A neuron-specific splicing switch mediated by an array of pre-mRNA repressor sites: Evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart

RNA

Volumn 3, Issue 9, 1997, Pages 996-1015

  Ashiya, Mona ^a   Grabowski, Paula J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Alternative splicing; HnRNP I; PTB; Splicing regulation; Splicing repression

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; MESSENGER RNA PRECURSOR; RNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN RNA BINDING; RAT; SPLICEOSOME; TISSUE SPECIFICITY; TRANSLATION REGULATION;

ALTERNATIVE SPLICING; ANIMALS; ANTIBODIES, MONOCLONAL; BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; BRAIN; CROSS REACTIONS; HELA CELLS; HUMANS; KIDNEY; MOLECULAR SEQUENCE DATA; NEURONS; POLYPYRIMIDINE TRACT-BINDING PROTEIN; RATS; RATS, SPRAGUE-DAWLEY; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SPLICEOSOMES; SUBSTRATE SPECIFICITY;

ANIMALIA; MAMMALIA;

EID: 0030777180     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Amendt BA, Hesslein D, Chang LJ, Stoltzfus CM. 1994. Presence of negative and positive cis-acting RNA splicing elements within and flanking the first tat coding exon of human immunodeficiency virus type 1. Mol Cell Biol 14:3960-3970.
2. Belsham GJ, Sonenberg N. 1996. RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol Rev 60:499-511.
3. Bovolin P, Santi MR, Puia G, Costa E, Grayson D. 1992. Expression patterns of y-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc Natl Acad Sci USA 89:9344-9348.
4. Brunei F, Alzari PM, Ferrara P, Zakin MM. 1991. Cloning and sequencing of PYBP, a pyrimidine-rich specific single strand DNA-binding protein. Nucleic Acids Res 79:5237-5245.
5. Caceres JF, Stamm S, Helfman DM, Krainer AR. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706-1709.
6. Chan RC, Black DL. 1995. Conserved intron elements repress splicing of a neuron-specific c-src exon in vitro. Mol Cell Biol 35:6377-6385.
7. Chebli K, Gattoni R, Schmitt P, Hildwein G, Stevenin J. 1989. The 216-nucleotide intron of the E1A pre-mRNA contains a hairpin structure that permits utilization of unusually distant branch acceptors. Mol Cell Biol 9:4852-4861.
8. Del Gatto F, Breathnach R. 1995. Exon and intron sequences, respectively, repress and activate splicing of a fibroblast growth factor receptor 2 alternative exon. Mol Cell Biol 35:4825-4834.
9. Del Gatto F, Gesnel MC, Breathnach R. 1996. The exon sequence TAGG can inhibit splicing. Nucleic Acids Res 24:2017-2021.
10. Dignam JD, Lebovitz RM, Roeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 33:1475-1489.
11. Domenjoud L, Gallinaro H, Kister L, Meyer S, Jacob M. 1991. Identification of a specific exon sequence that is a major determinant in the selection between a natural and a cryptic 5′ splice site. Mol Cell Biol 73:4581-4590.
12. D'Orval BC, Carafa YD, Sirand-Pugnet P, Gallego M, Brody E, Marie J. 1991. RNA secondary structure repression of a muscle-specific exon in HeLa cell nuclear extracts. Science 252:1823-1828.
13. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. 1993. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62:289-321.
14. Estes PA, Cooke NE, Liebhaber SA. 1992. A native RNA secondary structure controls alternative splice-site selection and generates two human growth hormone isoforms. J. Biol Chem 267:14902-14908.
15. Fu XD. 1993. Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature 365:82-85.
16. Fu XD. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 3:663-680.
17. Fu XD, Mayeda A, Maniatis T, Krainer AR. 1992. General splicing factors SF2 and SC35 have equivalent activities in vitro, and both affect alternative 5′ and 3′ splice site selection. Proc Natl Acad Sci USA 89:11224-11228.
18. Garcia-Blanco MA, Jamison SF, Sharp PA. 1989. Identification and purification of a 62,000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes & Dev 3:1874-1886.
19. 65 and a novel spliceosome-associated 28-kDa protein. RNA 3:407-417.
20. Ghetti A, Pinol-Roma S, Michael WM, Morandi C, Dreyfuss G. 1992. hnRNP I, the polypyrimidine tract-binding protein: Distinct nuclear localization and association with hnRNAs. Nucleic Acids Res 20:3671-3678.
