Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Oct 1;25(19):3950–3954. doi: 10.1093/nar/25.19.3950

Growth-dependent and growth-independent translation of messengers for heterogeneous nuclear ribonucleoproteins.

O Camacho-Vanegas 1, F Weighardt 1, C Ghigna 1, F Amaldi 1, S Riva 1, G Biamonti 1
PMCID: PMC146965  PMID: 9380522

Abstract

The hnRNP A1 transcript has a relatively short 5'- untranslated region (UTR) starting with a pyrimidine tract similar to that of mRNAs encoded by the TOP [terminal oligo(pyrimidine)] genes in vertebrates. Such genes code for ribosomal proteins and for other proteins directly or indirectly involved in the production and function of the translation apparatus. As expected from the role of the pyrimidine tract in the translational regulation of TOP mRNAs, the A1 mRNA is more efficiently loaded onto polysomes in growing than in resting cells. On the other hand, a less stringent regulation with respect to that of other TOP mRNAs is observed, partially due to the presence of multiple transcription start sites within the pyrimidine tract, where transcripts with shorter TOP sequences are less sensitive to regulation. Thus, from the point of view of structural features and translation behaviour the A1 mRNA can be included in the class of TOP genes, suggesting a possible role of A1 in translation. Interestingly, a TOP-like behaviour was observed for hnRNP I mRNA but not for hnRNP C1/C2 and A2/B1 mRNAs, indicating the existence of two classes of hnRNPs with different translational regulation.

Full Text

The Full Text of this article is available as a PDF (208.4 KB).

