing eukaryotic ribosomes lost in translation. Nat. Rev. Mol. Cell Biol. 2012, 13:727-735.
42. Green R.E., Lewis B.P., Hillman R.T., Blanchette M., Lareau L.F., Garnett A.T., Rio D.C., Brenner S.E. Widespread predicted nonsense-mediated mRNA decay of alternatively-spliced transcripts of human normal and disease genes. Bioinformatics 2003, 19(Suppl. 1):i118-i121.
43. Hattori D., Chen Y., Matthews B.J., Salwinski L., Sabatti C., Grueber W.B., Zipursky S.L. Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms. Nature 2009, 461:644-648.
44. Houseley J., Tollervey D. The many pathways of RNA degradation. Cell 2009, 136:763-776.
45. Huang L., Wilkinson M.F. Regulation of nonsense-mediated mRNA decay. Wiley Interdiscip. Rev. RNA 2012, 3:807-828.
46. Hwang J., Maquat L.E. Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr. Opin. Genet. Dev. 2011, 21:422-430.
47. International Human Genome Sequencing Consortium Finishing the euchromatic sequence of the human genome. Nature 2004, 431:931-945.
48. Ip J.Y., Schmidt D., Pan Q., Ramani A.K., Fraser A.G., Odom D.T., Blencowe B.J. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res. 2011, 21:390-401.
49. Isken O., Maquat L.E. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 2007, 21:1833-1856.
50. Ji Z., Tian B. Reprogramming of 3' untranslated regions of mRNAs by alternative polyadenylation in generation of pluripotent stem cells from different cell types. PLoS One 2009, 4:e8419.
51. Johnson C., Primorac D., McKinstry M., McNeil J., Rowe D., Lawrence J.B. Tracking COL1A1 RNA in osteogenesis imperfecta. splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain. J. Cell Biol. 2000, 150:417-432.
52. Kaida D., Motoyoshi H., Tashiro E., Nojima T., Hagiwara M., Ishigami K., Watanabe H., Kitahara T., Yoshida T., Nakajima H., Tani T., Horinouchi S., Yoshida M. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol. 2007, 3:576-583.
53. Karam R., Wilkinson M. A conserved microRNA/NMD regulatory circuit controls gene expression. RNA Biol. 2012, 9:22-26.
54. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8:533-543.
55. Keppetipola N., Sharma S., Li Q., Black D.L. Neuronal regulation of pre-mRNA splicing by polypyrimidine tract binding proteins, PTBP1 and PTBP2. Crit. Rev. Biochem. Mol. Biol. 2012, 47:360-378.
56. Keren H., Lev-Maor G., Ast G. Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 2010, 11:345-355.
57. Kervestin S., Jacobson A. NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 2012, 13:700-712.
58. Kim Y.K., Furic L., DesGroseillers L., Maquat L.E. Mammalian Staufen1 recruits Upf1 to specific mRNA 32UTRs so as to elicit mRNA decay. Cell 2005, 120:195-208.
59. Kim K.K., Adelstein R.S., Kawamoto S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J. Biol. Chem. 2009, 284:31052-31061.
60. Lareau L.F., Brooks A.N., Soergel D.A., Meng Q., Brenner S.E. The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv. Exp. Med. Biol. 2007, 623:190-211.
61. Lareau L.F., Inada M., Green R.E., Wengrod J.C., Brenner S.E. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 2007, 446:926-929.
62. Le Hir H., Izaurralde E., Maquat L.E., Moore M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 2000, 19:6860-6869.
63. Leclerc R.D. Survival of the sparsest: robust gene networks are parsimonious. Mol. Syst. Biol. 2008, 4.
64. Lee H.C., Oh N., Cho H., Choe J., Kim Y.K. Nonsense-mediated translational repression involves exon junction complex downstream of premature translation termination codon. FEBS Lett. 2010, 584:795-800.
65. Legrain P., Rosbash M. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell 1989, 57:573-583.
66. Lemieux C., Marguerat S., Lafontaine J., Barbezier N., Bähler J., Bachand F. A pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol. Cell 2011, 44:108-119.
67. Lenhard B., Sandelin A., Carninci P. Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat. Rev. Genet. 2012, 13:233-245.
68. Levine M., Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151.
69. Lewis B.P., Green R.E., Brenner S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. 2003, 100:189-192.
70. Li Y., Bor Y.C., Misawa Y., Xue Y., Rekosh D., Hammarskjold M.L. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 2006, 443:234-237.
71. Li Q., Lee J.A., Black D.L. Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci. 2007, 8:819-831.
72. Licatalosi D.D., Darnell R.B. RNA processing and its regulation: global insights into biological networks. Nat. Rev. Genet. 2010, 11:75-87.
