Counteractive control of polarized morphogenesis during mating by mitogen-activated protein kinase Fus3 and G1 cyclin-dependent kinase

• Published in: Molecular biology of the cell 2008-04, Vol.19 (4), p.1739-1752
• Main Authors: Yu, Lu, Qi, Maosong, Sheff, Mark A, Elion, Elaine A
• Format: Article
• Language: English
• Subjects: Actins - metabolism; Adaptor Proteins, Signal Transducing - genetics; Adaptor Proteins, Signal Transducing - metabolism; CDC28 Protein Kinase, S cerevisiae - genetics; CDC28 Protein Kinase, S cerevisiae - metabolism; Cell Cycle Proteins - genetics; Cell Cycle Proteins - metabolism; Cell Membrane - metabolism; Cell Polarity; Cyclin-Dependent Kinases - genetics; Cyclin-Dependent Kinases - metabolism; Cyclins - genetics; Cyclins - metabolism; G1 Phase; Genes, Fungal; Guanine Nucleotide Exchange Factors - genetics; Guanine Nucleotide Exchange Factors - metabolism; Intracellular Signaling Peptides and Proteins; MAP Kinase Kinase Kinases; MAP Kinase Signaling System; Microfilament Proteins - genetics; Microfilament Proteins - metabolism; Mitogen-Activated Protein Kinases - genetics; Mitogen-Activated Protein Kinases - metabolism; Models, Biological; Morphogenesis; Mutation; Protein Serine-Threonine Kinases - genetics; Protein Serine-Threonine Kinases - metabolism; Recombinant Fusion Proteins - genetics; Recombinant Fusion Proteins - metabolism; Saccharomyces cerevisiae - cytology; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - growth & development; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae Proteins - genetics; Saccharomyces cerevisiae Proteins - metabolism
• ISSN: 1059-1524; 1939-4586
• DOI: 10.1091/mbc.e07-08-0757

Cell polarization in response to external cues is critical to many eukaryotic cells. During pheromone-induced mating in Saccharomyces cerevisiae, the mitogen-activated protein kinase (MAPK) Fus3 induces polarization of the actin cytoskeleton toward a landmark generated by the pheromone receptor. Here, we analyze the role of Fus3 activation and cell cycle arrest in mating morphogenesis. The MAPK scaffold Ste5 is initially recruited to the plasma membrane in random patches that polarize before shmoo emergence. Polarized localization of Ste5 is important for shmooing. In fus3 mutants, Ste5 is recruited to significantly more of the plasma membrane, whereas recruitment of Bni1 formin, Cdc24 guanine exchange factor, and Ste20 p21-activated protein kinase are inhibited. In contrast, polarized recruitment still occurs in a far1 mutant that is also defective in G1 arrest. Remarkably, loss of Cln2 or Cdc28 cyclin-dependent kinase restores polarized localization of Bni1, Ste5, and Ste20 to a fus3 mutant. These and other findings suggest Fus3 induces polarized growth in G1 phase cells by down-regulating Ste5 recruitment and by inhibiting Cln/Cdc28 kinase, which prevents basal recruitment of Ste5, Cdc42-mediated asymmetry, and mating morphogenesis.