Home LiteratureArticle Details
PMID: 17719829 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

WW domains 2 and 3 of Rsp5p play overlapping roles in binding to the LPKY motif of Spt23p and Mga2p.

The international journal of biochemistry & cell biology ·Vol. 40 ·No. 1 ·2008-00-00 ·Pages 147-57

Bhattacharya S, Zoladek T, Haines DS

Abstract

Rsp5p of Saccharomyces cerevisiae is a member of the C2-WW-HECT family of ubiquitin ligases and it interacts with targets via its WW domains. Spt23p and Mga2p are Rsp5p substrates and Rsp5p activates the OLE1 inducing functions of these membrane-localized transcription factors by ubiquitination. Although it is known that Rsp5p binds Mga2p and Spt23p via an imperfect WW domain-binding site (LPKY) that is located within the carboxy-terminal domain of the proteins, it remains unclear which WW domains mediate binding. We show that Rsp5p mutants harboring mutations in single WW domains are Spt23p/Mga2p binding and ubiquitination proficient. This is also the case for WW domains 1/2 and WW domains 1/3 mutants. However, disrupting WW domains 2 and 3 abrogates a physical and functional interaction with substrates in vitro and in cells. We also show that abrogation of WW domains 2 and 3 eliminates the activity of an Rsp5p dominant-negative mutant and an rsp5 WW domain 2/3 mutant is unable to rescue the proliferative defects of rsp5 Delta cells. Interestingly, while rsp5 Delta cells are able to grow on oleic acid containing YPD media, they as well as those transformed with the WW domain 2/3 mutant are unable to proliferate on oleic acid containing synthetic drop-out media. We conclude from these studies that WW domains 2 and 3 of Rsp5p play overlapping roles in binding to the LPKY site on Spt23p and Mga2p. Also, we propose that WW domains 2 and 3 perform yet to be defined essential function(s) outside of the OLE1 pathway when cells are grown in nutrient restrictive media.

MeSH Terms
DNA, Fungal Endosomal Sorting Complexes Required for Transport Enzyme Induction Fatty Acid Desaturases/metabolism Gene Transfer Techniques Membrane Proteins Mutagenesis, Site-Directed Mutation Protein Interaction Domains and Motifs Radioligand Assay Recombinant Proteins/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Stearoyl-CoA Desaturase Substrate Specificity Trans-Activators/genetics,metabolism Transcription Factors Transcriptional Activation Ubiquitin-Protein Ligase Complexes/genetics,metabolism Ubiquitin-Protein Ligases/genetics,metabolism Ubiquitination
Chemicals
DNA, Fungal Endosomal Sorting Complexes Required for Transport Membrane Proteins Recombinant Proteins SPT23 protein, S cerevisiae Saccharomyces cerevisiae Proteins Trans-Activators Transcription Factors Fatty Acid Desaturases Stearoyl-CoA Desaturase delta-9 fatty acid desaturase Ubiquitin-Protein Ligase Complexes Ubiquitin-Protein Ligases RSP5 protein, S cerevisiae
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bhattacharya Sabyasachi
Fels Institute for Cancer Research and Molecular Biology and Department of Biochemistry, Temple University School of Medicine, Philadelphia, PA 19140, United States.
Zoladek Teresa
Haines Dale S
References (29)
29 references, click to expand
  1. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands.
    FEBS Lett. 2002 Feb 20;513(1):30-7 PMID: 11911877
  2. Determinants of ligand specificity in groups I and IV WW domains as studied by surface plasmon resonance and model building.
    J Biol Chem. 2002 Mar 22;277(12):10173-7 PMID: 11751914
  3. Rsp5p is required for ER bound Mga2p120 polyubiquitination and release of the processed/tethered transactivator Mga2p90.
    Curr Biol. 2003 Jul 15;13(14):1227-33 PMID: 12867034
  4. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture.
    Oncogene. 2004 Mar 15;23(11):1972-84 PMID: 15021885
  5. The ubiquitin ligase Rsp5p is required for modification and sorting of membrane proteins into multivesicular bodies.
    Traffic. 2004 May;5(5):383-92 PMID: 15086787
  6. Common mechanism of ligand recognition by group II/III WW domains: redefining their functional classification.
    J Biol Chem. 2004 Jul 23;279(30):31833-41 PMID: 15133021
  7. Characterization of a novel protein-binding module--the WW domain.
    FEBS Lett. 1995 Aug 1;369(1):67-71 PMID: 7641887
  8. Towards prediction of cognate complexes between the WW domain and proline-rich ligands.
    FEBS Lett. 1996 Apr 8;384(1):1-8 PMID: 8797792
  9. Ubiquitin-dependent protein degradation.
    Annu Rev Genet. 1996;30:405-39 PMID: 8982460
  10. The ubiquitin system.
    Annu Rev Biochem. 1998;67:425-79 PMID: 9759494
  11. Functional domains of the Rsp5 ubiquitin-protein ligase.
    Mol Cell Biol. 1999 Jan;19(1):342-52 PMID: 9858558
  12. MGA2 or SPT23 is required for transcription of the delta9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae.
    Genetics. 1999 Feb;151(2):473-83 PMID: 9927444
  13. Nedd4-like proteins: an emerging family of ubiquitin-protein ligases implicated in diverse cellular functions.
    Trends Cell Biol. 1999 May;9(5):166-9 PMID: 10322449
  14. Ubiquitin and endocytic internalization in yeast and animal cells.
    Biochim Biophys Acta. 2004 Nov 29;1695(1-3):89-111 PMID: 15571811
  15. A single PXY motif located within the carboxyl terminus of Spt23p and Mga2p mediates a physical and functional interaction with ubiquitin ligase Rsp5p.
    J Biol Chem. 2004 Dec 17;279(51):53892-8 PMID: 15466864
  16. E3 ubiquitin ligases.
    Essays Biochem. 2005;41:15-30 PMID: 16250895
  17. Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates.
    Mol Cell. 2006 Mar 17;21(6):861-71 PMID: 16543154
  18. Comparative analysis of Saccharomyces cerevisiae WW domains and their interacting proteins.
    Genome Biol. 2006;7(4):R30 PMID: 16606443
  19. Cdc48p(Npl4p/Ufd1p) binds and segregates membrane-anchored/tethered complexes via a polyubiquitin signal present on the anchors.
    Mol Cell. 2007 Feb 9;25(3):385-97 PMID: 17289586
  20. The HECT ubiquitin ligase Rsp5p is required for proper nuclear export of mRNA in Saccharomyces cerevisiae.
    Traffic. 2003 Aug;4(8):566-75 PMID: 12839499
  21. Substrate proteolysis is inhibited by dominant-negative Nedd4 and Rsp5 mutants harboring alterations in WW domain 1.
    J Cell Sci. 2002 Mar 1;115(Pt 5):1041-8 PMID: 11870222
  22. Mechanisms underlying ubiquitination.
    Annu Rev Biochem. 2001;70:503-33 PMID: 11395416
  23. Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone.
    Cell. 2001 Nov 30;107(5):667-77 PMID: 11733065
  24. Domains of the Rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis.
    Mol Biol Cell. 2001 Feb;12(2):421-35 PMID: 11179425
  25. WW domains of Rsp5p define different functions: determination of roles in fluid phase and uracil permease endocytosis in Saccharomyces cerevisiae.
    Genetics. 2001 Jan;157(1):91-101 PMID: 11139494
  26. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing.
    Cell. 2000 Sep 1;102(5):577-86 PMID: 11007476
  27. Rsp5 WW domains interact directly with the carboxyl-terminal domain of RNA polymerase II.
    J Biol Chem. 2000 Jul 7;275(27):20562-71 PMID: 10781604
  28. Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases.
    J Membr Biol. 2000 Jul 1;176(1):1-17 PMID: 10882424
  29. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains.
    FASEB J. 2000 Feb;14(2):231-41 PMID: 10657980
Article Info
Journal
The international journal of biochemistry & cell biology
Abbr.
Int J Biochem Cell Biol
ISSN
1357-2725
Published
2008-00-00
Epub
2007-00-22
Pages
147-57
Language
English
Region
Netherlands
NLM ID
9508482
PMCID
PMC2129131
Subset
IM
Grants
NIGMS NIH HHS · R01 GM070769 · United States
NIGMS NIH HHS · R01 GM070769-03 · United States
NIGMS NIH HHS · GM070769 · 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]