A Pair of RNA-binding proteins controls networks of splicing events contributing to specialization of neural cell types

Molecular Cell

Volumn 54, Issue 6, 2014, Pages 946-959

  Norris, Adam D ^a   Gao, Shangbang ^b   Norris, Megan L ^a   Ray, Debashish ^c   Ramani, Arun K ^c   Fraser, Andrew G ^c   Morris, Quaid ^c   Hughes, Timothy R ^c   Zhen, Mei ^b,c   Calarco, John A ^a  

^a HARVARD UNIVERSITY   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ISOPROTEIN; PROTEIN EXC 7; PROTEIN UNC 64; PROTEIN UNC 75; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CAENORHABDITIS ELEGANS; CELL SPECIFICITY; CELL TYPE; CHOLINERGIC NERVE CELL; EXON; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REGULATORY MECHANISM; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ALTERNATIVE SPLICING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHOLINERGIC NEURONS; GABAERGIC NEURONS; MUTATION; NERVOUS SYSTEM; PROTEIN ISOFORMS; RNA-BINDING PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNTAXIN 1;

EID: 84902687151     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.05.004     Document Type: Article

References (57)

1. Aoto J., Martinelli D.C., Malenka R.C., Tabuchi K., Südhof T.C. Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell 2013, 154:75-88.
2. Barberan-Soler S., Zahler A.M. Alternative splicing regulation during C. elegans development: splicing factors as regulated targets. PLoS Genetics 2008, 4:e1000001.
3. Barberan-Soler S., Medina P., Estella J., Williams J., Zahler A.M. Co-regulation of alternative splicing by diverse splicing factors in Caenorhabditis elegans. Nucleic Acids Res. 2011, 39:666-674.
4. Barbosa-Morais N.L., Irimia M., Pan Q., Xiong H.Y., Gueroussov S., Lee L.J., Slobodeniuc V., Kutter C., Watt S., Colak R., et al. The evolutionary landscape of alternative splicing in vertebrate species. Science 2012, 338:1587-1593.
5. Bigelow H., Doitsidou M., Sarin S., Hobert O. MAQGene: software to facilitate C. elegans mutant genome sequence analysis. Nat. Methods 2009, 6:549.
6. Boucard A.A., Chubykin A.A., Comoletti D., Taylor P., Südhof T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 2005, 48:229-236.
7. 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.
8. Braunschweig U., Gueroussov S., Plocik A.M., Graveley B.R., Blencowe B.J. Dynamic integration of splicing within gene regulatory pathways. Cell 2013, 152:1252-1269.
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
10. Calarco J.A., Superina S., O'Hanlon D., Gabut M., Raj B., Pan Q., Skalska U., Clarke L., Gelinas D., van der Kooy D., et al. Regulation of vertebrate nervous system alternative splicing and development by an SR-related protein. Cell 2009, 138:898-910.
11. Charlet B.N., Logan P., Singh G., Cooper T.A. Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol. Cell 2002, 9:649-658.
12. Chih B., Gollan L., Scheiffele P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 2006, 51:171-178.
13. Darnell R.B. RNA protein interaction in neurons. Annu. Rev. Neurosci. 2013, 36:243-270.
14. Dasgupta T., Ladd A.N. The importance of CELF control: molecular and biological roles of the CUG-BP, Elav-like family of RNA-binding proteins. Wiley Interdiscip. Rev. RNA 2012, 3:104-121.
15. Fleming V.A., Geng C., Ladd A.N., Lou H. 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 Mol. Biol. 2012, 13:35.
16. Fujita M., Kawano T., Ohta A., Sakamoto H. Neuronal expression of a Caenorhabditis elegans elav-like gene and the effect of its ectopic expression. Biochem. Biophys. Res. Commun. 1999, 260:646-652.
17. Fujita M., Hawkinson D., King K.V., Hall D.H., Sakamoto H., Buechner M. The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Dev. Biol. 2003, 256:290-301.
18. Gao S., Zhen M. Action potentials drive body wall muscle contractions in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2011, 108:2557-2562.
19. 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.
20. Gerstein M.B., Lu Z.J., Van Nostrand E.L., Cheng C., Arshinoff B.I., Liu T., Yip K.Y., Robilotto R., Rechtsteiner A., Ikegami K., et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2010, 330:1775-1787. modENCODE Consortium.
21. Golgi C. Sulla fina anatomia degli organi centrali del sistema nervoso [On the fine anatomy of the central organs of the nervous system]. Riv. Sper. Freniat. 1883, 9:1-17.
22. Goodman M.B., Lindsay T.H., Lockery S.R., Richmond J.E. Electrophysiological methods for Caenorhabditis elegans neurobiology. Methods Cell Biol. 2012, 107:409-436.
23. Grant G.R., Farkas M.H., Pizarro A.D., Lahens N.F., Schug J., Brunk B.P., Stoeckert C.J., Hogenesch J.B., Pierce E.A. Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics 2011, 27:2518-2528.
24. Greig L.C., Woodworth M.B., Galazo M.J., Padmanabhan H., Macklis J.D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 2013, 14:755-769.
25. Hobert O., Carrera I., Stefanakis N. The molecular and gene regulatory signature of a neuron. Trends Neurosci. 2010, 33:435-445.
26. Jensen K.B., Dredge B.K., Stefani G., Zhong R., Buckanovich R.J., Okano H.J., Yang Y.Y.L., Darnell R.B. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 2000, 25:359-371.
27. Kuroyanagi H., Kobayashi T., Mitani S., Hagiwara M. Transgenic alternative-splicing reporters reveal tissue-specific expression profiles and regulation mechanisms invivo. Nat. Methods 2006, 3:909-915.
28. Kuroyanagi H., Ohno G., Sakane H., Maruoka H., Hagiwara M. Visualization and genetic analysis of alternative splicing regulation invivo using fluorescence reporters in transgenic Caenorhabditis elegans. Nat. Protoc. 2010, 5:1495-1517.
29. Kuroyanagi H., Watanabe Y., Hagiwara M. CELF family RNA-binding protein UNC-75 regulates two sets of mutually exclusive exons of the unc-32 gene in neuron-specific manners in Caenorhabditis elegans. PLoS Genet. 2013, 9:e1003337.
30. Kuroyanagi H., Watanabe Y., Suzuki Y., Hagiwara M. Position-dependent and neuron-specific splicing regulation by the CELF family RNA-binding protein UNC-75 in Caenorhabditis elegans. Nucleic Acids Res. 2013, 41:4015-4025.
31. Lesa G.M., Palfreyman M., Hall D.H., Clandinin M.T., Rudolph C., Jorgensen E.M., Schiavo G. Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans. J.Cell Sci. 2003, 116:4965-4975.
32. Liewald J.F., Brauner M., Stephens G.J., Bouhours M., Schultheis C., Zhen M., Gottschalk A. Optogenetic analysis of synaptic function. Nat. Methods 2008, 5:895-902.
33. Loria P.M., Duke A., Rand J.B., Hobert O. Two neuronal, nuclear-localized RNA binding proteins involved in synaptic transmission. Curr. Biol. 2003, 13:1317-1323.
34. Markovtsov V., Nikolic J.M., Goldman J.A., Turck C.W., Chou M.Y., Black D.L. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol. Cell. Biol. 2000, 20:7463-7479.
35. Miura S.K., Martins A., Zhang K.X., Graveley B.R., Zipursky S.L. Probabilistic splicing of Dscam1 establishes identity at the level of single neurons. Cell 2013, 155:1166-1177.
36. Nilsen T.W., Graveley B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463.
37. Norris A.D., Calarco J.A. Emerging roles of alternative pre-mRNA splicing regulation in neuronal development and function. Front. Neurosci. 2012, 6:122.
38. Ogawa H., Harada S., Sassa T., Yamamoto H., Hosono R. Functional properties of the unc-64 gene encoding a Caenorhabditis elegans syntaxin. J.Biol. Chem. 1998, 273:2192-2198.
39. Ohno G., Hagiwara M., Kuroyanagi H. STAR family RNA-binding protein ASD-2 regulates developmental switching of mutually exclusive alternative splicing invivo. Genes Dev. 2008, 22:360-374.
40. Orengo J.P., Bundman D., Cooper T.A. A bichromatic fluorescent reporter for cell-based screens of alternative splicing. Nucleic Acids Res. 2006, 34:e148.
41. Raj B., O'Hanlon D., Vessey J.P., Pan Q., Ray D., Buckley N.J., Miller F.D., Blencowe B.J. Cross-regulation between an alternative splicing activator and a transcription repressor controls neurogenesis. Mol. Cell 2011, 43:843-850.
42. Ramani A.K., Calarco J.A., Pan Q., Mavandadi S., Wang Y., Nelson A.C., Lee L.J., Morris Q., Blencowe B.J., Zhen M., Fraser A.G. Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res. 2011, 21:342-348.
43. Ramón y Cajal S. Investigaciones de Histología Comparada en Los Centros Ópticos de Los Vertebrados [Comparative Histology Research in the Optical Centers of Vertebrates] 1890, Consejo Superior de Investigaciones Científicas, Instituto Ramón y Cajal, Madrid, Spain.
44. Ray D., Kazan H., Cook K.B., Weirauch M.T., Najafabadi H.S., Li X., Gueroussov S., Albu M., Zheng H., Yang A., et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177.
45. Richmond J.E., Jorgensen E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 1999, 2:791-797.
46. Saifee O., Wei L., Nonet M.L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol. Biol. Cell 1998, 9:1235-1252.
47. Shalek A.K., Satija R., Adiconis X., Gertner R.S., Gaublomme J.T., Raychowdhury R., Schwartz S., Yosef N., Malboeuf C., Lu D., et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498:236-240.
48. Sieburth D., Ch'ng Q., Dybbs M., Tavazoie M., Kennedy S., Wang D., Dupuy D., Rual J.F., Hill D.E., Vidal M., et al. Systematic analysis of genes required for synapse structure and function. Nature 2005, 436:510-517.
49. Tursun B., Cochella L., Carrera I., Hobert O. A toolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PLoS ONE 2009, 4:e4625.
50. Ule J., Ule A., Spencer J., Williams A., Hu J.S., Cline M., Wang H., Clark T., Fraser C., Ruggiu M., et al. Nova regulates brain-specific splicing to shape the synapse. Nat. Genet. 2005, 37:844-852.
51. Wang E.T., Cody N.A., Jog S., Biancolella M., Wang T.T., Treacy D.J., Luo S., Schroth G.P., Housman D.E., Reddy S., et al. Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 2012, 150:710-724.
52. Yamashita Y., Kumabe T., Cho Y.Y., Watanabe M., Kawagishi J., Yoshimoto T., Fujino T., Kang M.J., Yamamoto T.T. Fatty acid induced glioma cell growth is mediated by the acyl-CoA synthetase 5 gene located on chromosome 10q25.1-q25.2, a region frequently deleted in malignant gliomas. Oncogene 2000, 19:5919-5925.
53. Yano M., Hayakawa-Yano Y., Mele A., Darnell R.B. Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 2010, 66:848-858.
54. Zahler A.M. Alternative splicing in C. elegans. WormBook 2005, 1-13.
55. Zhang C., Zhang Z., Castle J., Sun S., Johnson J., Krainer A.R., Zhang M.Q. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev. 2008, 22:2550-2563.
56. Zheng S., Black D.L. Alternative pre-mRNA splicing in neurons: growing up and extending its reach. Trends Genet. 2013, 29:442-448.
57. Zheng S., Damoiseaux R., Chen L., Black D.L. A broadly applicable high-throughput screening strategy identifies new regulators of Dlg4 (Psd-95) alternative splicing. Genome Res. 2013, 23:998-1007.