Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain

Genes and Development

Volumn 26, Issue 14, 2012, Pages 1626-1642

  Licatalosi, Donny D ^a,b   Yano, Masato ^a,c   Fak, John J ^a   Mele, Aldo ^a   Grabinski, Sarah E ^b   Zhang, Chaolin ^a   Darnell, Robert B ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Alternative splicing; Brain development; HITS CLIP; Neuronal progenitor; Polypyrimidine tract binding protein; RNA binding map

Indexed keywords

MESSENGER RNA; POLYPYRIMIDINE TRACT RNA BINDING PROTEIN 1; POLYPYRIMIDINE TRACT RNA BINDING PROTEIN 2; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BRAIN; BRAIN DEVELOPMENT; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EXON; IMMUNOPRECIPITATION; MOUSE; NEOCORTEX; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING;

ALTERNATIVE SPLICING; ANIMALS; BRAIN; CELL DIFFERENTIATION; EXONS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; MICE; MICE, MUTANT STRAINS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; POLYPYRIMIDINE TRACT-BINDING PROTEIN; RNA, MESSENGER;

EID: 84864020005     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.191338.112     Document Type: Article

References (68)

1. Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ. 2010. Deciphering the splicing code. Nature 465: 53-59.
2. Bark C, Bellinger FP, Kaushal A, Mathews JR, Partridge LD, Wilson MC. 2004. Developmentally regulated switch in alternatively spliced SNAP-25 isoforms alters facilitation of synaptic transmission. J Neurosci 24: 8796-8805.
3. Baye LM, Link BA. 2008. Nuclear migration during retinal development. Brain Res 1192: 29-36.
4. Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares MJ, Black DL. 2007. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21: 1636-1652.
5. 2+/calmodulindependent protein kinase isoforms in rat brain. J Neurosci 15: 6797-6808.
6. Bunting M, Bernstein KE, Greer JM, Capecchi MR, Thomas KR. 1999. Targeting genes for self-excision in the germ line. Genes Dev 13: 1524-1528.
7. Castle JC, Zhang C, Shah JK, Kulkarni AV, Kalsotra A, Cooper TA, Johnson JM. 2008. Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat Genet 40: 1416-1425.
8. Chan RC, Black DL. 1997. The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream. Mol Cell Biol 17: 4667-4676.
9. Chen M, Manley JL. 2009. Mechanisms of alternative splicing regulation: Insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10: 741-754.
10. Clark TA, Schweitzer AC, Chen TX, Staples MK, Lu G, Wang H, Williams A, Blume JE. 2007. Discovery of tissue-specific exons using comprehensive human exon microarrays. Genome Biol 8: R64. doi: 10.1186/gb-2007-8-4-r64.
11. Cooper TA, Wan L, Dreyfuss G. 2009. RNA and disease. Cell 136: 777-793.
12. Corrionero A, Valcarcel J. 2009. RNA processing: Redrawing the map of charted territory. Mol Cell 36: 918-919.
13. Curlin M, Lucic V, Gajovic S. 2006. Splice variant of mouse Stam2 mRNA in nervous and muscle tissue contains additional exon with stop codon within region coding for VHS domain. Croat Med J 47: 16-24.
14. Darnell RB. 2010. HITS-CLIP: Panoramic views of protein-RNA regulation in living cells. Wiley Interdiscip Rev RNA 1: 266-286.
15. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, et al. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146: 247-261.
16. Del Bene F, Wehman AM, Link BA, Baier H. 2008. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134: 1055-1065.
17. Dho SE, French MB, Woods SA, McGlade CJ. 1999. Characterization of four mammalian numb protein isoforms. Identification of cytoplasmic and membrane-associated variants of the phosphotyrosine binding domain. J Biol Chem 274: 33097-33104.
18. Dredge BK, Stefani G, Engelhard CC, Darnell RB. 2005. Nova autoregulation reveals dual functions in neuronal splicing. EMBO J 24: 1608-1620.
19. Du H, Cline MS, Osborne RJ, Tuttle DL, Clark TA, Donohue JP, Hall MP, Shiue L, Swanson MS, Thornton CA, et al. 2010. Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol 17: 187-193.
20. Kalsotra A, Cooper TA. 2011. Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12: 715-729.
21. Knoblich JA. 2010. Asymmetric cell division: Recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11: 849-860.
22. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J. 2010. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17: 909-915.
23. Kremerskothen J, Teber I, Wendholt D, Liedtke T, Bockers TM, Barnekow A. 2002. Brain-specific splicing of a-actinin 1 (ACTN1) mRNA. Biochem Biophys Res Commun 295: 678-681.
24. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M. 2001. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410: 174-179.
25. Licatalosi DD, Darnell RB. 2006. Splicing regulation in neurologic disease. Neuron 52: 93-101.
26. Licatalosi DD, Darnell RB. 2010. RNA processing and its regulation: Global insights into biological networks. Nat Rev Genet 11: 75-87.
27. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, et al. 2008. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464-469.
28. Lin CH, Patton JG. 1995. Regulation of alternative 39 splice site selection by constitutive splicing factors. RNA 1: 234-245.
29. Llorian M, Schwartz S, Clark TA, Hollander D, Tan LY, Spellman R, Gordon A, Schweitzer AC, de la Grange P, Ast G, et al. 2010. Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat Struct Mol Biol 17: 1114-1123.
30. 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: 435-448.
31. 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: 7463-7479.