Selected References

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

  1. Amaldi F., Pierandrei-Amaldi P. TOP genes: a translationally controlled class of genes including those coding for ribosomal proteins. Prog Mol Subcell Biol. 1997;18:1–17. doi: 10.1007/978-3-642-60471-3_1. [DOI] [PubMed] [Google Scholar]
  2. Bagni C., Mariottini P., Annesi F., Amaldi F. Human ribosomal protein L4: cloning and sequencing of the cDNA and primary structure of the protein. Biochim Biophys Acta. 1993 Dec 14;1216(3):475–478. doi: 10.1016/0167-4781(93)90017-8. [DOI] [PubMed] [Google Scholar]
  3. Bagni C., Mariottini P., Terrenato L., Amaldi F. Individual variability in the translational regulation of ribosomal protein synthesis in Xenopus laevis. Mol Gen Genet. 1992 Jul;234(1):60–64. doi: 10.1007/BF00272345. [DOI] [PubMed] [Google Scholar]
  4. Biamonti G., Bassi M. T., Cartegni L., Mechta F., Buvoli M., Cobianchi F., Riva S. Human hnRNP protein A1 gene expression. Structural and functional characterization of the promoter. J Mol Biol. 1993 Mar 5;230(1):77–89. doi: 10.1006/jmbi.1993.1127. [DOI] [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. 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]
  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. Caizergues-Ferrer M., Mariottini P., Curie C., Lapeyre B., Gas N., Amalric F., Amaldi F. Nucleolin from Xenopus laevis: cDNA cloning and expression during development. Genes Dev. 1989 Mar;3(3):324–333. doi: 10.1101/gad.3.3.324. [DOI] [PubMed] [Google Scholar]
  10. Camacho-Vanegas O., Loreni F., Amaldi F. Flat absorbance background for sucrose gradients. Anal Biochem. 1995 Jun 10;228(1):172–173. doi: 10.1006/abio.1995.1332. [DOI] [PubMed] [Google Scholar]
  11. Celis J. E., Bravo R., Arenstorf H. P., LeStourgeon W. M. Identification of proliferation-sensitive human proteins amongst components of the 40 S hnRNP particles. Identity of hnRNP core proteins in the HeLa protein catalogue. FEBS Lett. 1986 Jan 1;194(1):101–109. doi: 10.1016/0014-5793(86)80059-x. [DOI] [PubMed] [Google Scholar]
  12. Cleveland D. W., Lopata M. A., MacDonald R. J., Cowan N. J., Rutter W. J., Kirschner M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. doi: 10.1016/0092-8674(80)90238-x. [DOI] [PubMed] [Google Scholar]
  13. Conway G., Wooley J., Bibring T., LeStourgeon W. M. Ribonucleoproteins package 700 nucleotides of pre-mRNA into a repeating array of regular particles. Mol Cell Biol. 1988 Jul;8(7):2884–2895. doi: 10.1128/mcb.8.7.2884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Geyer P. K., Meyuhas O., Perry R. P., Johnson L. F. Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol Cell Biol. 1982 Jun;2(6):685–693. doi: 10.1128/mcb.2.6.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kaspar R. L., Kakegawa T., Cranston H., Morris D. R., White M. W. A regulatory cis element and a specific binding factor involved in the mitogenic control of murine ribosomal protein L32 translation. J Biol Chem. 1992 Jan 5;267(1):508–514. [PubMed] [Google Scholar]
  18. LeStourgeon W. M., Beyer A. L., Christensen M. E., Walker B. W., Poupore S. M., Daniels L. P. The packaging proteins of core hnRNP particles and the maintenance of proliferative cell states. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):885–898. doi: 10.1101/sqb.1978.042.01.090. [DOI] [PubMed] [Google Scholar]
  19. Leser G. P., Martin T. E. Changes in heterogeneous nuclear RNP core polypeptide complements during the cell cycle. J Cell Biol. 1987 Nov;105(5):2083–2094. doi: 10.1083/jcb.105.5.2083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Loreni F., Amaldi F. Translational regulation of ribosomal protein synthesis in Xenopus cultured cells: mRNA relocation between polysomes and RNP during nutritional shifts. Eur J Biochem. 1992 May 1;205(3):1027–1032. doi: 10.1111/j.1432-1033.1992.tb16870.x. [DOI] [PubMed] [Google Scholar]
  21. Lothstein L., Arenstorf H. P., Chung S. Y., Walker B. W., Wooley J. C., LeStourgeon W. M. General organization of protein in HeLa 40S nuclear ribonucleoprotein particles. J Cell Biol. 1985 May;100(5):1570–1581. doi: 10.1083/jcb.100.5.1570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Mayeda A., Munroe S. H., Cáceres J. F., Krainer A. R. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 1994 Nov 15;13(22):5483–5495. doi: 10.1002/j.1460-2075.1994.tb06883.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Michael W. M., Choi M., Dreyfuss G. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 1995 Nov 3;83(3):415–422. doi: 10.1016/0092-8674(95)90119-1. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Nakielny S., Dreyfuss G. The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J Cell Biol. 1996 Sep;134(6):1365–1373. doi: 10.1083/jcb.134.6.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peters K. E., Commings D. E. Two-dimensinal gel electrophoresis of rat liver nuclear washes, nuclear matrix, and hnRNA proteins. J Cell Biol. 1980 Jul;86(1):135–155. doi: 10.1083/jcb.86.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Piñol-Roma S., Dreyfuss G. hnRNP proteins: localization and transport between the nucleus and the cytoplasm. Trends Cell Biol. 1993 May;3(5):151–155. doi: 10.1016/0962-8924(93)90135-n. [DOI] [PubMed] [Google Scholar]
  29. Pollard V. W., Michael W. M., Nakielny S., Siomi M. C., Wang F., Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell. 1996 Sep 20;86(6):985–994. doi: 10.1016/s0092-8674(00)80173-7. [DOI] [PubMed] [Google Scholar]
  30. Svitkin Y. V., Ovchinnikov L. P., Dreyfuss G., Sonenberg N. General RNA binding proteins render translation cap dependent. EMBO J. 1996 Dec 16;15(24):7147–7155. [PMC free article] [PubMed] [Google Scholar]
  31. Visa N., Alzhanova-Ericsson A. T., Sun X., Kiseleva E., Björkroth B., Wurtz T., Daneholt B. A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell. 1996 Jan 26;84(2):253–264. doi: 10.1016/s0092-8674(00)80980-0. [DOI] [PubMed] [Google Scholar]
  32. Weighardt F., Biamonti G., Riva S. Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. J Cell Sci. 1995 Feb;108(Pt 2):545–555. doi: 10.1242/jcs.108.2.545. [DOI] [PubMed] [Google Scholar]
  33. Weighardt F., Biamonti G., Riva S. The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism. Bioessays. 1996 Sep;18(9):747–756. doi: 10.1002/bies.950180910. [DOI] [PubMed] [Google Scholar]
  34. Wilk H. E., Werr H., Friedrich D., Kiltz H. H., Schäfer K. P. The core proteins of 35S hnRNP complexes. Characterization of nine different species. Eur J Biochem. 1985 Jan 2;146(1):71–81. doi: 10.1111/j.1432-1033.1985.tb08621.x. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES