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. 1995 Nov;15(11):6273–6282. doi: 10.1128/mcb.15.11.6273

Genetic enhancement of RNA-processing defects by a dominant mutation in B52, the Drosophila gene for an SR protein splicing factor.

X Peng 1, S M Mount 1
PMCID: PMC230879  PMID: 7565780

Abstract

SR proteins are essential for pre-mRNA splicing in vitro, act early in the splicing pathway, and can influence alternative splice site choice. Here we describe the isolation of both dominant and loss-of-function alleles of B52, the gene for a Drosophila SR protein. The allele B52ED was identified as a dominant second-site enhancer of white-apricot (wa), a retrotransposon insertion in the second intron of the eye pigmentation gene white with a complex RNA-processing defect. B52ED also exaggerates the mutant phenotype of a distinct white allele carrying a 5' splice site mutation (wDR18), and alters the pattern of sex-specific splicing at doublesex under sensitized conditions, so that the male-specific splice is favored. In addition to being a dominant enhancer of these RNA-processing defects, B52ED is a recessive lethal allele that fails to complement other lethal alleles of B52. Comparison of B52ED with the B52+ allele from which it was derived revealed a single change in a conserved amino acid in the beta 4 strand of the first RNA-binding domain of B52, which suggests that altered RNA binding is responsible for the dominant phenotype. Reversion of the B52ED dominant allele with X rays led to the isolation of a B52 null allele. Together, these results indicate a critical role for the SR protein B52 in pre-mRNA splicing in vivo.

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Selected References

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  1. Abovich N., Liao X. C., Rosbash M. The yeast MUD2 protein: an interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition. Genes Dev. 1994 Apr 1;8(7):843–854. doi: 10.1101/gad.8.7.843. [DOI] [PubMed] [Google Scholar]
  2. Amrein H., Hedley M. L., Maniatis T. The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by Transformer 2. Cell. 1994 Feb 25;76(4):735–746. doi: 10.1016/0092-8674(94)90512-6. [DOI] [PubMed] [Google Scholar]
  3. Baker B. S. Sex in flies: the splice of life. Nature. 1989 Aug 17;340(6234):521–524. doi: 10.1038/340521a0. [DOI] [PubMed] [Google Scholar]
  4. Ballinger D. G., Benzer S. Targeted gene mutations in Drosophila. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9402–9406. doi: 10.1073/pnas.86.23.9402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belote J. M., McKeown M. B., Andrew D. J., Scott T. N., Wolfner M. F., Baker B. S. Control of sexual differentiation in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1985;50:605–614. doi: 10.1101/sqb.1985.050.01.073. [DOI] [PubMed] [Google Scholar]
  6. Bingham P. M., Chapman C. H. Evidence that white-blood is a novel type of temperature-sensitive mutation resulting from temperature-dependent effects of a transposon insertion on formation of white transcripts. EMBO J. 1986 Dec 1;5(12):3343–3351. doi: 10.1002/j.1460-2075.1986.tb04649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bingham P. M., Chou T. B., Mims I., Zachar Z. On/off regulation of gene expression at the level of splicing. Trends Genet. 1988 May;4(5):134–138. doi: 10.1016/0168-9525(88)90136-9. [DOI] [PubMed] [Google Scholar]
  8. Birchler J. A., Hiebert J. C., Rabinow L. Interaction of the mottler of white with transposable element alleles at the white locus in Drosophila melanogaster. Genes Dev. 1989 Jan;3(1):73–84. doi: 10.1101/gad.3.1.73. [DOI] [PubMed] [Google Scholar]