73. Licatalosi D.D., Yano M., Fak J.J., Mele A., Grabinski S.E., Zhang C., Darnell R.B. Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev. 2012, 26:1626-1642.
74. Liu G., Razanau A., Hai Y., Yu J., Sohail M., Lobo V.G., Chu J., Kung S.K.P., Xie J. A conserved serine of heterogeneous nuclear ribonucleoprotein L (hnRNP L) mediates depolarization-regulated alternative splicing of potassium channels. J. Biol. Chem. 2012, 287(27):22709-22716.
75. Llorian M., Schwartz S., Clark T.A., Hollander D., Tan L.Y., Spellman R., Gordon A., Schweitzer A.C., de la Grange P., Ast G., Smith C.W. Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat. Struct. Mol. Biol. 2010, 17:1114-1123.
76. Long A.A., Mahapatra C.T., Woodruff E.A., Rohrbough J., Leung H.T., Shino S., An L., Doerge R.W., Metzstein M.M., Pak W.L., Broadie K. The nonsense-mediated decay pathway maintains synapse architecture and synaptic vesicle cycle efficacy. J. Cell Sci. 2010, 123:3303-3315.
77. Lutz C.S., Moreira A. Alternative mRNA polyadenylation in eukaryotes: an effective regulator of gene expression. Wiley Interdiscip. Rev. RNA 2011, 2:22-31.
78. Magen A., Ast G. The importance of being divisible by three in alternative splicing. Nucleic Acids Res. 2005, 33:5574-5582.
79. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 2007, 27:435-448.
80. Mansfield K.D., Keene J.D. Neuron-specific ELAV/Hu proteins suppress HuR mRNA during neuronal differentiation by alternative polyadenylation. Nucleic Acids Res. 2012, 40:2734-2746.
81. Maquat L.E., Gong C. Gene expression networks: competing mRNA decay pathways in mammalian cells. Biochem. Soc. Trans. 2009, 37:1287-1292.
82. Mayr C., Bartel D.P. Widespread shortening of 32UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009, 138:673-684.
83. McGlincy N.J., Smith C.W. Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense?. Trends Biochem. Sci. 2008, 33:385-393.
84. McGlincy N.J., Tan L.Y., Paul N., Zavolan M., Lilley K.S., Smith C.W. Expression proteomics of UPF1 knockdown in HeLa cells reveals autoregulation of hnRNP A2/B1 mediated by alternative splicing resulting in nonsense-mediated mRNA decay. BMC Genomics 2010, 11:565.
85. McKee A.E., Minet E., Stern C., Riahi S., Stiles C.D., Silver P.A. A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev. Biol. 2005, 5:14.
86. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G.M., Morrison J.H., O'Dell T.J., Grant S.G.N. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998, 396:433-439.
87. Moldon A., Malapeira J., Gabrielli N., Gogol M., Gomez-Escoda B., Ivanova T., Seidel C., Ayte J. Promoter-driven splicing regulation in fission yeast. Nature 2008, 455:997-1000.
88. Moore M.J., Proudfoot N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009, 136:688-700.
89. Mudge J.M., Frankish A., Fernandez-Banet J., Alioto T., Derrien T., Howald C., Reymond A., Guigo R., Hubbard T., Harrow J. The origins, evolution, and functional potential of alternative splicing in vertebrates. Mol. Biol. Evol. 2011, 28:2949-2959.
90. Munding E.M., Igel A.H., Shiue L., Dorighi K.M., Trevino L.R., Ares M. Integration of a splicing regulatory network within the meiotic gene expression program of Saccharomyces cerevisiae. Genes Dev. 2010, 24:2693-2704.
91. Neu-Yilik G., Kulozik A.E. Chapter 4 NMD: multitasking between mRNA surveillance and modulation of gene expression. Advances in Genetics 2008, 185-243. Academic Press. C.H. Jeffrey (Ed.).
92. Ni J.Z., Grate L., Donohue J.P., Preston C., Nobida N., O'Brien G., Shiue L., Clark T.A., Blume J.E., Ares M. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 2007, 21:708-718.
93. Nicholson P., Muhlemann O. Cutting the nonsense: the degradation of PTC-containing mRNAs. Biochem. Soc. Trans. 2010, 38:1615-1620.
94. Nicholson P., Yepiskoposyan H., Metze S., Zamudio Orozco R., Kleinschmidt N., Muhlemann O. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol. Life Sci. 2010, 67:677-700.
95. Nilsen T.W., Graveley B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463.
96. Norris A.D., Calarco J.A. Emerging roles of alternative pre-mRNA splicing regulation in neuronal development and function. Front. Neurosci. 2012, 6:122.
97. O'Brien J.E., Drews V.L., Jones J.M., Dugas J.C., Barres B.A., Meisler M.H. Rbfox proteins regulate alternative splicing of neuronal sodium channel SCN8A. Mol. Cell. Neurosci. 2012, 49:120-126.
98. Palancade B., Zuccolo M., Loeillet S., Nicolas A., Doye V. Pml39, a novel protein of the nuclear periphery required for nuclear retention of improper messenger ribonucleoparticles. Mol. Biol. Cell 2005, 16:5258-5268.
99. Pan Q., Saltzman A.L., Kim Y.K., Misquitta C., Shai O., Maquat L.E., Frey B.J., Blencowe B.J. Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev. 2006, 20:153-158.
100. Pan Q., Shai O., Lee L.J., Frey B.J., Blencowe B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 2008, 40:1413-1415.
101. Parenteau J., Durand M., Morin G., Gagnon J., Lucier J.-F., Wellinger Raymund J., Chabot B., Abou Elela S. Introns within ribosomal protein genes regulate the production and function of yeast ribosomes. Cell 2011, 147:320-331.
102. Park J.W., Graveley B.R. Complex alternative splicing. Adv. Exp. Med. Biol. 2007, 623:50-63.
103. Pinard A., Seddik R., Bettler B. GABAB receptors: physiological functions and mechanisms of diversity. Advances in Pharmacology 2010, 231-255. Academic Press. P.B. Thomas (Ed.).
104. Prasanth K.V., Prasanth S.G., Xuan Z., Hearn S., Freier S.M., Bennett C.F., Zhang M.Q., Spector D.L. Regulating gene expression through RNA nuclear retention. Cell 2005, 123:249-263.
105. Rain J.-C., Legrain P. In vivo commitment to splicing in yeast involves the nucleotide upstream from the branch site conserved sequence and the Mud2 protein. EMBO J. 1997, 16:1759-1771.
106. Rajanala K., Nandicoori V.K. Localization of nucleoporin Tpr to the nuclear pore complex is essential for Tpr mediated regulation of the export of unspliced RNA. PLoS One 2012, 7:e29921.
107. Rossbach O., Hung L.-H., Schreiner S., Grishina I., Heiner M., Hui J., Bindereif A. Auto- and cross-regulation of the hnRNP L proteins by alternative splicing. Mol. Cell. Biol. 2009, 29:1442-1451.
108. Saltzman A.L., Kim Y.K., Pan Q., Fagnani M.M., Maquat L.E., Blencowe B.J. Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol. Cell. Biol. 2008, 28:4320-4330.
109. Saltzman A.L., Pan Q., Blencowe B.J. Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev. 2011, 25:373-384.
110. Sandberg R., Neilson J.R., Sarma A., Sharp P.A., Burge C.B. Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 2008, 320:1643-1647.
111. Sauliere J., Murigneux V., Wang Z., Marquenet E., Barbosa I., Le Tonqueze O., Audic Y., Paillard L., Roest Crollius H., Le Hir H. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat. Struct. Mol. Biol. 2012, 19:1124-1131.
112. Schmid M., Jensen T.H. Nuclear quality control of RNA polymerase II transcripts. Wiley Interdiscip. Rev. RNA 2010, 1:474-485.
113. Schoenberg D.R., Maquat L.E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 2012, 13:246-259.
114. Sheng M., Hoogenraad C.C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007, 76:823-847.
115. Shibasaki, T., Tokunaga, A., Sakamoto, R., Sagara, H., Noguchi, S., Sasaoka, T., Yoshida, N., in press. PTB deficiency causes the loss of adherens junctions in the dorsal telencephalon and leads to lethal hydrocephalus. Cereb. Cortex. http://dx.doi.org/10.1093/cercor/bhs161.
116. Shibayama M., Ohno S., Osaka T., Sakamoto R., Tokunaga A., Nakatake Y., Sato M., Yoshida N. Polypyrimidine tract-binding protein is essential for early mouse development and embryonic stem cell proliferation. FEBS J. 2009, 276:6658-6668.
117. Singh G., Kucukural A., Cenik C., Leszyk J.D., Shaffer S.A., Weng Z., Moore M.J. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 2012, 151(4):750-764.
118. Sommer P., Nehrbass U. Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore. Curr. Opin. Cell Biol. 2005, 17:294-301.
119. Spellman R., Llorian M., Smith C.W.J. Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol. Cell 2007, 27:420-434.
120. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de Belleroche J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
121. Suckale J., Wendling O., Masjkur J., Jager M., Munster C., Anastassiadis K., Stewart A.F., Solimena M. PTBP1 is required for embryonic development before gastrulation. PLoS One 2011, 6:e16992.
122. Sun S., Zhang Z., Sinha R., Karni R., Krainer A.R. SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol. 2010, 17:306-312.
123. Sureau A., Gattoni R., Dooghe Y., Stévenin J., Soret J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 2001, 20:1785-1796.
124. Takemura R., Takeiwa T., Taniguchi I., McCloskey A., Ohno M. Multiple factors in the early splicing complex are involved in the nuclear retention of pre-mRNAs in mammalian cells. Genes Cells 2011, 16:1035-1049.
125. Taniguchi I., Masuyama K., Ohno M. Role of purine-rich exonic splicing enhancers in nuclear retention of pre-mRNAs. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13684-13689.
126. Tarpey P.S., Raymond F.L., Nguyen L.S., Rodriguez J., Hackett A., Vandeleur L., Smith R., Shoubridge C., Edkins S., Stevens C., O'Meara S., Tofts C., Barthorpe S., Buck G., Cole J., Halliday K., Hills K., Jones D., Mironenko T., Perry J., Varian J., West S., Widaa S., Teague J., Dicks E., Butler A., Menzies A., Richardson D., Jenkinson A., Shepherd R., Raine K., Moon J., Luo Y., Parnau J., Bhat S.S., Gardner A., Corbett M., Brooks D., Thomas P., Parkinson-Lawrence E., Porteous M.E., Warner J.P., Sanderson T., Pearson P., Simensen R.J., Skinner C., Hoganson G., Superneau D., Wooster R., Bobrow M., Turner G., Stevenson R.E., Schwartz C.E., Futreal P.A., Srivastava A.K., Stratton M.R., Gecz J. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat. Genet. 2007, 39:1127-1133.
127. Underwood J.G., Boutz P.L., Dougherty J.D., Stoilov P., Black D.L. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol. Cell. Biol. 2005, 25:10005-10016.
128. Wang Z., Burge C.B. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 2008, 14:802-813.
129. Wang E.T., Sandberg R., Luo S., Khrebtukova I., Zhang L., Mayr C., Kingsmore S.F., Schroth G.P., Burge C.B. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476.
130. Wollerton M.C., Gooding C., Wagner E.J., Garcia-Blanco M.A., Smith C.W. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 2004, 13:91-100.
131. Xu Q., Walker D., Bernardo A., Brodbeck J., Balestra M.E., Huang Y. Intron-3 retention/splicing controls neuronal expression of apolipoprotein E in the CNS. J. Neurosci. 2008, 28:1452-1459.
132. Xue Y., Zhou Y., Wu T., Zhu T., Ji X., Kwon Y.S., Zhang C., Yeo G., Black D.L., Sun H., Fu X.D., Zhang Y. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol. Cell 2009, 36:996-1006.
133. Yamashita A., Izumi N., Kashima I., Ohnishi T., Saari B., Katsuhata Y., Muramatsu R., Morita T., Iwamatsu A., Hachiya T., Kurata R., Hirano H., Anderson P., Ohno S. SMG-8 and SMG-9, two novel subunits of the SMG-1 complex, regulate remodeling of the mRNA surveillance complex during nonsense-mediated mRNA decay. Genes Dev. 2009, 23:1091-1105.
134. Yap K., Lim Z.Q., Khandelia P., Friedman B., Makeyev E.V. Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention. Genes Dev. 2012, 26:1209-1223.
135. You K.T., Li L.S., Kim N.G., Kang H.J., Koh K.H., Chwae Y.J., Kim K.M., Kim Y.K., Park S.M., Jang S.K., Kim H. Selective translational repression of truncated proteins from frameshift mutation-derived mRNAs in tumors. PLoS Biol. 2007, 5:e109.
136. 2+/calmodulin-dependent protein kinase IV-regulated alternative splicing through cytidine-adenosine repeats. J. Biol. Chem. 2009, 284:1505-1513.
137. Zhang Z., Xin D., Wang P., Zhou L., Hu L., Kong X., Hurst L.D. Noisy splicing, more than expression regulation, explains why some exons are subject to nonsense-mediated mRNA decay. BMC Biol. 2009, 7:23.
138. Zheng S., Gray E.E., Chawla G., Porse B.T., O'Dell T.J., Black D.L. PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2. Nat. Neurosci. 2012, 15:381-388.
139. Zubovic L., Baralle M., Baralle F.E. Mutually exclusive splicing regulates the Nav 1.6 sodium channel function through a combinatorial mechanism that involves three distinct splicing regulatory elements and their ligands. Nucleic Acids Res. 2012, 40:6255-6269.