Skip to main content
SpringerLink
Log in

Control of Ribosomal Protein Synthesis in Eukaryotic Cells

  • Chapter
Translational Regulation of Gene Expression 2

Abstract

Ribosomal assembly requires three or four separate ribosomal RNA (rRNA) molecules as well as ~50–80 ribosomal proteins (r-proteins); the exact numbers depend on the species (reviewed in Wool1). These components comprise a large portion of the total cellular RNA and protein and are synthesized in roughly equimolar amounts which are rapidly assembled into ribosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Wool, I. G., 1979, The structure and function ofeukaryotic ribosomes, Annu. Rev. Biochem. 48: 719–754.

    Article  PubMed  CAS  Google Scholar 

  2. Nomura, M., Gourse, R., and Baughman, G., 1984, Regulation of thesynthesis of ribosomes and ribosome components, Annu. Rev. Biochem. 53:75–117.

    Article  PubMed  CAS  Google Scholar 

  3. Lindahl, L.,Archer, R., and Zengel, J. M., 1983, Transcription of the S10 ribosomal proteinoperon is regulated by an attenuator in the leader, Cell 33:241–248.

    Article  PubMed  CAS  Google Scholar 

  4. Amaldi, F.,Bozzoni, I., Beccari, E., and Pierandrei-Amaldi, P., 1989, Expression ofribosomal protein genes and regulation ofribosome biosynthesis in Xenopus development, Trends Biochem. Sci.14:175–178.

    Article  PubMed  CAS  Google Scholar 

  5. Bowman, L. H.,1987, The synthesis of ribosomal proteins S16 and L32 is not autogenouslyregulated during mouse myoblast differentiation, Mol. Cell. Biol.7:4464–4471.

    PubMed  CAS  Google Scholar 

  6. Warner, J., 1989, Synthesis of ribosomes in Saccharomycescerevisiae, Microbiol. Rev. 53:256–271.

    PubMed  CAS  Google Scholar 

  7. Lucioli, A.Presutti, C., Ciafre, S., Caffarelli, E., Fragapane, P., and Bozzoni, I., 1988,Gene dosage alteration of L2 ribosomalprotein genes in Saccharomyces cerevisiae: Effects on ribosome synthesis,Mol. Cell. Biol. 8:4792–4798.

    PubMed  CAS  Google Scholar 

  8. El-Baradi, T. T.,van der Sande, C. A., Mager, W. H., Raue, H. A., and Planta, R. J., 1986, Thecellular level of yeast ribosomal protein L25 is controlled principally byrapid degradation of excess protein, Curr. Genet. 10:733–739.

    Article  CAS  Google Scholar 

  9. Maicas, E., Pluthero, F. G., and Friesen, J. D., 1988, The accumulationof three yeast ribosomal proteinsunder conditions of excess mRNA is determined primarily by fast protein decay, Mol.Cell. Biol. 8:169–175.

    PubMed  CAS  Google Scholar 

  10. Tsay, Y., Thompson, J. R., Rotenberg, M. O., Larkin, J. C., andWoolford, J. L., 1988, Ribosomal protein synthesisis not regulated at the translational level in Saccharomyces cerevisiae: Balancedaccumulation of ribosomal proteins L16 and rp59 is mediatedby turnover of excess protein, Genes Dev. 2:664–676.

    Article  PubMed  CAS  Google Scholar 

  11. Wormington, W. M., 1988, Expression of ribosomalprotein gene during Xenopus development, in: Developmental Biology: A Comprehensive Synthesis, Volume 5(L. E. Browder, ed.), pp. 227–240, Plenum Press, New York.

    Google Scholar 

  12. Agrawal,M. G., and Bowman, L. H., 1987, Transcriptional and translational regulation ofribosomal protein formation during mouse myoblast differentiation, J. Biol.Chem. 262:4868–4875.

    PubMed  CAS  Google Scholar 

  13. Kaspar, R. L., Kakegawa, T., Cranston, H.,Morris, D. R., and White, M. W., 1992, A regulatory cis element and aspecific binding factor involved in the mitogenic control of murine ribosomal proteinL32 translation, J. Biol. Chem. 267:508–514.