21. Gil A, Sharp PA, Jamison SF, Garcia-Blanco MA. 1991. Characterization of cDNAs encoding the polypyrimidine tract-binding protein. Genes & Dev 5:1224-1236.
22. Gooding C, Roberts GC, Moreau G, Nadal-Ginard B, Smith CWJ. 1994. Smooth muscle-specific switching of α-tropomyosin mutually exclusive exon selection by specific inhibition of the strong default exon. EMBO J. 23:3861-3872.
23. Gozani O, Feld R, Reed R. 1996. Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes & Dev 30:233-243.
24. Graham IR, Hamshere M, Eperon IC. 1992. Alternative splicing of a human α-tropomyosin muscle-specific exon: Identification of determining sequences. Mol Cell Biol 22:3872-3882.
25. Guo W, Mulligan GJ, Wormsley S, Helfman DM. 1991. Alternative splicing of β-tropomyosin pre-mRNA: Cis-acting elements and cellular factors that block the use of a skeletal muscle exon in nonmuscle cells. Genes & Dev 5:2096-2107.
26. Harris RA, McQuilkin SJ, Paylor R, Abeliovich A, Tonegawa S, Wehner JM. 1995. Mutant mice lacking the γ isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of γ-aminobutyrate type A receptors. Proc Natl Acad Sci USA 92:3658-3662.
27. Horabin JI, Schedl P. 1993. Sex-lethal autoregulation requires multiple cis-acting elements upstream and downstream of the male exon and appears to depend largely on controlling the use of the male exon 5′ splice site. Mol Cell Biol 23:7734-7746.
28. Kaminski A, Hunt SL, Patton JG, Jackson RJ. 1995. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA 2:924-938.
29. Kamma H, Portman DS, Dreyfus G. 1995. Cell type-specific expression of hnRNP proteins. Exp Cell Res 222:187-196.
30. Kanopka A, Muhlemann O, Akusjarvi G. 1996. Inhibition by SR proteins of splicing of a regulated adenovirus pre-mRNA. Nature 382:535-538.
31. King PH, Levine TD, Fremeau RT Jr, Keene JD. 1994. Mammalian homologs of Drosophila ELAV localized to a neuronal subset can bind in vitro to the 3′ UTR of mRNA encoding the Id transcriptional repressor. J. Neurosci 24:1943-1952.
32. Koushika SP, Lisbin MJ, White K. 1996. ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr Biol 6:1634-1641.
33. 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 mRNAs. Mol. Cell Biol 23:3494-3504.
34. Libri D, Piseri A, Fiszman MY. 1991. Tissue-specific splicing in vivo of the β-tropomyosin gene: Dependence on an RNA secondary structure. Science 252:1842-1845.
35. Lin CH, Patton JG. 1995. Regulation of alternative 3′ splice site selection by constitutive splicing factors. RNA 2:234-245.
36. Lin YS, Green MR. 1991. Mechanism of action of an acidic transcriptional activator in vitro. Cell 64:971-981.
37. Lou H, Gagel RF, Berget SM. 1996. An intron enhancer recognized by splicing factors activates polyadenylation. Genes & Dev 20:208-219.
38. MacMillan AM, Query CC, Allerson CR, Chen S, Verdine GL, Sharp PA. 1994. Dynamic association of proteins with the pre-mRNA branch region. Genes & Dev 8:3008-3020.
39. Manley JL, Tacke R. 1996. SR proteins and splicing control. Genes & Dev 20:1569-1579.
40. Mayeda A, Krainer AR. 1992. Regulation of alternative pre-mRNA splicing by hnRNP Al and splicing factor SF2. Cell 68:365-375.
41. Milligan JF, Uhlenbeck OC. 1989. Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol 280:51-62.
42. Min H, Chan RC, Black DL. 1995. The generally expressed hnRNP F is involved in a neural-specific pre-mRNA splicing event. Genes & Dev 9:2659-2671.
43. Min H, Turck CW, Nikolic JM, Black DL. 1997. A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer. Genes & Dev 22:1023-1036.
44. Mullen MP, Smith CWJ, Patton JG, Nadal-Ginard B. 1991. α-Tropo-myosin mutually exclusive exon selection: Competition between branchpoint/polypyrimidine tracts determines default exon choice. Genes & Dev 5:642-655.
45. Mulligan GJ, Guo W, Wormsley S, Helfman DM. 1992. Polypyrimidine tract binding protein interacts with sequences involved in alternative splicing of β-tropomyosin pre-mRNA. J. Biol Chem 267:25480-25487.
46. Nandabalan K, Roeder GS. 1995. Binding of a cell-type-specific RNA splicing factor to its target regulatory sequence. Mol Cell Biol 25:1953-1960.
