Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1985 Dec;5(12):3583–3592. doi: 10.1128/mcb.5.12.3583

Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster.

M A Kay, M Jacobs-Lorena
PMCID: PMC369189  PMID: 3939320

Abstract

We have previously characterized a cloned cDNA coding for a developmentally regulated mRNA in Drosophila melanogaster whose expression is selectively regulated at the translational level during oogenesis and embryogenesis. In this report we show that this translationally regulated mRNA (rpA1) codes for an acidic ribosomal protein. Furthermore, our results indicate that most ribosomal protein mRNAs are regulated similarly to rpA1 mRNA. This conclusion is based on cell-free translation of mRNAs derived from polysomes and postpolysomal supernatants as well as in vivo labeling experiments. Thus, the translation of many ribosomal protein mRNAs appears to be temporally related to the synthesis of rRNA during D. melanogaster development. The relationship between rRNA transcription and ribosomal protein mRNA translation was further investigated by genetically reducing rRNA synthesis with the use of bobbed mutants. Unexpectedly, neither ribosomal protein mRNA abundance nor translation was altered in these mutants.

Full text

PDF
3583

Images in this article

3585Image
on p.3585
3586Image
on p.3586
3587Image
on p.3587
3588Image
on p.3588
3588Image
on p.3588
3589Image
on p.3589
3590Image
on p.3590

Selected References

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

  1. Al-Atia G. R., Fruscoloni P., Jacobs-Lorena M. Translational regulation of mRNAs for ribosomal proteins during early Drosophila development. Biochemistry. 1985 Oct 8;24(21):5798–5803. doi: 10.1021/bi00342a017. [DOI] [PubMed] [Google Scholar]
  2. Anderson K. V., Lengyel J. A. Changing rates of histone mRNA synthesis and turnover in Drosophila embryos. Cell. 1980 Oct;21(3):717–727. doi: 10.1016/0092-8674(80)90435-3. [DOI] [PubMed] [Google Scholar]
  3. Anderson K. V., Lengyel J. A. Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol. 1979 May;70(1):217–231. doi: 10.1016/0012-1606(79)90018-6. [DOI] [PubMed] [Google Scholar]
  4. Ballinger D. G., Pardue M. L. The control of protein synthesis during heat shock in Drosophila cells involves altered polypeptide elongation rates. Cell. 1983 May;33(1):103–113. doi: 10.1016/0092-8674(83)90339-2. [DOI] [PubMed] [Google Scholar]
  5. Baughman G., Nomura M. Translational regulation of the L11 ribosomal protein operon of Escherichia coli: analysis of the mRNA target site using oligonucleotide-directed mutagenesis. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5389–5393. doi: 10.1073/pnas.81.17.5389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chamberlain J. P. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal Biochem. 1979 Sep 15;98(1):132–135. doi: 10.1016/0003-2697(79)90716-4. [DOI] [PubMed] [Google Scholar]
  7. Chooi W. Y. A comparison of the ribosomal proteins of Drosophila ovary, adult, and embryo. Mol Gen Genet. 1981;184(3):342–346. doi: 10.1007/BF00352502. [DOI] [PubMed] [Google Scholar]
  8. Chooi W. Y., James S. M., Burns D. K. Decrease in ribosomal proteins 1, 2/3, L4, and L7 in Drosophila melanogaster in the absence of X rDNA. Mol Gen Genet. 1982;187(3):364–369. doi: 10.1007/BF00332613. [DOI] [PubMed] [Google Scholar]
  9. Chooi W. Y., Sabatini L. M., Macklin M., Fraser D. Group fractionation and determination of the number of ribosomal subunit proteins from Drosophila melanogaster embryos. Biochemistry. 1980 Apr 1;19(7):1425–1433. doi: 10.1021/bi00548a025. [DOI] [PubMed] [Google Scholar]
  10. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  11. Faust C. H., Jr, Diggelmann H., Mach B. Isolation of poly(adenylic acid)-rich ribonucleic acid from mouse myeloma and synthesis of complementary deoxyribonucleic acid. Biochemistry. 1973 Feb 27;12(5):925–931. doi: 10.1021/bi00729a021. [DOI] [PubMed] [Google Scholar]
  12. Fruscoloni P., Al-Atia G. R., Jacobs-Lorena M. Translational regulation of a specific gene during oogenesis and embryogenesis of Drosophila. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3359–3363. doi: 10.1073/pnas.80.11.3359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fyrberg E. A., Kindle K. L., Davidson N., Kindle K. L. The actin genes of Drosophila: a dispersed multigene family. Cell. 1980 Feb;19(2):365–378. doi: 10.1016/0092-8674(80)90511-5. [DOI] [PubMed] [Google Scholar]
  14. Gorenstein C., Warner J. R. Coordinate regulation of the synthesis of eukaryotic ribosomal proteins. Proc Natl Acad Sci U S A. 1976 May;73(5):1547–1551. doi: 10.1073/pnas.73.5.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LaMarca M. J., Wassarman P. M. Program of early development in the mammal: changes in absolute rates of synthesis of ribosomal proteins during oogenesis and early embryogenesis in the mouse. Dev Biol. 1979 Nov;73(1):103–119. doi: 10.1016/0012-1606(79)90141-6. [DOI] [PubMed] [Google Scholar]
  16. LaMarca M. J., Wassarman P. M. Relationship between rates of synthesis and intracellular distribution of ribosomal proteins during oogenesis in the mouse. Dev Biol. 1984 Apr;102(2):525–530. doi: 10.1016/0012-1606(84)90221-5. [DOI] [PubMed] [Google Scholar]
  17. Lambertsson A. G. The ribosomal proteins of drosophila melanogaster. IV. Characterization by two-dimensional gel electrophoresis of the ribosomal proteins from nine postembryonic developmental stages. Mol Gen Genet. 1975 Aug 5;139(2):133–144. [PubMed] [Google Scholar]
  18. Lastick S. M., McConkey E. H. Exchange and stability of HeLa ribosomal proteins in vivo. J Biol Chem. 1976 May 25;251(10):2867–2875. [PubMed] [Google Scholar]
  19. Lifton R. P., Goldberg M. L., Karp R. W., Hogness D. S. The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1047–1051. doi: 10.1101/sqb.1978.042.01.105. [DOI] [PubMed] [Google Scholar]
  20. Lindahl L., Zengel J. M. Expression of ribosomal genes in bacteria. Adv Genet. 1982;21:53–121. doi: 10.1016/s0065-2660(08)60297-7. [DOI] [PubMed] [Google Scholar]
  21. Long E. O., Collins M., Kiefer B. I., Dawid I. B. Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster. Mol Gen Genet. 1981;182(3):377–384. doi: 10.1007/BF00293925. [DOI] [PubMed] [Google Scholar]
  22. Long E. O., Dawid I. B. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 1979 Dec;18(4):1185–1196. doi: 10.1016/0092-8674(79)90231-9. [DOI] [PubMed] [Google Scholar]
  23. Loyd J. E., Raff E. C., Raff R. A. Site and timing of synthesis of tubulin and other proteins during oogenesis in Drosophila melanogaster. Dev Biol. 1981 Sep;86(2):272–284. doi: 10.1016/0012-1606(81)90185-8. [DOI] [PubMed] [Google Scholar]
  24. McKnight S. L., Miller O. L., Jr Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell. 1976 Jun;8(2):305–319. doi: 10.1016/0092-8674(76)90014-3. [DOI] [PubMed] [Google Scholar]
  25. Mermod J. J., Crippa M. Variations in the amount of polysomes in mature oocytes of Drosophila melanogaster. Dev Biol. 1978 Oct;66(2):586–592. doi: 10.1016/0012-1606(78)90264-6. [DOI] [PubMed] [Google Scholar]
  26. Mermod J. J., Jacobs-Lorena M., Crippa M. Changes in rate of RNA synthesis and ribosomal gene number during oogenesis of Drosophila melanogaster. Dev Biol. 1977 Jun;57(2):393–402. doi: 10.1016/0012-1606(77)90224-x. [DOI] [PubMed] [Google Scholar]
  27. Mermod J. J., Schatz G., Crippa M. Specific control of messenger translation in Drosophila oocytes and embryos. Dev Biol. 1980 Mar;75(1):177–186. doi: 10.1016/0012-1606(80)90153-0. [DOI] [PubMed] [Google Scholar]
  28. Mohan J. Influence of the RNA content on oogenesis in the bobbed mutants of Drosophila melanogaster. J Embryol Exp Morphol. 1971 Apr;25(2):237–246. [PubMed] [Google Scholar]
  29. Nomura M., Gourse R., Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451. [DOI] [PubMed] [Google Scholar]
  30. Nomura M., Yates J. L., Dean D., Post L. E. Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7084–7088. doi: 10.1073/pnas.77.12.7084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pearson N. J., Fried H. M., Warner J. R. Yeast use translational control to compensate for extra copies of a ribosomal protein gene. Cell. 1982 Jun;29(2):347–355. doi: 10.1016/0092-8674(82)90151-9. [DOI] [PubMed] [Google Scholar]
  32. Pierandrei-Amaldi P., Campioni N., Beccari E., Bozzoni I., Amaldi F. Expression of ribosomal-protein genes in Xenopus laevis development. Cell. 1982 Aug;30(1):163–171. doi: 10.1016/0092-8674(82)90022-8. [DOI] [PubMed] [Google Scholar]
  33. Ramagopal S., Ennis H. L. Ribosomal protein synthesis during spore germination and vegetative growth in Dictyostelium discoideum. J Biol Chem. 1982 Jan 25;257(2):1025–1031. [PubMed] [Google Scholar]
  34. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  35. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  36. Ruddell A., Jacobs-Lorena M. Biphasic pattern of histone gene expression during Drosophila oogenesis. Proc Natl Acad Sci U S A. 1985 May;82(10):3316–3319. doi: 10.1073/pnas.82.10.3316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ruddell A., Jacobs-Lorena M. Preferential expression of actin genes during oogenesis of Drosophila. Dev Biol. 1984 Sep;105(1):115–120. doi: 10.1016/0012-1606(84)90266-5. [DOI] [PubMed] [Google Scholar]
  38. Sakoyama Y., Okubo S. Two-dimensional gel patterns of protein species during development of Drosophila embryos. Dev Biol. 1981 Jan 30;81(2):361–365. doi: 10.1016/0012-1606(81)90301-8. [DOI] [PubMed] [Google Scholar]
  39. Santon J. B., Pellegrini M. Expression of ribosomal proteins during Drosophila early development. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5649–5653. doi: 10.1073/pnas.77.10.5649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Santon J. B., Pellegrini M. Rates of ribosomal protein and total protein synthesis during Drosophila early embryogenesis. Dev Biol. 1981 Jul 15;85(1):252–257. doi: 10.1016/0012-1606(81)90255-4. [DOI] [PubMed] [Google Scholar]
  41. Shermoen A. W., Kiefer B. I. Regulation in rDNA-deficient Drosophila melanogaster. Cell. 1975 Mar;4(3):275–280. doi: 10.1016/0092-8674(75)90176-2. [DOI] [PubMed] [Google Scholar]
  42. Sherton C. C., Wool I. G. Two-dimensional polyacrylamide gel electrophoresis of eukaryotic ribosomal proteins. Methods Enzymol. 1974;30:506–526. doi: 10.1016/0076-6879(74)30051-1. [DOI] [PubMed] [Google Scholar]
  43. Tartof K. D. Unequal mitotic sister chromatin exchange as the mechanism of ribosomal RNA gene magnification. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1272–1276. doi: 10.1073/pnas.71.4.1272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Vaslet C. A., O'Connell P., Izquierdo M., Rosbash M. Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster. Nature. 1980 Jun 26;285(5767):674–676. doi: 10.1038/285674a0. [DOI] [PubMed] [Google Scholar]
  45. Weiss Y. C., Vaslet C. A., Rosbash M. Ribosomal protein mRNAs increase dramatically during Xenopus development. Dev Biol. 1981 Oct 30;87(2):330–339. doi: 10.1016/0012-1606(81)90156-1. [DOI] [PubMed] [Google Scholar]
  46. Wensink P. C., Tabata S., Pachl C. The clustered and scrambled arrangement of moderately repetitive elements in Drosophila DNA. Cell. 1979 Dec;18(4):1231–1246. doi: 10.1016/0092-8674(79)90235-6. [DOI] [PubMed] [Google Scholar]
  47. Woodland H. R. Changes in the polysome content of developing Xenopus laevis embryos. Dev Biol. 1974 Sep;40(1):90–101. doi: 10.1016/0012-1606(74)90111-0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES