Abstract
hnRNP A1 is a pre-mRNA binding protein that antagonizes the alternative splicing activity of splicing factors SF2/ASF or SC35, causing activation of distal 5' splice sites. The structural requirements for hnRNP A1 function were determined by mutagenesis of recombinant human hnRNP A1. Two conserved Phe residues in the RNP-1 submotif of each of two RNA recognition motifs appear to be involved in specific RNA-protein interactions and are essential for modulating alternative splicing. These residues are not required for general pre-mRNA binding or RNA annealing activity. The C-terminal Gly-rich domain is necessary for alternative splicing activity, for stable RNA binding and for optimal RNA annealing activity. hnRNP A1B, which is an alternatively spliced isoform of hnRNP A1 with a longer Gly-rich domain, binds more strongly to pre-mRNA but has only limited alternative splicing activity. In contrast, hnRNP A2 and B1, which have 68% amino acid identity with hnRNP A1, bind more weakly to pre-mRNA and have stronger splice site switching activities than hnRNP A1. We propose that specific combinations of antagonistic hnRNP A/B and SR proteins are involved in regulating alternative splicing of distinct subsets of cellular premRNAs.
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Selected References
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- Ben-David Y., Bani M. R., Chabot B., De Koven A., Bernstein A. Retroviral insertions downstream of the heterogeneous nuclear ribonucleoprotein A1 gene in erythroleukemia cells: evidence that A1 is not essential for cell growth. Mol Cell Biol. 1992 Oct;12(10):4449–4455. doi: 10.1128/mcb.12.10.4449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bennett M., Michaud S., Kingston J., Reed R. Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev. 1992 Oct;6(10):1986–2000. doi: 10.1101/gad.6.10.1986. [DOI] [PubMed] [Google Scholar]
- Bennett M., Piñol-Roma S., Staknis D., Dreyfuss G., Reed R. Differential binding of heterogeneous nuclear ribonucleoproteins to mRNA precursors prior to spliceosome assembly in vitro. Mol Cell Biol. 1992 Jul;12(7):3165–3175. doi: 10.1128/mcb.12.7.3165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beyer A. L., Christensen M. E., Walker B. W., LeStourgeon W. M. Identification and characterization of the packaging proteins of core 40S hnRNP particles. Cell. 1977 May;11(1):127–138. doi: 10.1016/0092-8674(77)90323-3. [DOI] [PubMed] [Google Scholar]
- Biamonti G., Buvoli M., Bassi M. T., Morandi C., Cobianchi F., Riva S. Isolation of an active gene encoding human hnRNP protein A1. Evidence for alternative splicing. J Mol Biol. 1989 Jun 5;207(3):491–503. doi: 10.1016/0022-2836(89)90459-2. [DOI] [PubMed] [Google Scholar]
- Biamonti G., Ruggiu M., Saccone S., Della Valle G., Riva S. Two homologous genes, originated by duplication, encode the human hnRNP proteins A2 and A1. Nucleic Acids Res. 1994 Jun 11;22(11):1996–2002. doi: 10.1093/nar/22.11.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Burd C. G., Dreyfuss G. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 1994 Mar 1;13(5):1197–1204. doi: 10.1002/j.1460-2075.1994.tb06369.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burd C. G., Swanson M. S., Görlach M., Dreyfuss G. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9788–9792. doi: 10.1073/pnas.86.24.9788. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buvoli M., Biamonti G., Tsoulfas P., Bassi M. T., Ghetti A., Riva S., Morandi C. cDNA cloning of human hnRNP protein A1 reveals the existence of multiple mRNA isoforms. Nucleic Acids Res. 1988 May 11;16(9):3751–3770. doi: 10.1093/nar/16.9.3751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buvoli M., Cobianchi F., Bestagno M. G., Mangiarotti A., Bassi M. T., Biamonti G., Riva S. Alternative splicing in the human gene for the core protein A1 generates another hnRNP protein. EMBO J. 1990 Apr;9(4):1229–1235. doi: 10.1002/j.1460-2075.1990.tb08230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buvoli M., Cobianchi F., Riva S. Interaction of hnRNP A1 with snRNPs and pre-mRNAs: evidence for a possible role of A1 RNA annealing activity in the first steps of spliceosome assembly. Nucleic Acids Res. 1992 Oct 11;20(19):5017–5025. doi: 10.1093/nar/20.19.5017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carey J., Cameron V., de Haseth P. L., Uhlenbeck O. C. Sequence-specific interaction of R17 coat protein with its ribonucleic acid binding site. Biochemistry. 1983 May 24;22(11):2601–2610. doi: 10.1021/bi00280a002. [DOI] [PubMed] [Google Scholar]
