Home LiteratureArticle Details
PMID: 9822592 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Localization of the 26S proteasome during mitosis and meiosis in fission yeast.

The EMBO journal ·Vol. 17 ·No. 22 ·1998-11-16 ·Pages 6465-76

Wilkinson CR, Wallace M, Morphew M, Perry P, Allshire R, Javerzat JP, McIntosh JR, Gordon C

Abstract

The 26S proteasome is a large multisubunit complex involved in degrading both cytoplasmic and nuclear proteins. We have investigated the localization of this complex in the fission yeast, Schizosaccharomyces pombe. Immunofluorescence microscopy shows a striking localization pattern whereby the proteasome is found predominantly at the nuclear periphery, both in interphase and throughout mitosis. Electron microscopic analysis revealed a concentration of label near the inner side of the nuclear envelope. The localization of green fluorescent protein (GFP)-tagged 26S proteasomes was analyzed in live cells during mitosis and meiosis. Throughout mitosis the proteasome remained predominantly at the nuclear periphery. During meiosis the proteasome was found to undergo dramatic changes in its localization. Throughout the first meiotic division, the signal is more dispersed over the nucleus. During meiosis II, there was a dramatic re-localization, and the signal became restricted to the area between the separating DNA until the end of meiosis when the signal dispersed before returning to the nuclear periphery during spore formation. These findings strongly imply that the nuclear periphery is a major site of protein degradation in fission yeast both in interphase and throughout mitosis. Furthermore they raise interesting questions as to the spatial organization of protein degradation during meiosis.

