Essential roles for the splicing regulator nSR100/SRRM4 during nervous system development

Genes and Development

Volumn 29, Issue 7, 2015, Pages 746-759

  Quesnel Vallières, Mathieu ^a,b   Irimia, Manuel ^a,c   Cordes, Sabine P ^a,b   Blencowe, Benjamin J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

Alternative splicing; Microexons; Nervous system development; SR proteins

Indexed keywords

NSR100 PROTEIN; PROTEIN; SRRM4 PROTEIN; UNCLASSIFIED DRUG; NERVE PROTEIN; NSR100 PROTEIN, MOUSE;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CORPUS CALLOSUM; EMBRYO; EMBRYONIC STEM CELL; FOREBRAIN; GENE EXPRESSION; HEAD TILTING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; INNER HAIR CELL; LOXP SITE; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROFILAMENT; NEUROLOGIC DISEASE; NONHUMAN; PERINATAL MORTALITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; EMBRYOLOGY; EXON; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MUTATION; NERVOUS SYSTEM; RNA SPLICING; SEQUENCE ANALYSIS;

MUS; VERTEBRATA;

ANIMALS; EMBRYO, MAMMALIAN; EXONS; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MUTATION; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEUROGENESIS; RNA SPLICING; SEQUENCE ANALYSIS, RNA;

EID: 84926386137     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.256115.114     Document Type: Article

References (56)

1. Akbarian S, Bunney WE Jr, Potkin SG, Wigal SB, Hagman JO, Sandman CA, Jones EG. 1993. Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 50: 169-177.
2. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Colak R, et al. 2012. The evolutionary landscape of alternative splicing in vertebrate species. Science 338: 1587-1593.
3. Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC. 2005. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α-and β-neurexins. Neuron 48: 229-236.
4. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. 2013. Dynamic integration of splicing within gene regulatory pathways. Cell 152: 1252-1269.
5. Braunschweig U, Barbosa-Morais NL, Pan Q, Nachman EN, Alipanahi B, Gonatopoulos-Pournatzis T, Frey B, Irimia M, Blencowe BJ. 2014. Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res 24: 1774-1786.
6. Broeke JHP, Roelandse M, Luteijn MJ, Boiko T, Matus A, Toonen RF, Verhage M. 2010. Munc18 and Munc13 regulate early neurite outgrowth. Biol Cell 102: 479-488.
7. 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: 657-672.
8. Buljan M, Chalancon G, Eustermann S, Wagner GP, Fuxreiter M, Bateman A, Babu MM. 2012. Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks. Mol Cell 46: 871-883.
9. Calarco JA, Superina S, O'Hanlon D, Gabut M, Raj B, Pan Q, Skalska U, Clarke L, Gelinas D, van der Kooy D, et al. 2009. Regulation of vertebrate nervous system alternative splicing and development by an SR-related protein. Cell 138: 898-910.
10. Caviness VSJ. 1982. Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res 256: 293-302.
11. Champagnat J, Morin-Surun MP, Bouvier J, Thoby-Brisson M, Fortin G. 2011. Prenatal development of central rhythm generation. Respir Physiol Neurobiol 178: 146-155.
12. Chedotal A. 2007. Slits and their receptors. Adv Exp Med Biol 621: 65-80.
13. Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10: 741-754.
14. Chen Z, Gore BB, Long H, Ma L, Tessier-Lavigne M. 2008. Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58: 325-332.
15. Cheung HN, Dunbar C, Morotz GM, Cheng WH, Chan HY, Miller CC, Lau KF. 2014. FE65 interacts with ADP-ribosylation factor 6 to promote neurite outgrowth. FASEB J 28: 337-349.
16. Deol MS, Gluecksohn-Waelsch S. 1979. The role of inner hair cells in hearing. Nature 278: 250-252.
17. Donahoo AL, Richards LJ. 2009. Understanding the mechanisms of callosal development through the use of transgenic mouse models. Semin Pediatr Neurol 16: 127-142.
18. Ellis JD, Barrios-Rodiles M, Colak R, Irimia M, Kim T, Calarco JA, Wang X, Pan Q, O'Hanlon D, Kim PM, et al. 2012. Tissue-specific alternative splicing remodels protein-protein interaction networks. Mol Cell 46: 884-892.
19. Feng Y, Walsh CA. 2004. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44: 279-293.
20. Friedel RH, Seisenberger C, Kaloff C, Wurst W. 2007. EUCOMM-the European conditional mouse mutagenesis program. Brief Funct Genomic Proteomic 6: 180-185.
21. Gao P, Sultan KT, Zhang XJ, Shi SH. 2013. Lineage-dependent circuit assembly in the neocortex. Development 140: 2645-2655.
22. Gehman LT, Meera P, Stoilov P, Shiue L, O'Brien JE, Meisler MH, Ares MJr, Otis TS, Black DL. 2012. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev 26: 445-460.
23. Giraudin A, Le Bon-Jego M, Cabirol MJ, Simmers J, Morin D. 2012. Spinal and pontine relay pathways mediating respiratory rhythm entrainment by limb proprioceptive inputs in the neonatal rat. J Neurosci 32: 11841-11853.
24. HuangDW, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
25. Irimia M, Weatheritt RJ, Ellis JD, Parikshak NN, Gonatopoulos-Pournatzis T, Babor M, Quesnel-Vallieres M, Tapial J, Raj B, O'Hanlon D, et al. 2014. A highly conserved program of neuronal microexons is misregulated in autistic brains. Cell 159: 1511-1523.
26. Kwan KY, Lam MM, Krsnik Z, Kawasawa YI, Lefebvre V, Sestan N. 2008. SOX5 postmitotically regulates migration, postmigratory differentiation, and projections of subplate and deeplayer neocortical neurons. Proc Natl Acad Sci 105: 16021-16026.
27. Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ, Brown DD, Ross EJ, Voisin V, Bader GD, Blencowe BJ, et al. 2012. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30: 1734-1745.
28. Li Q, Lee JA, Black DL. 2007. Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 8: 819-831.
29. Li Q, Zheng S, Han A, Lin CH, Stoilov P, Fu XD, Black DL. 2014. The splicing regulator PTBP2 controls a programof embryonic splicing required for neuronal maturation. eLife 3: e01201.
30. Li YI, Sanchez-Pulido L, HaertyW, Ponting CP. 2015. RBFOX and PTBP1 proteins regulate the alternative splicing of micro-exons in human brain transcripts. Genome Res 25: 1-13.
31. Licatalosi DD, Yano M, Fak JJ, Mele A, Grabinski SE, Zhang C, Darnell RB. 2012. Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev 26: 1626-1642.
32. Lipscombe D. 2005. Neuronal proteins custom designed by alternative splicing. Curr Opin Neurobiol 15: 358-363.
33. Lipscombe D, Allen SE, Toro CP. 2013a. Control of neuronal voltage-gated calcium ion channels from RNA to protein. Trends Neurosci 36: 598-609.
34. Lipscombe D, Andrade A, Allen SE. 2013b. Alternative splicing: functional diversity among voltage-gated calcium channels and behavioral consequences. Biochim Biophys Acta 1828: 1522-1529.
35. Mellen NM, Thoby-Brisson M. 2012. Respiratory circuits: development, function and models. Curr Opin Neurobiol 22: 676-685.
36. Merkin J, Russell C, Chen P, Burge CB. 2012. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science 338: 1593-1599.
37. Nakano Y, Jahan I, Bonde G, Sun X, Hildebrand MS, Engelhardt JF, Smith RJ, Cornell RA, Fritzsch B, Banfi B. 2012.Amutation in the Srrm4 gene causes alternative splicing defects and deafness in the Bronx waltzer mouse. PLoS Genet 8: e1002966.
38. Norris AD, Calarco JA. 2012. Emerging roles of alternative premRNAsplicing regulation in neuronal development and function. Front Neurosci 6: 122.
39. Ohnishi T, Shirane M, Hashimoto Y, Saita S, Nakayama KI. 2014. Identification and characterization of a neuron-specific isoform of protrudin. Genes Cells 19: 97-111.
40. Ovadia G, Shifman S. 2011. The genetic variation of RELN expression in schizophrenia and bipolar disorder. PLoS One 6: e19955.
41. Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH. 2007. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8: 287-299.
42. Raj B, O'Hanlon D, Vessey JP, Pan Q, Ray D, Buckley NJ, Miller FD, Blencowe BJ. 2011. Cross-regulation between an alternative splicing activator and a transcription repressor controls neurogenesis. Mol Cell 43: 843-850.
43. Raj B, Irimia M, Braunschweig U, Sterne-Weiler T, O'Hanlon D, Lin ZY, Chen GI, Easton LE, Ule J, Gingras AC, et al. 2014. A global regulatory mechanism for activating an exon network required for neurogenesis. Mol Cell 56: 90-103.
44. Ross CA, Margolis RL, Reading SA, Pletnikov M, Coyle JT. 2006. Neurobiology of schizophrenia. Neuron 52: 139-153.
45. Ruggiu M, Herbst R, Kim N, Jevsek M, Fak JJ, Mann MA, Fischbach G, Burden SJ, Darnell RB. 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 106: 3513-3518.
46. Rusconi F, Paganini L, Braida D, Ponzoni L, Toffolo E, Maroli A, Landsberger N, Bedogni F, Turco E, Pattini L, et al. 2014. LSD1 neurospecific alternative splicing controls neuronal excitability in mouse models of epilepsy. Cereb Cortex doi: 10.1093/cercor/bhu070.
47. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Shen H, Green MR. 2004. A pathway of sequential arginine-serine-rich domain-splicing signal interactions during mammalian spliceosome assembly. Mol Cell 16: 363-373.
49. Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E. 2014. Patches of disorganization in the neocortex of children with autism. N Engl J Med 370: 1209-1219.
50. Tsyba L, Gryaznova T, Dergai O, Dergai M, Skrypkina I, Kropyvko S, Boldyryev O, Nikolaienko O, Novokhatska O, Rynditch A. 2008. Alternative splicing affecting the SH3A domain controls the binding properties of intersectin 1 in neurons. Biochem Biophys Res Commun 372: 929-934.
51. UleJ, DarnellRB.2006.RNAbindingproteinsandtheregulationof neuronalsynapticplasticity.CurrOpinNeurobiol16:102-110.
52. Unni DK, Piper M, Moldrich RX, Gobius I, Liu S, Fothergill T, Donahoo AL, Baisden JM, CooperHM, Richards LJ. 2012. Multiple Slits regulate the development of midline glial populations and the corpus callosum. Dev Biol (N Y 1985) 365: 36-49.
53. Wu JY, Maniatis T. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75: 1061-1070.
54. 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 95: 13254-13259.
55. Yano M, Hayakawa-Yano Y, Mele A, Darnell RB. 2010. Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 66: 848-858.
56. Zheng S, Black DL. 2013. Alternative pre-mRNA splicing in neurons: growing up and extending its reach. Trends Genet 29: 442-448.