Home LiteratureArticle Details
PMID: 9305625 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome.

The EMBO journal ·Vol. 16 ·No. 16 ·1997-08-15 ·Pages 4826-38

Amerik AYu, Swaminathan S, Krantz BA, Wilkinson KD, Hochstrasser M

Abstract

Degradation of many eukaryotic proteins requires their prior ligation to polyubiquitin chains, which target substrates to the 26S proteasome, an abundant cellular protease. We describe a yeast deubiquitinating enzyme, Ubp14, that specifically disassembles unanchored ('free') ubiquitin chains in vitro, a specificity shared by mammalian isopeptidase T. Correspondingly, deletion of the UBP14 gene from yeast cells results in a striking accumulation of free ubiquitin chains, which correlates with defects in ubiquitin-dependent proteolysis. Increasing the steady-state levels of ubiquitin chains in wild-type cells (by expressing a derivative of ubiquitin with an altered C-terminus) inhibits protein degradation to a degree comparable with that observed in ubp14delta cells. Inhibition of degradation is also seen when an active site mutant of Ubp14 is overproduced in vivo. Surprisingly, overproduction of wild-type Ubp14 can inhibit degradation of some proteins as well. Finally, Ubp14 and human isopeptidase T are shown to be functional homologs by complementation analysis. We propose that Ubp14 and isopeptidase T facilitate proteolysis in vivo by preventing unanchored ubiquitin chains from competitively inhibiting polyubiquitin-substrate binding to the 26S proteasome.

MeSH Terms
Amino Acid Sequence Binding Sites Carbon-Nitrogen Lyases Endopeptidases/chemistry,genetics,metabolism Fungal Proteins/metabolism Gene Expression Regulation, Fungal Genes, Fungal Humans Immunoblotting Lyases/antagonists & inhibitors,chemistry,metabolism Molecular Sequence Data Mutagenesis, Site-Directed Peptide Hydrolases/chemistry,metabolism Phenotype Proteasome Endopeptidase Complex Protein Binding Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins Sequence Alignment Substrate Specificity Ubiquitins/chemistry,metabolism
Chemicals
Fungal Proteins Saccharomyces cerevisiae Proteins Ubiquitins Endopeptidases Peptide Hydrolases Proteasome Endopeptidase Complex ATP dependent 26S protease UBP14 protein, S cerevisiae Lyases Carbon-Nitrogen Lyases isopeptidase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Amerik AYu
University of Chicago, Department of Biochemistry and Molecular Biology, IL 60637, USA.
Swaminathan S
Krantz B A
Wilkinson K D
Hochstrasser M
References (37)
37 references, click to expand
  1. A human de-ubiquitinating enzyme with both isopeptidase and peptidase activities in vitro.
    FEBS Lett. 1995 Feb 6;359(1):73-7 PMID: 7851534
  2. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome.
    Nature. 1997 Feb 20;385(6618):737-40 PMID: 9034192
  3. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation.
    Curr Opin Cell Biol. 1995 Apr;7(2):215-23 PMID: 7612274
  4. A proteolytic pathway that recognizes ubiquitin as a degradation signal.
    J Biol Chem. 1995 Jul 21;270(29):17442-56 PMID: 7615550
  5. 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
  6. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T.
    Biochemistry. 1995 Nov 7;34(44):14535-46 PMID: 7578059
  7. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene.
    Science. 1995 Dec 15;270(5243):1828-31 PMID: 8525378
  8. Roles of ubiquitinylation in proteolysis and cellular regulation.
    Annu Rev Nutr. 1995;15:161-89 PMID: 8527216
  9. Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting.
    Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):861-6 PMID: 8570649
  10. Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5.
    J Biol Chem. 1996 Feb 2;271(5):2823-31 PMID: 8576261
  11. DUB-1, a deubiquitinating enzyme with growth-suppressing activity.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3275-9 PMID: 8622927
  12. The DOA pathway: studies on the functions and mechanisms of ubiquitin-dependent protein degradation in the yeast Saccharomyces cerevisiae.
    Cold Spring Harb Symp Quant Biol. 1995;60:503-13 PMID: 8824423
  13. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway.
    Trends Biochem Sci. 1996 May;21(5):172-3 PMID: 8871400
  14. Ubiquitin-dependent protein degradation.
    Annu Rev Genet. 1996;30:405-39 PMID: 8982460
  15. ATP-dependent degradation of ubiquitin-protein conjugates.
    Proc Natl Acad Sci U S A. 1984 Mar;81(6):1619-23 PMID: 6324208
  16. The yeast ubiquitin gene: head-to-tail repeats encoding a polyubiquitin precursor protein.
    Nature. 1984 Dec 13-19;312(5995):663-6 PMID: 6095120
  17. Ubiquitin-lysozyme conjugates. Purification and susceptibility to proteolysis.
    J Biol Chem. 1986 Feb 15;261(5):2391-9 PMID: 3003113
  18. A family of yeast expression vectors containing the phage f1 intergenic region.
    Gene. 1987;52(2-3):225-33 PMID: 3038686
  19. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  20. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein.
    Science. 1989 Mar 24;243(4898):1576-83 PMID: 2538923
  21. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins.
    EMBO J. 1990 Feb;9(2):543-50 PMID: 2154373
  22. In vivo degradation of a transcriptional regulator: the yeast alpha 2 repressor.
    Cell. 1990 May 18;61(4):697-708 PMID: 2111732
  23. A 25-kilodalton ubiquitin carrier protein (E2) catalyzes multi-ubiquitin chain synthesis via lysine 48 of ubiquitin.
    J Biol Chem. 1990 Dec 15;265(35):21835-42 PMID: 2174887
  24. The short-lived MAT alpha 2 transcriptional regulator is ubiquitinated in vivo.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4606-10 PMID: 1647011
  25. Epitope-tagged ubiquitin. A new probe for analyzing ubiquitin function.
    J Biol Chem. 1991 Nov 5;266(31):21150-7 PMID: 1718971
  26. Cloning and characterization of a 20-kDa ubiquitin carrier protein from wheat that catalyzes multiubiquitin chain formation in vitro.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10297-301 PMID: 1658801
  27. A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains. Role in protein degradation.
    J Biol Chem. 1992 Jan 15;267(2):719-27 PMID: 1309773
  28. The N-end rule.
    Cell. 1992 May 29;69(5):725-35 PMID: 1317266
  29. Ubiquitin-specific proteases of Saccharomyces cerevisiae. Cloning of UBP2 and UBP3, and functional analysis of the UBP gene family.
    J Biol Chem. 1992 Nov 15;267(32):23364-75 PMID: 1429680
  30. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 Jul 11;21(14):3329-30 PMID: 8341614
  31. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MAT alpha 2 repressor.
    Cell. 1993 Jul 30;74(2):357-69 PMID: 8393731
  32. Multiubiquitin chains linked through lysine 48 are abundant in vivo and are competent intermediates in the ubiquitin proteolytic pathway.
    J Biol Chem. 1993 Nov 25;268(33):24766-73 PMID: 8227036
  33. The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene.
    Nature. 1993 Nov 25;366(6453):313-9 PMID: 8247125
  34. A 26 S protease subunit that binds ubiquitin conjugates.
    J Biol Chem. 1994 Mar 11;269(10):7059-61 PMID: 8125911
  35. The ubiquitin-proteasome proteolytic pathway.
    Cell. 1994 Oct 7;79(1):13-21 PMID: 7923371
  36. Stress resistance in Saccharomyces cerevisiae is strongly correlated with assembly of a novel type of multiubiquitin chain.
    Mol Cell Biol. 1994 Dec;14(12):7876-83 PMID: 7969127
  37. Biogenesis, structure and function of the yeast 20S proteasome.
    EMBO J. 1995 Jun 1;14(11):2620-30 PMID: 7781614
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1997-08-15
Pages
4826-38
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170118
Subset
IM
Grants
NIGMS NIH HHS · GM30308 · United States
NIGMS NIH HHS · GM53756 · United States
Databases
GENBANK
D38378, U35116, U48271, U75362
SWISSPROT
P38237, P45974
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: product@genelibs.com