  9. Birney E., Kumar S., Krainer A. R. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 1993 Dec 25;21(25):5803–5816. doi: 10.1093/nar/21.25.5803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burtis K. C., Baker B. S. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989 Mar 24;56(6):997–1010. doi: 10.1016/0092-8674(89)90633-8. [DOI] [PubMed] [Google Scholar]
  11. Chabot B., Frappier D., La Branche H. Differential ASF/SF2 activity in extracts from normal WI38 and transformed WI38VA13 cells. Nucleic Acids Res. 1992 Oct 11;20(19):5197–5204. doi: 10.1093/nar/20.19.5197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chadwick R., Jones B., Jack T., McGinnis W. Ectopic expression from the Deformed gene triggers a dominant defect in Drosophila adult head development. Dev Biol. 1990 Sep;141(1):130–140. doi: 10.1016/0012-1606(90)90108-u. [DOI] [PubMed] [Google Scholar]
  13. Champlin D. T., Frasch M., Saumweber H., Lis J. T. Characterization of a Drosophila protein associated with boundaries of transcriptionally active chromatin. Genes Dev. 1991 Sep;5(9):1611–1621. doi: 10.1101/gad.5.9.1611. [DOI] [PubMed] [Google Scholar]
  14. Crispino J. D., Blencowe B. J., Sharp P. A. Complementation by SR proteins of pre-mRNA splicing reactions depleted of U1 snRNP. Science. 1994 Sep 23;265(5180):1866–1869. doi: 10.1126/science.8091213. [DOI] [PubMed] [Google Scholar]
  15. Cáceres J. F., Krainer A. R. Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J. 1993 Dec;12(12):4715–4726. doi: 10.1002/j.1460-2075.1993.tb06160.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Diamond R. H., Du K., Lee V. M., Mohn K. L., Haber B. A., Tewari D. S., Taub R. Novel delayed-early and highly insulin-induced growth response genes. Identification of HRS, a potential regulator of alternative pre-mRNA splicing. J Biol Chem. 1993 Jul 15;268(20):15185–15192. [PubMed] [Google Scholar]
  17. Dreyfuss G., Matunis M. J., Piñol-Roma S., Burd C. G. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993;62:289–321. doi: 10.1146/annurev.bi.62.070193.001445. [DOI] [PubMed] [Google Scholar]
  18. Eperon I. C., Ireland D. C., Smith R. A., Mayeda A., Krainer A. R. Pathways for selection of 5' splice sites by U1 snRNPs and SF2/ASF. EMBO J. 1993 Sep;12(9):3607–3617. doi: 10.1002/j.1460-2075.1993.tb06034.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Erdman S. E., Burtis K. C. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J. 1993 Feb;12(2):527–535. doi: 10.1002/j.1460-2075.1993.tb05684.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fu X. D., Mayeda A., Maniatis T., Krainer A. R. 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 U S A. 1992 Dec 1;89(23):11224–11228. doi: 10.1073/pnas.89.23.11224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fu X. D. Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature. 1993 Sep 2;365(6441):82–85. doi: 10.1038/365082a0. [DOI] [PubMed] [Google Scholar]
  22. Ge H., Zuo P., Manley J. L. Primary structure of the human splicing factor ASF reveals similarities with Drosophila regulators. Cell. 1991 Jul 26;66(2):373–382. doi: 10.1016/0092-8674(91)90626-a. [DOI] [PubMed] [Google Scholar]
  23. Görlach M., Wittekind M., Beckman R. A., Mueller L., Dreyfuss G. Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 1992 Sep;11(9):3289–3295. doi: 10.1002/j.1460-2075.1992.tb05407.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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. 1991 May 17;65(4):579–586. doi: 10.1016/0092-8674(91)90090-l. [DOI] [PubMed] [Google Scholar]
  25. Hoffman D. W., Query C. C., Golden B. L., White S. W., Keene J. D. RNA-binding domain of the A protein component of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2495–2499. doi: 10.1073/pnas.88.6.2495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kao H. Y., Siliciano P. G. The yeast homolog of the U1 snRNP protein 70K is encoded by the SNP1 gene. Nucleic Acids Res. 1992 Aug 11;20(15):4009–4013. doi: 10.1093/nar/20.15.4009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kelley R. L. Initial organization of the Drosophila dorsoventral axis depends on an RNA-binding protein encoded by the squid gene. Genes Dev. 1993 Jun;7(6):948–960. doi: 10.1101/gad.7.6.948. [DOI] [PubMed] [Google Scholar]
