The final cut: cell polarity meets cytokinesis at the bud neck in S. cerevisiae

Chia W, Somers WG, Wang H (2008) Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J Cell Biol 180:267–272 Doe CQ (2008) Neural stem cells: balancing self-renewal with differentiation. Development 135(9):1575–1587 Knoblich JA (2008) Mechanisms of asymmetric stem cell division. Cell 132(4):583–597 Gonzalez C (2007) Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat Rev Genet 8(6):462–472 Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441(7097):1068–1074 Neumuller RA, Knoblich JA (2009) Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23(23):2675–2699 Siller KH, Doe CQ (2009) Spindle orientation during asymmetric cell division. Nat Cell Biol 11(4):365–374 Barr FA, Gruneberg U (2007) Cytokinesis: placing and making the final cut. Cell 131(5):847–860 Bringmann H, Hyman AA (2005) A cytokinesis furrow is positioned by two consecutive signals. Nature 436(7051):731–734 Dechant R, Glotzer M (2003) Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev Cell 4(3):333–344 Oliferenko S, Chew TG, Balasubramanian MK (2009) Positioning cytokinesis. Genes Dev 23(6):660–674 Caydasi AK, Ibrahim B, Pereira G (2010) Monitoring spindle orientation: spindle position checkpoint in charge. Cell Div 5:28 Fraschini R, Venturetti M, Chiroli E, Piatti S (2008) The spindle position checkpoint: how to deal with spindle misalignment during asymmetric cell division in budding yeast. Biochem Soc Trans 36(Pt 3):416–420 Mortimer RK, Johnston JR (1959) Life span of individual yeast cells. Nature 183(4677):1751–1752 Colman-Lerner A, Chin TE, Brent R (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107(6):739–750 Mazanka E, Alexander J, Yeh BJ, Charoenpong P, Lowery DM, Yaffe M, Weiss EL (2008) The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry. PLoS Biol 6(8):e203 Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422(6933):766–774 Park HO, Bi E (2007) Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71(1):48–96 Macara IG, McCaffrey L (2013) Cell polarity in morphogenesis and metastasis. Philos Trans R Soc Lond B Biol Sci 368(1629):20130012 Muthuswamy SK, Xue B (2012) Cell polarity as a regulator of cancer cell behavior plasticity. Annu Rev Cell Dev Biol 28:599–625 Pruyne D, Bretscher A (2000) Polarization of cell growth in yeast. J Cell Sci 113(Pt 4):571–585 Pruyne D, Bretscher A (2000) Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113(3):365–375 Martin SG, Arkowitz RA (2014) Cell polarization in budding and fission yeasts. FEMS Microbiol Rev 38(2):228–253 Moseley JB, Goode BL (2006) The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol Mol Biol Rev 70(3):605–645 Engqvist-Goldstein AE, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287–332 Goode BL, Eskin JA, Wendland B (2015) Actin and endocytosis in budding yeast. Genetics 199(2):315–358 Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119(Pt 22):4589–4598 Adams AE, Pringle JR (1984) Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol 98(3):934–945 Pruyne DW, Schott DH, Bretscher A (1998) Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J Cell Biol 143(7):1931–1945 Kilmartin JV, Adams AE (1984) Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol 98(3):922–933 Sagot I, Klee SK, Pellman D (2002) Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat Cell Biol 4(1):42–50 Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4(8):626–631 Zahner JE, Harkins HA, Pringle JR (1996) Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae. Mol Cell Biol 16(4):1857–1870 Bi E, Maddox P, Lew DJ, Salmon ED, McMillan JN, Yeh E, Pringle JR (1998) Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J Cell Biol 142(5):1301–1312 Lippincott J, Li R (1998) Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J Cell Biol 140(2):355–366 Chant J, Herskowitz I (1991) Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65(7):1203–1212 Park HO, Bi E, Pringle JR, Herskowitz I (1997) Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc Natl Acad Sci USA 94(9):4463–4468 Park HO, Chant J, Herskowitz I (1993) BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature 365(6443):269–274 Bi E, Park HO (2012) Cell polarization and cytokinesis in budding yeast. Genetics 191(2):347–387 Casamayor A, Snyder M (2002) Bud-site selection and cell polarity in budding yeast. Curr Opin Microbiol 5(2):179–186 Howell AS, Lew DJ (2012) Morphogenesis and the cell cycle. Genetics 190(1):51–77 Lew DJ, Reed SI (1993) Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol 120(6):1305–1320 Bourne HR, Sanders DA, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348(6297):125–132 Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294(5545):1299–1304 Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349(6305):117–127 Schweins T, Wittinghofer A (1994) GTP-binding proteins. Structures, interactions and relationships. Curr Biol 4(6):547–550 Dransart E, Olofsson B, Cherfils J (2005) RhoGDIs revisited: novel roles in Rho regulation. Traffic 6(11):957–966 Bose I, Irazoqui JE, Moskow JJ, Bardes ES, Zyla TR, Lew DJ (2001) Assembly of scaffold-mediated complexes containing Cdc42p, the exchange factor Cdc24p, and the effector Cla4p required for cell cycle-regulated phosphorylation of Cdc24p. J Biol Chem 276(10):7176–7186 Howell AS, Savage NS, Johnson SA, Bose I, Wagner AW, Zyla TR, Nijhout HF, Reed MC, Goryachev AB, Lew DJ (2009) Singularity in polarization: rewiring yeast cells to make two buds. Cell 139(4):731–743 Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ (2008) Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 18(22):1719–1726 Jose M, Tollis S, Nair D, Sibarita JB, McCusker D (2013) Robust polarity establishment occurs via an endocytosis-based cortical corralling mechanism. J Cell Biol 200(4):407–418 Slaughter BD, Das A, Schwartz JW, Rubinstein B, Li R (2009) Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev Cell 17(6):823–835 Cvrckova F, De Virgilio C, Manser E, Pringle JR, Nasmyth K (1995) Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast. Genes Dev 9(15):1817–1830 Goehring AS, Mitchell DA, Tong AH, Keniry ME, Boone C, Sprague GF Jr (2003) Synthetic lethal analysis implicates Ste20p, a p21-activated protein kinase, in polarisome activation. Mol Biol Cell 14(4):1501–1516 Holly SP, Blumer KJ (1999) PAK-family kinases regulate cell and actin polarization throughout the cell cycle of Saccharomyces cerevisiae. J Cell Biol 147(4):845–856 Kadota J, Yamamoto T, Yoshiuchi S, Bi E, Tanaka K (2004) Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Mol Biol Cell 15(12):5329–5345 Versele M, Thorner J (2004) Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J Cell Biol 164(5):701–715 Weiss EL, Bishop AC, Shokat KM, Drubin DG (2000) Chemical genetic analysis of the budding-yeast p21-activated kinase cla4p [In Process Citation]. Nat Cell Biol 2(10):677–685 Dong Y, Pruyne D, Bretscher A (2003) Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J Cell Biol 161(6):1081–1092 Brown JL, Jaquenoud M, Gulli MP, Chant J, Peter M (1997) Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev 11(22):2972–2982 Chen GC, Kim YJ, Chan CS (1997) The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev 11(22):2958–2971 Chen H, Kuo CC, Kang H, Howell AS, Zyla TR, Jin M, Lew DJ (2012) Cdc42p regulation of the yeast formin Bni1p mediated by the effector Gic2p. Mol Biol Cell 23(19):3814–3826 Iwase M, Luo J, Nagaraj S, Longtine M, Kim HB, Haarer BK, Caruso C, Tong Z, Pringle JR, Bi E (2006) Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol Biol Cell 17(3):1110–1125 Zhang X, Bi E, Novick P, Du L, Kozminski KG, Lipschutz JH, Guo W (2001) Cdc42 interacts with the exocyst and regulates polarized secretion. J Biol Chem 276(50):46745–46750 Zhang X, Orlando K, He B, Xi F, Zhang J, Zajac A, Guo W (2008) Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J Cell Biol 180(1):145–158 Imamura H, Tanaka K, Hihara T, Umikawa M, Kamei T, Takahashi K, Sasaki T, Takai Y (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J 16(10):2745–2755 Kohno H, Tanaka K, Mino A, Umikawa M, Imamura H, Fujiwara T, Fujita Y, Hotta K, Qadota H, Watanabe T, Ohya Y, Takai Y (1996) Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J 15(22):6060–6068 Qadota H, Python CP, Inoue SB, Arisawa M, Anraku Y, Zheng Y, Watanabe T, Levin DE, Ohya Y (1996) Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-beta-glucan synthase. Science 272(5259):279–281 Kamada Y, Qadota H, Python CP, Anraku Y, Ohya Y, Levin DE (1996) Activation of yeast protein kinase C by Rho1 GTPase. J Biol Chem 271(16):9193–9196 Nonaka H, Tanaka K, Hirano H, Fujiwara T, Kohno H, Umikawa M, Mino A, Takai Y (1995) A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J 14(23):5931–5938 Guo W, Tamanoi F, Novick P (2001) Spatial regulation of the exocyst complex by Rho1 GTPase. Nat Cell Biol 3(4):353–360 Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M (2008) Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol 25(12):2717–2733 Chesarone MA, DuPage AG, Goode BL (2010) Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rev Mol Cell Biol 11(1):62–74 Evangelista M, Blundell K, Longtine MS, Chow CJ, Adames N, Pringle JR, Peter M, Boone C (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276(5309):118–122 Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4(3):260–269 Pruyne D, Gao L, Bi E, Bretscher A (2004) Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol Biol Cell 15(11):4971–4989 Buttery SM, Yoshida S, Pellman D (2007) Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol Biol Cell 18(5):1826–1838 Delgehyr N, Lopes CS, Moir CA, Huisman SM, Segal M (2008) Dissecting the involvement of formins in Bud6p-mediated cortical capture of microtubules in S. cerevisiae. J Cell Sci 121(Pt 22):3803–3814 Moseley JB, Goode BL (2005) Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J Biol Chem 280(30):28023–28033 Wen KK, Rubenstein PA (2009) Differential regulation of actin polymerization and structure by yeast formin isoforms. J Biol Chem 284(25):16776–16783 Kamei T, Tanaka K, Hihara T, Umikawa M, Imamura H, Kikyo M, Ozaki K, Takai Y (1998) Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J Biol Chem 273(43):28341–28345 Ozaki-Kuroda K, Yamamoto Y, Nohara H, Kinoshita M, Fujiwara T, Irie K, Takai Y (2001) Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol Cell Biol 21(3):827–839 Fujiwara T, Tanaka K, Mino A, Kikyo M, Takahashi K, Shimizu K, Takai Y (1998) Rho1p–Bni1p–Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol Biol Cell 9(5):1221–1233 Sheu YJ, Santos B, Fortin N, Costigan C, Snyder M (1998) Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol Cell Biol 18(7):4053–4069 Graziano BR, DuPage AG, Michelot A, Breitsprecher D, Moseley JB, Sagot I, Blanchoin L, Goode BL (2011) Mechanism and cellular function of Bud6 as an actin nucleation-promoting factor. Mol Biol Cell 22(21):4016–4028. doi:10.1091/mbc.E11-05-0404 Graziano BR, Jonasson EM, Pullen JG, Gould CJ, Goode BL (2013) Ligand-induced activation of a formin-NPF pair leads to collaborative actin nucleation. J Cell Biol 201(4):595–611 Moseley JB, Sagot I, Manning AL, Xu Y, Eck MJ, Pellman D, Goode BL (2004) A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol Biol Cell 15(2):896–907 Xu Y, Moseley JB, Sagot I, Poy F, Pellman D, Goode BL, Eck MJ (2004) Crystal structures of a formin homology-2 domain reveal a tethered dimer architecture. Cell 116(5):711–723 Pring M, Evangelista M, Boone C, Yang C, Zigmond SH (2003) Mechanism of formin-induced nucleation of actin filaments. Biochemistry 42(2):486–496 Castrillon DH, Wasserman SA (1994) Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120(12):3367–3377 Alberts AS (2001) Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 276(4):2824–2830 Li F, Higgs HN (2005) Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J Biol Chem 280(8):6986–6992 Gould CJ, Maiti S, Michelot A, Graziano BR, Blanchoin L, Goode BL (2011) The formin DAD domain plays dual roles in autoinhibition and actin nucleation. Curr Biol 21(5):384–390 Lammers M, Rose R, Scrima A, Wittinghofer A (2005) The regulation of mDia1 by autoinhibition and its release by Rho*GTP. EMBO J 24(23):4176–4187 Wallar BJ, Stropich BN, Schoenherr JA, Holman HA, Kitchen SM, Alberts AS (2006) The basic region of the diaphanous-autoregulatory domain (DAD) is required for autoregulatory interactions with the diaphanous-related formin inhibitory domain. J Biol Chem 281(7):4300–4307 Li F, Higgs HN (2003) The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13(15):1335–1340 Liu W, Sato A, Khadka D, Bharti R, Diaz H, Runnels LW, Habas R (2008) Mechanism of activation of the Formin protein Daam1. Proc Natl Acad Sci USA 105(1):210–215 Nezami AG, Poy F, Eck MJ (2006) Structure of the autoinhibitory switch in formin mDia1. Structure 14(2):257–263 Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A (2005) Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435(7041):513–518 Seth A, Otomo C, Rosen MK (2006) Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1. J Cell Biol 174(5):701–713 Lees JG, Bach CT, O’Neill GM (2011) Interior decoration: tropomyosin in actin dynamics and cell migration. Cell Adhes Migr 5(2):181–186 Vindin H, Gunning P (2013) Cytoskeletal tropomyosins: choreographers of actin filament functional diversity. J Muscle Res Cell Motil 34(3–4):261–274 Liu HP, Bretscher A (1989) Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57(2):233–242 Skau CT, Neidt EM, Kovar DR (2009) Role of tropomyosin in formin-mediated contractile ring assembly in fission yeast. Mol Biol Cell 20(8):2160–2173 Chesarone-Cataldo M, Guerin C, Yu JH, Wedlich-Soldner R, Blanchoin L, Goode BL (2011) The myosin passenger protein Smy1 controls actin cable structure and dynamics by acting as a formin damper. Dev Cell 21(2):217–230 Eskin JA, Rankova A, Johnston AB, Alioto SL, Goode BL (2016) Common formin-regulating sequences in Smy1 and Bud14 are required for the control of actin cable assembly in vivo. Mol Biol Cell 27:828–837 Mohapatra L, Goode BL, Kondev J (2015) Antenna mechanism of length control of actin cables. PLoS Comput Biol 11(6):e1004160 Chesarone M, Gould CJ, Moseley JB, Goode BL (2009) Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Dev Cell 16(2):292–302 Gould CJ, Chesarone-Cataldo M, Alioto SL, Salin B, Sagot I, Goode BL (2014) Saccharomyces cerevisiae Kelch proteins and Bud14 protein form a stable 520-kDa formin regulatory complex that controls actin cable assembly and cell morphogenesis. J Biol Chem 289(26):18290–18301 Philips J, Herskowitz I (1998) Identification of Kel1p, a kelch domain-containing protein involved in cell fusion and morphology in Saccharomyces cerevisiae. J Cell Biol 143(2):375–389 Oh Y, Schreiter J, Nishihama R, Wloka C, Bi E (2013) Targeting and functional mechanisms of the cytokinesis-related F-BAR protein Hof1 during the cell cycle. Mol Biol Cell 24(9):1305–1320 Vallen EA, Caviston J, Bi E (2000) Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol Biol Cell 11(2):593–611 Graziano BR, Yu HY, Alioto SL, Eskin JA, Ydenberg CA, Waterman DP, Garabedian M, Goode BL (2014) The F-BAR protein Hof1 tunes formin activity to sculpt actin cables during polarized growth. Mol Biol Cell 25(11):1730–1743 Buttery SM, Kono K, Stokasimov E, Pellman D (2012) Regulation of the formin Bnr1 by septins anda MARK/Par1-family septin-associated kinase. Mol Biol Cell 23(20):4041–4053 Wang J, Neo SP, Cai M (2009) Regulation of the yeast formin Bni1p by the actin-regulating kinase Prk1p. Traffic 10(5):528–535 Matheos D, Metodiev M, Muller E, Stone D, Rose MD (2004) Pheromone-induced polarization is dependent on the Fus3p MAPK acting through the formin Bni1p. J Cell Biol 165(1):99–109 Bloom J, Cristea IM, Procko AL, Lubkov V, Chait BT, Snyder M, Cross FR (2011) Global analysis of Cdc14 phosphatase reveals diverse roles in mitotic processes. J Biol Chem 286(7):5434–5445 Orii M, Kono K, Wen HI, Nakanishi M (2016) PP1-dependent formin Bnr1 dephosphorylation and delocalization from a cell division site. PLoS One 11(1):e0146941 Kono K, Saeki Y, Yoshida S, Tanaka K, Pellman D (2012) Proteasomal degradation resolves competition between cell polarization and cellular wound healing. Cell 150(1):151–164 VerPlank L, Li R (2005) Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. Mol Biol Cell 16(5):2529–2543 Amberg DC, Zahner JE, Mulholland JW, Pringle JR, Botstein D (1997) Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol Biol Cell 8(4):729–753 Finger FP, Hughes TE, Novick P (1998) Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92(4):559–571 Meitinger F, Richter H, Heisel S, Hub B, Seufert W, Pereira G (2013) A safeguard mechanism regulates Rho GTPases to coordinate cytokinesis with the establishment of cell polarity. PLoS Biol 11(2):e1001495 Tolliday N, VerPlank L, Li R (2002) Rho1 directs formin-mediated actin ring assembly during budding yeast cytokinesis. Curr Biol 12(21):1864–1870 Annan RB, Lee AY, Reid ID, Sayad A, Whiteway M, Hallett M, Thomas DY (2009) A biochemical genomics screen for substrates of Ste20p kinase enables the in silico prediction of novel substrates. PLoS One 4(12):e8279 Tong Z, Gao XD, Howell AS, Bose I, Lew DJ, Bi E (2007) Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition. J Cell Biol 179(7):1375–1384 Ziman M, Preuss D, Mulholland J, O’Brien JM, Botstein D, Johnson DI (1993) Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol Biol Cell 4(12):1307–1316 Atkins BD, Yoshida S, Saito K, Wu CF, Lew DJ, Pellman D (2013) Inhibition of Cdc42 during mitotic exit is required for cytokinesis. J Cell Biol 202(2):231–240 Yoshida S, Bartolini S, Pellman D (2009) Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev 23(7):810–823. doi:10.1101/gad.1785209 Yoshida S, Kono K, Lowery DM, Bartolini S, Yaffe MB, Ohya Y, Pellman D (2006) Polo-like kinase Cdc5 controls the local activation of Rho1 to promote cytokinesis. Science 313(5783):108–111 Heider MR, Gu M, Duffy CM, Mirza AM, Marcotte LL, Walls AC, Farrall N, Hakhverdyan Z, Field MC, Rout MP, Frost A, Munson M (2016) Subunit connectivity, assembly determinants and architecture of the yeast exocyst complex. Nat Struct Mol Biol 23(1):59–66 TerBush DR, Maurice T, Roth D, Novick P (1996) The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15(23):6483–6494 TerBush DR, Novick P (1995) Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J Cell Biol 130(2):299–312 Aronov S, Gerst JE (2004) Involvement of the late secretory pathway in actin regulation and mRNA transport in yeast. J Biol Chem 279(35):36962–36971 Mulholland J, Wesp A, Riezman H, Botstein D (1997) Yeast actin cytoskeleton mutants accumulate a new class of Golgi-derived secretary vesicle. Mol Biol Cell 8(8):1481–1499 Jourdain I, Dooley HC, Toda T (2012) Fission yeast sec3 bridges the exocyst complex to the actin cytoskeleton. Traffic 13(11):1481–1495 Adamo JE, Moskow JJ, Gladfelter AS, Viterbo D, Lew DJ, Brennwald PJ (2001) Yeast Cdc42 functions at a late step in exocytosis, specifically during polarized growth of the emerging bud. J Cell Biol 155(4):581–592 Roumanie O, Wu H, Molk JN, Rossi G, Bloom K, Brennwald P (2005) Rho GTPase regulation of exocytosis in yeast is independent of GTP hydrolysis and polarization of the exocyst complex. J Cell Biol 170(4):583–594 Oh Y, Bi E (2010) Septin structure and function in yeast and beyond. Trends Cell Biol 21(3):141–148 Weirich CS, Erzberger JP, Barral Y (2008) The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 9(6):478–489 Hartwell LH (1971) Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69(2):265–276 Berlin A, Paoletti A, Chang F (2003) Mid2p stabilizes septin rings during cytokinesis in fission yeast. J Cell Biol 160(7):1083–1092 Tasto JJ, Morrell JL, Gould KL (2003) An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J Cell Biol 160(7):1093–1103 An H, Morrell JL, Jennings JL, Link AJ, Gould KL (2004) Requirements of fission yeast septins for complex formation, localization, and function. Mol Biol Cell 15(12):5551–5564 Martin-Cuadrado AB, Morrell JL, Konomi M, An H, Petit C, Osumi M, Balasubramanian M, Gould KL, Del Rey F, de Aldana CR (2005) Role of septins and the exocyst complex in the function of hydrolytic enzymes responsible for fission yeast cell separation. Mol Biol Cell 16(10):4867–4881 Bertin A, McMurray MA, Grob P, Park SS, Garcia G 3rd, Patanwala I, Ng HL, Alber T, Thorner J, Nogales E (2008) Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci USA 105(24):8274–8279 Garcia G 3rd, Bertin A, Li Z, Song Y, McMurray MA, Thorner J, Nogales E (2011) Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J Cell Biol 195(6):993–1004 Bridges AA, Zhang H, Mehta SB, Occhipinti P, Tani T, Gladfelter AS (2014) Septin assemblies form by diffusion-driven annealing on membranes. Proc Natl Acad Sci USA 111(6):2146–2151 Lee PR, Song S, Ro HS, Park CJ, Lippincott J, Li R, Pringle JR, De Virgilio C, Longtine MS, Lee KS (2002) Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Mol Cell Biol 22(19):6906–6920 Patasi C, Godocikova J, Michlikova S, Nie Y, Kacerikova R, Kvalova K, Raunser S, Farkasovsky M (2015) The role of Bni5 in the regulation of septin higher-order structure formation. Biol Chem 396(12):1325–1337 Fang X, Luo J, Nishihama R, Wloka C, Dravis C, Travaglia M, Iwase M, Vallen EA, Bi E (2010) Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin II. J Cell Biol 191(7):1333–1350 Finnigan GC, Booth EA, Duvalyan A, Liao EN, Thorner J (2015) The carboxy-terminal tails of septins Cdc11 and Shs1 recruit myosin-II binding factor Bni5 to the bud neck in Saccharomyces cerevisiae. Genetics 200(3):843–862 Schneider C, Grois J, Renz C, Gronemeyer T, Johnsson N (2013) Septin rings act as a template for myosin higher-order structures and inhibit redundant polarity establishment. J Cell Sci 126(Pt 15):3390–3400 Bertin A, McMurray MA, Thai L, Garcia G 3rd, Votin V, Grob P, Allyn T, Thorner J, Nogales E (2010) Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J Mol Biol 404:711–731 Casamayor A, Snyder M (2003) Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol Cell Biol 23(8):2762–2777 Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS (1999) Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol 9(24):1458–1467 Garrenton LS, Stefan CJ, McMurray MA, Emr SD, Thorner J (2010) Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling. Proc Natl Acad Sci USA 107(26):11805–11810 McMurray MA, Bertin A, Garcia G 3rd, Lam L, Nogales E, Thorner J (2011) Septin filament formation is essential in budding yeast. Dev Cell 20(4):540–549 Caviston JP, Longtine M, Pringle JR, Bi E (2003) The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol Biol Cell 14(10):4051–4066 Dobbelaere J, Gentry MS, Hallberg RL, Barral Y (2003) Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell 4(3):345–357 Lippincott J, Shannon KB, Shou W, Deshaies RJ, Li R (2001) The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J Cell Sci 114(Pt 7):1379–1386 Wloka C, Nishihama R, Onishi M, Oh Y, Hanna J, Pringle JR, Krauss M, Bi E (2011) Evidence that a septin diffusion barrier is dispensable for cytokinesis in budding yeast. Biol Chem 392(8–9):813–829 Demay BS, Bai X, Howard L, Occhipinti P, Meseroll RA, Spiliotis ET, Oldenbourg R, Gladfelter AS (2011) Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals. J Cell Biol 193(6):1065–1081 Vrabioiu AM, Mitchison TJ (2006) Structural insights into yeast septin organization from polarized fluorescence microscopy. Nature 443(7110):466–469 Byers B, Goetsch L (1976) A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol 69(3):717–721 Ong K, Wloka C, Okada S, Svitkina T, Bi E (2014) Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle. Nat Commun 5:5698 Cid VJ, Adamikova L, Sanchez M, Molina M, Nombela C (2001) Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147(Pt 6):1437–1450 Gladfelter AS, Bose I, Zyla TR, Bardes ES, Lew DJ (2002) Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J Cell Biol 156(2):315–326. doi:10.1083/jcb.200109062 Sadian Y, Gatsogiannis C, Patasi C, Hofnagel O, Goody RS, Farkasovsky M, Raunser S (2013) The role of Cdc42 and Gic1 in the regulation of septin filament formation and dissociation. eLife 2:e01085 Okada S, Leda M, Hanna J, Savage NS, Bi E, Goryachev AB (2013) Daughter cell identity emerges from the interplay of cdc42, septins, and exocytosis. Dev Cell 26(2):148–161 McMurray MA, Thorner J (2008) Septin stability and recycling during dynamic structural transitions in cell division and development. Curr Biol 18(16):1203–1208 Piekny AJ, Maddox AS (2010) The myriad roles of anillin during cytokinesis. Semin Cell Dev Biol 21(9):881–891 Kang PJ, Angerman E, Jung CH, Park HO (2012) Bud4 mediates the cell-type-specific assembly of the axial landmark in budding yeast. J Cell Sci 125(Pt 16):3840–3849 Sanders SL, Herskowitz I (1996) The BUD4 protein of yeast, required for axial budding, is localized to the mother/BUD neck in a cell cycle-dependent manner. J Cell Biol 134(2):413–427 Wu H, Guo J, Zhou YT, Gao XD (2015) The anillin-related region of Bud4 is the major functional determinant for Bud4’s function in septin organization during bud growth and axial bud site selection in budding yeast. Eukaryot Cell 14(3):241–251 Eluere R, Varlet I, Bernadac A, Simon MN (2012) Cdk and the anillin homolog Bud4 define a new pathway regulating septin organization in yeast. Cell Cycle 11(1):151–158 Merlini L, Bolognesi A, Juanes MA, Vandermoere F, Courtellemont T, Pascolutti R, Seveno M, Barral Y, Piatti S (2015) Rho1- and Pkc1-dependent phosphorylation of the F-BAR protein Syp1 contributes to septin ring assembly. Mol Biol Cell 26(18):3245–3262 Qiu W, Neo SP, Yu X, Cai M (2008) A novel septin-associated protein, Syp1p, is required for normal cell cycle-dependent septin cytoskeleton dynamics in yeast. Genetics 180(3):1445–1457 Reider A, Barker SL, Mishra SK, Im YJ, Maldonado-Baez L, Hurley JH, Traub LM, Wendland B (2009) Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation. EMBO J 28(20):3103–3116 Stimpson HE, Toret CP, Cheng AT, Pauly BS, Drubin DG (2009) Early-arriving Syp1p and Ede1p function in endocytic site placement and formation in budding yeast. Mol Biol Cell 20(22):4640–4651 Kuilman T, Maiolica A, Godfrey M, Scheidel N, Aebersold R, Uhlmann F (2014) Identification of Cdk targets that control cytokinesis. EMBO J 34(1):81–96 Caudron F, Barral Y (2009) Septins and the lateral compartmentalization of eukaryotic membranes. Dev Cell 16(4):493–506 Saarikangas J, Barral Y (2011) The emerging functions of septins in metazoans. EMBO Rep 12(11):1118–1126 Castillon GA, Adames NR, Rosello CH, Seidel HS, Longtine MS, Cooper JA, Heil-Chapdelaine RA (2003) Septins have a dual role in controlling mitotic exit in budding yeast. Curr Biol 13(8):654–658 Shepard KA, Gerber AP, Jambhekar A, Takizawa PA, Brown PO, Herschlag D, DeRisi JL, Vale RD (2003) Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. Proc Natl Acad Sci USA 100(20):11429–11434 Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD (2000) Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290(5490):341–344 Luedeke C, Frei SB, Sbalzarini I, Schwarz H, Spang A, Barral Y (2005) Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth. J Cell Biol 169(6):897–908 Kusch J, Meyer A, Snyder MP, Barral Y (2002) Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev 16(13):1627–1639 King K, Jin M, Lew D (2012) Roles of Hsl1p and Hsl7p in Swe1p degradation: beyond septin tethering. Eukaryot Cell 11(12):1496–1502 Longtine MS, Theesfeld CL, McMillan JN, Weaver E, Pringle JR, Lew DJ (2000) Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol Cell Biol 20(11):4049–4061 McMillan JN, Longtine MS, Sia RA, Theesfeld CL, Bardes ES, Pringle JR, Lew DJ (1999) The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol 19(10):6929–6939 Shulewitz MJ, Inouye CJ, Thorner J (1999) Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol Cell Biol 19(10):7123–7137 Versele M, Thorner J (2005) Some assembly required: yeast septins provide the instruction manual. Trends Cell Biol 15(8):414–424 Sreenivasan A, Kellogg D (1999) The elm1 kinase functions in a mitotic signaling network in budding yeast. Mol Cell Biol 19(12):7983–7994 Asano S, Park JE, Yu LR, Zhou M, Sakchaisri K, Park CJ, Kang YH, Thorner J, Veenstra TD, Lee KS (2006) Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J Biol Chem 281(37):27090–27098 Mortensen EM, McDonald H, Yates J 3rd, Kellogg DR (2002) Cell cycle-dependent assembly of a Gin4-septin complex. Mol Biol Cell 13(6):2091–2105 Egelhofer TA, Villen J, McCusker D, Gygi SP, Kellogg DR (2008) The septins function in G1 pathways that influence the pattern of cell growth in budding yeast. PLoS One 3(4):e2022 Tang CS, Reed SI (2002) Phosphorylation of the septin cdc3 in g1 by the cdc28 kinase is essential for efficient septin ring disassembly. Cell Cycle 1(1):42–49 Dobbelaere J, Barral Y (2004) Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305(5682):393–396 Johnson ES, Blobel G (1999) Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol 147(5):981–994 Johnson ES, Gupta AA (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106(6):735–744 Chahwan R, Gravel S, Matsusaka T, Jackson SP (2013) Dma/RNF8 proteins are evolutionarily conserved E3 ubiquitin ligases that target septins. Cell Cycle 12(6):1000–1008 Fraschini R, Bilotta D, Lucchini G, Piatti S (2004) Functional characterization of Dma1 and Dma2, the budding yeast homologues of Schizosaccharomyces pombe Dma1 and human Chfr. Mol Biol Cell 15(8):3796–3810 Merlini L, Fraschini R, Boettcher B, Barral Y, Lucchini G, Piatti S (2012) Budding yeast dma proteins control septin dynamics and the spindle position checkpoint by promoting the recruitment of the Elm1 kinase to the bud neck. PLoS Genet 8(4):e1002670 Mitchell L, Lau A, Lambert JP, Zhou H, Fong Y, Couture JF, Figeys D, Baetz K (2011) Regulation of septin dynamics by the Saccharomyces cerevisiae lysine acetyltransferase NuA4. PLoS One 6(10):e25336 Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ (2002) Self- and actin-templated assembly of mammalian septins. Dev Cell 3(6):791–802 Vrabioiu AM, Mitchison TJ (2007) Symmetry of septin hourglass and ring structures. J Mol Biol 372(1):37–49 Kozubowski L, Larson JR, Tatchell K (2005) Role of the septin ring in the asymmetric localization of proteins at the mother-bud neck in Saccharomyces cerevisiae. Mol Biol Cell 16(8):3455–3466 Longtine MS, Fares H, Pringle JR (1998) Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J Cell Biol 143(3):719–736 Glotzer M (2005) The molecular requirements for cytokinesis. Science 307(5716):1735–1739 Rancati G, Pavelka N, Fleharty B, Noll A, Trimble R, Walton K, Perera A, Staehling-Hampton K, Seidel CW, Li R (2008) Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135(5):879–893 Schmidt M, Bowers B, Varma A, Roh DH, Cabib E (2002) In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J Cell Sci 115(Pt 2):293–302 Tolliday N, Pitcher M, Li R (2003) Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II. Mol Biol Cell 14(2):798–809 Luo J, Vallen EA, Dravis C, Tcheperegine SE, Drees B, Bi E (2004) Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J Cell Biol 165(6):843–855 Watts FZ, Shiels G, Orr E (1987) The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J 6(11):3499–3505 Boyne JR, Yosuf HM, Bieganowski P, Brenner C, Price C (2000) Yeast myosin light chain, Mlc1p, interacts with both IQGAP and class II myosin to effect cytokinesis. J Cell Sci 113(Pt 24):4533–4543 Epp JA, Chant J (1997) An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr Biol 7(12):921–929 Shannon KB, Li R (1999) The multiple roles of Cyk1p in the assembly and function of the actomyosin ring in budding yeast. Mol Biol Cell 10(2):283–296 Shannon KB, Li R (2000) A myosin light chain mediates the localization of the budding yeast IQGAP-like protein during contractile ring formation. Curr Biol 10(12):727–730 Tian C, Wu Y, Johnsson N (2014) Stepwise and cooperative assembly of a cytokinetic core complex in Saccharomyces cerevisiae. J Cell Sci 127(Pt 16):3614–3624 Feng Z, Okada S, Cai G, Zhou B, Bi E (2015) MyosinII heavy chain and formin mediate the targeting of myosin essential light chain to the division site before and during cytokinesis. Mol Biol Cell 26(7):1211–1224. doi:10.1091/mbc.E14-09-1363 Carnahan RH, Gould KL (2003) The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J Cell Biol 162(5):851–862. doi:10.1083/jcb.200305012 Fankhauser C, Reymond A, Cerutti L, Utzig S, Hofmann K, Simanis V (1995) The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 82(3):435–444 Laporte D, Coffman VC, Lee IJ, Wu JQ (2011) Assembly and architecture of precursor nodes during fission yeast cytokinesis. J Cell Biol 192(6):1005–1021 Wachtler V, Huang Y, Karagiannis J, Balasubramanian MK (2006) Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. Mol Biol Cell 17(7):3254–3266 Willet AH, McDonald NA, Bohnert KA, Baird MA, Allen JR, Davidson MW, Gould KL (2015) The F-BAR Cdc15 promotes contractile ring formation through the direct recruitment of the formin Cdc12. J Cell Biol 208(4):391–399 Lippincott J, Li R (1998) Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J Cell Biol 143(7):1947–1960 Meitinger F, Boehm ME, Hofmann A, Hub B, Zentgraf H, Lehmann WD, Pereira G (2011) Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev 25(8):875–888 Nkosi PJ, Targosz BS, Labib K, Sanchez-Diaz A (2013) Hof1 and Rvs167 have redundant roles in actomyosin ring function during cytokinesis in budding yeast. PLoS One 8(2):e57846 Huckaba TM, Lipkin T, Pon LA (2006) Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J Cell Biol 175(6):957–969 Wloka C, Vallen EA, The L, Fang X, Oh Y, Bi E (2013) Immobile myosin-II plays a scaffolding role during cytokinesis in budding yeast. J Cell Biol 200(3):271–286 Piekny A, Werner M, Glotzer M (2005) Cytokinesis: welcome to the Rho zone. Trends Cell Biol 15(12):651–658 Pelham RJ, Chang F (2002) Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature 419(6902):82–86 Fukata M, Kuroda S, Fujii K, Nakamura T, Shoji I, Matsuura Y, Okawa K, Iwamatsu A, Kikuchi A, Kaibuchi K (1997) Regulation of cross-linking of actin filament by IQGAP1, a target for Cdc42. J Biol Chem 272(47):29579–29583 Hart MJ, Callow MG, Souza B, Polakis P (1996) IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J 15(12):2997–3005 Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, Didry D, Le D, Egile C, Carlier MF, Kroschewski R (2007) IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway. J Biol Chem 282(1):426–435 Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R (2007) Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J Cell Biol 178(2):193–200 Li CR, Wang YM, Wang Y (2008) The IQGAP Iqg1 is a regulatory target of CDK for cytokinesis in Candida albicans. EMBO J 27(22):2998–3010 Huxley H, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173(4412):973–976 Huxley HE (1969) The mechanism of muscular contraction. Science 164(3886):1356–1365 Tully GH, Nishihama R, Pringle JR, Morgan DO (2009) The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol Biol Cell 20(4):1201–1212 Lord M, Laves E, Pollard TD (2005) Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol Biol Cell 16(11):5346–5355 Mendes Pinto I, Rubinstein B, Kucharavy A, Unruh JR, Li R (2012) Actin depolymerization drives actomyosin ring contraction during budding yeast cytokinesis. Dev Cell 22(6):1247–1260 Rahal R, Amon A (2008) The Polo-like kinase Cdc5 interacts with FEAR network components and Cdc14. Cell Cycle 7(20):3262–3272 Zumdieck A, Kruse K, Bringmann H, Hyman AA, Julicher F (2007) Stress generation and filament turnover during actin ring constriction. PLoS One 2(8):e696 Miller DP, Hall H, Chaparian R, Mara M, Mueller A, Hall MC, Shannon KB (2015) Dephosphorylation of Iqg1 by Cdc14 regulates cytokinesis in budding yeast. Mol Biol Cell 26(16):2913–2926 Wagner W, Bielli P, Wacha S, Ragnini-Wilson A (2002) Mlc1p promotes septum closure during cytokinesis via the IQ motifs of the vesicle motor Myo2p. EMBO J 21(23):6397–6408 Zhang G, Kashimshetty R, Ng KE, Tan HB, Yeong FM (2006) Exit from mitosis triggers Chs2p transport from the endoplasmic reticulum to mother-daughter neck via the secretory pathway in budding yeast. J Cell Biol 174(2):207–220 Chin CF, Bennett AM, Ma WK, Hall MC, Yeong FM (2012) Dependence of Chs2 ER export on dephosphorylation by cytoplasmic Cdc14 ensures that septum formation follows mitosis. Mol Biol Cell 23(1):45–58 Meitinger F, Petrova B, Lombardi IM, Bertazzi DT, Hub B, Zentgraf H, Pereira G (2010) Targeted localization of Inn1, Cyk3 and Chs2 by the mitotic-exit network regulates cytokinesis in budding yeast. J Cell Sci 123(Pt 11):1851–1861 Oh Y, Chang KJ, Orlean P, Wloka C, Deshaies R, Bi E (2012) Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast. Mol Biol Cell 23(13):2445–2456 Chuang JS, Schekman RW (1996) Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J Cell Biol 135(3):597–610 Jendretzki A, Ciklic I, Rodicio R, Schmitz HP, Heinisch JJ (2009) Cyk3 acts in actomyosin ring independent cytokinesis by recruiting Inn1 to the yeast bud neck. Mol Genet Genomics 282(4):437–451 Korinek WS, Bi E, Epp JA, Wang L, Ho J, Chant J (2000) Cyk3, a novel SH3-domain protein, affects cytokinesis in yeast. Curr Biol 10(15):947–950 Nishihama R, Schreiter JH, Onishi M, Vallen EA, Hanna J, Moravcevic K, Lippincott MF, Han H, Lemmon MA, Pringle JR, Bi E (2009) Role of Inn1 and its interactions with Hof1 and Cyk3 in promoting cleavage furrow and septum formation in S. cerevisiae. J Cell Biol 185(6):995–1012 Onishi M, Ko N, Nishihama R, Pringle JR (2013) Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis. J Cell Biol 202(2):311–329 Sanchez-Diaz A, Marchesi V, Murray S, Jones R, Pereira G, Edmondson R, Allen T, Labib K (2008) Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat Cell Biol 10(4):395–406 Devrekanli A, Foltman M, Roncero C, Sanchez-Diaz A, Labib K (2012) Inn1 and Cyk3 regulate chitin synthase during cytokinesis in budding yeasts. J Cell Sci 125(Pt 22):5453–5466 Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189(4):1145–1175 Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70(2):317–343 Shaw JA, Mol PC, Bowers B, Silverman SJ, Valdivieso MH, Duran A, Cabib E (1991) The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J Cell Biol 114(1):111–123 Sburlati A, Cabib E (1986) Chitin synthetase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J Biol Chem 261(32):15147–15152 Cabib E, Schmidt M (2003) Chitin synthase III activity, but not the chitin ring, is required for remedial septa formation in budding yeast. FEMS Microbiol Lett 224(2):299–305 Kuranda MJ, Robbins PW (1991) Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266(29):19758–19767 Baladron V, Ufano S, Duenas E, Martin-Cuadrado AB, del Rey F, Vazquez de Aldana CR (2002) Eng1p, an endo-1,3-beta-glucanase localized at the daughter side of the septum, is involved in cell separation in Saccharomyces cerevisiae. Eukaryot Cell 1(5):774–786 Kovacech B, Nasmyth K, Schuster T (1996) EGT2 gene transcription is induced predominantly by Swi5 in early G1. Mol Cell Biol 16(7):3264–3274 Mazanka E, Weiss EL (2010) Sequential counteracting kinases restrict an asymmetric gene expression program to early G1. Mol Biol Cell 21(16):2809–2820 Bardin AJ, Amon A (2001) Men and sin: what’s the difference? Nat Rev Mol Cell Biol 2(11):815–826 Hergovich A, Hemmings BA (2012) Hippo signalling in the G2/M cell cycle phase: lessons learned from the yeast MEN and SIN pathways. Semin Cell Dev Biol 23(7):794–802 Krapp A, Gulli MP, Simanis V (2004) SIN and the art of splitting the fission yeast cell. Curr Biol 14(17):R722–R730 Scarfone I, Piatti S (2015) Coupling spindle position with mitotic exit in budding yeast: the multifaceted role of the small GTPase Tem1. Small GTPases 6(4):1–6 Garcia-Rodriguez LJ, Crider DG, Gay AC, Salanueva IJ, Boldogh IR, Pon LA (2009) Mitochondrial inheritance is required for MEN-regulated cytokinesis in budding yeast. Curr Biol 19(20):1730–1735 Jaspersen SL, Morgan DO (2000) Cdc14 activates cdc15 to promote mitotic exit in budding yeast. Curr Biol 10(10):615–618 Konig C, Maekawa H, Schiebel E (2010) Mutual regulation of cyclin-dependent kinase and the mitotic exit network. J Cell Biol 188(3):351–368 Pereira G, Manson C, Grindlay J, Schiebel E (2002) Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J Cell Biol 157(3):367–379 Pereira G, Schiebel E (2001) The role of the yeast spindle pole body and the mammalian centrosome in regulating late mitotic events. Curr Opin Cell Biol 13(6):762–769 Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A (1998) The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk- dependent phosphorylation. Mol Cell 2(6):709–718 Stegmeier F, Amon A (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38:203–232 Bembenek J, Kang J, Kurischko C, Li B, Raab JR, Belanger KD, Luca FC, Yu H (2005) Crm1-mediated nuclear export of Cdc14 is required for the completion of cytokinesis in budding yeast. Cell Cycle 4(7):961–971 Frenz LM, Lee SE, Fesquet D, Johnston LH (2000) The budding yeast Dbf2 protein kinase localises to the centrosome and moves to the bud neck in late mitosis. J Cell Sci 113(Pt 19):3399–3408 Hwa Lim H, Yeong FM, Surana U (2003) Inactivation of mitotic kinase triggers translocation of MEN components to mother-daughter neck in yeast. Mol Biol Cell 14(11):4734–4743 Luca FC, Mody M, Kurischko C, Roof DM, Giddings TH, Winey M (2001) Saccharomyces cerevisiae Mob1p is required for cytokinesis and mitotic exit. Mol Cell Biol 21(20):6972–6983 Song S, Grenfell TZ, Garfield S, Erikson RL, Lee KS (2000) Essential function of the polo box of Cdc5 in subcellular localization and induction of cytokinetic structures. Mol Cell Biol 20(1):286–298 Xu S, Huang HK, Kaiser P, Latterich M, Hunter T (2000) Phosphorylation and spindle pole body localization of the Cdc15p mitotic regulatory protein kinase in budding yeast. Curr Biol 10(6):329–332 Yoshida S, Toh-e A (2001) Regulation of the localization of Dbf2 and mob1 during cell division of Saccharomyces cerevisiae. Genes Genet Syst 76(2):141–147 Simanis V (2003) The mitotic exit and septation initiation networks. J Cell Sci 116(Pt 21):4261–4262 Corbett M, Xiong Y, Boyne JR, Wright DJ, Munro E, Price C (2006) IQGAP and mitotic exit network (MEN) proteins are required for cytokinesis and re-polarization of the actin cytoskeleton in the budding yeast, Saccharomyces cerevisiae. Eur J Cell Biol 85(11):1201–1215 Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325(5948):1682–1686 Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, Krogan NJ, Villen J (2013) Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 10(7):676–682 Naylor SG, Morgan DO (2014) Cdk1-dependent phosphorylation of Iqg1 governs actomyosin ring assembly prior to cytokinesis. J Cell Sci 127(Pt 5):1128–1137 Sanchez-Diaz A, Nkosi PJ, Murray S, Labib K (2012) The mitotic exit network and Cdc14 phosphatase initiate cytokinesis by counteracting CDK phosphorylations and blocking polarised growth. EMBO J 31(17):3620–3634 Bidlingmaier S, Weiss EL, Seidel C, Drubin DG, Snyder M (2001) The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae. Mol Cell Biol 21(7):2449–2462 Brace J, Hsu J, Weiss EL (2011) Mitotic exit control of the Saccharomyces cerevisiae Ndr/LATS kinase Cbk1 regulates daughter cell separation after cytokinesis. Mol Cell Biol 31(4):721–735