Abstract
In addition to their role in pre-mRNA splicing, the human spliceosomal proteins U1A and U2B" are important models of how RNP motif-containing proteins execute sequence-specific RNA binding. Genes encoding U1A and U2B" have been isolated from potato and thereby provide the only evolutionary comparison available for both proteins and represent the only full-length genes encoding plant spliceosomal proteins to have been cloned and characterized. In vitro RNA binding experiments revealed the ability of potato U2B" to interact with human U2A' to enhance sequence-specific binding and to distinguish cognate RNAs of either plant or animal origin. A comparison of the sequence of U1A and U2B" proteins indicated that multiple residues which could affect RNP motif conformation probably govern the specific distinction in RNA binding by these proteins. Since human U1A modulates polyadenylation in vertebrates, the possibility that plant U1A might be exploited in the characterization of this process in plants was examined. However, unlike vertebrate U1A, neither U1A from potato nor Arabidopsis bound their own mRNA and no evidence for binding to upstream efficiency elements in polyadenylation signals was obtained, suggesting that plant U1A is not involved in polyadenylation.
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- Bandziulis R. J., Swanson M. S., Dreyfuss G. RNA-binding proteins as developmental regulators. Genes Dev. 1989 Apr;3(4):431–437. doi: 10.1101/gad.3.4.431. [DOI] [PubMed] [Google Scholar]
- Bennett M. M., Baron M. A., Craft J. Nucleotide sequence analysis of the A protein of the U1 small nuclear ribonucleoprotein particle: the murine protein contains a 5' amino-terminal tag. Nucleic Acids Res. 1993 Sep 11;21(18):4404–4404. doi: 10.1093/nar/21.18.4404. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bentley R. C., Keene J. D. Recognition of U1 and U2 small nuclear RNAs can be altered by a 5-amino-acid segment in the U2 small nuclear ribonucleoprotein particle (snRNP) B" protein and through interactions with U2 snRNP-A' protein. Mol Cell Biol. 1991 Apr;11(4):1829–1839. doi: 10.1128/mcb.11.4.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beven A. F., Simpson G. G., Brown J. W., Shaw P. J. The organization of spliceosomal components in the nuclei of higher plants. J Cell Sci. 1995 Feb;108(Pt 2):509–518. doi: 10.1242/jcs.108.2.509. [DOI] [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]
- Boelens W. C., Jansen E. J., van Venrooij W. J., Stripecke R., Mattaj I. W., Gunderson S. I. The human U1 snRNP-specific U1A protein inhibits polyadenylation of its own pre-mRNA. Cell. 1993 Mar 26;72(6):881–892. doi: 10.1016/0092-8674(93)90577-d. [DOI] [PubMed] [Google Scholar]
- Boelens W., Scherly D., Beijer R. P., Jansen E. J., Dathan N. A., Mattaj I. W., van Venrooij W. J. A weak interaction between the U2A' protein and U2 snRNA helps to stabilize their complex with the U2B" protein. Nucleic Acids Res. 1991 Feb 11;19(3):455–460. doi: 10.1093/nar/19.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boelens W., Scherly D., Jansen E. J., Kolen K., Mattaj I. W., van Venrooij W. J. Analysis of in vitro binding of U1-A protein mutants to U1 snRNA. Nucleic Acids Res. 1991 Sep 11;19(17):4611–4618. doi: 10.1093/nar/19.17.4611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., Tamaki S., Dunsmuir P., Favreau M., Katayama C., Dooner H., Bedbrook J. mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucleic Acids Res. 1986 Mar 11;14(5):2229–2240. doi: 10.1093/nar/14.5.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flickinger T. W., Salz H. K. The Drosophila sex determination gene snf encodes a nuclear protein with sequence and functional similarity to the mammalian U1A snRNP protein. Genes Dev. 1994 Apr 15;8(8):914–925. doi: 10.1101/gad.8.8.914. [DOI] [PubMed] [Google Scholar]
- Fresco L. D., Harper D. S., Keene J. D. Leucine periodicity of U2 small nuclear ribonucleoprotein particle (snRNP) A' protein is implicated in snRNP assembly via protein-protein interactions. Mol Cell Biol. 1991 Mar;11(3):1578–1589. doi: 10.1128/mcb.11.3.1578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodall G. J., Filipowicz W. The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell. 1989 Aug 11;58(3):473–483. doi: 10.1016/0092-8674(89)90428-5. [DOI] [PubMed] [Google Scholar]
- Goodall G. J., Wiebauer K., Filipowicz W. Analysis of pre-mRNA processing in transfected plant protoplasts. Methods Enzymol. 1990;181:148–161. doi: 10.1016/0076-6879(90)81117-d. [DOI] [PubMed] [Google Scholar]
- Gunderson S. I., Beyer K., Martin G., Keller W., Boelens W. C., Mattaj L. W. The human U1A snRNP protein regulates polyadenylation via a direct interaction with poly(A) polymerase. Cell. 1994 Feb 11;76(3):531–541. doi: 10.1016/0092-8674(94)90116-3. [DOI] [PubMed] [Google Scholar]
- Habets W. J., Sillekens P. T., Hoet M. H., Schalken J. A., Roebroek A. J., Leunissen J. A., van de Ven W. J., van Venrooij W. J. Analysis of a cDNA clone expressing a human autoimmune antigen: full-length sequence of the U2 small nuclear RNA-associated B" antigen. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2421–2425. doi: 10.1073/pnas.84.8.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hall K. B. Interaction of RNA hairpins with the human U1A N-terminal RNA binding domain. Biochemistry. 1994 Aug 23;33(33):10076–10088. doi: 10.1021/bi00199a035. [DOI] [PubMed] [Google Scholar]
- Hamm J., Dathan N. A., Mattaj I. W. Functional analysis of mutant Xenopus U2 snRNAs. Cell. 1989 Oct 6;59(1):159–169. doi: 10.1016/0092-8674(89)90878-7. [DOI] [PubMed] [Google Scholar]
- Hanley B. A., Schuler M. A. Developmental expression of plant snRNAs. Nucleic Acids Res. 1991 Nov 25;19(22):6319–6325. doi: 10.1093/nar/19.22.6319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harper D. S., Fresco L. D., Keene J. D. RNA binding specificity of a Drosophila snRNP protein that shares sequence homology with mammalian U1-A and U2-B" proteins. Nucleic Acids Res. 1992 Jul 25;20(14):3645–3650. doi: 10.1093/nar/20.14.3645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hedley P. E., Machray G. C., Davies H. V., Burch L., Waugh R. Potato (Solanum tuberosum) invertase-encoding cDNAs and their differential expression. Gene. 1994 Aug 5;145(2):211–214. doi: 10.1016/0378-1119(94)90007-8. [DOI] [PubMed] [Google Scholar]
- Howe P. W., Nagai K., Neuhaus D., Varani G. NMR studies of U1 snRNA recognition by the N-terminal RNP domain of the human U1A protein. EMBO J. 1994 Aug 15;13(16):3873–3881. doi: 10.1002/j.1460-2075.1994.tb06698.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jessen T. H., Oubridge C., Teo C. H., Pritchard C., Nagai K. Identification of molecular contacts between the U1 A small nuclear ribonucleoprotein and U1 RNA. EMBO J. 1991 Nov;10(11):3447–3456. doi: 10.1002/j.1460-2075.1991.tb04909.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joshi C. P. Putative polyadenylation signals in nuclear genes of higher plants: a compilation and analysis. Nucleic Acids Res. 1987 Dec 10;15(23):9627–9640. doi: 10.1093/nar/15.23.9627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kambach C., Mattaj I. W. Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA. J Cell Biol. 1992 Jul;118(1):11–21. doi: 10.1083/jcb.118.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kambach C., Mattaj I. W. Nuclear transport of the U2 snRNP-specific U2B'' protein is mediated by both direct and indirect signalling mechanisms. J Cell Sci. 1994 Jul;107(Pt 7):1807–1816. doi: 10.1242/jcs.107.7.1807. [DOI] [PubMed] [Google Scholar]
- Keene J. D., Query C. C. Nuclear RNA-binding proteins. Prog Nucleic Acid Res Mol Biol. 1991;41:179–202. doi: 10.1016/s0079-6603(08)60009-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Li Y. Q., Ye L. Z., Sugita M., Sugiura M. Tobacco nuclear gene for the 31 kd chloroplast ribonucleoprotein: genomic organization, sequence analysis and expression. Nucleic Acids Res. 1991 Jun 11;19(11):2987–2991. doi: 10.1093/nar/19.11.2987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liao X. C., Tang J., Rosbash M. An enhancer screen identifies a gene that encodes the yeast U1 snRNP A protein: implications for snRNP protein function in pre-mRNA splicing. Genes Dev. 1993 Mar;7(3):419–428. doi: 10.1101/gad.7.3.419. [DOI] [PubMed] [Google Scholar]
- Lu J., Hall K. B. An RBD that does not bind RNA: NMR secondary structure determination and biochemical properties of the C-terminal RNA binding domain from the human U1A protein. J Mol Biol. 1995 Apr 7;247(4):739–752. doi: 10.1006/jmbi.1995.0177. [DOI] [PubMed] [Google Scholar]
- Lutz-Freyermuth C., Query C. C., Keene J. D. Quantitative determination that one of two potential RNA-binding domains of the A protein component of the U1 small nuclear ribonucleoprotein complex binds with high affinity to stem-loop II of U1 RNA. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6393–6397. doi: 10.1073/pnas.87.16.6393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lutz C. S., Alwine J. C. Direct interaction of the U1 snRNP-A protein with the upstream efficiency element of the SV40 late polyadenylation signal. Genes Dev. 1994 Mar 1;8(5):576–586. doi: 10.1101/gad.8.5.576. [DOI] [PubMed] [Google Scholar]
- Mattaj I. W. RNA recognition: a family matter? Cell. 1993 Jun 4;73(5):837–840. doi: 10.1016/0092-8674(93)90265-r. [DOI] [PubMed] [Google Scholar]
- Musci M. A., Egeland D. B., Schuler M. A. Molecular comparison of monocot and dicot U1 and U2 snRNAs. Plant J. 1992 Jul;2(4):589–599. doi: 10.1046/j.1365-313x.1992.t01-28-00999.x. [DOI] [PubMed] [Google Scholar]
- Muser J., Kaech S., Moroni C., Ballmer-Hofer K. Stimulation of pp60c-src kinase activity in FDC-P1 cells by polyoma middle-T antigen and hematopoietic growth factors. Oncogene. 1989 Dec;4(12):1433–1439. [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]
- Nelissen R. L., Sillekens P. T., Beijer R. P., Geurts van Kessel A. H., van Venrooij W. J. Structure, chromosomal localization and evolutionary conservation of the gene encoding human U1 snRNP-specific A protein. Gene. 1991 Jun 30;102(2):189–196. doi: 10.1016/0378-1119(91)90077-o. [DOI] [PubMed] [Google Scholar]
- 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]
- Rothnie H. M., Reid J., Hohn T. The contribution of AAUAAA and the upstream element UUUGUA to the efficiency of mRNA 3'-end formation in plants. EMBO J. 1994 May 1;13(9):2200–2210. doi: 10.1002/j.1460-2075.1994.tb06497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scherly D., Boelens W., Dathan N. A., van Venrooij W. J., Mattaj I. W. Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B'' and their cognate RNAs. Nature. 1990 Jun 7;345(6275):502–506. doi: 10.1038/345502a0. [DOI] [PubMed] [Google Scholar]
- Scherly D., Boelens W., van Venrooij W. J., Dathan N. A., Hamm J., Mattaj I. W. Identification of the RNA binding segment of human U1 A protein and definition of its binding site on U1 snRNA. EMBO J. 1989 Dec 20;8(13):4163–4170. doi: 10.1002/j.1460-2075.1989.tb08601.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scherly D., Dathan N. A., Boelens W., van Venrooij W. J., Mattaj I. W. The U2B'' RNP motif as a site of protein-protein interaction. EMBO J. 1990 Nov;9(11):3675–3681. doi: 10.1002/j.1460-2075.1990.tb07579.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scherly D., Kambach C., Boelens W., van Venrooij W. J., Mattaj I. W. Conserved amino acid residues within and outside of the N-terminal ribonucleoprotein motif of U1A small nuclear ribonucleoprotein involved in U1 RNA binding. J Mol Biol. 1991 Jun 20;219(4):577–584. doi: 10.1016/0022-2836(91)90651-l. [DOI] [PubMed] [Google Scholar]
- Shannon K. W., Guthrie C. Suppressors of a U4 snRNA mutation define a novel U6 snRNP protein with RNA-binding motifs. Genes Dev. 1991 May;5(5):773–785. doi: 10.1101/gad.5.5.773. [DOI] [PubMed] [Google Scholar]
- Sillekens P. T., Habets W. J., Beijer R. P., van Venrooij W. J. cDNA cloning of the human U1 snRNA-associated A protein: extensive homology between U1 and U2 snRNP-specific proteins. EMBO J. 1987 Dec 1;6(12):3841–3848. doi: 10.1002/j.1460-2075.1987.tb02721.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simpson G. G., Vaux P., Clark G., Waugh R., Beggs J. D., Brown J. W. Evolutionary conservation of the spliceosomal protein, U2B''. Nucleic Acids Res. 1991 Oct 11;19(19):5213–5217. doi: 10.1093/nar/19.19.5213. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stump W. T., Hall K. B. Crosslinking of an iodo-uridine-RNA hairpin to a single site on the human U1A N-terminal RNA binding domain. RNA. 1995 Mar;1(1):55–63. [PMC free article] [PubMed] [Google Scholar]
- Tsai D. E., Harper D. S., Keene J. D. U1-snRNP-A protein selects a ten nucleotide consensus sequence from a degenerate RNA pool presented in various structural contexts. Nucleic Acids Res. 1991 Sep 25;19(18):4931–4936. doi: 10.1093/nar/19.18.4931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wahle E., Keller W. The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev Biochem. 1992;61:419–440. doi: 10.1146/annurev.bi.61.070192.002223. [DOI] [PubMed] [Google Scholar]
- Waugh R., Clark G., Vaux P., Brown J. W. Sequence and expression of potato U2 snRNA genes. Nucleic Acids Res. 1991 Jan 25;19(2):249–256. doi: 10.1093/nar/19.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Gelder C. W., Gunderson S. I., Jansen E. J., Boelens W. C., Polycarpou-Schwarz M., Mattaj I. W., van Venrooij W. J. A complex secondary structure in U1A pre-mRNA that binds two molecules of U1A protein is required for regulation of polyadenylation. EMBO J. 1993 Dec 15;12(13):5191–5200. doi: 10.1002/j.1460-2075.1993.tb06214.x. [DOI] [PMC free article] [PubMed] [Google Scholar]