MeSH Terms
Base Sequence Carrier Proteins/metabolism Cysteine Endopeptidases/metabolism DNA Primers Immunohistochemistry Intracellular Signaling Peptides and Proteins Meiosis Microscopy, Electron Mitosis Multienzyme Complexes/metabolism Nuclear Envelope/enzymology Proteasome Endopeptidase Complex Schizosaccharomyces/cytology,enzymology,ultrastructure Schizosaccharomyces pombe Proteins Trans-Activators/metabolism
Chemicals
Carrier Proteins DNA Primers Intracellular Signaling Peptides and Proteins MTS4 protein, S pombe Multienzyme Complexes Schizosaccharomyces pombe Proteins Trans-Activators rpn11 protein, S pombe Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Wilkinson C R
MRC Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, UK.
Wallace M
Morphew M
Perry P
Allshire R
Javerzat J P
McIntosh J R
Gordon C
References (71)
71 references, click to expand
  1. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome.
    Nature. 1997 Feb 20;385(6618):737-40 PMID: 9034192
  2. Structure of 20S proteasome from yeast at 2.4 A resolution.
    Nature. 1997 Apr 3;386(6624):463-71 PMID: 9087403
  3. A proteasome cap subunit required for spindle pole body duplication in yeast.
    J Cell Biol. 1997 May 5;137(3):539-53 PMID: 9151663
  4. The 26S proteasome: subunits and functions.
    Mol Biol Rep. 1997 Mar;24(1-2):3-11 PMID: 9228274
  5. Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation.
    Nature. 1997 Aug 28;388(6645):891-5 PMID: 9278052
  6. The active sites of the eukaryotic 20 S proteasome and their involvement in subunit precursor processing.
    J Biol Chem. 1997 Oct 3;272(40):25200-9 PMID: 9312134
  7. Mts4, a non-ATPase subunit of the 26 S protease in fission yeast is essential for mitosis and interacts directly with the ATPase subunit Mts2.
    J Biol Chem. 1997 Oct 10;272(41):25768-77 PMID: 9325304
  8. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  9. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation.
    Curr Opin Cell Biol. 1995 Apr;7(2):215-23 PMID: 7612274
  10. Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae.
    EMBO J. 1995 Jul 3;14(13):3105-15 PMID: 7621825
  11. Cloning and sequencing a non-ATPase subunit of the regulatory complex of the Drosophila 26S protease.
    Eur J Biochem. 1995 Aug 1;231(3):720-5 PMID: 7649173
  12. Selective protein degradation: a journey's end within the proteasome.
    Cell. 1995 Sep 22;82(6):881-4 PMID: 7553848
  13. The yeast SEN3 gene encodes a regulatory subunit of the 26S proteasome complex required for ubiquitin-dependent protein degradation in vivo.
    Mol Cell Biol. 1995 Nov;15(11):6311-21 PMID: 7565784
  14. Subunits of the regulatory complex of the 26S protease.
    Mol Biol Rep. 1995;21(1):27-34 PMID: 7565660
  15. In vivo assembly of the proteasomal complexes, implications for antigen processing.
    J Biol Chem. 1995 Nov 17;270(46):27687-94 PMID: 7499235
  16. Dynamics of proteasome distribution in living cells.
    EMBO J. 1997 Oct 15;16(20):6087-94 PMID: 9321388
  17. Resistance to diverse drugs and ultraviolet light conferred by overexpression of a novel human 26 S proteasome subunit.
    J Biol Chem. 1997 Nov 28;272(48):30470-5 PMID: 9374539
  18. Nucleocytoplasmic transport: the last 200 nanometers.
    Cell. 1998 Feb 6;92(3):327-36 PMID: 9476893
  19. The regulatory particle of the Saccharomyces cerevisiae proteasome.
    Mol Cell Biol. 1998 Jun;18(6):3149-62 PMID: 9584156
  20. Importins and exportins: how to get in and out of the nucleus.
    Trends Biochem Sci. 1998 May;23(5):185-9 PMID: 9612083
  21. Transport routes through the nuclear pore complex.
    Curr Opin Cell Biol. 1998 Jun;10(3):392-9 PMID: 9640541
  22. The Pad1+ gene encodes a subunit of the 26 S proteasome in fission yeast.
    J Biol Chem. 1998 Sep 11;273(37):23938-45 PMID: 9727008
  23. High efficiency transformation of Schizosaccharomyces pombe by electroporation.
    Nucleic Acids Res. 1992 Feb 11;20(3):621 PMID: 1741305
  24. Cell cycle-dependent change of proteasome distribution during embryonic development of the ascidian Halocynthia roretzi.
    Dev Biol. 1992 May;151(1):27-33 PMID: 1577192
  25. Electron microscopic localization of the multicatalytic proteinase complex in rat liver and in cultured cells.
    J Histochem Cytochem. 1992 Aug;40(8):1165-72 PMID: 1619280
  26. The ubiquitin system for protein degradation.
    Annu Rev Biochem. 1992;61:761-807 PMID: 1323239
  27. Immunocytochemical localization of the multicatalytic proteinase (proteasome) in crustacean striated muscles.
    Muscle Nerve. 1992 Sep;15(9):1023-35 PMID: 1518511
  28. Molecular trafficking across the nuclear pore complex.
    Curr Opin Cell Biol. 1992 Aug;4(4):637-45 PMID: 1329868
  29. Changes in intracellular localization of proteasomes in immortalized ovarian granulosa cells during mitosis associated with a role in cell cycle control.
    Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):99-103 PMID: 8380501
  30. Thiamine-repressible expression vectors pREP and pRIP for fission yeast.
    Gene. 1993 Jan 15;123(1):127-30 PMID: 8422996
  31. The multicatalytic and 26 S proteases.
    J Biol Chem. 1993 Mar 25;268(9):6065-8 PMID: 8454582
  32. Isolation of the yeast nuclear pore complex.
    J Cell Biol. 1993 Nov;123(4):771-83 PMID: 8227139
  33. Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit.
    Nature. 1993 Nov 25;366(6453):355-7 PMID: 8247131
  34. S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase.
    Nature. 1993 Nov 25;366(6453):358-62 PMID: 8247132
  35. A 26 S protease subunit that binds ubiquitin conjugates.
    J Biol Chem. 1994 Mar 11;269(10):7059-61 PMID: 8125911
  36. Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm.
    J Biol Chem. 1994 Mar 11;269(10):7709-18 PMID: 8125997
  37. Telomere-led premeiotic chromosome movement in fission yeast.
    Science. 1994 Apr 8;264(5156):270-3 PMID: 8146661
  38. Molecular characterization of the "26S" proteasome complex from rat liver.
    J Struct Biol. 1993 Nov-Dec;111(3):200-11 PMID: 8003381
  39. The ubiquitin-proteasome proteolytic pathway.
    Cell. 1994 Oct 7;79(1):13-21 PMID: 7923371
  40. Proteasomes: protein degradation machines of the cell.
    Trends Biochem Sci. 1994 Sep;19(9):377-82 PMID: 7985232
  41. Molecular structure of 20S and 26S proteasomes.
    Enzyme Protein. 1993;47(4-6):241-51 PMID: 7697123
  42. Structural features of 26S and 20S proteasomes.
    Enzyme Protein. 1993;47(4-6):252-73 PMID: 7697124
  43. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution.
    Science. 1995 Apr 28;268(5210):533-9 PMID: 7725097
  44. A novel essential fission yeast gene pad1+ positively regulates pap1(+)-dependent transcription and is implicated in the maintenance of chromosome structure.
    J Cell Sci. 1995 Feb;108 ( Pt 2):569-79 PMID: 7769002
  45. Sequential alterations in the nuclear chromatin region during mitosis of the fission yeast Schizosaccharomyces pombe: video fluorescence microscopy of synchronously growing wild-type and cold-sensitive cdc mutants by using a DNA-binding fluorescent probe.
    J Cell Sci. 1981 Dec;52:271-87 PMID: 7334057
  46. Movement of a karyophilic protein through the nuclear pores of oocytes.
    J Cell Biol. 1984 Dec;99(6):2216-22 PMID: 6501421
  47. Sea urchin prosome: characterization and changes during development.
    Proc Natl Acad Sci U S A. 1987 Mar;84(6):1595-9 PMID: 2951733
  48. The 19S ring-type particles of Drosophila. Cytological and biochemical analysis of their intracellular association and distribution.
    Exp Cell Res. 1987 May;170(1):204-13 PMID: 2436933
  49. Localization of a multi-catalytic, high-molecular mass proteinase in the nuclei of muscle cells.
    Histochem J. 1987 Oct-Nov;19(10-11):594-7 PMID: 3326862
  50. Ubiquitin-mediated protein degradation.
    J Biol Chem. 1988 Oct 25;263(30):15237-40 PMID: 2844803
  51. The association of prosomes with some of the intermediate filament networks of the animal cell.
    J Cell Biol. 1988 Oct;107(4):1517-30 PMID: 2459130
  52. The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe.
    J Cell Sci. 1988 Mar;89 ( Pt 3):343-57 PMID: 3198697
  53. Presence and distribution of specific prosome antigens change as a function of embryonic development and tissue-type differentiation in Pleurodeles waltl.
    J Cell Sci. 1988 Aug;90 ( Pt 4):555-67 PMID: 3075617
  54. Possible mechanism of nuclear translocation of proteasomes.
    FEBS Lett. 1990 Oct 1;271(1-2):41-6 PMID: 2226812
  55. Cell-specific accumulation of Drosophila proteasomes (MCP) during early development.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2275-82 PMID: 2126012
  56. Nuclear localization signals of human and Thermoplasma proteasomal alpha subunits are functional in vitro.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12060-4 PMID: 8618844
  57. Arabidopsis MBP1 gene encodes a conserved ubiquitin recognition component of the 26S proteasome.
    Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):856-60 PMID: 8570648
  58. Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway.
    EMBO J. 1996 May 1;15(9):2069-76 PMID: 8641272
  59. A conditional lethal mutant in the fission yeast 26 S protease subunit mts3+ is defective in metaphase to anaphase transition.
    J Biol Chem. 1996 Mar 8;271(10):5704-11 PMID: 8621436
  60. Functional analysis of eukaryotic 20S proteasome nuclear localization signal.
    Exp Cell Res. 1996 May 25;225(1):67-74 PMID: 8635518
  61. cDNA cloning of p42, a shared subunit of two proteasome regulatory proteins, reveals a novel member of the AAA protein family.
    FEBS Lett. 1996 Jun 3;387(2-3):184-8 PMID: 8674546
  62. Subpopulations of proteasomes in rat liver nuclei, microsomes and cytosol.
    Biochem J. 1996 Jun 1;316 ( Pt 2):401-7 PMID: 8687380
  63. Autocatalytic processing of the 20S proteasome.
    Nature. 1996 Aug 1;382(6590):468-71 PMID: 8684489
  64. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway.
    Science. 1996 Sep 20;273(5282):1725-8 PMID: 8781238
  65. Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly.
    Cell. 1996 Sep 20;86(6):961-72 PMID: 8808631
  66. Structure and functions of the 20S and 26S proteasomes.
    Annu Rev Biochem. 1996;65:801-47 PMID: 8811196
  67. Characteristics of 26 S proteases from fission yeast mutants, which arrest in mitosis.
    J Mol Biol. 1996 Nov 1;263(3):423-31 PMID: 8918598
  68. How proteolysis drives the cell cycle.
    Science. 1996 Dec 6;274(5293):1652-9 PMID: 8939846
  69. Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13797-801 PMID: 8943015
  70. Analysis of mammalian 20S proteasome biogenesis: the maturation of beta-subunits is an ordered two-step mechanism involving autocatalysis.
    EMBO J. 1996 Dec 16;15(24):6887-98 PMID: 9003765
  71. Yeast counterparts of subunits S5a and p58 (S3) of the human 26S proteasome are encoded by two multicopy suppressors of nin1-1.
    Mol Biol Cell. 1997 Jan;8(1):171-87 PMID: 9017604
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-11-16
Pages
6465-76
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170994
Subset
IM
Grants
NCRR NIH HHS · RR00592 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]