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Chemical Gradients and Chemotropism in Yeast Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press Chemical Gradients and Chemotropism in Yeast Robert A. Arkowitz Institute of Developmental Biology and Cancer, Universite´ de Nice - Sophia Antipolis – CNRS UMR6543, Centre de Biochimie, Faculte´ des Sciences, Parc Valrose, 06108 Nice Cedex 2, FRANCE Correspondence: [email protected] Chemical gradients of peptide mating pheromones are necessary for directional growth, which is critical for yeast mating. These gradients are generated by cell-type specific secretion or export and specific degradation in receiving cells. Spatial information is sensed by dedicated seven-transmembrane G-protein coupled receptors and yeast cells are able to detect extremely small differences in ligand concentration across their 5-mm cell surface. Here, I will discuss our current knowledge of how cells detect and respond to such shallow chemical gradients and in particular what is known about the proteins that are involved in directional growth and the establishment of the polarity axis during yeast mating. hemical gradients play critical roles in a G-proteins, as well the mechanisms involved Clarge number of developmental processes. in detection of small differences in ligand con- These gradients, which are precisely controlled centration across a yeast cell. The third section at both temporal and spatial levels, provide focuses on the different cellular responses an efficient means of encoding vectorial during chemotropism, in addition to what is information. Although diverse fungi generate known about how a growth site and an axis of chemical pheromone gradients during mating, polarity are established in response to an exter- because of its genetic tractability, most studies nal gradient. on chemical gradients in yeast have focused on Saccharomyces cerevisiae. This review will GRADIENTS focus on the role of chemical pheromone gradients during S. cerevisiae mating, as our Most fungi produce diffusible peptide mating knowledge of the molecular details of this pheromones and in general, there are two chemotropic process is most advanced. This different peptide mating factors (reviewed in review is divided into four main sections: Caldwell et al. 1995) in each species. Given the gradients, sensing and detection, cellular dynamic nature of pheromone gradients, it is responses, and signal amplification. The not surprising that they have not been directly second and third sections are further divided, measured. Rather, various methods have been with the second section addressing the roles of used to generate such gradients artificially and pheromone receptors and hetero-trimeric to determine cellular responses over a range of Editors: James Briscoe, Peter Lawrence, and Jean-Paul Vincent Additional Perspectives on Generation and Interpretation of Morphogen Gradients available at www.cshperspectives.org Copyright # 2009 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a001958 Cite this article as Cold Spring Harb Perspect Biol 2009;1:a001958 1 Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press R.A. Arkowitz chemical gradient concentrations and slopes. essentially cell-associated (Marcus et al. 1991). During S. cerevisiae mating, pheromone gradi- A gradient of secreted a-factor protease, or ents are generated by the secretion of a- and cell-associated a-factor protease, is likely to a-factor. There are three factors that are likely sharpen the pheromone gradient. Finally, to be important for the generation of phero- pheromone degradation via a cell-associated mone gradients: first, the physical character- protease has been proposed as a means for dis- istics of the mating pheromone; second, tinguishing potential mating partners amongst the site(s) of pheromone secretion or export; many cells (Barkai et al. 1998). and third, the distribution of proteases that degrade mating pheromone. The shape of a mating pheromone gradient is likely to be SENSING AND DETECTION dependent on the diffusibility of the mating Pheromone Receptors peptide, and as a-factor is farnesylated, its diffu- sion in aqueous environments is decreased. This Yeast cells must detect a mating pheromone posttranslational modification may be critical gradient to initiate a range of cellular responses. in hydrophobic milieu, such as cellular mem- Critical for such detection are the classi- branes or natural habitats including biofilms. cal seven-transmembrane domain receptors The increased hydrophobicity and reduced coupled to hetero-trimeric G-proteins (for diffusibility of a-factor (Caldwell et al. 1994; review, see Xue et al. 2008), the a-cell specific Khouri et al. 1996) may contribute to the Ste2 (which binds a-factor), and the a-cell further sharpening (increasing the steepness) or specific Ste3 (which binds a-factor). These stabilizing of its gradient compared with that of receptors do not share substantial sequence a-factor. Furthermore, pheromones are likely to homology. Transcription of both receptors is be secreted (a-factor) or exported (a-factor via rapidly increased on addition of the respective the Ste6 transporter) from the tip of shmoos pheromone (Hagen and Sprague 1984; Hartig (Kuchler et al. 1993), and this site-specific et al. 1986). Haploid a-cells have 10,000 release will dictate the shape of the gradient. cell-surface binding sites for a-factor with a Site-specific secretion or export will generate Kd of 4–6 nM (Jenness et al. 1986; Stefan anisotropy in the mating pheromone gradient, et al. 1998). This high-affinity receptor resting which should provide information on cell po- state is converted to a low-affinity state, with sition. Specifically, the location of a particular an 10-fold increase in ligand off-rate and shmoo tip should be evident by the position, corresponding increase in Kd, in the presence direction, and shape of its pheromone gradient. of GTPgS (Blumer and Thorner 1990). Mating pheromone proteases are also When haploid a-cells bind a-factor, Ste2 secreted, yet little is known about whether receptors are internalized with a tavg. of 8 their secretion occurs at a specific site. min (Schandel and Jenness 1994) and reappear Proteases, such as the barrier aspartyl protease on the cell surface after 60 min (Jenness and Bar1, limits the distance of the a-factor trideca- Spatrick 1986; Ayscough and Drubin 1998; peptide gradient (Barkai et al. 1998). Similarly, Stefan et al. 1998). Both a- and a-factor re- a protease activity that degrades a-factor has ceptors have substantial—183 and 133 amino been identified in MATa cells (Marcus et al. acids, respectively—cytoplasmic carboxy ter- 1991). Each of these pheromone proteases are mini. Truncation of the Ste2 carboxy- expressed only in receiving cells. The a-factor terminal 105 amino acids results in a fivefold protease Bar1 is largely secreted, with 95% of increase in cell surface pheromone binding the Bar1 activity found extracellularly (Ciejek sites, a 10-fold increase in pheromone sensi- and Thorner 1979; Ballensiefen and Schmitt tivity, and a defect in pheromone induced 1997). This protease has also been found, morphogenesis (Konopka et al. 1988). Ste2 however, attached to the cell wall (Moukadiri receptors also oligomerize in vivo, yet this et al. 1999). a-factor protease activity is also association does not depend on ligand 2 Cite this article as Cold Spring Harb Perspect Biol 2009;1:a001958 Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press Chemical Gradients and Chemotropism in Yeast nor hetero-trimeric G-protein (Overton and Hetero-trimeric G-protein Blumer 2000; Yesilaltay and Jenness 2000). The pheromone receptor functions as a guanine Ste2 transmembrane domains five and six nucleotide exchange factor for Ga. On phero- together with the intervening third intracellular mone binding, the receptor catalyzes the loop are important for G-protein activation, via exchange of GDP for GTP in the Ga†GDP Ga (Konopka and Jenness 1991; Clark et al. Gbg complex, resulting in the dissociation of 1994; Stefan and Blumer 1994; Dube et al. Ga†GTP from Gbg (reviewed in Dohlman 2000; Celic et al. 2003; Lin et al. 2003). The and Thorner 2001; Dohlman 2002). Ga and carboxy-terminal cytoplasmic domain of the Gbg are then able to associate and activate receptor interacts with Ga in a preactivation downstream effectors. This signaling compe- complex (Dosil et al. 2000; Wu et al. 2004). tent state of the Ga and Gbg subunits exists The extracellular end of transmembrane until the Ga†GTP is hydrolyzed. RGS domain 1, together with the extracellular (Regulators of G protein Signaling) proteins loops 1 and 2, interact directly with pheromone such as Sst2, function as GTPase accelerating (Son et al. 2004; Hauser et al. 2007). Although proteins or GAPs facilitating Ga GTP hydro- pheromone receptors are necessary for detect- lysis (Apanovitch et al. 1998; DiBello et al. ing pheromone, it is likely that their internali- 1998). Receptor and hetero-trimeric G-protein zation and recycling play an important role in turnover, either by cellular uptake (endocytosis) signal amplification and desensitization. or posttranslational modification (including In the absence of mating pheromone, modifications that target proteins for degra- both pheromone receptors localize uniformly dation) also contribute to down-regulation. over the cell surface as well as endosomal and Initial
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