Home LiteratureArticle Details
PMID: 12374868 Published · ppublish English Journal Article

Cell surface polarization during yeast mating.

Bagnat M, Simons K

Abstract

Exposure to mating pheromone in haploid Saccharomyces cerevisiae cells results in the arrest of the cell cycle, expression of mating-specific genes, and polarized growth toward the mating partner. Proteins involved in signaling, polarization, cell adhesion, and fusion are localized to the tip of the mating cell (shmoo) where fusion will eventually occur. The mechanisms ensuring the correct targeting and retention of these proteins are poorly understood. Here we show that in pheromone-treated cells, a reorganization of the plasma membrane involving lipid rafts results in the retention of proteins at the tip of the mating projection, segregated from the rest of the membrane. Sphingolipid and ergosterol biosynthetic mutants fail to polarize proteins to the tip of the shmoo and are deficient in mating. Our results show that membrane microdomain clustering at the mating projection is involved in the generation and maintenance of polarity during mating.

MeSH Terms
Acyltransferases/genetics,metabolism Adaptor Proteins, Signal Transducing Amino Acid Transport Systems Carrier Proteins/genetics,metabolism Cell Membrane/metabolism Fungal Proteins/genetics,metabolism Glucose Transport Proteins, Facilitative Mating Factor Membrane Microdomains/metabolism Membrane Proteins/genetics,metabolism Methyltransferases/genetics,metabolism Monosaccharide Transport Proteins/genetics,metabolism Peptides/metabolism Phosphoric Monoester Hydrolases/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Saccharomyces cerevisiae/metabolism,physiology Saccharomyces cerevisiae Proteins/genetics,metabolism Serine C-Palmitoyltransferase Ubiquitin-Protein Ligases ras GTPase-Activating Proteins/genetics,metabolism
Chemicals
Adaptor Proteins, Signal Transducing Amino Acid Transport Systems BUL1 protein, S cerevisiae BUL2 protein, S cerevisiae Carrier Proteins FUS1 protein, S cerevisiae Fungal Proteins GAP1 protein, S cerevisiae Glucose Transport Proteins, Facilitative HXT2 protein, S cerevisiae Membrane Proteins Monosaccharide Transport Proteins Peptides Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins ras GTPase-Activating Proteins Mating Factor Methyltransferases delta 24-sterol methyltransferase Acyltransferases Serine C-Palmitoyltransferase Ubiquitin-Protein Ligases LCB3 protein, S cerevisiae Phosphoric Monoester Hydrolases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bagnat Michel
Max Planck Institute for Molecular Cell Biology and Genetics, 01307 Dresden, Germany.
Simons Kai
References (39)
39 references, click to expand
  1. Effect of sterol alterations on conjugation in Saccharomyces cerevisiae.
    Yeast. 1992 Dec;8(12):1015-24 PMID: 1293881
  2. The a-factor transporter (STE6 gene product) and cell polarity in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1993 Mar;120(5):1203-15 PMID: 7679674
  3. Fus2 localizes near the site of cell fusion and is required for both cell fusion and nuclear alignment during zygote formation.
    J Cell Biol. 1995 Sep;130(6):1283-96 PMID: 7559752
  4. Pheromone signalling and polarized morphogenesis in yeast.
    Curr Opin Genet Dev. 1997 Feb;7(1):59-66 PMID: 9024634
  5. Pheromone-regulated genes required for yeast mating differentiation.
    J Cell Biol. 1998 Feb 9;140(3):461-83 PMID: 9456310
  6. Rvs161p interacts with Fus2p to promote cell fusion in Saccharomyces cerevisiae.
    J Cell Biol. 1998 May 4;141(3):567-84 PMID: 9566960
  7. A role for the yeast actin cytoskeleton in pheromone receptor clustering and signalling.
    Curr Biol. 1998 Jul 30-Aug 13;8(16):927-30 PMID: 9707405
  8. New constructs and strategies for efficient PCR-based gene manipulations in yeast.
    Yeast. 1998 Sep 15;14(12):1139-46 PMID: 9778799
  9. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  10. Cell polarity and morphogenesis in budding yeast.
    Annu Rev Microbiol. 1998;52:687-744 PMID: 9891811
  11. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease.
    J Cell Biol. 2001 May 14;153(4):649-62 PMID: 11352928
  12. Lipid rafts and signal transduction.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9 PMID: 11413487
  13. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9642-7 PMID: 11493690
  14. Cytoskeleton-dependent membrane domain segregation during neutrophil polarization.
    Mol Biol Cell. 2001 Nov;12(11):3550-62 PMID: 11694588
  15. The Ste5p scaffold.
    J Cell Sci. 2001 Nov;114(Pt 22):3967-78 PMID: 11739629
  16. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast.
    Mol Biol Cell. 2001 Dec;12(12):4129-38 PMID: 11739806
  17. Septins: a ring to part mother and daughter.
    Curr Genet. 2002 Jun;41(3):123-31 PMID: 12111093
  18. The tight junction does not allow lipid molecules to diffuse from one epithelial cell to the next.
    Nature. 1986 Aug 14-20;322(6080):639-41 PMID: 3748143
  19. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein.
    Mol Cell Biol. 1987 Jul;7(7):2316-28 PMID: 3302672
  20. The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol.
    Mol Cell Biol. 1989 Aug;9(8):3447-56 PMID: 2677674
  21. The yeast cell fusion protein FUS1 is O-glycosylated and spans the plasma membrane.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9916-20 PMID: 2690078
  22. Courtship in Saccharomyces cerevisiae: an early cell-cell interaction during mating.
    Mol Cell Biol. 1990 May;10(5):2202-13 PMID: 2183023
  23. Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal.
    Cell. 1990 Nov 30;63(5):1039-51 PMID: 2257622
  24. S. cerevisiae alpha pheromone receptors activate a novel signal transduction pathway for mating partner discrimination.
    Cell. 1991 Oct 18;67(2):389-402 PMID: 1655282
  25. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains.
    Nature. 1992 Mar 5;356(6364):77-9 PMID: 1538785
  26. Membrane raft microdomains mediate front-rear polarity in migrating cells.
    EMBO J. 1999 Nov 15;18(22):6211-20 PMID: 10562533
  27. Specific sterols required for the internalization step of endocytosis in yeast.
    Mol Biol Cell. 1999 Nov;10(11):3943-57 PMID: 10564282
  28. Cell polarity in yeast.
    Annu Rev Cell Dev Biol. 1999;15:365-91 PMID: 10611966
  29. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3254-9 PMID: 10716729
  30. Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae.
    EMBO J. 2000 Jun 15;19(12):2824-33 PMID: 10856228
  31. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast.
    Mol Cell. 2000 May;5(5):841-51 PMID: 10882120
  32. G proteins mediate changes in cell shape by stabilizing the axis of polarity.
    Mol Cell. 2000 May;5(5):853-64 PMID: 10882121
  33. Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway.
    EMBO J. 2000 Sep 1;19(17):4623-31 PMID: 10970855
  34. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier.
    Science. 2000 Oct 13;290(5490):341-4 PMID: 11030653
  35. A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12158-63 PMID: 11027318
  36. Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating.
    J Cell Biol. 2000 Oct 30;151(3):719-30 PMID: 11062271
  37. Protein sorting upon exit from the endoplasmic reticulum.
    Cell. 2001 Jan 26;104(2):313-20 PMID: 11207371
  38. The immunological synapse.
    Annu Rev Immunol. 2001;19:375-96 PMID: 11244041
  39. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression.
    Nucleic Acids Res. 1994 Dec 25;22(25):5767-8 PMID: 7838736
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-10-29
Epub
2002-00-08
Pages
14183-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC137858
Subset
IM
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]