The rod-shaped fission yeast Schizosaccharomyces pombe, which undergoes cycles of monopolar-to-bipolar tip growth, is an attractive organism for studying cell-cycle regulation of polarity establishment. While previous research has described factors mediating this process from interphase cell tips, we found that division site signaling also impacts the re-establishment of bipolar cell growth in the ensuing cell cycle. Complete loss or targeted disruption of the non-essential cytokinesis protein Fic1 at the division site, but not at interphase cell tips, resulted in many cells failing to grow at new ends created by cell division. This appeared due to faulty disassembly and abnormal persistence of the cell division machinery at new ends of fic1Δ cells. Moreover, additional mutants defective in the final stages of cytokinesis exhibited analogous growth polarity defects, supporting that robust completion of cell division contributes to new end-growth competency. To test this model, we genetically manipulated S. pombe cells to undergo new end take-off immediately after cell division. Intriguingly, such cells elongated constitutively at new ends unless cytokinesis was perturbed. Thus, cell division imposes constraints that partially override positive controls on growth. We posit that such constraints facilitate invasive fungal growth, as cytokinesis mutants displaying bipolar growth defects formed numerous pseudohyphae. Collectively, these data highlight a role for previous cell cycles in defining a cell's capacity to polarize at specific sites, and they additionally provide insight into how a unicellular yeast can transition into a quasi-multicellular state.
Vyšlo v časopise: Cytokinesis-Based Constraints on Polarized Cell Growth in Fission Yeast. PLoS Genet 8(10): e32767. doi:10.1371/journal.pgen.1003004 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003004
1. HowellAS, LewDJ (2012) Morphogenesis and the cell cycle. Genetics 190 : 51–77.
2. ClarkAG, PaluchE (2011) Mechanics and regulation of cell shape during the cell cycle. Results Probl Cell Differ 53 : 31–73.
3. MartinSG, ChangF (2005) New end take off: regulating cell polarity during the fission yeast cell cycle. Cell Cycle 4 : 1046–1049.
4. HuismanSM, BrunnerD (2011) Cell polarity in fission yeast: a matter of confining, positioning, and switching growth zones. Semin Cell Dev Biol 22 : 799–805.
5. MitchisonJM, NurseP (1985) Growth in cell length in the fission yeast Schizosaccharomyces pombe. J Cell Sci 75 : 357–376.
6. BehrensR, NurseP (2002) Roles of fission yeast tea1p in the localization of polarity factors and in organizing the microtubular cytoskeleton. J Cell Biol 157 : 783–793.
7. FeierbachB, VerdeF, ChangF (2004) Regulation of a formin complex by the microtubule plus end protein tea1p. J Cell Biol 165 : 697–707.
8. MartinSG, McDonaldWH, YatesJR3rd, ChangF (2005) Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev Cell 8 : 479–491.
9. MataJ, NurseP (1997) tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89 : 939–949.
10. BichoCC, KellyDA, SnaithHA, GoryachevAB, SawinKE (2010) A catalytic role for Mod5 in the formation of the Tea1 cell polarity landmark. Curr Biol 20 : 1752–1757.
11. SnaithHA, SawinKE (2003) Fission yeast mod5p regulates polarized growth through anchoring of tea1p at cell tips. Nature 423 : 647–651.
12. FeierbachB, ChangF (2001) Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr Biol 11 : 1656–1665.
13. NakanoK, ImaiJ, AraiR, TohEA, MatsuiY, et al. (2002) The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. J Cell Sci 115 : 4629–4639.
14. GachetY, HyamsJS (2005) Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J Cell Sci 118 : 4231–4242.
15. IwakiT, TanakaN, TakagiH, Giga-HamaY, TakegawaK (2004) Characterization of end4+, a gene required for endocytosis in Schizosaccharomyces pombe. Yeast 21 : 867–881.
16. CabreraR, SuoJ, YoungE, ChangEC (2011) Schizosaccharomyces pombe Arc3 is a conserved subunit of the Arp2/3 complex required for polarity, actin organization, and endocytosis. Yeast 28 : 495–503.
17. CastagnettiS, BehrensR, NurseP (2005) End4/Sla2 is involved in establishment of a new growth zone in Schizosaccharomyces pombe. J Cell Sci 118 : 1843–1850.
18. HuangY, ChewTG, GeW, BalasubramanianMK (2007) Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev Cell 12 : 987–996.
