Home LiteratureArticle Details
PMID: 2065660 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Yeast RAD6 encoded ubiquitin conjugating enzyme mediates protein degradation dependent on the N-end-recognizing E3 enzyme.

The EMBO journal ·Vol. 10 ·No. 8 ·1991-08-00 ·Pages 2187-93

Sung P, Berleth E, Pickart C, Prakash S, Prakash L

Abstract

The RAD6 gene of Saccharomyces cerevisiae encodes a 20 kd ubiquitin conjugating (E2) enzyme that is required for DNA repair, DNA damage-induced mutagenesis, and sporulation. Here, we demonstrate a novel activity of RAD6 protein--its ability to mediate protein degradation dependent on the N-end-recognizing ubiquitin protein ligase (E3). In reaction mixtures containing E1, E3 and the ubiquitin specific protease from rabbit reticulocytes, RAD6 is as effective as mammalian E214k in E3 dependent ubiquitin--protein conjugate formation and subsequent protein degradation. The ubiquitin conjugating activity of RAD6 is required for these reactions as indicated by the ineffectiveness of the rad6 Ala88 and rad6 Val88 mutant proteins, which lack the ability to form a thioester adduct with ubiquitin and therefore do not conjugate ubiquitin to substrates. We also show that the highly acidic carboxyl-terminus of RAD6 is dispensable for the interaction with E3, and that purified S. cerevisiae E2(30k), product of the UBC1 gene, does not function with E3. These findings demonstrate a specific interaction between RAD6 and E3, and highlight the strong conservation of the ubiquitin conjugating system in eukaryotes. We suggest a function for RAD6 mediated E3 dependent protein degradation in sporulation, and discuss the possible role of this activity during vegetative growth.

Related Genes
MeSH Terms
Animals Catalysis DNA Repair Electrophoresis, Polyacrylamide Gel Fungal Proteins/genetics,metabolism Genes, Fungal Hydrolysis Ligases/genetics,metabolism Rabbits Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins Substrate Specificity Ubiquitin-Conjugating Enzymes
Chemicals
Fungal Proteins Saccharomyces cerevisiae Proteins RAD6 protein, S cerevisiae Ubiquitin-Conjugating Enzymes Ligases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sung P
Department of Biology, University of Rochester, NY 14627.
Berleth E
Pickart C
Prakash S
Prakash L
References (37)
37 references, click to expand
  1. Ubiquitin-dependent proteolysis of native and alkylated bovine serum albumin: effects of protein structure and ATP concentration on selectivity.
    Biochemistry. 1985 Jun 4;24(12):2915-23 PMID: 2990536
  2. RAD6 gene of Saccharomyces cerevisiae encodes a protein containing a tract of 13 consecutive aspartates.
    Proc Natl Acad Sci U S A. 1985 Jan;82(1):168-72 PMID: 3881753
  3. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses.
    Cell. 1987 Mar 27;48(6):1035-46 PMID: 3030556
  4. Role of arginine-tRNA in protein degradation by the ubiquitin pathway.
    Nature. 1987 Apr 23-29;326(6115):808-11 PMID: 3033511
  5. The yeast ubiquitin genes: a family of natural gene fusions.
    EMBO J. 1987 May;6(5):1429-39 PMID: 3038523
  6. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme.
    Nature. 1987 Sep 10-16;329(6135):131-4 PMID: 3306404
  7. Specificity of binding of NH2-terminal residue of proteins to ubiquitin-protein ligase. Use of amino acid derivatives to characterize specific binding sites.
    J Biol Chem. 1988 Feb 25;263(6):2693-8 PMID: 3343227
  8. Expression of the yeast UB14 gene increases in response to DNA-damaging agents and in meiosis.
    Mol Cell Biol. 1988 Mar;8(3):1132-6 PMID: 2835662
  9. Domain structure and functional analysis of the carboxyl-terminal polyacidic sequence of the RAD6 protein of Saccharomyces cerevisiae.
    Mol Cell Biol. 1988 Mar;8(3):1179-85 PMID: 3285176
  10. Levels of active ubiquitin carrier proteins decline during erythroid maturation.
    J Biol Chem. 1988 Aug 25;263(24):12028-35 PMID: 2841342
  11. The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme.
    Science. 1988 Sep 9;241(4871):1331-5 PMID: 2842867
  12. The resolution and characterization of putative ubiquitin carrier protein isozymes from rabbit reticulocytes.
    J Biol Chem. 1988 Sep 15;263(26):13258-67 PMID: 3417657
  13. Ubiquitin-mediated protein degradation.
    J Biol Chem. 1988 Oct 25;263(30):15237-40 PMID: 2844803
  14. The RAD6 protein of Saccharomyces cerevisiae polyubiquitinates histones, and its acidic domain mediates this activity.
    Genes Dev. 1988 Nov;2(11):1476-85 PMID: 2850263
  15. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis.
    Nature. 1989 Mar 30;338(6214):394-401 PMID: 2538753
  16. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein.
    Science. 1989 Mar 24;243(4898):1576-83 PMID: 2538923
  17. A novel, arsenite-sensitive E2 of the ubiquitin pathway: purification and properties.
    Biochemistry. 1989 Jul 11;28(14):6035-41 PMID: 2550069
  18. Universality and structure of the N-end rule.
    J Biol Chem. 1989 Oct 5;264(28):16700-12 PMID: 2506181
  19. 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
  20. Affinity purification of ubiquitin-protein ligase on immobilized protein substrates. Evidence for the existence of separate NH2-terminal binding sites on a single enzyme.
    J Biol Chem. 1990 Mar 5;265(7):3685-90 PMID: 2303472
  21. Expression of the Saccharomyces cerevisiae DNA repair gene RAD6 that encodes a ubiquitin conjugating enzyme, increases in response to DNA damage and in meiosis but remains constant during the mitotic cell cycle.
    Nucleic Acids Res. 1990 Feb 25;18(4):771-8 PMID: 2179869
  22. Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2695-9 PMID: 2157209
  23. The rhp6+ gene of Schizosaccharomyces pombe: a structural and functional homolog of the RAD6 gene from the distantly related yeast Saccharomyces cerevisiae.
    EMBO J. 1990 May;9(5):1423-30 PMID: 2184030
  24. The human ubiquitin carrier protein E2(Mr = 17,000) is homologous to the yeast DNA repair gene RAD6.
    EMBO J. 1990 May;9(5):1431-5 PMID: 2158443
  25. Ubiquitin-conjugating enzymes: novel regulators of eukaryotic cells.
    Trends Biochem Sci. 1990 May;15(5):195-8 PMID: 2193438
  26. Several mammalian ubiquitin carrier proteins, but not E2(20K), are related to the 20-kDa yeast E2, RAD6.
    Biochem Biophys Res Commun. 1990 Sep 14;171(2):705-10 PMID: 2169731
  27. The recognition component of the N-end rule pathway.
    EMBO J. 1990 Oct;9(10):3179-89 PMID: 2209542
  28. Ubiquitin-mediated degradation of histone H3 does not require the substrate-binding ubiquitin protein ligase, E3, or attachment of polyubiquitin chains.
    J Biol Chem. 1990 Dec 15;265(35):21664-9 PMID: 2174883
  29. UBC1 encodes a novel member of an essential subfamily of yeast ubiquitin-conjugating enzymes involved in protein degradation.
    EMBO J. 1990 Dec;9(13):4535-41 PMID: 2265617
  30. Dhr6, a Drosophila homolog of the yeast DNA-repair gene RAD6.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3832-6 PMID: 1902572
  31. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  32. Proposed role of ATP in protein breakdown: conjugation of protein with multiple chains of the polypeptide of ATP-dependent proteolysis.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):1783-6 PMID: 6990414
  33. "Covalent affinity" purification of ubiquitin-activating enzyme.
    J Biol Chem. 1982 Mar 10;257(5):2537-42 PMID: 6277904
  34. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown.
    J Biol Chem. 1983 Jul 10;258(13):8206-14 PMID: 6305978
  35. ATP-dependent degradation of ubiquitin-protein conjugates.
    Proc Natl Acad Sci U S A. 1984 Mar;81(6):1619-23 PMID: 6324208
  36. Functional heterogeneity of ubiquitin carrier proteins.
    J Biol Chem. 1985 Feb 10;260(3):1573-81 PMID: 2981864
  37. In vivo half-life of a protein is a function of its amino-terminal residue.
    Science. 1986 Oct 10;234(4773):179-86 PMID: 3018930
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-08-00
Pages
2187-93
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452907
Subset
IM
Grants
NCI NIH HHS · CA41261 · United States
NIGMS NIH HHS · GM19261 · 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]