Nova regulates brain-specific splicing to shape the synapse

Nature Genetics

Volumn 37, Issue 8, 2005, Pages 844-852

  Ule, Jernej ^a   Ule, Aljaž ^b   Spencer, Joanna ^a   Williams, Alan ^c   Hu, Jing Shan ^c   Cline, Melissa ^c   Wang, Hui ^c   Clark, Tyson ^c   Fraser, Claire ^a   Ruggiu, Matteo ^a   Zeeberg, Barry R ^d   Kane, David ^e   Weinstein, John N ^d   Blume, John ^c   Darnell, Robert B ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c Thermo Fisher Scientific   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e GENERAL DYNAMICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER RECEPTOR; NOVA RNA BINDING PROTEIN; PROTEIN; PROTEOME; RNA; RNA BINDING PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN; EXON; GENOME; MOUSE; NEOCORTEX; NEWBORN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SYNAPSE;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, NEOPLASM; MICE; MICE, KNOCKOUT; NEOCORTEX; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA-BINDING PROTEINS; SYNAPSES;

ANIMALIA;

EID: 23044431574     PISSN: 10614036     EISSN: None     Source Type: Journal    
DOI: 10.1038/ng1610     Document Type: Article

References (50)

1. International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 431, 931-945 (2004).
2. Black, D.L. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103, 367-370 (2000).
3. Harbison, C.T. et al. Transcriptional regulatory code of a eukaryotic genome. Nature 431, 99-104 (2004).
4. McClung, C.A. & Nestler, E.J. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci. 6, 1208-1215 (2003).
5. Livesey, F.J., Furukawa, T., Steffen, M.A., Church, G.M. & Cepko, C.L. Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene. Crx. Curr. Biol. 10, 301-310 (2000).
6. Brivanlou, A.H. & Darnell, J.E. Jr. Signal transduction and the control of gene expression. Science 295, 813-818 (2002).
7. Shin, C. & Manley, J.L. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 5, 727-738 (2004).
8. Jensen, K.B. et al. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25, 359-371 (2000).
9. Ule, J. et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 302, 1212-1215 (2003).
10. Kanadia, R.N. et al. A muscleblind knockout model for myotonic dystrophy. Science 302, 1978-1980 (2003).
11. Xu, X. et al. ASF/SF2-regulated CaMKIIdelta alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle. Cell 120, 59-72 (2005).
12. Clark, T.A., Sugnet, C.W. & Ares, M. Jr. Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296, 907-910 (2002).
13. Johnson, J.M. et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144 (2003).
14. Pan, Q. et al. Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Mol. Cell 16, 929-941 (2004).
15. Le, K. et al. Detecting tissue-specific regulation of alternative splicing as a qualitative change in microarray data. Nucleic Acids Res. 32, e180 (2004).
16. Buckanovich, R.J., Yang, Y.Y. & Darnell, R.B. The onconeural antigen Nova-1 is a neuron-specific RNA-binding protein, the activity of which is inhibited by paraneoplastic antibodies. J. Neurosci. 16, 1114-1122 (1996).
17. Yang, Y.Y, Yin, G.L. & Darnell, R.B. The neuronal RNA-binding protein Nova-2 is implicated as the autoantigen targeted in POMA patients with dementia. Proc. Natl. Acad. Sci. USA 95, 13254-13259 (1998).
18. Buckanovich, R.J. & Darnell, R.B. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol. Cell. Biol. 17, 3194-3201 (1997).
19. Lewis, H.A. et al. Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 100, 323-332 (2000).
20. Dredge, B.K. & Darnell, R.B. Nova regulates GABA(A) receptor gamma2 alternative splicing via a distal downstream UCAU-rich intronic splicing enhancer. Mol. Cell. Biol. 23, 4687-4700 (2003).
21. Dredge, B.K., Stefani, G., Engelhard, C.C. & Darnell, R.B. Nova autoregulation reveals dual functions in neuronal splicing. EMBO J. 24, 1608-1620 (2005).
22. Wang, H. et al. Gene structure-based splice variant deconvolution using a microarray platform. Bioinformatics 19 Suppl 1, i315-i322 (2003).
23. Zeeberg, B.R. et al. GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 4, R28 (2003).
24. Zeeberg, B.R. et al. High-Throughput GoMiner, an 'industrial-strength' integrative Gene Ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics 6, 168 (2005).
25. Huang, C.S. et al. Long-term potentiation of slow synaptic inhibition induced by coincidence detection of excitation in the CA1 pyramidal neuron requires Nova-2 function. Cell (in the press).
26. Balla, Z., Hoch, B., Karczewski, P. & Blasig, I.E. Calcium/calmodulin-dependent protein kinase IIdelta 2 and gamma isoforms regulate potassium currents of rat brain capillary endothelial cells under hypoxic conditions. J. Biol. Chem. 277, 21306-21314 (2002).
27. Lu, C.S., Hodge, J.J., Mehren, J., Sun, X.X. & Griffith, L.C. Regulation of the Ca2+/CaM-responsive pool of CaMKII by scaffold-dependent autophosphorylation. Neuron 40, 1185-1197 (2003).
28. Dateki, M. et al. Neurochondrin negatively regulates CaMKII phosphorylation and nervous system specific gene disruption results in epileptic seizure. J. Biol. Chem. 280, 20503-20508 (2005).
29. Kobrinsky, E., Mirshahi, T., Zhang, H., Jin, T. & Logothetis, D.E. Receptor-mediated hydrolysis of plasma membrane messenger PIP2 leads to K+-current desensitization. Nat. Cell Biol. 2, 507-514 (2000).
30. Abraham, W.C. & Bear, M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126-130 (1996).
31. Ango, F. et al. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119, 257-272 (2004).
32. Parra, M. et al. Differential domain evolution and complex RNA processing in a family of paralogous EPB41 (protein 4.1) genes facilitate expression of diverse tissue-specific isoforms. Genomics 84, 637-646 (2004).
33. Schischmanoff, P.O. et al. Defining of the minimal domain of protein 4.1 involved in spectrin-actin binding. J. Biol. Chem. 270, 21243-21250 (1995).
34. Burgess, R.W., Nguyen, Q.T., Son, Y.J., Lichtman, J.W. & Sanes, J.R. Alternatively spliced isoforms of nerve- and muscle-derived agrin: their roles at the neuromuscular junction. Neuron 23, 33-44 (1999).
35. Biederer, T. et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525-1531 (2002).
36. Gao, W.Q. et al. Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5. Mol. Cell. Neurosci. 11, 247-259 (1998).
37. Holmberg, J., Clarke, D.L. & Frisen, J. Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408, 203-206 (2000).
38. Hartwell, L.H., Hopfield, J.J., Leibler, S. & Murray, A.W. From molecular to modular cell biology. Nature 402, C47-C52 (1999).
39. Nagoshi, R.N., McKeown, M., Burtis, K.C., Belote, J.M. & Baker, B.S. The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 53, 229-236 (1988).
40. Hedley, M.L. & Maniatis, T. Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vitro. Cell 65, 579-586 (1991).
41. Hentze, M.W. & Kuhn, L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 93, 8175-8182 (1996).
42. Hieronymus, H. & Silver, P.A. Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat. Genet. 33, 155-161 (2003).
43. Gerber, A.P., Herschlag, D. & Brown, P.O. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2, E79 (2004).
44. Kim, S., Shi, H., Lee, D.K. & Lis, J.T. Specific SR protein-dependent splicing substrates identified through genomic SELEX. Nucleic Acids Res. 31, 1955-1961 (2003).
45. Tenenbaum, S.A., Carson, C.C., Lager, P.J. & Keene, J.D. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 97, 14085-14090 (2000).
46. Waggoner, S.A. & Liebhaber, S.A. Identification of mRNAs associated with alphaCP2-containing RNP complexes. Mol. Cell. Biol. 23, 7055-7067 (2003).
47. Darnell, J.C. et al. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489-499 (2001).
48. Brown, V. et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107, 477-487 (2001).
49. Fodor, S.P. et al. Light-directed, spatially addressable parallel chemical synthesis. Science 251, 767-773 (1991).
50. Wheeler, R. A method of consolidating and combining EST and mRNA alignments to a genome to enumerate supported splice variants. Lecture Notes in Computer Science 2452, 201-209 (2002).