19. SipiczkiM, GrallertB, MiklosI (1993) Mycelial and syncytial growth in Schizosaccharomyces pombe induced by novel septation mutations. J Cell Sci 104 (Pt 2) 485–493.
20. SipiczkiM, TakeoK, YamaguchiM, YoshidaS, MiklosI (1998) Environmentally controlled dimorphic cycle in a fission yeast. Microbiology 144 (Pt 5) 1319–1330.
21. GarciaP, TajaduraV, GarciaI, SanchezY (2006) Rgf1p is a specific Rho1-GEF that coordinates cell polarization with cell wall biogenesis in fission yeast. Mol Biol Cell 17 : 1620–1631.
22. TatebeH, ShimadaK, UzawaS, MorigasakiS, ShiozakiK (2005) Wsh3/Tea4 is a novel cell-end factor essential for bipolar distribution of Tea1 and protects cell polarity under environmental stress in S. pombe. Curr Biol 15 : 1006–1015.
23. GlynnJM, LustigRJ, BerlinA, ChangF (2001) Role of bud6p and tea1p in the interaction between actin and microtubules for the establishment of cell polarity in fission yeast. Curr Biol 11 : 836–845.
24. PollardTD, WuJQ (2010) Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 11 : 149–155.
25. LippincottJ, LiR (2000) Involvement of PCH family proteins in cytokinesis and actin distribution. Microsc Res Tech 49 : 168–172.
26. Roberts-GalbraithRH, OhiMD, BallifBA, ChenJS, McLeodI, et al. (2010) Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol Cell 39 : 86–99.
27. CarnahanRH, GouldKL (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 : 851–862.
28. Roberts-GalbraithRH, ChenJS, WangJ, GouldKL (2009) The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J Cell Biol 184 : 113–127.
29. NishihamaR, SchreiterJH, OnishiM, VallenEA, HannaJ, et al. (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 : 995–1012.
30. Sanchez-DiazA, MarchesiV, MurrayS, JonesR, PereiraG, et al. (2008) Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat Cell Biol 10 : 395–406.
31. GuertinDA, TrautmannS, McCollumD (2002) Cytokinesis in eukaryotes. Microbiol Mol Biol Rev 66 : 155–178.
32. KrappA, SimanisV (2008) An overview of the fission yeast septation initiation network (SIN). Biochem Soc Trans 36 : 411–415.
33. JohnsonBF, YooBY, CallejaGB, KozelaCP (2005) Second thoughts on septation by the fission yeast, Schizosaccharomyces pombe: pull vs. push mechanisms with an appendix–dimensional modelling of the flat and variable septa. Antonie Van Leeuwenhoek 88 : 1–12.
34. DekkerN, SpeijerD, GrunCH, van den BergM, de HaanA, et al. (2004) Role of the alpha-glucanase Agn1p in fission-yeast cell separation. Mol Biol Cell 15 : 3903–3914.
35. Martin-CuadradoAB, DuenasE, SipiczkiM, Vazquez de AldanaCR, del ReyF (2003) The endo-beta-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J Cell Sci 116 : 1689–1698.
36. Amoah-BuahinE, BoneN, ArmstrongJ (2005) Hyphal Growth in the Fission Yeast Schizosaccharomyces pombe. Eukaryot Cell 4 : 1287–1297.
37. BrandA (2012) Hyphal growth in human fungal pathogens and its role in virulence. Int J Microbiol 2012 : 517529.
38. GagianoM, BauerFF, PretoriusIS (2002) The sensing of nutritional status and the relationship to filamentous growth in Saccharomyces cerevisiae. FEMS Yeast Res 2 : 433–470.
39. DodgsonJ, BrownW, RosaCA, ArmstrongJ (2010) Reorganization of the growth pattern of Schizosaccharomyces pombe in invasive filament formation. Eukaryot Cell 9 : 1788–1797.
40. PohlmannJ, FleigU (2010) Asp1, a conserved 1/3 inositol polyphosphate kinase, regulates the dimorphic switch in Schizosaccharomyces pombe. Mol Cell Biol 30 : 4535–4547.
41. BahlerJ (2005) A transcriptional pathway for cell separation in fission yeast. Cell Cycle 4 : 39–41.
42. PelhamRJJr, ChangF (2001) Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nat Cell Biol 3 : 235–244.
43. ArellanoM, DuranA, PerezP (1997) Localisation of the Schizosaccharomyces pombe rho1p GTPase and its involvement in the organisation of the actin cytoskeleton. J Cell Sci 110 (Pt 20) 2547–2555.
