NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure

eLife

Volumn 2013, Issue 2, 2013, Pages

  Eom, Taesun ^a   Zhang, Chaolin ^a   Wang, Huidong ^a   Lay, Kenneth ^a   Fak, John ^a   Noebels, Jeffrey L ^b   Darnell, Robert B ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NERVE PROTEIN; NOVA PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; NOVA ANTIGEN; TUMOR ANTIGEN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXON; HIGH THROUGHPUT SEQUENCING; IMMUNOFLUORESCENCE; INTRON; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NORTHERN BLOTTING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS REGULATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; STOP CODON; SYNAPSE; WESTERN BLOTTING; 3' UNTRANSLATED REGION; ANIMAL; BRAIN; CELL FRACTIONATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, NEOPLASM; BRAIN; EXONS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; SEIZURES; SUBCELLULAR FRACTIONS; SYNAPSES;

EID: 84879048904     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00178     Document Type: Article

References (91)

1. Blainey PC, van Oijen AM, Banerjee A, Verdine GL, Xie XS. 2006. A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc Natl Acad Sci USA 103:5752-7.
2. Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, et al. 2007. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21:1636-52.
3. Brennan CM, Steitz JA. 2001. HuR and mRNA stability. Cell Mol Life Sci 58:266-77.
4. Buckanovich RJ, Darnell RB. 1997. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol Cell Biol 17:3194-201.
5. Buckanovich RJ, Posner JB, Darnell RB. 1993. Nova, the paraneoplastic Ri antigen, is homologous to an RNA-binding protein and is specifically expressed in the developing motor system. Neuron 11:657-72.
6. Chao JA, Patskovsky Y, Patel V, Levy M, Almo SC, Singer RH. 2010. ZBP1 recognition of beta-actin zipcode induces RNA looping. Genes Dev 24:148-58.
7. Cooper TA, Wan L, Dreyfuss G. 2009. RNA and disease. Cell 136:777-93.
8. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, et al. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660-3.
9. Darnell RB. 2004. Paraneoplastic neurologic disorders: windows into neuronal function and tumor immunity. Arch Neurol 61:30-2.
10. Darnell RB. 2006. Developing global insight into RNA regulation. Cold Spring Harb Symp Quant Biol 71:321-7.
11. Darnell RB, Posner JB. 2006. Paraneoplastic syndromes affecting the nervous system. Semin Oncol 33:270-98.
12. Darnell RB. 1996. Onconeural antigens and the paraneoplastic neurologic disorders: at the intersection of cancer, immunity, and the brain. Proc Natl Acad Sci USA 93:4529-36.
13. Darnell RB. 2010. HITS-CLIP: panoramic views of protein-RNA regulation in living cells. Wiley Interdiscip Rev RNA 1:266-86.
14. Darnell RB, Posner JB. 2011. Paraneoplastic syndromes (contemporary neurology series). USA:Oxford University Press.
15. Dennis G Jnr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. 2003. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4:P3.
16. Dredge BK, Darnell RB. 2003. Nova regulates GABA(A) receptor gamma2 alternative splicing via a distal downstream UCAU-rich intronic splicing enhancer. Mol Cell Biol 23:4687-700.
17. Dredge BK, Stefani G, Engelhard CC, Darnell RB. 2005. Nova autoregulation reveals dual functions in neuronal splicing. EMBO J 24:1608-20.
18. Dredge BK, Jensen KB. 2011. NeuN/Rbfox3 nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS One 6:e21585.
19. Eom T, Antar LN, Singer RH, Bassell GJ. 2003. Localization of a beta-actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses. J Neurosci 23:10433-44.
20. Fabian MR, Sonenberg N, Filipowicz W. 2010. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351-79.
21. Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, Shiue L, et al. 2011. The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 43:706-11. doi: 10.1038/ng.841.
22. Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, et al. 2007. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179-91.
23. Goina E, Skoko N, Pagani F. 2008. Binding of DAZAP1 and hnRNPA1/A2 to an exonic splicing silencer in a natural BRCA1 exon 18 mutant. Mol Cell Biol 28:3850-60.
24. Goodrich JS, Clouse KN, Schupbach T. 2004. Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development 131:1949-58.
25. Gu W, Pan F, Zhang H, Bassell GJ, Singer RH. 2002. A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J Cell Biol 156:41-51.
26. Guan Q, Zheng W, Tang S, Liu X, Zinkel RA, Tsui KW, et al. 2006. Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast. PLoS Genet 2, e203.
27. Gurnett CA, Veile R, Zempel J, Blackburn L, Lovett M, Bowcock A. 2008. Disruption of sodium bicarbonate transporter SLC4A10 in a patient with complex partial epilepsy and mental retardation. Arch Neurol 65:550-3.
28. Hachet O, Ephrussi A. 2004. Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428:959-63.
29. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57.
30. Huang L, Wilkinson MF. 2012. Regulation of nonsense-mediated mRNA decay. Wiley Interdiscip Rev RNA 3:807-28. doi: 10.1002/wrna.1137.
31. Huang Y, Steitz JA. 2005. SRprises along a messenger's journey. Mol Cell 17:613-5.
32. Hur EM, Zhou FQ. 2010. GSK3 signalling in neural development. Nat Rev Neurosci 11:539-51.
33. Hyvönen MT, Uimari A, Keinänen TA, Heikkinen S, Pellinen R, Wahlfors T, et al. 2006. Polyamine-regulated unproductive splicing and translation of spermidine/spermine N1-acetyltransferase. RNA 12, 1569-82.
34. Ince-Dunn G, Okano HJ, Jensen KB, Park WY, Zhong R, Ule J, et al. 2012. Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75:1067-80. doi: 10.1016/j.neuron.2012.07.009.
35. Jensen KB, Musunuru K, Lewis HA, Burley SK, Darnell RB. 2000a. The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain. Proc Natl Acad Sci USA 97:5740-5.
36. Jensen KB, Darnell RB. 2008. CLIP: crosslinking and immunoprecipitation of in vivo RNA targets of RNA-binding proteins. Methods Mol Biol 488:85-98.
37. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, Okano HJ, et al. 2000b. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25:359-71.
38. Kennedy MJ, Ehlers MD. 2011. Mechanisms and function of dendritic exocytosis. Neuron 69:856-75.
39. Khabar KS. 2010. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell Mol Life Sci 67:2937-55.
40. Kim KK, Adelstein RS, Kawamoto S. 2009. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:31052-61.
41. Kishore S, Luber S, Zavolan M. 2010. Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression. Brief Funct Genomics 9:391-404.
42. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11:597-610.
43. Levine TD, Gao F, King PH, Andrews LG, Keene JD. 1993. Hel-N1: an autoimmune RNA-binding protein with specificity for 3' uridylate-rich untranslated regions of growth factor mRNA's. Mol Cell Biol 13:3494-504.
44. Lewis BP, Green RE, Brenner SE. 2003. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci USA 100:189-92.
45. Lewis HA, Musunuru K, Jensen KB, Edo C, Chen H, Darnell RB, et al. 2000. Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 100:323-32.
46. Licatalosi DD, Darnell RB. 2006. Splicing regulation in neurologic disease. Neuron 52, 93-101.
47. Licatalosi DD, Darnell RB. 2010. RNA processing and its regulation: global insights into biological networks. Nat Rev Genet 11:75-87.
48. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, et al. 2008. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456:464-9.
49. Licatalosi DD, Yano M, Fak JJ, Mele A, Grabinski SE, Zhang C, et al. 2012. Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev 26:1626-42.
50. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. 2007. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435-48.
51. Maniatis T, Reed R. 2002. An extensive network of coupling among gene expression machines. Nature 416:499-506.
52. Markovtsov V, Nikolic JM, Goldman JA, Turck CW, Chou MY, Black DL. 2000. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol Cell Biol 20:7463-79.
53. Martin KC, Ephrussi A. 2009. mRNA localization: gene expression in the spatial dimension. Cell 136:719-30.
54. Matsuda D, Sato H, Maquat LE. 2008. Chapter 9. Studying nonsense-mediated mRNA decay in mammalian cells. Methods Enzymol 449:177-201.
55. Meisler MH, O'Brien JE, Sharkey LM. 2010. Sodium channel gene family: epilepsy mutations, gene interactions and modifier effects. J Physiol 588:1841-8.
56. Meisner NC, Filipowicz W. 2011. Properties of the Regulatory RNA-Binding Protein HuR and its Role in Controlling miRNA Repression. Adv Exp Med Biol 700:106-23.
57. Mendell JT, Rhys CM, Dietz HC. 2002. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 298:419-22.
58. Myer VE, Fan XC, Steitz JA. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J 16:2130-9.
59. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, O'Brien G, et al. 2007. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 21:708-18.
60. Okano HJ, Darnell RB. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-37.
61. Pan F, Hüttelmaier S, Singer RH, Gu W. 2007. ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription. Mol Cell Biol 27:8340-51.
62. Peng SS, Chen CY, Xu N, Shyu AB. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17:3461-70.
63. Polydorides AD, Okano HJ, Yang YY, Stefani G, Darnell RB. 2000. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc Natl Acad Sci USA 97:6350-5.
64. Poulos MG, Batra R, Charizanis K, Swanson MS. 2011. Developments in RNA splicing and disease. Cold Spring Harb Perspect Biol 3:a000778. doi: 10.1101/cshperspect.a000778.
65. Qu M, Aronica E, Boer K, Fallmar D, Kumlien E, Nister M, et al. 2009. DLG3/SAP102 protein expression in malformations of cortical development: a study of human epileptic cortex by tissue microarray. Epilepsy Res 84:33-41.
66. Quenault T, Lithgow T, Traven A. 2011. PUF proteins: repression, activation and mRNA localization. Trends Cell Biol 21:104-12.
67. Racca C, Gardiol A, Eom T, Ule J, Triller A, Darnell RB. 2010. The neuronal splicing factor Nova co-localizes with target RNAs in the dendrite. Front Neural Circuits 4:5.
68. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev 23:1-11.
69. Ruggiu M, Herbst R, Kim N, Jevsek M, Fak JJ, Mann MA, et al. 2009. Rescuing Z+ agrin splicing in Nova null mice restores synapse formation and unmasks a physiologic defect in motor neuron firing. Proc Natl Acad Sci USA 106:3513-8.
70. Saltzman AL, Kim YK, Pan Q, Fagnani MM, Maquat LE, Blencowe BJ. 2008. Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 28:4320-30.
71. Sander T, Toliat MR, Heils A, Leschik G, Becker C, Ruschendorf F, et al. 2002. Association of the 867Asp variant of the human anion exchanger 3 gene with common subtypes of idiopathic generalized epilepsy. Epilepsy Res 51:249-55.
72. Schoenberg DR, Maquat LE. 2012. Regulation of cytoplasmic mRNA decay. Nat Rev Genet 13:246-59. doi: 10.1038/nrg3160.
73. Singh NA, Pappas C, Dahle EJ, Claes LR, Pruess TH, De Jonghe P, et al. 2009. A role of SCN9A in human epilepsies, as a cause of febrile seizures and as a potential modifier of Dravet syndrome. PLoS Genet 5:e1000649.
74. Szabo A, Dalmau J, Manley G, Rosenfeld M, Wong E, Henson J, et al. 1991. HuD, a paraneoplastic encephalomyelitis antigen contains RNA-binding domains and is homologous to Elav and sex lethal. Cell 67:325-33.
75. Tarpey PS, Raymond FL, Nguyen LS, Rodriguez J, Hackett A, Vandeleur L, et al. 2007. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 39:1127-33.
76. Turski L, Cavalheiro EA, Sieklucka-Dziuba M, Ikonomidou-Turski C, Czuczwar SJ, Turski WA. 1986. Seizures produced by pilocarpine: neuropathological sequelae and activity of glutamate decarboxylase in the rat forebrain. Brain Res 398:37-48.
77. Ule J, Darnell RB. 2006. RNA binding proteins and the regulation of neuronal synaptic plasticity. Curr Opin Neurobiol 16:102-10.
78. Ule J, Jensen K, Mele A, Darnell RB. 2005a. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37:376-86.
79. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB. 2003. CLIP identifies Nova-regulated RNA networks in the brain. Science 302:1212-5.
80. Ule J, Stefani G, Mele A, Ruggiu M, Wang X, Taneri B, et al. 2006. An RNA map predicting Nova-dependent splicing regulation. Nature 444:580-6.
81. Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, et al. 2005b. Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37:844-52.
82. Wang F, Greene EC. 2011. Single-molecule studies of transcription: from one RNA polymerase at a time to the gene expression profile of a cell. J Mol Biol 412:814-31.
83. Wollerton MC, Gooding C, Wagner EJ, Garcia-Blanco MA, Smith CW. 2004. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol Cell 13:91-100.
84. Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, et al. 2003. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13, 1863-72.
85. Yang YY, Yin GL, Darnell RB. 1998. The neuronal RNA-binding protein Nova-2 is implicated as the autoantigen targeted in POMA patients with dementia. Proc Natl Acad Sci USA 95:13254-9.
86. Yano M, Hayakawa-Yano Y, Mele A, Darnell RB. 2010. Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 66:848-58.
87. Yap K, Lim ZQ, Khandelia P, Friedman B, Makeyev EV. 2012. Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention. Genes Dev 26:1209-23.
88. Ying Z, Bingaman W, Najm IM. 2004. Increased numbers of coassembled PSD-95 to NMDA-receptor subunits NR2B and NR1 in human epileptic cortical dysplasia. Epilepsia 45:314-21.
89. Yoshii A, Constantine-Paton M. 2010. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol 70:304-22.
90. Zhang C, Frias MA, Mele A, Ruggiu M, Eom T, Marney CB, et al. 2010. Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls. Science 329:439-43.
91. Zheng S, Gray EE, Chawla G, Porse BT, O'Dell TJ, Black DL. 2012. PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2. Nat Neurosci 15:381-8, S1. doi: 10.1038/nn.3026.