  28. Kenan D. J., Query C. C., Keene J. D. RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci. 1991 Jun;16(6):214–220. doi: 10.1016/0968-0004(91)90088-d. [DOI] [PubMed] [Google Scholar]
  29. Kim Y. J., Zuo P., Manley J. L., Baker B. S. The Drosophila RNA-binding protein RBP1 is localized to transcriptionally active sites of chromosomes and shows a functional similarity to human splicing factor ASF/SF2. Genes Dev. 1992 Dec;6(12B):2569–2579. doi: 10.1101/gad.6.12b.2569. [DOI] [PubMed] [Google Scholar]
  30. Kohtz J. D., Jamison S. F., Will C. L., Zuo P., Lührmann R., Garcia-Blanco M. A., Manley J. L. Protein-protein interactions and 5'-splice-site recognition in mammalian mRNA precursors. Nature. 1994 Mar 10;368(6467):119–124. doi: 10.1038/368119a0. [DOI] [PubMed] [Google Scholar]
  31. Krainer A. R., Conway G. C., Kozak D. Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev. 1990 Jul;4(7):1158–1171. doi: 10.1101/gad.4.7.1158. [DOI] [PubMed] [Google Scholar]
  32. Krainer A. R., Mayeda A., Kozak D., Binns G. Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell. 1991 Jul 26;66(2):383–394. doi: 10.1016/0092-8674(91)90627-b. [DOI] [PubMed] [Google Scholar]
  33. Kraus M. E., Lis J. T. The concentration of B52, an essential splicing factor and regulator of splice site choice in vitro, is critical for Drosophila development. Mol Cell Biol. 1994 Aug;14(8):5360–5370. doi: 10.1128/mcb.14.8.5360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kurkulos M., Weinberg J. M., Pepling M. E., Mount S. M. Polyadenylylation in copia requires unusually distant upstream sequences. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3038–3042. doi: 10.1073/pnas.88.8.3038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lavigueur A., La Branche H., Kornblihtt A. R., Chabot B. A splicing enhancer in the human fibronectin alternate ED1 exon interacts with SR proteins and stimulates U2 snRNP binding. Genes Dev. 1993 Dec;7(12A):2405–2417. doi: 10.1101/gad.7.12a.2405. [DOI] [PubMed] [Google Scholar]
  36. Lee A. L., Kanaar R., Rio D. C., Wemmer D. E. Resonance assignments and solution structure of the second RNA-binding domain of sex-lethal determined by multidimensional heteronuclear magnetic resonance. Biochemistry. 1994 Nov 22;33(46):13775–13786. doi: 10.1021/bi00250a031. [DOI] [PubMed] [Google Scholar]
  37. Levis R., O'Hare K., Rubin G. M. Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell. 1984 Sep;38(2):471–481. doi: 10.1016/0092-8674(84)90502-6. [DOI] [PubMed] [Google Scholar]
  38. Lo P. C., Roy D., Mount S. M. Suppressor U1 snRNAs in Drosophila. Genetics. 1994 Oct;138(2):365–378. doi: 10.1093/genetics/138.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lynch K. W., Maniatis T. Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev. 1995 Feb 1;9(3):284–293. doi: 10.1101/gad.9.3.284. [DOI] [PubMed] [Google Scholar]
  40. Mancebo R., Lo P. C., Mount S. M. Structure and expression of the Drosophila melanogaster gene for the U1 small nuclear ribonucleoprotein particle 70K protein. Mol Cell Biol. 1990 Jun;10(6):2492–2502. doi: 10.1128/mcb.10.6.2492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Maniatis T. Mechanisms of alternative pre-mRNA splicing. Science. 1991 Jan 4;251(4989):33–34. doi: 10.1126/science.1824726. [DOI] [PubMed] [Google Scholar]
  42. Manley J. RNA splicing. Question of commitment. Nature. 1993 Sep 2;365(6441):14–14. doi: 10.1038/365014a0. [DOI] [PubMed] [Google Scholar]