47. Nemeroff ME, Utans U, Kramer A, Krug RM. 1992. Identification of cis-acting intron and exon regions in influenza virus NS1 mRNA that inhibit splicing and cause the formation of aberrantly sedimenting presplicing complexes. Mol Cell Biol 32:962-970.
48. Norton PA. 1994. Polypyrimidine tract sequences direct selection of alternative branch sites and influence protein binding. Nucleic Acids Res 22:3854-3860.
49. Parker R, Siliciano PG, Guthrie C. 1987. Recognition of the TACT AAC box during mRNA splicing in yeast involves base pairing to the U2-like snRNA. Cell 49:229-239.
50. Patton JG, Mayer SA, Tempst P, Nadal-Ginard B. 1991. Characterization and molecular cloning of polypyrimidine tract-binding protein: A component of a complex necessary for pre-mRNA splicing. Genes & Dev 5:1237-1251.
51. - currents in Purkinje versus Granule neurons in rat cerebellar slices. Neuron 32:117-126.
52. Qiu Y, Nemeroff M, Krug RM. 1995. The influenza virus NS1 protein binds to a specific region in human U6 snRNA and inhibits U6-U2 and U6-U4 snRNA interactions during splicing. RNA 2:304-316.
53. Ramchatesingh J, Zahler AM, Neugebauer KM, Roth MB, Cooper TA. 1995. A subset of SR proteins activates splicing of the cardiac troponin T alternative exon by direct interactions with an exonic enhancer. Mol Cell Biol 35:4898-4907.
54. Ruskin B, Zamore PD, Green MR. 1988. A factor, U2AF, is required for U2 snRNP binding and splicing complex assembly. Cell 52:207-219.
55. Screaton GR, Caceres JF, Mayeda A, Bell MV, Plebanski M, Jackson DG, Bell JI, Krainer AR. 1995. Identification and characterization of three members of the human SR family of pre-mRNA splicing factors. EMBO J 14:4336-4349.
56. Si Zh, Amendt BA, Stoltzfus CM. 1997. Splicing efficiency of human immunodeficiency virus type 1 tat RNA is determined by both a suboptimal 3' splice site and a 10 nucleotide exon splicing silencer element located within tat exon 2. Nucleic Acids Res 25:861-867.
57. Siebel CW, Admon A, Rio DC. 1995. Soma-specific expression and cloning of PSI, a negative regulator of P element pre-mRNA splicing. Genes & Dev 9:269-283.
58. Siebel CW, Fresco LD, Rio DC. 1992. The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: Multiprotein complexes at an exon pseudo-5′ splice site control U1 snRNP binding. Genes & Dev 6:1386-1401.
59. Sierra F, Tian JM, Schibler U. 1993. In vitro transcription with nuclear extracts from differentiated tissues. In: Hames BD, Higgins SJ, eds. Gene transcription - A practical approach. New York: Oxford University Press, pp 125-152.
60. Singh R, Valcarcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 265:1173-1176.
61. Staknis D, Reed R. 1994. Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol Cell Biol 14:2994-3005.
62. Tian M, Maniatis T. 1992. Positive control of pre-mRNA splicing in vitro. Science 256:237-240.
63. Tian M, Maniatis T. 1993. A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 74:105-114.
64. Valcarcel J, Singh R, Zamore PD, Green MR. 1993. The protein sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 362:171-175.
65. Wang J, Manley JL. 1995. Overexpression of the SR proteins ASF/ SF2 and SC35 influences alternative splicing in vivo in diverse ways. RNA 3:335-346.
66. Wang Z, Grabowski PJ. 1996. Cell- and stage-specific splicing events resolved in specialized neurons of the rat cerebellum. RNA 2:1241-1253.
67. Wane Z, Hoffmann HM, Grabowski PJ. 1995. Intrinsic U2AF binding is modulated by exon enhancer signals in parallel with changes in splicing activity. RNA 7:21-35.
68. Watakabe A, Inoue K, Sakamoto H, Shimura Y. 1989. A secondary structure at the 3′ splice site affects the in vitro splicing reaction of mouse immunoglobulin μ chain pre-mRNAs. Nucleic Acids Res 17:8159-8169.
69. Wu J, Manley JL. 1989. Mammalian pre-mRNA branch site selection by U2 snRNP involves base pairing. Genes & Dev 3:1553-1561.
70. Zahler AM, Neugebauer KM, Lane WS, Roth MB. 1993. Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260:219-222.
71. Zhang L, Ashiya M, Sherman TG, Grabowski PJ. 1996. Essential nucleotides direct neuron-specific splicing of γ2 pre-mRNA. RNA 2:682-698.
72. Zhuang Y, Weiner AM. 1989. A compensatory base change in human U2 snRNA can suppress a branch site mutation. Genes & Dev 3:1545-1552.