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Microbiol Rev. Mar 1992; 56(1): 180–194.
PMCID: PMC372860

Sexual agglutination in budding yeasts: structure, function, and regulation of adhesion glycoproteins.

Abstract

The sexual agglutinins of the budding yeasts are cell adhesion proteins that promote aggregation of cells during mating. In each yeast species, complementary agglutinins are expressed by cells of opposite mating type that interact to mediate aggregation. Saccharomyces cerevisiae alpha-agglutinin and its analogs from other yeasts are single-subunit glycoproteins that contain N-linked and O-linked oligosaccharides. The N-glycosidase-sensitive carbohydrate is not necessary for activity. The proposed binding domain of alpha-agglutinin has features characteristic of the immunoglobulin fold structures of cell adhesion proteins of higher eukaryotes. The C-terminal region of alpha-agglutinin plays a role in anchoring the glycoprotein to the cell surface. The S. cerevisiae alpha-agglutinin and its analogs from other species contain multiple subunits; one or more binding subunits, which interact with the opposite agglutinin, are disulfide bonded to a core subunit, which mediates cell wall anchorage. The core subunits are composed of 80 to 95% O-linked carbohydrate. The binding subunits have less carbohydrate, and both carbohydrate and peptide play roles in binding. The alpha-agglutinin and alpha-agglutinin genes from S. cerevisiae have been cloned and shown to be regulated by the mating-type locus, MAT, and by pheromone induction. The agglutinins are necessary for mating under conditions that do not promote cell-cell contact. The role of the agglutinins therefore is to promote close interactions between cells of opposite mating type and possibly to facilitate the response to phermone, thus increasing the efficiency of mating. We speculate that they mediate enhanced response to sex pheromones by providing a synapse at the point of cell-cell contact, at which both pheromone secretion and cell fusion occur.

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  • Albelda SM, Buck CA. Integrins and other cell adhesion molecules. FASEB J. 1990 Aug;4(11):2868–2880. [PubMed]
  • Atkinson KD, Kolat AI, Henry SA. Osmotic imbalance in inositol-starved spheroplasts of Saccharomyces cerevisiae. J Bacteriol. 1977 Dec;132(3):806–817. [PMC free article] [PubMed]
  • Baffi RA, Becker JM, Lipke PN, Naider F. Structure-activity relationships in the dodecapeptide alpha-factor of Saccharomyces cerevisiae: position 6 analogues are poor inducers of agglutinability. Biochemistry. 1985 Jun 18;24(13):3332–3337. [PubMed]
  • Baffi RA, Shenbagamurthi P, Terrance K, Becker JM, Naider F, Lipke PN. Different structure-function relationships for alpha-factor-induced morphogenesis and agglutination in Saccharomyces cerevisiae. J Bacteriol. 1984 Jun;158(3):1152–1156. [PMC free article] [PubMed]
  • Brandley BK, Swiedler SJ, Robbins PW. Carbohydrate ligands of the LEC cell adhesion molecules. Cell. 1990 Nov 30;63(5):861–863. [PubMed]
  • BROCK TD. Mating reaction in the yeast Hansenula wingei; preliminary observations and quantitation. J Bacteriol. 1958 Jun;75(6):697–701. [PMC free article] [PubMed]
  • Burke D, Mendonça-Previato L, Ballou CE. Cell-cell recognition in yeast: purification of Hansenula wingei 21-cell sexual agglutination factor and comparison of the factors from three genera. Proc Natl Acad Sci U S A. 1980 Jan;77(1):318–322. [PMC free article] [PubMed]
  • Campbell DA. Kinetics of the mating-specific aggregation in Saccharomyces cerevisiae. J Bacteriol. 1973 Oct;116(1):323–330. [PMC free article] [PubMed]
  • Conzelmann A, Fankhauser C, Desponds C. Myoinositol gets incorporated into numerous membrane glycoproteins of Saccharomyces cerevisiae; incorporation is dependent on phosphomannomutase (sec53). EMBO J. 1990 Mar;9(3):653–661. [PMC free article] [PubMed]
  • Conzelmann A, Riezman H, Desponds C, Bron C. A major 125-kd membrane glycoprotein of Saccharomyces cerevisiae is attached to the lipid bilayer through an inositol-containing phospholipid. EMBO J. 1988 Jul;7(7):2233–2240. [PMC free article] [PubMed]
  • Crandall MA, Brock TD. Molecular basis of mating in the yeast hansenula wingei. Bacteriol Rev. 1968 Sep;32(3):139–163. [PMC free article] [PubMed]
  • Crandall M, Caulton JH. Induction of haploid glycoprotein mating factors in diploid yeasts. Methods Cell Biol. 1975;12:185–207. [PubMed]
  • Crandall M, Lawrence LM, Saunders RM. Molecular complementarity of yeast glycoprotein mating factors. Proc Natl Acad Sci U S A. 1974 Jan;71(1):26–29. [PMC free article] [PubMed]
  • Crandall M, Egel R, Mackay VL. Physiology of mating in three yeasts. Adv Microb Physiol. 1977;15:307–398. [PubMed]
  • Cross F, Hartwell LH, Jackson C, Konopka JB. Conjugation in Saccharomyces cerevisiae. Annu Rev Cell Biol. 1988;4:429–457. [PubMed]
  • Cross GA. Glycolipid anchoring of plasma membrane proteins. Annu Rev Cell Biol. 1990;6:1–39. [PubMed]
  • Doi S, Tanabe K, Watanabe M, Yamaguchi M, Yoshimura M. An alpha-specific gene, SAG1 is required for sexual agglutination in Saccharomyces cerevisiae. Curr Genet. 1989 Jun;15(6):393–398. [PubMed]
  • Doi S, Yoshimura M. Alpha mating type-specific expression of mutations leading to constitutive agglutinability in Saccharomyces cerevisiae. J Bacteriol. 1985 Feb;161(2):596–601. [PMC free article] [PubMed]
  • Farkas V. Biosynthesis of cell walls of fungi. Microbiol Rev. 1979 Jun;43(2):117–144. [PMC free article] [PubMed]
  • Fehrenbacher G, Perry K, Thorner J. Cell-cell recognition in Saccharomyces cerevisiae: regulation of mating-specific adhesion. J Bacteriol. 1978 Jun;134(3):893–901. [PMC free article] [PubMed]
  • Hagiya M, Yoshida K, Yanagishima N. The release of sex-specific substances responsible for sexual agglutination from haploid cells of Saccharomyces cerevisiae. Exp Cell Res. 1977 Feb;104(2):263–272. [PubMed]
  • Hanson BA, Lester RL. Effects of inositol starvation on phospholipid and glycan syntheses in Saccharomyces cerevisiae. J Bacteriol. 1980 Apr;142(1):79–89. [PMC free article] [PubMed]
  • Hartwell LH. Mutants of Saccharomyces cerevisiae unresponsive to cell division control by polypeptide mating hormone. J Cell Biol. 1980 Jun;85(3):811–822. [PMC free article] [PubMed]
  • Hauser K, Tanner W. Purification of the inducible alpha-agglutinin of S. cerevisiae and molecular cloning of the gene. FEBS Lett. 1989 Sep 25;255(2):290–294. [PubMed]
  • Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Dec;52(4):536–553. [PMC free article] [PubMed]
  • Hunter DD, Shah V, Merlie JP, Sanes JR. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature. 1989 Mar 16;338(6212):229–234. [PubMed]
  • Jackson CL, Hartwell LH. Courtship in Saccharomyces cerevisiae: an early cell-cell interaction during mating. Mol Cell Biol. 1990 May;10(5):2202–2213. [PMC free article] [PubMed]
  • Jackson CL, Hartwell LH. Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal. Cell. 1990 Nov 30;63(5):1039–1051. [PubMed]
  • Jenness DD, Spatrick P. Down regulation of the alpha-factor pheromone receptor in S. cerevisiae. Cell. 1986 Aug 1;46(3):345–353. [PubMed]
  • Klebl F, Tanner W. Molecular cloning of a cell wall exo-beta-1,3-glucanase from Saccharomyces cerevisiae. J Bacteriol. 1989 Nov;171(11):6259–6264. [PMC free article] [PubMed]
  • Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [PubMed]
  • Lasky RD, Ballou CE. Cell-cell recognition in yeast: isolation of intact alpha-agglutinin from Saccharomyces kluyveri. Proc Natl Acad Sci U S A. 1988 Jan;85(2):349–353. [PMC free article] [PubMed]
  • Laurent BC, Treitel MA, Carlson M. The SNF5 protein of Saccharomyces cerevisiae is a glutamine- and proline-rich transcriptional activator that affects expression of a broad spectrum of genes. Mol Cell Biol. 1990 Nov;10(11):5616–5625. [PMC free article] [PubMed]
  • Lemontt JF, Fugit DR, Mackay VL. Pleiotropic Mutations at the TUP1 Locus That Affect the Expression of Mating-Type-Dependent Functions in SACCHAROMYCES CEREVISIAE. Genetics. 1980 Apr;94(4):899–920. [PMC free article] [PubMed]
  • Lipke PN, Hull-Pillsbury C. Flocculation of Saccharomyces cerevisiae tup1 mutants. J Bacteriol. 1984 Aug;159(2):797–799. [PMC free article] [PubMed]
  • Lipke PN, Terrance K, Wu YS. Interaction of alpha-agglutinin with Saccharomyces cerevisiae a cells. J Bacteriol. 1987 Feb;169(2):483–488. [PMC free article] [PubMed]
  • Lipke PN, Wojciechowicz D, Kurjan J. AG alpha 1 is the structural gene for the Saccharomyces cerevisiae alpha-agglutinin, a cell surface glycoprotein involved in cell-cell interactions during mating. Mol Cell Biol. 1989 Aug;9(8):3155–3165. [PMC free article] [PubMed]
  • Low MG, Saltiel AR. Structural and functional roles of glycosyl-phosphatidylinositol in membranes. Science. 1988 Jan 15;239(4837):268–275. [PubMed]
  • MacKay VL, Welch SK, Insley MY, Manney TR, Holly J, Saari GC, Parker ML. The Saccharomyces cerevisiae BAR1 gene encodes an exported protein with homology to pepsin. Proc Natl Acad Sci U S A. 1988 Jan;85(1):55–59. [PMC free article] [PubMed]
  • Manney TR. Expression of the BAR1 gene in Saccharomyces cerevisiae: induction by the alpha mating pheromone of an activity associated with a secreted protein. J Bacteriol. 1983 Jul;155(1):291–301. [PMC free article] [PubMed]
  • Marcus S, Xue CB, Naider F, Becker JM. Degradation of a-factor by a Saccharomyces cerevisiae alpha-mating-type-specific endopeptidase: evidence for a role in recovery of cells from G1 arrest. Mol Cell Biol. 1991 Feb;11(2):1030–1039. [PMC free article] [PubMed]
  • Marykwas DL, Fox TD. Control of the Saccharomyces cerevisiae regulatory gene PET494: transcriptional repression by glucose and translational induction by oxygen. Mol Cell Biol. 1989 Feb;9(2):484–491. [PMC free article] [PubMed]
  • McLellan WL, Jr, Lampen JO. Phosphomannanase (PR-factor), an enzyme required for the formation of yeast protoplasts. J Bacteriol. 1968 Mar;95(3):967–974. [PMC free article] [PubMed]
  • Mendonça-Previato L, Burke D, Ballou CE. Sexual agglutination factors from the yeast Pichia amethionina. J Cell Biochem. 1982;19(2):171–178. [PubMed]
  • Miki BL, Poon NH, James AP, Seligy VL. Possible mechanism for flocculation interactions governed by gene FLO1 in Saccharomyces cerevisiae. J Bacteriol. 1982 May;150(2):878–889. [PMC free article] [PubMed]
  • Moore SA. Yeast cells recover from mating pheromone alpha factor-induced division arrest by desensitization in the absence of alpha factor destruction. J Biol Chem. 1984 Jan 25;259(2):1004–1010. [PubMed]
  • Moore SA. Comparison of dose-response curves for alpha factor-induced cell division arrest, agglutination, and projection formation of yeast cells. Implication for the mechanism of alpha factor action. J Biol Chem. 1983 Nov 25;258(22):13849–13856. [PubMed]
  • Nakagawa Y. Genetic analysis of inducible sexual agglutination ability in the yeast Saccharomyces cerevisiae. Arch Microbiol. 1989;151(3):198–202. [PubMed]
  • Nakagawa Y, Yanagishima N. Recessive and dominant genes controlling inducible sexual agglutinability in Saccharomyces cerevisiae. Mol Gen Genet. 1981;183(3):459–462. [PubMed]
  • Nakagawa Y, Yanagishima N. Changes in production of the mating-type-specific glycoproteins, agglutination substances in association with mating type interconversion in homothallic strains of the yeast, Saccharomyces cerevisiae. Mol Gen Genet. 1982;185(2):207–210. [PubMed]
  • Nuoffer C, Jenö P, Conzelmann A, Riezman H. Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiae GAS1 protein to the plasma membrane. Mol Cell Biol. 1991 Jan;11(1):27–37. [PMC free article] [PubMed]
  • Orlean P. Dolichol phosphate mannose synthase is required in vivo for glycosyl phosphatidylinositol membrane anchoring, O mannosylation, and N glycosylation of protein in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Nov;10(11):5796–5805. [PMC free article] [PubMed]
  • Orlean P, Ammer H, Watzele M, Tanner W. Synthesis of an O-glycosylated cell surface protein induced in yeast by alpha factor. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6263–6266. [PMC free article] [PubMed]
  • Osumi M, Shimoda C, Yanagishima N. Mating reaction in Saccharomyces cerevisiae. V. Changes in the fine structure during the mating reaction. Arch Mikrobiol. 1974 Apr 10;97(1):27–38. [PubMed]
  • Pierce M, Ballou CE. Cell-cell recognition in yeast. Characterization of the sexual agglutination factors from Saccharomyces kluyveri. J Biol Chem. 1983 Mar 25;258(6):3576–3582. [PubMed]
  • Roseman S. The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion. Chem Phys Lipids. 1970 Oct;5(1):270–297. [PubMed]
  • Roy A, Lu CF, Marykwas DL, Lipke PN, Kurjan J. The AGA1 product is involved in cell surface attachment of the Saccharomyces cerevisiae cell adhesion glycoprotein a-agglutinin. Mol Cell Biol. 1991 Aug;11(8):4196–4206. [PMC free article] [PubMed]
  • Ruoslahti E. Fibronectin and its receptors. Annu Rev Biochem. 1988;57:375–413. [PubMed]
  • Shenbagamurthi P, Baffi R, Khan SA, Lipke P, Pousman C, Becker JM, Naider F. Structure-activity relationships in the dodecapeptide alpha factor of Saccharomyces cerevisiae. Biochemistry. 1983 Mar 1;22(5):1298–1304. [PubMed]
  • Shimoda C, Yanagishima N. Mating reaction in Saccharomyces cerevisiae. VIII. Mating-type-specific substances responsible for sexual cell agglutination. Antonie Van Leeuwenhoek. 1975;41(4):521–532. [PubMed]
  • Shimoda C, Yanagishima N, Sakurai A, Tamura S. Mating reaction in Saccharomyces cerevisiae. IX. Regulation of sexual cell agglutinability of a type cells by a sex factor produced by alpha type cells. Arch Microbiol. 1976 May 3;108(1):27–33. [PubMed]
  • Sijmons PC, Nederbragt AJ, Klis FM, Van den Ende H. Isolation and composition of the constitutive agglutinins from haploid Saccharomyces cerevisiae cells. Arch Microbiol. 1987 Sep;148(3):208–212. [PubMed]
  • Sprague GF, Jr, Blair LC, Thorner J. Cell interactions and regulation of cell type in the yeast Saccharomyces cerevisiae. Annu Rev Microbiol. 1983;37:623–660. [PubMed]
  • Steiner S, Smith S, Waechter CJ, Lester RL. Isolation and partial characterization of a major inositol-containing lipid in baker's yeast, mannosyl-diinositol, diphosphoryl-ceramide. Proc Natl Acad Sci U S A. 1969 Nov;64(3):1042–1048. [PMC free article] [PubMed]
  • Suzuki K, Yanagishima N. Genetic characterization of an alpha-specific gene responsible for sexual agglutinability in Saccharomyces cerevisiae: mapping and gene dose effect. Curr Genet. 1986;10(5):353–357. [PubMed]
  • TAYLOR NW. SPECIFIC, SOLUBLE FACTOR INVOLVED IN SEXUAL AGGLUTINATION OF THE YEAST HANSENULA WINGEI. J Bacteriol. 1964 Apr;87:863–866. [PMC free article] [PubMed]
  • Taylor NW, Orton WL. Association constant of the sex-specific agglutinin in the yeast, Hansenula wingei. Biochemistry. 1970 Jul 7;9(14):2931–2934. [PubMed]
  • Taylor NW, Orton WL. Cooperation among the active binding sites in the sex-specific agglutinin from the yeast, Hansenula wingei. Biochemistry. 1971 May 25;10(11):2043–2049. [PubMed]
  • Terrance K, Heller P, Wu YS, Lipke PN. Identification of glycoprotein components of alpha-agglutinin, a cell adhesion protein from Saccharomyces cerevisiae. J Bacteriol. 1987 Feb;169(2):475–482. [PMC free article] [PubMed]
  • Terrance K, Lipke PN. Sexual agglutination in Saccharomyces cerevisiae. J Bacteriol. 1981 Dec;148(3):889–896. [PMC free article] [PubMed]
  • Terrance K, Lipke PN. Pheromone induction of agglutination in Saccharomyces cerevisiae a cells. J Bacteriol. 1987 Oct;169(10):4811–4815. [PMC free article] [PubMed]
  • von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. [PMC free article] [PubMed]
  • Watzele M, Klis F, Tanner W. Purification and characterization of the inducible a agglutinin of Saccharomyces cerevisiae. EMBO J. 1988 May;7(5):1483–1488. [PMC free article] [PubMed]
  • Weinstock K, Ballou CE. Cell-cell recognition in yeast. Molecular nature of the sexual agglutinin from Saccharomyces kluyveri 17-cells. J Biol Chem. 1986 Dec 5;261(34):16174–16179. [PubMed]
  • WICKERHAM LJ. Sexual agglutination of heterothallic yeasts in diverse taxonomic areas. Science. 1958 Dec 12;128(3337):1504–1505. [PubMed]
  • Williams AF, Barclay AN. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. [PubMed]
  • Williams FE, Trumbly RJ. Characterization of TUP1, a mediator of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6500–6511. [PMC free article] [PubMed]
  • Yamaguchi M, Yoshida K, Yanagishima N. Isolation and partial characterization of cytoplasmic alpha agglutination substance in the yeast Saccharomyces cerevisiae. FEBS Lett. 1982 Mar 8;139(1):125–129. [PubMed]
  • Yen PH, Ballou CE. Structure and immunochemistry of Hansenula wingei Y-2340 mannan. Biochemistry. 1974 May 21;13(11):2420–2427. [PubMed]
  • Yen PH, Ballou CE. Partial characterization of the sexual agglutination factor from Hansenula wingei Y-2340 type 5 cells. Biochemistry. 1974 May 21;13(11):2428–2437. [PubMed]
  • Yoshida K, HAGIYA M, Yanagishima N. Isolation and purification of the sexual agglutination substance of mating type a cells in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1976 Aug 23;71(4):1085–1094. [PubMed]
  • Yoshida K, Hisatomi T, Yanagishima N. Sexual behavior and its pheromonal regulation in ascosporogenous yeasts. J Basic Microbiol. 1989;29(2):99–128. [PubMed]
  • Zlotnik H, Fernandez MP, Bowers B, Cabib E. Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J Bacteriol. 1984 Sep;159(3):1018–1026. [PMC free article] [PubMed]

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