    PubMed  CAS  Google Scholar 

  14. DePhilip,R. M., Rudert, W. A., and Lieberman, I., 1980, Preferential stimulation ofribosomal protein synthesis by insulin and in the absence of ribosomal andmessenger ribonucleic acid formation, Biochemistry 19:1662–1669.

    Article  PubMed  CAS  Google Scholar 

  15. Geyer,P. K., Meyuhas, O., Perry, R. P., and Johnson, L. F., 1982, Regulation ofribosomal protein mRNA content andtranslation in growth-stimulated mouse fibroblasts, Mol. Cell. Biol. 2: 685–693.

    PubMed  CAS  Google Scholar 

  16. Tushinski, R. J., and Warner, J. R., 1982, Ribosomal proteinsare synthesized preferentially in cells commencing growth, J. Cell. Physiol. 112:128–135.

    Article  PubMed  CAS  Google Scholar 

  17. Kaspar, R.L., Rychlik, W., White, M. W., Rhoads, R. E., and Morris, D. R., 1990,Simultaneous cytoplasmic redistribution of ribosomal protein L32 mRNA andphosphorylation of eukaryotic initiation factor 4E aftermitogenic stimulation of Swiss 3T3 cells, J. Biol. Chem. 265:3619–3622.

    PubMed  CAS  Google Scholar 

  18. Meyuhas,O., Thompson, E. A., and Perry, R. P., 1987, Glucocorticoids selectivelyinhibit translation of ribosomal proteinmRNAs in P1798 lymphosarcoma cells, Mol. Cell. Biol. 7:2691–2699.

    PubMed  CAS  Google Scholar 

  19. Mariottini, P., and Amaldi,F., 1990, The 5’ untranslated region of mRNA for ribosomal protein S19 is involved in its translational regulationduring Xenopus development, Mol. Cell. Biol. 10: 816–822.

    PubMed  CAS  Google Scholar 

  20. Levy, S., Avni,D., Hariharan, N., Perry, R. P., and Meyuhas, O., 1991, Oligopyrimidine tract at the 5’ end of mammalian ribosomal proteinmRNAs is required for their translational control, Proc. Natl. Acad.Sci. USA 88:3319–3323.

    Article  PubMed  CAS  Google Scholar 

  21. Hammond, M. L., Merrick, W., and Bowman, L. H., 1991, Sequencesmediating the translation of mouse S16 ribosomal proteinmRNA during myoblast differentiation and in vitro and possible control pointsfor the in vitro translation, Genes Dev. 5:1723–1736.

    Article  PubMed  CAS  Google Scholar 

  22. Wagner, M., and Perry, R. P., 1985, Characterization of the multigenefamily encoding the mouse S16 ribosomal protein: Strategy for distinguishing anexpressed gene from its processed pseudogene counterparts by an analysis oftotal genomic DNA, Mol. Cell. Biol. 5:3560–3576.

    PubMed  CAS  Google Scholar 

  23. Dudov, K. P., and Perry, R. P., 1984, The gene family encoding the mouseribosomal protein L32 contains a uniquely expressed intron-containing gene andan unmutated processed gene, Cell 37: 457–468.

    Article  PubMed  CAS  Google Scholar 

  24. Wiedemann, L. M., and Perry, R. P., 1984,Characterization of the expressed gene and several processed pseudogenes for the mouse ribosomalprotein L32 gene family, Mol. Cell. Biol. 4:2518–2528.

    PubMed  CAS  Google Scholar 

  25. Wool, I. G., Endo, Y., Chan, Y. L., and Gluck, A., 1990, Structure,function, and evolution of mammalian ribosomes, in: The Structure, Functionand Evolution of Ribosomes (W. E. Hill, ed.), pp 203–214, AmericanSociety for Microbiology, Washington, D.C.

    Google Scholar 

  26. Mariottini, P., Bagni, C., Annesi, F., and Amaldi, F., 1988, Isolationand nucleotide sequences of cDNAs for Xenopus laevis ribosomal proteinS8: Similarities in the 5’ and 3’ untranslated regions of mRNAs forvarious r-proteins, Gene 67:69–74.

    Article  PubMed  CAS  Google Scholar 

  27. Hariharan, N., and Perry, R. P., 1990, Functional dissection of mouseribosomal protein promoter: Significance of the polypyrimidine initiator and anelement in the TATA-box region, Proc. Natl. Acad. Sci. USA 87:1526–1530.

    Article  PubMed  CAS  Google Scholar 

  28. Yenofsky, R., Cereghini, S., Krowczynska, A., and Brawerman, G., 1983,Regulation of mRNA utilizationin mouse erythroleukemia cells induced to differentiate by exposure to dimethylsulfoxide, Mol. Cell. Biol. 3:1197–1203.

    PubMed  CAS  Google Scholar 

  29. Chitpatima, S.T., Makrides, S., Bandyopadhyay, R., and Brawerman, G., 1988, Nucleotidesequence of a major messenger RNA for a 21 kilodalton polypeptide that is undertranslational control in mouse tumor cells, Nucleic Acids Res. 16:2350.

    Article  PubMed  CAS  Google Scholar 

  30. Kerfelec, B.,LaForge, K. S., Vasiloudes, P., Puigserver, A., and Scheele, G. A., 1990,Isolation and sequence of the canine pancreatic phospholipase A2gene, Eur. J. Biochem. 190:299–304.

    Article  PubMed  CAS  Google Scholar 

  31. Pinsky, S. D.,LaForge, K. S., and Scheele, G., 1985, Differential regulation of trypsinogen mRNA translation: Full length mRNA sequencesencoding two oppositely charge trypsinogen isoenzymes in the dogpancreas, Mol. Cell. Biol. 5:2669–2676.

    PubMed  CAS  Google Scholar 

  32. Makrides, S.,Chitpatima, S., Bandyopadhyay, R., and Brawerman. G., 1988, Nucleotide sequence for a major messenger RNA for a 40kilodalton polypeptide that is under translational control in mousetumor cells, Nucleic Acids Res. 16:2349.

    Article  PubMed  CAS  Google Scholar 

  33. Leibold, E. A., and Munro, H. N., 1988, Cytoplasmic protein binds invitro to a highly conserved sequence in the 5’ untranslated region of ferritinheavy- and light-subunit mRNAs, Proc. Natl. Acad. Sci. USA 85:2171–2175.

    Article  PubMed  CAS  Google Scholar 

  34. Klausner, R. D.,and Harford, J. B., 1989, Cis-trans models for posttranscriptional generegulation, Science 246: 870–872.

    Article  PubMed  CAS  Google Scholar 

  35. Garcia-Blanco, M. A., Jamison, S. F., and Sharp, P. A., 1989,Identification and purification of a 62,000-daltonprotein that binds specifically to the polypyrimidine tract of introns, GenesDev. 3: 1874–1886.

    Article  CAS  Google Scholar 

  36. Zamore, P. D., and Green, M. R., 1989,Identification, purification, and biochemical characterization of U2 small nuclear ribonucleoproteinauxiliary factor, Proc. Natl. Acad. Sci. USA 86:9243–9247.

    Article  PubMed  CAS  Google Scholar 

  37. Kuhn, R., Luz, N., and Beck,E., 1990, Functional analysis of the internal translation initiation site offoot-and-mouth disease virus, J. Virol. 64:4625–4631.

    PubMed  CAS  Google Scholar 

  38. Jang, S. K., and Wimmer, E., 1990, Cap-independent translation ofencephalomyocarditis virus RNA: Structural elements of theinternal ribosomal entry site and involvement of a cellular 57-kD RNA-bindingprotein, Genes Dev. 4:1560–1572.

    Article  PubMed  CAS  Google Scholar 

  39. Nicholson, R., Pelletier, J., Le, S., and Sonenberg, N., 1991,Structural and functional analysis of the ribosome landing pad of poliovirus: Invivo translation studies, J. Virol. 65:5886–5894.

    PubMed  CAS  Google Scholar 

  40. Meerovitch, K.,Pelletier, J., and Sonenberg, N., 1989, A cellular protein that binds to the 5-noncoding region of poliovirus RNA:Implications for internal translation initiation, Genes Dev. 3:1026–1034.

    Article  PubMed  CAS  Google Scholar 

  41. Hershey, J. W.B., 1991, Translational control in mammalian cells, Annu. Rev. Biochem. 60:717–755.

    Article  PubMed  CAS  Google Scholar 

  42. Lodish, H. F.,1974, Model for the regulation of mRNA translation applied to haemoglobinsynthesis, Nature 251:385–388.

    Article  PubMed  CAS  Google Scholar 

  43. Lodish,H. F., 1976, Translational control of protein synthesis, Annu. Rev. Biochem.45:39–72.

    Article  PubMed  CAS  Google Scholar 

  44. Godefroy-Colburn,T., and Thach, R. E., 1981, The role of mRNA competition in regulatingtranslation, J. Biol. Chem. 256:11762–11773.

    PubMed  CAS  Google Scholar 

  45. Lodish, H. F., 1971, Alpha and beta globinmessenger ribonucleic acid, J. Biol. Chem. 246:7131–7138.

    PubMed  CAS  Google Scholar 

  46. White, M. W., Kameji, T., Pegg, A.E., and Morris, D. R., 1987, Increased efficiency of translation of ornithine decarboxylase mRNA in mitogen-activatedlymphocytes, Eur. J. Biochem. 170:87–92.

    Article  PubMed  CAS  Google Scholar 

  47. Jacobs-Lorena,M., and Fried, H. M., 1987, Translational regulation of ribosomal protein gene expression in eukaryotes, in: TranslationalRegulation of Gene Expression (J. Ilan, ed.), pp. 63–85, PlenumPress, New York.

    Chapter  Google Scholar 

  48. Itoh, N., Ohta,K., Ohta, M., Kawasaki, T., and Yamashina, I., 1989, The nucleotide sequence ofa gene for a putative ribosomal protein S31 of Drosophila, Nucleic AcidsRes. 17:2121.

    Article  CAS  Google Scholar 

  49. Qian, S., Zhang,J., Kay, M. A., and Jacobs-Lorena, M., 1987, Structural analysis of the Drosophila rpAl gene, a member of the eucryotic A type ribosomal protein family, NucleicAcids Res. 15:987–1003.

    Article  CAS  Google Scholar 

  50. Steel, L. F., and Jacobson, A., 1987, Translational control ofribosomal protein synthesis during early Dictyostelium discodeum development,Mol. Cell. Biol. 7:965–972.

    PubMed  CAS  Google Scholar 

  51. Steel, L. F., and Jacobson, A., 1991, Sequence elements that affect mRNAtranslational activity in developingDictyostelium cells, Dev. Genet. 12:98–103.

    Article  PubMed  CAS  Google Scholar 

  52. Steel, L. F., Smyth, A., and Jacobson, A., 1987, Nucleotide sequenceand characterization of the transcript of a Dictyostelium ribosomalprotein gene, Nucleic Acids Res. 15:10285–10298.

    Article  PubMed  CAS  Google Scholar 

  53. Kim, C. H., and Warner, J. R., 1983, The mRNA for ribosomal proteins inyeast, J. Mol. Biol. 165: 79–89.

    Article  PubMed  CAS  Google Scholar 

  54. Maicas, E., and Friesen, J. D., 1990, A sequence pattern that occurs atthe transcription initiation region of yeast RNA polymerase II promoters, NucleicAcids Res. 18:3387–3393.

    Article  CAS  Google Scholar 

  55. Warner, J. R., and Gorenstein, C., 1977, The synthesis of eukaryoticribosomal proteins in vitro, Cell 11:201–212.

    Article  PubMed  CAS  Google Scholar 

  56. Donovan, D. M., and Pearson, N. J., 1986,Transcriptional regulation of ribosomal proteins during a nutritionalupshift in Saccharomyces cerevisiae, Mol. Cell. Biol. 6:2429–2435.

    PubMed  CAS  Google Scholar 

  57. Mager, W. H., and Planta, R. J., 1990 Multifunctional DNA-bindingproteins mediate concerted transcription activation of yeast ribosomal proteingenes, Biochim. Biophys. Acta 1050:351–355.

    Article  PubMed  CAS  Google Scholar 

  58. Rotenberg, M. O., and Woolford, J. L., 1986, Tripartite upstreampromoter element essential for expression of Saccharomyces cerevisiae ribosomalprotein genes, Mol. Cell. Biol. 6:674–687.

    PubMed  CAS  Google Scholar 

  59. Mager, W. H., 1988, Control of ribosomal protein gene expression, Biochim.Biophys. Acta 949:1–15.

    Article  PubMed  CAS  Google Scholar 

  60. Huet, J.,Cottrelle, P., Cool, M., Vignais, M. L., Thiele, D., Marck, C., Buhler, J. M.,Sentenac, A., and Fromageot, P., 1985, Ageneral upstream binding factor for genes of the yeast translational apparatus,EMBO J. 4:3539–3547.

    PubMed  CAS  Google Scholar 

  61. Vignais,M. L., Woudt, L. P., Wassenaar, G. M., Mager, W.H., Sentenac, A., and Planta,R. J., 1987, Specific binding of TUF factorto upstream activation sites of yeast ribosomal protein genes, EMBOJ. 6:1451–1457.

    CAS  Google Scholar 

  62. Shore, D.,Stillman, D. J., Brand, A. H., and Nasmyth, K. A., 1987, Identification ofsilencer binding proteins from yeast: Possible roles in SIR control and DNAreplication, EMBO J. 6: 461–467.

    PubMed  CAS  Google Scholar 

  63. Shore,D., and Nasmyth, K. A., 1987, Purification and cloning of a DNA-binding proteinthat binds to both silencer and activator elements, Cell 51:721–732.

    Article  PubMed  CAS  Google Scholar 

  64. Herruer, M. H., Mager, W. H., Doorenbosch, T. M., Wessels, P. L.,Wassenaar, T. M., and Planta, R. J., 1989, The extended promoter of theencoding ribosomal protein S33 in yeasts consists of multiple bindingelements, Nucleic Acids Res. 17:1421–1439.

    Article  Google Scholar 

  65. Hamil, K. G., Nam, H. G., and Fried, H. M., 1988, Constitutivetranscription of yeast ribosomal protein gene TCM1is promoted by uncommon cis- and trans-acting elements, Mol.Cell. Biol. 8: 4328–4341.

    PubMed  CAS  Google Scholar 

  66. Rhode, P. R., Sweder, K. S., Oegema, K. F., andCampbell, J. L., 1989, The gene encoding ARS-binding factor 1 isessential for the viability of yeast, Genes Dev. 3:1926–1939.

    Article  PubMed  CAS  Google Scholar 

  67. Halfter, H.,Kavety, B., Vandekerckhove, J., Kiefer, F., and Gallwitz, D., 1989, Sequence, expression and mutational analysis of BAF1, atranscriptional activator and ARSl-binding protein of the yeast Saccharomycescerevisiae, EMBO J. 8:4265–4272.

    PubMed  CAS  Google Scholar 

  68. Diffley, J. F., and Stillman, B., 1989, Similaritybetween the transcriptional silencer proteins ABF1 and RAP1, Science246:1034–1038.

    Article  PubMed  CAS  Google Scholar 

  69. Buchman, A. R., Kimmerly, W. J., Rine, J., and Kornberg,R. D., 1988, Two DNA-binding factors recognize specificsequences at silencers, upstream activating sequences, autonomously replicating sequences,and telomeres in Saccharomyces cerevisiae, Mol. Cell. Biol. 8:210–225.

    PubMed  CAS  Google Scholar 

  70. Diffley, J. F., and Stillman, B., 1988, Purification ofa yeast protein that binds to origins of DNA replication and a transcriptionalsilencer, Proc. Natl. Acad. Sci. USA 85:2120–2124.

    Article  PubMed  CAS  Google Scholar 

  71. Seta, F. D.,Ciafre, S. A., Marck, C., Santoro, B., Presutti, C., Sentenac, A., and Bozzoni,I., 1990, The ABF1 factor is thetranscriptional activator of the L2 ribosomal protein genes in Saccharomycescerevisiae, Mol. Cell. Biol. 10:2437–2441.

    PubMed  Google Scholar 

  72. Hariharan, N., and Perry, R. P., 1989, A characterization of theelements comprising the promoter of the mouse ribosomal protein geneRPS16, Nucleic Acids Res. 17:5323–5337.

    Article  PubMed  CAS  Google Scholar 

  73. Dudov, K. P., andPerry, R. P., 1986, Properties of a mouse ribosomal protein promoter, Proc.Natl. Acad. Sci. USA 83:8545–8549.

    Article  PubMed  CAS  Google Scholar 

  74. Moura-Neto, R., Dudov, K. P., and Perry, R. P., 1989, An elementdownstream of the cap site is required for transcription of the gene encodingmouse ribosomal protein L32, Proc. Natl. Acad. Sci. USA 86:3997–4001.

    Article  PubMed  CAS  Google Scholar 

  75. Chung, S., and Perry, R. P., 1989, Importance of introns for expressionof mouse ribosomal protein gene rpL32, Mol. Cell. Biol. 9:2075–2082.

    PubMed  CAS  Google Scholar 

  76. Atchison, M. L., Meyuhas, O., and Perry, R. P., 1989, Localization oftranscriptional regulatory elements and nuclear factorbinding sites in mouse ribosomal protein gene rpL32, Mol. Cell. Biol. 9:2067–2074.

    PubMed  CAS  Google Scholar 

  77. Dabeva,M. D., Post-Beittenmiller, M. A., and Warner, J. R., 1986, Autogenousregulation of splicing of the transcript ofa yeast ribosomal protein gene, Proc. Natl. Acad. Sci. USA 83:5854–5857.

    Article  PubMed  CAS  Google Scholar 

  78. Wittekind, M., Kolb, J.M., Dodd, J., Yamagishi, M., Memet, S., Buhler, J., and Nomura, M, 1990, Conditional expression of RPA190, the geneencoding the largest subunit of yeast RNA polymerase I: Effects ofdecreased rRNA synthesis on ribosomal protein synthesis, Mol. Cell. Biol. 10:2049–2059.

    PubMed  CAS  Google Scholar 

  79. Eng, F. J., andWarner, J. R., 1991, Structural basis for the regulation of splicing of a yeastmessenger RNA, Cell 65:797–804.

    Article  PubMed  CAS  Google Scholar 

  80. Bozzoni, I., Fragapane, P., Annesi, F., Pierandrei-Amaldi, P., Amaldi,F., and Beccari, E., 1984, Expression of two Xenopus laevis ribosomalprotein genes in injected frog oocytes. A specific splicing blockinterferes with the L1 RNA maturation, J. Mol. Biol. 180:987–1005.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Washington, Seattle, Washington, 98133, USA

    Roger L. Kaspar & David R. Morris

  2. Department of Veterinary Molecular Biology, Montana State University, Bozeman, Montana, 59717, USA

    Michael W. White

Authors
  1. Roger L. Kaspar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David R. Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael W. White
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute of Pathology, Case Western Reserve University School of Medicine, Cleveland, Ohio, 44106, USA

    Joseph Ilan

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer Science+Business Media New York

About this chapter

Cite this chapter

Kaspar, R.L., Morris, D.R., White, M.W. (1993). Control of Ribosomal Protein Synthesis in Eukaryotic Cells. In: Ilan, J. (eds) Translational Regulation of Gene Expression 2. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2894-4_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-2894-4_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6254-8

  • Online ISBN: 978-1-4615-2894-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation