Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Dec 1;111(6):2275–2282. doi: 10.1083/jcb.111.6.2275

Cell-specific accumulation of Drosophila proteasomes (MCP) during early development

PMCID: PMC2116374  PMID: 2126012

Abstract

The proteasome (MCP) is a high relative molecular mass multicatalytic proteinase complex composed of nonidentical protein subunits. We have investigated the cellular distribution of the enzyme complex during Drosophila embryogenesis using the proteasome specific antibodies N19- 35 and N19-28 for immunocytology. Antibody staining of whole-mount embryos shows that during embryogenesis proteasomes are present in proliferating cells and that their accumulation and turnover is differentially regulated. Our data suggest that the proteasome may serve different proteolytic processes and that the enzyme may be involved in cell-specific proteolytic events required for cell proliferation and morphogenesis during early Drosophila development.

Full Text

The Full Text of this article is available as a PDF (7.8 MB).

Selected References

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

  1. Akhayat O., Grossi de Sa F., Infante A. A. Sea urchin prosome: characterization and changes during development. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1595–1599. doi: 10.1073/pnas.84.6.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arrigo A. P., Darlix J. L., Khandjian E. W., Simon M., Spahr P. F. Characterization of the prosome from Drosophila and its similarity to the cytoplasmic structures formed by the low molecular weight heat-shock proteins. EMBO J. 1985 Feb;4(2):399–406. doi: 10.1002/j.1460-2075.1985.tb03642.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arrigo A. P., Tanaka K., Goldberg A. L., Welch W. J. Identity of the 19S 'prosome' particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature. 1988 Jan 14;331(6152):192–194. doi: 10.1038/331192a0. [DOI] [PubMed] [Google Scholar]
  4. Baumeister W., Dahlmann B., Hegerl R., Kopp F., Kuehn L., Pfeifer G. Electron microscopy and image analysis of the multicatalytic proteinase. FEBS Lett. 1988 Dec 5;241(1-2):239–245. doi: 10.1016/0014-5793(88)81069-x. [DOI] [PubMed] [Google Scholar]
  5. Chasan R., Anderson K. V. The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo. Cell. 1989 Feb 10;56(3):391–400. doi: 10.1016/0092-8674(89)90242-0. [DOI] [PubMed] [Google Scholar]
  6. Dahlmann B., Kopp F., Kuehn L., Niedel B., Pfeifer G., Hegerl R., Baumeister W. The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett. 1989 Jul 17;251(1-2):125–131. doi: 10.1016/0014-5793(89)81441-3. [DOI] [PubMed] [Google Scholar]
  7. Dahlmann B., Rutschmann M., Kuehn L., Reinauer H. Activation of the multicatalytic proteinase from rat skeletal muscle by fatty acids or sodium dodecyl sulphate. Biochem J. 1985 May 15;228(1):171–177. doi: 10.1042/bj2280171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DeLotto R., Spierer P. A gene required for the specification of dorsal-ventral pattern in Drosophila appears to encode a serine protease. Nature. 1986 Oct 23;323(6090):688–692. doi: 10.1038/323688a0. [DOI] [PubMed] [Google Scholar]
  9. Falkenburg P. E., Haass C., Kloetzel P. M., Niedel B., Kopp F., Kuehn L., Dahlmann B. Drosophila small cytoplasmic 19S ribonucleoprotein is homologous to the rat multicatalytic proteinase. Nature. 1988 Jan 14;331(6152):190–192. doi: 10.1038/331190a0. [DOI] [PubMed] [Google Scholar]
  10. Falkenburg P. E., Kloetzel P. M. Identification and characterization of three different subpopulations of the Drosophila multicatalytic proteinase (proteasome). J Biol Chem. 1989 Apr 25;264(12):6660–6666. [PubMed] [Google Scholar]
  11. Foe V. E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development. 1989 Sep;107(1):1–22. [PubMed] [Google Scholar]
  12. Fujiwara T., Tanaka K., Kumatori A., Shin S., Yoshimura T., Ichihara A., Tokunaga F., Aruga R., Iwanaga S., Kakizuka A. Molecular cloning of cDNA for proteasomes (multicatalytic proteinase complexes) from rat liver: primary structure of the largest component (C2). Biochemistry. 1989 Sep 5;28(18):7332–7340. doi: 10.1021/bi00444a028. [DOI] [PubMed] [Google Scholar]
  13. Haass C., Kloetzel P. M. The Drosophila proteasome undergoes changes in its subunit pattern during development. Exp Cell Res. 1989 Jan;180(1):243–252. doi: 10.1016/0014-4827(89)90228-0. [DOI] [PubMed] [Google Scholar]
  14. Haass C., Pesold-Hurt B., Multhaup G., Beyreuther K., Kloetzel P. M. The Drosophila PROS-28.1 gene is a member of the proteasome gene family. Gene. 1990 Jun 15;90(2):235–241. doi: 10.1016/0378-1119(90)90185-t. [DOI] [PubMed] [Google Scholar]
  15. Haass C., Pesold-Hurt B., Multhaup G., Beyreuther K., Kloetzel P. M. The PROS-35 gene encodes the 35 kd protein subunit of Drosophila melanogaster proteasome. EMBO J. 1989 Aug;8(8):2373–2379. doi: 10.1002/j.1460-2075.1989.tb08366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jin Y. S., Anderson K. V. Dominant and recessive alleles of the Drosophila easter gene are point mutations at conserved sites in the serine protease catalytic domain. Cell. 1990 Mar 9;60(5):873–881. doi: 10.1016/0092-8674(90)90100-s. [DOI] [PubMed] [Google Scholar]
  17. Kleinschmidt J. A., Escher C., Wolf D. H. Proteinase yscE of yeast shows homology with the 20 S cylinder particles of Xenopus laevis. FEBS Lett. 1988 Oct 24;239(1):35–40. doi: 10.1016/0014-5793(88)80540-4. [DOI] [PubMed] [Google Scholar]
  18. Kleinschmidt J. A., Hügle B., Grund C., Franke W. W. The 22 S cylinder particles of Xenopus laevis. I. Biochemical and electron microscopic characterization. Eur J Cell Biol. 1983 Nov;32(1):143–156. [PubMed] [Google Scholar]
  19. Kloetzel P. M., Falkenburg P. E., Hössl P., Glätzer K. H. The 19S ring-type particles of Drosophila. Cytological and biochemical analysis of their intracellular association and distribution. Exp Cell Res. 1987 May;170(1):204–213. doi: 10.1016/0014-4827(87)90130-3. [DOI] [PubMed] [Google Scholar]
  20. Kremp A., Schliephacke M., Kull U., Schmid H. P. Prosomes exist in plant cells too. Exp Cell Res. 1986 Oct;166(2):553–557. doi: 10.1016/0014-4827(86)90500-8. [DOI] [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  23. Rivett A. J. Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase. Characterization as a high molecular weight cysteine proteinase. J Biol Chem. 1985 Oct 15;260(23):12600–12606. [PubMed] [Google Scholar]
  24. Rivett A. J. The multicatalytic proteinase of mammalian cells. Arch Biochem Biophys. 1989 Jan;268(1):1–8. doi: 10.1016/0003-9861(89)90558-4. [DOI] [PubMed] [Google Scholar]
  25. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
  26. Schmid H. P., Akhayat O., Martins De Sa C., Puvion F., Koehler K., Scherrer K. The prosome: an ubiquitous morphologically distinct RNP particle associated with repressed mRNPs and containing specific ScRNA and a characteristic set of proteins. EMBO J. 1984 Jan;3(1):29–34. doi: 10.1002/j.1460-2075.1984.tb01757.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schuldt C., Kloetzel P. M. Analysis of cytoplasmic 19 S ring-type particles in Drosophila which contain hsp 23 at normal growth temperature. Dev Biol. 1985 Jul;110(1):65–74. doi: 10.1016/0012-1606(85)90064-8. [DOI] [PubMed] [Google Scholar]
  28. Siwicki K. K., Eastman C., Petersen G., Rosbash M., Hall J. C. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron. 1988 Apr;1(2):141–150. doi: 10.1016/0896-6273(88)90198-5. [DOI] [PubMed] [Google Scholar]
  29. Tanaka K., Fujiwara T., Kumatori A., Shin S., Yoshimura T., Ichihara A., Tokunaga F., Aruga R., Iwanaga S., Kakizuka A. Molecular cloning of cDNA for proteasomes from rat liver: primary structure of component C3 with a possible tyrosine phosphorylation site. Biochemistry. 1990 Apr 17;29(15):3777–3785. doi: 10.1021/bi00467a026. [DOI] [PubMed] [Google Scholar]
  30. Tanaka K., Ii K., Ichihara A., Waxman L., Goldberg A. L. A high molecular weight protease in the cytosol of rat liver. I. Purification, enzymological properties, and tissue distribution. J Biol Chem. 1986 Nov 15;261(32):15197–15203. [PubMed] [Google Scholar]
  31. Tanaka K., Yoshimura T., Kumatori A., Ichihara A., Ikai A., Nishigai M., Kameyama K., Takagi T. Proteasomes (multi-protease complexes) as 20 S ring-shaped particles in a variety of eukaryotic cells. J Biol Chem. 1988 Nov 5;263(31):16209–16217. [PubMed] [Google Scholar]
  32. Waxman L., Fagan J. M., Goldberg A. L. Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates. J Biol Chem. 1987 Feb 25;262(6):2451–2457. [PubMed] [Google Scholar]
  33. Wilk S., Orlowski M. Cation-sensitive neutral endopeptidase: isolation and specificity of the bovine pituitary enzyme. J Neurochem. 1980 Nov;35(5):1172–1182. doi: 10.1111/j.1471-4159.1980.tb07873.x. [DOI] [PubMed] [Google Scholar]
  34. Wilk S., Orlowski M. Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex. J Neurochem. 1983 Mar;40(3):842–849. doi: 10.1111/j.1471-4159.1983.tb08056.x. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES