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
-
WW and SH3 domains, two different scaffolds to recognize proline-rich ligands.
FEBS Lett. 2002 Feb 20;513(1):30-7
PMID: 11911877
-
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
-
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
-
The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture.
Oncogene. 2004 Mar 15;23(11):1972-84
PMID: 15021885
-
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
-
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
-
Characterization of a novel protein-binding module--the WW domain.
FEBS Lett. 1995 Aug 1;369(1):67-71
PMID: 7641887
-
Towards prediction of cognate complexes between the WW domain and proline-rich ligands.
FEBS Lett. 1996 Apr 8;384(1):1-8
PMID: 8797792
-
Ubiquitin-dependent protein degradation.
Annu Rev Genet. 1996;30:405-39
PMID: 8982460
-
The ubiquitin system.
Annu Rev Biochem. 1998;67:425-79
PMID: 9759494
-
Functional domains of the Rsp5 ubiquitin-protein ligase.
Mol Cell Biol. 1999 Jan;19(1):342-52
PMID: 9858558
-
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
-
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
-
Ubiquitin and endocytic internalization in yeast and animal cells.
Biochim Biophys Acta. 2004 Nov 29;1695(1-3):89-111
PMID: 15571811
-
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
-
E3 ubiquitin ligases.
Essays Biochem. 2005;41:15-30
PMID: 16250895
-
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
-
Comparative analysis of Saccharomyces cerevisiae WW domains and their interacting proteins.
Genome Biol. 2006;7(4):R30
PMID: 16606443
-
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
-
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
-
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
-
Mechanisms underlying ubiquitination.
Annu Rev Biochem. 2001;70:503-33
PMID: 11395416
-
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
-
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
-
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
-
Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing.
Cell. 2000 Sep 1;102(5):577-86
PMID: 11007476
-
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
-
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
-
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