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. 1993 Feb 25;21(4):999–1006. doi: 10.1093/nar/21.4.999

Three new members of the RNP protein family in Xenopus.

P J Good 1, M L Rebbert 1, I B Dawid 1
PMCID: PMC309235  PMID: 8451200

Abstract

Many RNP proteins contain one or more copies of the RNA recognition motif (RRM) and are thought to be involved in cellular RNA metabolism. We have previously characterized in Xenopus a nervous system specific gene, nrp1, that is more similar to the hnRNP A/B proteins than to other known proteins (K. Richter, P. J. Good, and I. B. Dawid (1990), New Biol. 2, 556-565). PCR amplification with degenerate primers was used to identify additional cDNAs encoding two RRMs in Xenopus. Three previously uncharacterized genes were identified. Two genes encode hnRNP A/B proteins with two RRMs and a glycine-rich domain. One of these is the Xenopus homolog of the human A2/B1 gene; the other, named hnRNP A3, is similar to both the A1 and A2 hnRNP genes. The Xenopus hnRNP A1, A2 and A3 genes are expressed throughout development and in all adult tissues. Multiple protein isoforms for the hnRNP A2 gene are predicted that differ by the insertion of short peptide sequences in the glycine-rich domain. The third newly isolated gene, named xrp1, encodes a protein that is related by sequence to the nrp1 protein but is expressed ubiquitously. Despite the similarity to nuclear RNP proteins, both the nrp1 and xrp1 proteins are localized to the cytoplasm in the Xenopus oocyte. The xrp1 gene may have a function in all cells that is similar to that executed by nrp1 specifically within the nervous system.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ayane M., Preuss U., Köhler G., Nielsen P. J. A differentially expressed murine RNA encoding a protein with similarities to two types of nucleic acid binding motifs. Nucleic Acids Res. 1991 Mar 25;19(6):1273–1278. doi: 10.1093/nar/19.6.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Bell L. R., Maine E. M., Schedl P., Cline T. W. Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell. 1988 Dec 23;55(6):1037–1046. doi: 10.1016/0092-8674(88)90248-6. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Burd C. G., Matunis E. L., Dreyfuss G. The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities. Mol Cell Biol. 1991 Jul;11(7):3419–3424. doi: 10.1128/mcb.11.7.3419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. Cobianchi F., SenGupta D. N., Zmudzka B. Z., Wilson S. H. Structure of rodent helix-destabilizing protein revealed by cDNA cloning. J Biol Chem. 1986 Mar 15;261(8):3536–3543. [PubMed] [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dreyfuss G., Philipson L., Mattaj I. W. Ribonucleoprotein particles in cellular processes. J Cell Biol. 1988 May;106(5):1419–1425. doi: 10.1083/jcb.106.5.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dreyfuss G. Structure and function of nuclear and cytoplasmic ribonucleoprotein particles. Annu Rev Cell Biol. 1986;2:459–498. doi: 10.1146/annurev.cb.02.110186.002331. [DOI] [PubMed] [Google Scholar]
  15. Dreyfuss G., Swanson M. S., Piñol-Roma S. Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem Sci. 1988 Mar;13(3):86–91. doi: 10.1016/0968-0004(88)90046-1. [DOI] [PubMed] [Google Scholar]
  16. Evans J. P., Kay B. K. Biochemical fractionation of oocytes. Methods Cell Biol. 1991;36:133–148. doi: 10.1016/s0091-679x(08)60275-7. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Good P. J., Richter K., Dawid I. B. A nervous system-specific isotype of the beta subunit of Na+,K(+)-ATPase expressed during early development of Xenopus laevis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9088–9092. doi: 10.1073/pnas.87.23.9088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Good P. J., Welch R. C., Barkan A., Somasekhar M. B., Mertz J. E. Both VP2 and VP3 are synthesized from each of the alternative spliced late 19S RNA species of simian virus 40. J Virol. 1988 Mar;62(3):944–953. doi: 10.1128/jvi.62.3.944-953.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Graf J. D., Kobel H. R. Genetics of Xenopus laevis. Methods Cell Biol. 1991;36:19–34. doi: 10.1016/s0091-679x(08)60270-8. [DOI] [PubMed] [Google Scholar]
  21. Haynes S. R., Johnson D., Raychaudhuri G., Beyer A. L. The Drosophila Hrb87F gene encodes a new member of the A and B hnRNP protein group. Nucleic Acids Res. 1991 Jan 11;19(1):25–31. doi: 10.1093/nar/19.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Haynes S. R., Raychaudhuri G., Beyer A. L. The Drosophila Hrb98DE locus encodes four protein isoforms homologous to the A1 protein of mammalian heterogeneous nuclear ribonucleoprotein complexes. Mol Cell Biol. 1990 Jan;10(1):316–323. doi: 10.1128/mcb.10.1.316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hovemann B. T., Dessen E., Mechler H., Mack E. Drosophila snRNP associated protein P11 which specifically binds to heat shock puff 93D reveals strong homology with hnRNP core protein A1. Nucleic Acids Res. 1991 Sep 25;19(18):4909–4914. doi: 10.1093/nar/19.18.4909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Iwasaki M., Okumura K., Kondo Y., Tanaka T., Igarashi H. cDNA cloning of a novel heterogeneous nuclear ribonucleoprotein gene homologue in Caenorhabditis elegans using hamster prion protein cDNA as a hybridization probe. Nucleic Acids Res. 1992 Aug 11;20(15):4001–4007. doi: 10.1093/nar/20.15.4001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kay B. K., Sawhney R. K., Wilson S. H. Potential for two isoforms of the A1 ribonucleoprotein in Xenopus laevis. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1367–1371. doi: 10.1073/pnas.87.4.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kay B. K. Xenopus laevis: Practical uses in cell and molecular biology. Injections of oocytes and embryos. Methods Cell Biol. 1991;36:663–669. [PubMed] [Google Scholar]
  27. 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]
  28. Kiledjian M., Dreyfuss G. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 1992 Jul;11(7):2655–2664. doi: 10.1002/j.1460-2075.1992.tb05331.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kim Y. J., Baker B. S. Isolation of RRM-type RNA-binding protein genes and the analysis of their relatedness by using a numerical approach. Mol Cell Biol. 1993 Jan;13(1):174–183. doi: 10.1128/mcb.13.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kolodziej P. A., Young R. A. Epitope tagging and protein surveillance. Methods Enzymol. 1991;194:508–519. doi: 10.1016/0076-6879(91)94038-e. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Lantz V., Ambrosio L., Schedl P. The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. Development. 1992 May;115(1):75–88. doi: 10.1242/dev.115.1.75. [DOI] [PubMed] [Google Scholar]
  33. Leser G. P., Escara-Wilke J., Martin T. E. Monoclonal antibodies to heterogeneous nuclear RNA-protein complexes. The core proteins comprise a conserved group of related polypeptides. J Biol Chem. 1984 Feb 10;259(3):1827–1833. [PubMed] [Google Scholar]
  34. Matunis E. L., Matunis M. J., Dreyfuss G. Characterization of the major hnRNP proteins from Drosophila melanogaster. J Cell Biol. 1992 Jan;116(2):257–269. doi: 10.1083/jcb.116.2.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Matunis M. J., Matunis E. L., Dreyfuss G. Isolation of hnRNP complexes from Drosophila melanogaster. J Cell Biol. 1992 Jan;116(2):245–255. doi: 10.1083/jcb.116.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Matunis M. J., Michael W. M., Dreyfuss G. Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol Cell Biol. 1992 Jan;12(1):164–171. doi: 10.1128/mcb.12.1.164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Mieszczak M., Klahre U., Levy J. H., Goodall G. J., Filipowicz W. Multiple plant RNA binding proteins identified by PCR: expression of cDNAs encoding RNA binding proteins targeted to chloroplasts in Nicotiana plumbaginifolia. Mol Gen Genet. 1992 Sep;234(3):390–400. doi: 10.1007/BF00538698. [DOI] [PubMed] [Google Scholar]
  39. Minoo P., Martin T. E., Riehl R. M. Nucleic acid binding characteristics of group A/B hnRNP proteins. Biochem Biophys Res Commun. 1991 Apr 30;176(2):747–755. doi: 10.1016/s0006-291x(05)80248-7. [DOI] [PubMed] [Google Scholar]
  40. Minoo P., Sullivan W., Solomon L. R., Martin T. E., Toft D. O., Scott R. E. Loss of proliferative potential during terminal differentiation coincides with the decreased abundance of a subset of heterogeneous ribonuclear proteins. J Cell Biol. 1989 Nov;109(5):1937–1946. doi: 10.1083/jcb.109.5.1937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nakagawa T. Y., Swanson M. S., Wold B. J., Dreyfuss G. Molecular cloning of cDNA for the nuclear ribonucleoprotein particle C proteins: a conserved gene family. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2007–2011. doi: 10.1073/pnas.83.7.2007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Piñol-Roma S., Dreyfuss G. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 1992 Feb 20;355(6362):730–732. doi: 10.1038/355730a0. [DOI] [PubMed] [Google Scholar]
  44. Piñol-Roma S., Dreyfuss G. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science. 1991 Jul 19;253(5017):312–314. doi: 10.1126/science.1857966. [DOI] [PubMed] [Google Scholar]
  45. Piñol-Roma S., Swanson M. S., Gall J. G., Dreyfuss G. A novel heterogeneous nuclear RNP protein with a unique distribution on nascent transcripts. J Cell Biol. 1989 Dec;109(6 Pt 1):2575–2587. doi: 10.1083/jcb.109.6.2575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Preugschat F., Wold B. Isolation and characterization of a Xenopus laevis C protein cDNA: structure and expression of a heterogeneous nuclear ribonucleoprotein core protein. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9669–9673. doi: 10.1073/pnas.85.24.9669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Richter K., Good P. J., Dawid I. B. A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. New Biol. 1990 Jun;2(6):556–565. [PubMed] [Google Scholar]
  48. Richter K., Grunz H., Dawid I. B. Gene expression in the embryonic nervous system of Xenopus laevis. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8086–8090. doi: 10.1073/pnas.85.21.8086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Robinow S., Campos A. R., Yao K. M., White K. The elav gene product of Drosophila, required in neurons, has three RNP consensus motifs. Science. 1988 Dec 16;242(4885):1570–1572. doi: 10.1126/science.3144044. [DOI] [PubMed] [Google Scholar]
  50. Swanson M. S., Dreyfuss G. Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol Cell Biol. 1988 May;8(5):2237–2241. doi: 10.1128/mcb.8.5.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Szabo A., Dalmau J., Manley G., Rosenfeld M., Wong E., Henson J., Posner J. B., Furneaux H. M. HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal. Cell. 1991 Oct 18;67(2):325–333. doi: 10.1016/0092-8674(91)90184-z. [DOI] [PubMed] [Google Scholar]
  52. Taira M., Jamrich M., Good P. J., Dawid I. B. The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev. 1992 Mar;6(3):356–366. doi: 10.1101/gad.6.3.356. [DOI] [PubMed] [Google Scholar]
  53. Wilusz J., Shenk T. A uridylate tract mediates efficient heterogeneous nuclear ribonucleoprotein C protein-RNA cross-linking and functionally substitutes for the downstream element of the polyadenylation signal. Mol Cell Biol. 1990 Dec;10(12):6397–6407. doi: 10.1128/mcb.10.12.6397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Zeller R., Nyffenegger T., De Robertis E. M. Nucleocytoplasmic distribution of snRNPs and stockpiled snRNA-binding proteins during oogenesis and early development in Xenopus laevis. Cell. 1983 Feb;32(2):425–434. doi: 10.1016/0092-8674(83)90462-2. [DOI] [PubMed] [Google Scholar]

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