Home LiteratureArticle Details
PMID: 12052895 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Rad23 promotes the targeting of proteolytic substrates to the proteasome.

Molecular and cellular biology ·Vol. 22 ·No. 13 ·2002-07-00 ·Pages 4902-13

Chen L, Madura K

Abstract

Rad23 contains a ubiquitin-like domain (UbL(R23)) that interacts with catalytically active proteasomes and two ubiquitin (Ub)-associated (UBA) sequences that bind Ub. The UBA domains can bind Ub in vitro, although the significance of this interaction in vivo is poorly understood. Rad23 can interfere with the assembly of multi-Ub chains in vitro, and high-level expression caused stabilization of proteolytic substrates in vivo. We report here that Rad23 interacts with ubiquitinated cellular proteins through the synergistic action of its UBA domains. Rad23 plays an overlapping role with Rpn10, a proteasome-associated multi-Ub chain binding protein. Mutations in the UBA domains prevent efficient interaction with ubiquitinated proteins and result in poor suppression of the growth and proteolytic defects of a rad23 Delta rpn10 Delta mutant. High-level expression of Rad23 revealed, for the first time, an interaction between ubiquitinated proteins and the proteasome. This increase was not observed in rpn10 Delta mutants, suggesting that Rpn10 participates in the recognition of proteolytic substrates that are delivered by Rad23. Overexpression of UbL(R23) caused stabilization of a model substrate, indicating that an unregulated UbL(R23)-proteasome interaction can interfere with the efficient delivery of proteolytic substrates by Rad23. Because the suppression of a rad23 Delta rpn10 Delta mutant phenotype required both UbL(R23) and UBA domains, our findings support the hypothesis that Rad23 encodes a novel regulatory factor that translocates ubiquitinated substrates to the proteasome.

MeSH Terms
Base Sequence Carrier Proteins/genetics,metabolism Cell Cycle Proteins Cell Division/genetics Checkpoint Kinase 2 Cysteine Endopeptidases/metabolism DNA Damage Fungal Proteins/metabolism Molecular Sequence Data Multienzyme Complexes/metabolism Mutation Proteasome Endopeptidase Complex Protein Serine-Threonine Kinases/genetics,metabolism Protein Structure, Tertiary Saccharomyces cerevisiae Proteins Ubiquitin/metabolism Yeasts/genetics,metabolism
Chemicals
Carrier Proteins Cell Cycle Proteins Fungal Proteins Multienzyme Complexes RPN10 protein, S cerevisiae Saccharomyces cerevisiae Proteins Ubiquitin Checkpoint Kinase 2 Protein Serine-Threonine Kinases RAD53 protein, S cerevisiae Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Chen Li
Department of Biochemistry, Robert Wood Johnson Medical School, Piscataway, New Jersey 08854, USA.
Madura Kiran
References (49)
49 references, click to expand
  1. Evidence for an interaction between ubiquitin-conjugating enzymes and the 26S proteasome.
    Mol Cell Biol. 2000 Jul;20(13):4691-8 PMID: 10848595
  2. A proteolytic pathway that recognizes ubiquitin as a degradation signal.
    J Biol Chem. 1995 Jul 21;270(29):17442-56 PMID: 7615550
  3. The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome.
    Mol Cell. 2000 Aug;6(2):409-19 PMID: 10983987
  4. The DNA repair protein rad23 is a negative regulator of multi-ubiquitin chain assembly.
    Nat Cell Biol. 2000 Sep;2(9):601-8 PMID: 10980700
  5. Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes.
    Mol Biol Cell. 2000 Oct;11(10):3425-39 PMID: 11029046
  6. Dosage suppressors of pds1 implicate ubiquitin-associated domains in checkpoint control.
    Mol Cell Biol. 2001 Mar;21(6):1997-2007 PMID: 11238935
  7. UBA domains of DNA damage-inducible proteins interact with ubiquitin.
    Nat Struct Biol. 2001 May;8(5):417-22 PMID: 11323716
  8. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair.
    J Biol Chem. 2001 Jun 1;276(22):18665-72 PMID: 11279143
  9. Rad23 provides a link between the Png1 deglycosylating enzyme and the 26 S proteasome in yeast.
    J Biol Chem. 2001 Jun 15;276(24):21601-7 PMID: 11259433
  10. The 19S complex of the proteasome regulates nucleotide excision repair in yeast.
    Genes Dev. 2001 Jun 15;15(12):1528-39 PMID: 11410533
  11. Reaction mechanism of human DNA repair excision nuclease.
    J Biol Chem. 1996 Apr 5;271(14):8285-94 PMID: 8626523
  12. Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center.
    J Cell Biol. 1996 Jun;133(6):1331-46 PMID: 8682868
  13. HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro.
    Mol Cell Biol. 1996 Sep;16(9):4852-61 PMID: 8756644
  14. Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23.
    Genomics. 1996 Jan 1;31(1):20-7 PMID: 8808275
  15. 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
  16. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover.
    Mol Cell Biol. 1996 Nov;16(11):6020-8 PMID: 8887631
  17. Inhibition of the 26 S proteasome by polyubiquitin chains synthesized to have defined lengths.
    J Biol Chem. 1997 Sep 19;272(38):23712-21 PMID: 9295315
  18. The ubiquitin system.
    Trends Biochem Sci. 1997 Oct;22(10):383-7 PMID: 9357313
  19. Identification and characterization of XPC-binding domain of hHR23B.
    Mol Cell Biol. 1997 Dec;17(12):6915-23 PMID: 9372923
  20. Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity.
    Mol Cell Biol. 1997 Dec;17(12):6924-31 PMID: 9372924
  21. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1.
    J Biol Chem. 1998 Jan 23;273(4):1970-81 PMID: 9442033
  22. Rad23 links DNA repair to the ubiquitin/proteasome pathway.
    Nature. 1998 Feb 12;391(6668):715-8 PMID: 9490418
  23. The hydrophobic effect contributes to polyubiquitin chain recognition.
    Biochemistry. 1998 Mar 3;37(9):2925-34 PMID: 9485444
  24. The regulatory particle of the Saccharomyces cerevisiae proteasome.
    Mol Cell Biol. 1998 Jun;18(6):3149-62 PMID: 9584156
  25. Reconstituting ubiquitination reactions with affinity-purified components and 32P-ubiquitin.
    Anal Biochem. 1998 Jul 1;260(2):135-41 PMID: 9657869
  26. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3.
    Cell. 1998 Sep 4;94(5):615-23 PMID: 9741626
  27. Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA.
    J Biol Chem. 1998 Nov 20;273(47):31541-6 PMID: 9813069
  28. Preferential binding of yeast Rad4.Rad23 complex to damaged DNA.
    J Biol Chem. 1998 Dec 11;273(50):33111-4 PMID: 9837874
  29. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly.
    Cell. 1999 Mar 5;96(5):635-44 PMID: 10089879
  30. The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair.
    Mol Cell. 1999 Jun;3(6):687-95 PMID: 10394357
  31. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae.
    Nature. 2000 Feb 10;403(6770):623-7 PMID: 10688190
  32. Physical association of ubiquitin ligases and the 26S proteasome.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2497-502 PMID: 10688918
  33. Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae.
    Genetics. 1999 Sep;153(1):69-79 PMID: 10471701
  34. Identification of XDRP1; a Xenopus protein related to yeast Dsk2p binds to the N-terminus of cyclin A and inhibits its degradation.
    EMBO J. 1999 Sep 15;18(18):5009-18 PMID: 10487753
  35. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome.
    J Biol Chem. 1999 Sep 24;274(39):28019-25 PMID: 10488153
  36. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains.
    Nat Cell Biol. 2001 Oct;3(10):939-43 PMID: 11584278
  37. Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly.
    EMBO Rep. 2001 Oct;2(10):933-8 PMID: 11571271
  38. UBA domains mediate protein-protein interactions between two DNA damage-inducible proteins.
    J Mol Biol. 2001 Nov 9;313(5):955-63 PMID: 11700052
  39. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):745-50 PMID: 11805328
  40. Recognition of the polyubiquitin proteolytic signal.
    EMBO J. 2000 Jan 4;19(1):94-102 PMID: 10619848
  41. Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23.
    J Biol Chem. 2002 Apr 5;277(14):11691-5 PMID: 11805121
  42. 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
  43. Transcript levels of the Saccharomyes cerevisiae DNA repair gene RAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle.
    Nucleic Acids Res. 1990 Aug 25;18(16):4737-42 PMID: 2204027
  44. Structure of a diubiquitin conjugate and a model for interaction with ubiquitin conjugating enzyme (E2).
    J Biol Chem. 1992 Aug 15;267(23):16467-71 PMID: 1322903
  45. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function.
    Mol Cell Biol. 1993 Dec;13(12):7757-65 PMID: 8246991
  46. A 26 S protease subunit that binds ubiquitin conjugates.
    J Biol Chem. 1994 Mar 11;269(10):7059-61 PMID: 8125911
  47. Yeast DNA repair protein RAD23 promotes complex formation between transcription factor TFIIH and DNA damage recognition factor RAD14.
    J Biol Chem. 1995 Apr 14;270(15):8385-8 PMID: 7721729
  48. Reconstitution of yeast nucleotide excision repair with purified Rad proteins, replication protein A, and transcription factor TFIIH.
    J Biol Chem. 1995 Jun 2;270(22):12973-6 PMID: 7768886
  49. Nucleotide excision repair in yeast.
    Mutat Res. 2000 Jun 30;451(1-2):13-24 PMID: 10915862
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2002-07-00
Pages
4902-13
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC133919
Subset
IM
Grants
NCI NIH HHS · R01 CA083875 · United States
NCI NIH HHS · CA-83875 · 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: product@genelibs.com