32. Matlin AJ, Southby J, Gooding C, Smith CW. 2007. Repression of a-actinin SM exon splicing by assisted binding of PTB to the polypyrimidine tract. RNA 13: 1214-1223.
33. Meisenheimer KM, Meisenheimer PL, Koch TH. 2000. Nucleoprotein photo-cross-linking using halopyrimidine-substituted RNAs. Methods Enzymol 318: 88-104.
34. Murciano A, Zamora J, Lopez-Sanchez J, Frade JM. 2002. Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol Cell Neurosci 21: 285-300.
35. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
36. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wenter P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, et al. 2005. Structure of PTB bound to RNA: Specific binding and implications for splicing regulation. Science 309: 2054-2057.
37. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
38. Perez I, McAfee JG, Patton JG. 1997a. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein. Biochemistry 36: 11881-11890.
39. Perez I, Lin CH, McAfee JG, Patton JG. 1997b. Mutation of PTB binding sites causes misregulation of alternative 39 splice site selection in vivo. RNA 3: 764-778.
40. 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 97: 6350-6355.
41. Pyper JM, Bolen JB. 1990. Identification of a novel neuronal C-SRC exon expressed in human brain. Mol Cell Biol 10: 2035-2040.
42. Reid DC, Chang BL, Gunderson SI, Alpert L, Thompson WA, Fairbrother WG. 2009. Next-generation SELEX identifies sequence and structural determinants of splicing factor binding in human pre-mRNA sequence. RNA 15: 2385-2397.
43. Sawicka K, Bushell M, Spriggs KA, Willis AE. 2008. Polypyrimidinetract-binding protein: A multifunctional RNA-binding protein. Biochem Soc Trans 36: 641-647.
44. Sharma S, Maris C, Allain FH, Black DL. 2011. U1 snRNA directly interacts with polypyrimidine tract-binding protein during splicing repression. Mol Cell 41: 579-588.
45. Shirao T, Kojima N, Terada S, Obata K. 1990. Expression of three drebrin isoforms in the developing nervous system. Neurosci Res Suppl 13: S106-S111. doi: 10.1016/0921-8696(90)90039-6.
46. Singh R, Valcarcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268: 1173-1176.
47. Spellman R, Smith CW. 2006. Novel modes of splicing repression by PTB. Trends Biochem Sci 31: 73-76.
48. Spellman R, Rideau A, Matlin A, Gooding C, Robinson F, McGlincy N, Grellscheid SN, Southby J, Wollerton M, Smith CW. 2005. Regulation of alternative splicing by PTB and associated factors. Biochem Soc Trans 33: 457-460.
49. Spellman R, Llorian M, Smith CW. 2007. Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol Cell 27: 420-434.
50. Sugnet CW, Srinivasan K, Clark TA, O'Brien G, Cline MS, Wang H, Williams A, Kulp D, Blume JE, Haussler D, et al. 2006. Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput Biol 2: e4. doi: 10.1371/journal.pcbi.0020004.
51. Taverna E, Huttner WB. 2010. Neural progenitor nuclei IN motion. Neuron 67: 906-914.
52. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, Kayikci M, Konig J, Hortobagyi T, Nishimura AL, Zupunski V, et al. 2011. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14: 452-458.
53. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB. 2003. CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212-1215.
54. Ule J, Jensen K, Mele A, Darnell RB. 2005a. CLIP: A method for identifying protein-RNA interaction sites in living cells. Methods 37: 376-386.
55. Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, Wang H, Clark T, Fraser C, Ruggiu M, et al. 2005b. Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37: 844-852.
56. Ule J, Stefani G, Mele A, Ruggiu M, Wang X, Taneri B, Gaasterland T, Blencowe BJ, Darnell RB. 2006. An RNA map predicting Nova-dependent splicing regulation. Nature 444: 580-586.
57. Urlaub H, Hartmuth K, Luhrmann R. 2002. A two-tracked approach to analyze RNA-protein crosslinking sites in native, nonlabeled small nuclear ribonucleoprotein particles. Methods 26: 170-181.
58. Wagner EJ, Garcia-Blanco MA. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol Cell Biol 21: 3281-3288.
59. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
60. Wang Z, Kayikci M, Briese M, Zarnack K, Luscombe NM, Rot G, Zupan B, Curk T, Ule J. 2010. iCLIP predicts the dual splicing effects of TIA-RNA interactions. PLoS Biol 8: 1-16.
61. Witten JT, Ule J. 2011. Understanding splicing regulation through RNA splicing maps. Trends Genet 27: 89-97.
62. Xu M, Hecht NB. 2007. Polypyrimidine tract binding protein 2 stabilizes phosphoglycerate kinase 2 mRNA in murine male germcells by binding to its 39UTR. Biol Reprod 76: 1025-1033.
63. Xue Y, Zhou Y, Wu T, Zhu T, Ji X, Kwon YS, Zhang C, Yeo G, Black DL, Sun H, et al. 2009. Genome-wide analysis of PTBRNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol Cell 36: 996-1006.
64. 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.
65. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, Gage FH. 2009. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16: 130-137.
66. Zhang C, Darnell RB. 2011. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 29: 607-614.
67. Zhang C, Zhang Z, Castle J, Sun S, Johnson J, Krainer AR, Zhang MQ. 2008. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev 22: 2550-2563.
68. Zhang C, FriasMA, Mele A, RuggiuM, Eom T, Marney CB, Wang H, Licatalosi DD, Fak JJ, Darnell RB. 2010. Integrative modeling defines the nova splicing-regulatory network and its combinatorial controls. Science 329: 439-443.