- Casas-Finet J. R., Karpel R. L., Maki A. H., Kumar A., Wilson S. H. Physical studies of tyrosine and tryptophan residues in mammalian A1 heterogeneous nuclear ribonucleoprotein. Support for a segmented structure. J Mol Biol. 1991 Sep 20;221(2):693–709. doi: 10.1016/0022-2836(91)80081-5. [DOI] [PubMed] [Google Scholar]
- Casas-Finet J. R., Smith J. D., Jr, Kumar A., Kim J. G., Wilson S. H., Karpel R. L. Mammalian heterogeneous ribonucleoprotein A1 and its constituent domains. Nucleic acid interaction, structural stability and self-association. J Mol Biol. 1993 Feb 20;229(4):873–889. doi: 10.1006/jmbi.1993.1093. [DOI] [PubMed] [Google Scholar]
- Choi Y. D., Grabowski P. J., Sharp P. A., Dreyfuss G. Heterogeneous nuclear ribonucleoproteins: role in RNA splicing. Science. 1986 Mar 28;231(4745):1534–1539. doi: 10.1126/science.3952495. [DOI] [PubMed] [Google Scholar]
- Cobianchi F., Karpel R. L., Williams K. R., Notario V., Wilson S. H. Mammalian heterogeneous nuclear ribonucleoprotein complex protein A1. Large-scale overproduction in Escherichia coli and cooperative binding to single-stranded nucleic acids. J Biol Chem. 1988 Jan 15;263(2):1063–1071. [PubMed] [Google Scholar]
- 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]
- Cáceres J. F., Stamm S., Helfman D. M., Krainer A. R. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science. 1994 Sep 16;265(5179):1706–1709. doi: 10.1126/science.8085156. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Garrett D. S., Lodi P. J., Shamoo Y., Williams K. R., Clore G. M., Gronenborn A. M. Determination of the secondary structure and folding topology of an RNA binding domain of mammalian hnRNP A1 protein using three-dimensional heteronuclear magnetic resonance spectroscopy. Biochemistry. 1994 Mar 15;33(10):2852–2858. doi: 10.1021/bi00176a015. [DOI] [PubMed] [Google Scholar]
- Ge H., Manley J. L. A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell. 1990 Jul 13;62(1):25–34. doi: 10.1016/0092-8674(90)90236-8. [DOI] [PubMed] [Google Scholar]
- 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]
- Ghetti A., Piñol-Roma S., Michael W. M., Morandi C., Dreyfuss G. hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res. 1992 Jul 25;20(14):3671–3678. doi: 10.1093/nar/20.14.3671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gil A., Sharp P. A., Jamison S. F., Garcia-Blanco M. A. Characterization of cDNAs encoding the polypyrimidine tract-binding protein. Genes Dev. 1991 Jul;5(7):1224–1236. doi: 10.1101/gad.5.7.1224. [DOI] [PubMed] [Google Scholar]
- 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]
- Hamilton B. J., Nagy E., Malter J. S., Arrick B. A., Rigby W. F. Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J Biol Chem. 1993 Apr 25;268(12):8881–8887. [PubMed] [Google Scholar]
- Harper J. E., Manley J. L. A novel protein factor is required for use of distal alternative 5' splice sites in vitro. Mol Cell Biol. 1991 Dec;11(12):5945–5953. doi: 10.1128/mcb.11.12.5945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrick G., Alberts B. Nucleic acid helix-coil transitions mediated by helix-unwinding proteins from calf thymus. J Biol Chem. 1976 Apr 10;251(7):2133–2141. [PubMed] [Google Scholar]
- 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]
- Horowitz D. S., Krainer A. R. Mechanisms for selecting 5' splice sites in mammalian pre-mRNA splicing. Trends Genet. 1994 Mar;10(3):100–106. doi: 10.1016/0168-9525(94)90233-x. [DOI] [PubMed] [Google Scholar]
- Huang M., Rech J. E., Northington S. J., Flicker P. F., Mayeda A., Krainer A. R., LeStourgeon W. M. The C-protein tetramer binds 230 to 240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles. Mol Cell Biol. 1994 Jan;14(1):518–533. doi: 10.1128/mcb.14.1.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishikawa F., Matunis M. J., Dreyfuss G., Cech T. R. Nuclear proteins that bind the pre-mRNA 3' splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n. Mol Cell Biol. 1993 Jul;13(7):4301–4310. doi: 10.1128/mcb.13.7.4301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karsch-Mizrachi I., Haynes S. R. The Rb97D gene encodes a potential RNA-binding protein required for spermatogenesis in Drosophila. Nucleic Acids Res. 1993 May 11;21(9):2229–2235. doi: 10.1093/nar/21.9.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Krainer A. R., Conway G. C., Kozak D. The essential pre-mRNA splicing factor SF2 influences 5' splice site selection by activating proximal sites. Cell. 1990 Jul 13;62(1):35–42. doi: 10.1016/0092-8674(90)90237-9. [DOI] [PubMed] [Google Scholar]
- Krainer A. R., Maniatis T. Multiple factors including the small nuclear ribonucleoproteins U1 and U2 are necessary for pre-mRNA splicing in vitro. Cell. 1985 Oct;42(3):725–736. doi: 10.1016/0092-8674(85)90269-7. [DOI] [PubMed] [Google Scholar]
- Krainer A. R., Maniatis T., Ruskin B., Green M. R. Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell. 1984 Apr;36(4):993–1005. doi: 10.1016/0092-8674(84)90049-7. [DOI] [PubMed] [Google Scholar]
- 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]
- Kumar A., Casas-Finet J. R., Luneau C. J., Karpel R. L., Merrill B. M., Williams K. R., Wilson S. H. Mammalian heterogeneous nuclear ribonucleoprotein A1. Nucleic acid binding properties of the COOH-terminal domain. J Biol Chem. 1990 Oct 5;265(28):17094–17100. [PubMed] [Google Scholar]
- Kumar A., Sierakowska H., Szer W. Purification and RNA binding properties of a C-type hnRNP protein from HeLa cells. J Biol Chem. 1987 Dec 15;262(35):17126–17137. [PubMed] [Google Scholar]
- Kumar A., Williams K. R., Szer W. Purification and domain structure of core hnRNP proteins A1 and A2 and their relationship to single-stranded DNA-binding proteins. J Biol Chem. 1986 Aug 25;261(24):11266–11273. [PubMed] [Google Scholar]
- Kumar A., Wilson S. H. Studies of the strand-annealing activity of mammalian hnRNP complex protein A1. Biochemistry. 1990 Dec 4;29(48):10717–10722. doi: 10.1021/bi00500a001. [DOI] [PubMed] [Google Scholar]
- Lee C. G., Zamore P. D., Green M. R., Hurwitz J. RNA annealing activity is intrinsically associated with U2AF. J Biol Chem. 1993 Jun 25;268(18):13472–13478. [PubMed] [Google Scholar]
- Matunis E. L., Kelley R., Dreyfuss G. Essential role for a heterogeneous nuclear ribonucleoprotein (hnRNP) in oogenesis: hrp40 is absent from the germ line in the dorsoventral mutant squid. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2781–2784. doi: 10.1073/pnas.91.7.2781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayeda A., Helfman D. M., Krainer A. R. Modulation of exon skipping and inclusion by heterogeneous nuclear ribonucleoprotein A1 and pre-mRNA splicing factor SF2/ASF. Mol Cell Biol. 1993 May;13(5):2993–3001. doi: 10.1128/mcb.13.5.2993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayeda A., Krainer A. R. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell. 1992 Jan 24;68(2):365–375. doi: 10.1016/0092-8674(92)90477-t. [DOI] [PubMed] [Google Scholar]
- Mayeda A., Ohshima Y. Beta-globin transcripts carrying a single intron with three adjacent nucleotides of 5' exon are efficiently spliced in vitro irrespective of intron position or surrounding exon sequences. Nucleic Acids Res. 1990 Aug 25;18(16):4671–4676. doi: 10.1093/nar/18.16.4671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayeda A., Ohshima Y. Short donor site sequences inserted within the intron of beta-globin pre-mRNA serve for splicing in vitro. Mol Cell Biol. 1988 Oct;8(10):4484–4491. doi: 10.1128/mcb.8.10.4484. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayeda A., Tatei K., Kitayama H., Takemura K., Ohshima Y. Three distinct activities possibly involved in mRNA splicing are found in a nuclear fraction lacking U1 and U2 RNA. Nucleic Acids Res. 1986 Apr 11;14(7):3045–3057. doi: 10.1093/nar/14.7.3045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mayrand S. H., Pederson T. Crosslinking of hnRNP proteins to pre-mRNA requires U1 and U2 snRNPs. Nucleic Acids Res. 1990 Jun 11;18(11):3307–3318. doi: 10.1093/nar/18.11.3307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McKay S. J., Cooke H. hnRNP A2/B1 binds specifically to single stranded vertebrate telomeric repeat TTAGGGn. Nucleic Acids Res. 1992 Dec 25;20(24):6461–6464. doi: 10.1093/nar/20.24.6461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merrill B. M., Stone K. L., Cobianchi F., Wilson S. H., Williams K. R. Phenylalanines that are conserved among several RNA-binding proteins form part of a nucleic acid-binding pocket in the A1 heterogeneous nuclear ribonucleoprotein. J Biol Chem. 1988 Mar 5;263(7):3307–3313. [PubMed] [Google Scholar]
- Mulligan G. J., Guo W., Wormsley S., Helfman D. M. Polypyrimidine tract binding protein interacts with sequences involved in alternative splicing of beta-tropomyosin pre-mRNA. J Biol Chem. 1992 Dec 15;267(35):25480–25487. [PubMed] [Google Scholar]
- Munroe S. H. Antisense RNA inhibits splicing of pre-mRNA in vitro. EMBO J. 1988 Aug;7(8):2523–2532. doi: 10.1002/j.1460-2075.1988.tb03100.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Munroe S. H., Dong X. F. Heterogeneous nuclear ribonucleoprotein A1 catalyzes RNA.RNA annealing. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):895–899. doi: 10.1073/pnas.89.3.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nadler S. G., Merrill B. M., Roberts W. J., Keating K. M., Lisbin M. J., Barnett S. F., Wilson S. H., Williams K. R. Interactions of the A1 heterogeneous nuclear ribonucleoprotein and its proteolytic derivative, UP1, with RNA and DNA: evidence for multiple RNA binding domains and salt-dependent binding mode transitions. Biochemistry. 1991 Mar 19;30(11):2968–2976. doi: 10.1021/bi00225a034. [DOI] [PubMed] [Google Scholar]
- 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]
- Patton J. G., Mayer S. A., Tempst P., Nadal-Ginard B. Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev. 1991 Jul;5(7):1237–1251. doi: 10.1101/gad.5.7.1237. [DOI] [PubMed] [Google Scholar]
- Piñol-Roma S., Choi Y. D., Matunis M. J., Dreyfuss G. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev. 1988 Feb;2(2):215–227. doi: 10.1101/gad.2.2.215. [DOI] [PubMed] [Google Scholar]
- Pontius B. W., Berg P. Rapid assembly and disassembly of complementary DNA strands through an equilibrium intermediate state mediated by A1 hnRNP protein. J Biol Chem. 1992 Jul 15;267(20):13815–13818. [PubMed] [Google Scholar]
- Pontius B. W., Berg P. Renaturation of complementary DNA strands mediated by purified mammalian heterogeneous nuclear ribonucleoprotein A1 protein: implications for a mechanism for rapid molecular assembly. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8403–8407. doi: 10.1073/pnas.87.21.8403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pontius B. W. Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular association. Trends Biochem Sci. 1993 May;18(5):181–186. doi: 10.1016/0968-0004(93)90111-y. [DOI] [PubMed] [Google Scholar]
- Portman D. S., Dreyfuss G. RNA annealing activities in HeLa nuclei. EMBO J. 1994 Jan 1;13(1):213–221. doi: 10.1002/j.1460-2075.1994.tb06251.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reed R., Maniatis T. A role for exon sequences and splice-site proximity in splice-site selection. Cell. 1986 Aug 29;46(5):681–690. doi: 10.1016/0092-8674(86)90343-0. [DOI] [PubMed] [Google Scholar]
- Sierakowska H., Szer W., Furdon P. J., Kole R. Antibodies to hnRNP core proteins inhibit in vitro splicing of human beta-globin pre-mRNA. Nucleic Acids Res. 1986 Jul 11;14(13):5241–5254. doi: 10.1093/nar/14.13.5241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stolow D. T., Berget S. M. Identification of nuclear proteins that specifically bind to RNAs containing 5' splice sites. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):320–324. doi: 10.1073/pnas.88.2.320. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Swanson M. S., Dreyfuss G. RNA binding specificity of hnRNP proteins: a subset bind to the 3' end of introns. EMBO J. 1988 Nov;7(11):3519–3529. doi: 10.1002/j.1460-2075.1988.tb03228.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Williams K. R., Stone K. L., LoPresti M. B., Merrill B. M., Planck S. R. Amino acid sequence of the UP1 calf thymus helix-destabilizing protein and its homology to an analogous protein from mouse myeloma. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5666–5670. doi: 10.1073/pnas.82.17.5666. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wyatt J. R., Sontheimer E. J., Steitz J. A. Site-specific cross-linking of mammalian U5 snRNP to the 5' splice site before the first step of pre-mRNA splicing. Genes Dev. 1992 Dec;6(12B):2542–2553. doi: 10.1101/gad.6.12b.2542. [DOI] [PubMed] [Google Scholar]
- Yang X., Bani M. R., Lu S. J., Rowan S., Ben-David Y., Chabot B. The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5' splice site selection in vivo. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6924–6928. doi: 10.1073/pnas.91.15.6924. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]