  43. Mayeda A., Zahler A. M., Krainer A. R., Roth M. B. Two members of a conserved family of nuclear phosphoproteins are involved in pre-mRNA splicing. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1301–1304. doi: 10.1073/pnas.89.4.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Minvielle-Sebastia L., Preker P. J., Keller W. RNA14 and RNA15 proteins as components of a yeast pre-mRNA 3'-end processing factor. Science. 1994 Dec 9;266(5191):1702–1705. doi: 10.1126/science.7992054. [DOI] [PubMed] [Google Scholar]
  45. Mitchelson A., Simonelig M., Williams C., O'Hare K. Homology with Saccharomyces cerevisiae RNA14 suggests that phenotypic suppression in Drosophila melanogaster by suppressor of forked occurs at the level of RNA stability. Genes Dev. 1993 Feb;7(2):241–249. doi: 10.1101/gad.7.2.241. [DOI] [PubMed] [Google Scholar]
  46. Mohler J., Vani K. Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development. 1992 Aug;115(4):957–971. doi: 10.1242/dev.115.4.957. [DOI] [PubMed] [Google Scholar]
  47. Nagai K., Oubridge C., Jessen T. H., Li J., Evans P. R. Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature. 1990 Dec 6;348(6301):515–520. doi: 10.1038/348515a0. [DOI] [PubMed] [Google Scholar]
  48. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Oubridge C., Ito N., Evans P. R., Teo C. H., Nagai K. Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature. 1994 Dec 1;372(6505):432–438. doi: 10.1038/372432a0. [DOI] [PubMed] [Google Scholar]
  50. Peng X. B., Mount S. M. Characterization of enhancer-of-white-apricot in Drosophila melanogaster. Genetics. 1990 Dec;126(4):1061–1069. doi: 10.1093/genetics/126.4.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Potashkin J., Naik K., Wentz-Hunter K. U2AF homolog required for splicing in vivo. Science. 1993 Oct 22;262(5133):573–575. doi: 10.1126/science.8211184. [DOI] [PubMed] [Google Scholar]
  52. Query C. C., Bentley R. C., Keene J. D. A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell. 1989 Apr 7;57(1):89–101. doi: 10.1016/0092-8674(89)90175-x. [DOI] [PubMed] [Google Scholar]
  53. Rabinow L., Birchler J. A. A dosage-sensitive modifier of retrotransposon-induced alleles of the Drosophila white locus. EMBO J. 1989 Mar;8(3):879–889. doi: 10.1002/j.1460-2075.1989.tb03449.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Ring H. Z., Lis J. T. The SR protein B52/SRp55 is essential for Drosophila development. Mol Cell Biol. 1994 Nov;14(11):7499–7506. doi: 10.1128/mcb.14.11.7499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Roth M. B., Zahler A. M., Stolk J. A. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J Cell Biol. 1991 Nov;115(3):587–596. doi: 10.1083/jcb.115.3.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Ryner L. C., Baker B. S. Regulation of doublesex pre-mRNA processing occurs by 3'-splice site activation. Genes Dev. 1991 Nov;5(11):2071–2085. doi: 10.1101/gad.5.11.2071. [DOI] [PubMed] [Google Scholar]
  57. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  58. Smith V., Barrell B. G. Cloning of a yeast U1 snRNP 70K protein homologue: functional conservation of an RNA-binding domain between humans and yeast. EMBO J. 1991 Sep;10(9):2627–2634. doi: 10.1002/j.1460-2075.1991.tb07805.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Spikes D. A., Kramer J., Bingham P. M., Van Doren K. SWAP pre-mRNA splicing regulators are a novel, ancient protein family sharing a highly conserved sequence motif with the prp21 family of constitutive splicing proteins. Nucleic Acids Res. 1994 Oct 25;22(21):4510–4519. doi: 10.1093/nar/22.21.4510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Staknis D., Reed R. SR proteins promote the first specific recognition of Pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex. Mol Cell Biol. 1994 Nov;14(11):7670–7682. doi: 10.1128/mcb.14.11.7670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sun Q., Mayeda A., Hampson R. K., Krainer A. R., Rottman F. M. General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev. 1993 Dec;7(12B):2598–2608. doi: 10.1101/gad.7.12b.2598. [DOI] [PubMed] [Google Scholar]
  62. Takagaki Y., Manley J. L. A polyadenylation factor subunit is the human homologue of the Drosophila suppressor of forked protein. Nature. 1994 Dec 1;372(6505):471–474. doi: 10.1038/372471a0. [DOI] [PubMed] [Google Scholar]
  63. Tarn W. Y., Steitz J. A. SR proteins can compensate for the loss of U1 snRNP functions in vitro. Genes Dev. 1994 Nov 15;8(22):2704–2717. doi: 10.1101/gad.8.22.2704. [DOI] [PubMed] [Google Scholar]
  64. Tian M., Maniatis T. A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell. 1993 Jul 16;74(1):105–114. doi: 10.1016/0092-8674(93)90298-5. [DOI] [PubMed] [Google Scholar]
  65. Tian M., Maniatis T. A splicing enhancer exhibits both constitutive and regulated activities. Genes Dev. 1994 Jul 15;8(14):1703–1712. doi: 10.1101/gad.8.14.1703. [DOI] [PubMed] [Google Scholar]
  66. Tian M., Maniatis T. Positive control of pre-mRNA splicing in vitro. Science. 1992 Apr 10;256(5054):237–240. doi: 10.1126/science.1566072. [DOI] [PubMed] [Google Scholar]
  67. Voelker R. A., Gibson W., Graves J. P., Sterling J. F., Eisenberg M. T. The Drosophila suppressor of sable gene encodes a polypeptide with regions similar to those of RNA-binding proteins. Mol Cell Biol. 1991 Feb;11(2):894–905. doi: 10.1128/mcb.11.2.894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wittekind M., Görlach M., Friedrichs M., Dreyfuss G., Mueller L. 1H, 13C, and 15N NMR assignments and global folding pattern of the RNA-binding domain of the human hnRNP C proteins. Biochemistry. 1992 Jul 14;31(27):6254–6265. doi: 10.1021/bi00142a013. [DOI] [PubMed] [Google Scholar]
  69. Wu J. Y., Maniatis T. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell. 1993 Dec 17;75(6):1061–1070. doi: 10.1016/0092-8674(93)90316-i. [DOI] [PubMed] [Google Scholar]
  70. Yun B., Farkas R., Lee K., Rabinow L. The Doa locus encodes a member of a new protein kinase family and is essential for eye and embryonic development in Drosophila melanogaster. Genes Dev. 1994 May 15;8(10):1160–1173. doi: 10.1101/gad.8.10.1160. [DOI] [PubMed] [Google Scholar]
  71. Zachar Z., Chou T. B., Bingham P. M. Evidence that a regulatory gene autoregulates splicing of its transcript. EMBO J. 1987 Dec 20;6(13):4105–4111. doi: 10.1002/j.1460-2075.1987.tb02756.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zachar Z., Chou T. B., Kramer J., Mims I. P., Bingham P. M. Analysis of autoregulation at the level of pre-mRNA splicing of the suppressor-of-white-apricot gene in Drosophila. Genetics. 1994 May;137(1):139–150. doi: 10.1093/genetics/137.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Zahler A. M., Lane W. S., Stolk J. A., Roth M. B. SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 1992 May;6(5):837–847. doi: 10.1101/gad.6.5.837. [DOI] [PubMed] [Google Scholar]
  74. Zahler A. M., Neugebauer K. M., Lane W. S., Roth M. B. Distinct functions of SR proteins in alternative pre-mRNA splicing. Science. 1993 Apr 9;260(5105):219–222. doi: 10.1126/science.8385799. [DOI] [PubMed] [Google Scholar]
  75. Zahler A. M., Neugebauer K. M., Stolk J. A., Roth M. B. Human SR proteins and isolation of a cDNA encoding SRp75. Mol Cell Biol. 1993 Jul;13(7):4023–4028. doi: 10.1128/mcb.13.7.4023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Zuo P., Manley J. L. Functional domains of the human splicing factor ASF/SF2. EMBO J. 1993 Dec;12(12):4727–4737. doi: 10.1002/j.1460-2075.1993.tb06161.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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