44. ChangL, GouldKL (2000) Sid4p is required to localize components of the septation initiation pathway to the spindle pole body in fission yeast. Proc Natl Acad Sci U S A 97 : 5249–5254.
45. JendretzkiA, CiklicI, RodicioR, SchmitzHP, HeinischJJ (2009) Cyk3 acts in actomyosin ring independent cytokinesis by recruiting Inn1 to the yeast bud neck. Mol Genet Genomics 282 : 437–451.
46. PollardLW, OnishiM, PringleJR, LordM (2012) Fission yeast Cyk3p is a transglutaminase-like protein that participates in cytokinesis and cell morphogenesis. Mol Biol Cell
47. Le GoffX, MotegiF, SalimovaE, MabuchiI, SimanisV (2000) The S. pombe rlc1 gene encodes a putative myosin regulatory light chain that binds the type II myosins myo3p and myo2p. J Cell Sci 113 Pt 23 : 4157–4163.
48. NaqviNI, WongKC, TangX, BalasubramanianMK (2000) Type II myosin regulatory light chain relieves auto-inhibition of myosin-heavy-chain function. Nat Cell Biol 2 : 855–858.
49. CortesJC, IshiguroJ, DuranA, RibasJC (2002) Localization of the (1,3)beta-D-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J Cell Sci 115 : 4081–4096.
50. LiuJ, TangX, WangH, OliferenkoS, BalasubramanianMK (2002) The localization of the integral membrane protein Cps1p to the cell division site is dependent on the actomyosin ring and the septation-inducing network in Schizosaccharomyces pombe. Mol Biol Cell 13 : 989–1000.
51. DemeterJ, SazerS (1998) imp2, a new component of the actin ring in the fission yeast Schizosaccharomyces pombe. J Cell Biol 143 : 415–427.
52. AnH, MorrellJL, JenningsJL, LinkAJ, GouldKL (2004) Requirements of fission yeast septins for complex formation, localization, and function. Mol Biol Cell 15 : 5551–5564.
53. Martin-CuadradoAB, MorrellJL, KonomiM, AnH, PetitC, et al. (2005) Role of septins and the exocyst complex in the function of hydrolytic enzymes responsible for fission yeast cell separation. Mol Biol Cell 16 : 4867–4881.
54. HachetO, SimanisV (2008) Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev 22 : 3205–3216.
55. PeelS, MacheboeufP, MartinelliN, WeissenhornW (2011) Divergent pathways lead to ESCRT-III-catalyzed membrane fission. Trends Biochem Sci 36 : 199–210.
56. KourantiI, McLeanJR, FeoktistovaA, LiangP, JohnsonAE, et al. (2010) A global census of fission yeast deubiquitinating enzyme localization and interaction networks reveals distinct compartmentalization profiles and overlapping functions in endocytosis and polarity. PLoS Biol 8: e1000471 doi:10.1371/journal.pbio.1000471
57. GeW, BalasubramanianMK (2008) Pxl1p, a paxillin-related protein, stabilizes the actomyosin ring during cytokinesis in fission yeast. Mol Biol Cell 19 : 1680–1692.
58. PinarM, CollPM, RinconSA, PerezP (2008) Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol Biol Cell 19 : 1727–1738.
59. PrevorovskyM, StanurovaJ, PutaF, FolkP (2009) High environmental iron concentrations stimulate adhesion and invasive growth of Schizosaccharomyces pombe. FEMS Microbiol Lett 293 : 130–134.
60. St JohnstonD, AhringerJ (2010) Cell polarity in eggs and epithelia: parallels and diversity. Cell 141 : 757–774.
61. FlescherEG, MaddenK, SnyderM (1993) Components required for cytokinesis are important for bud site selection in yeast. J Cell Biol 122 : 373–386.
62. SnyderM, GehrungS, PageBD (1991) Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol 114 : 515–532.
63. PollaroloG, SchulzJG, MunckS, DottiCG (2011) Cytokinesis remnants define first neuronal asymmetry in vivo. Nat Neurosci 14 : 1525–1533.
64. LuoJ, MatsuoY, GulisG, HinzH, Patton-VogtJ, et al. (2009) Phosphatidylethanolamine is required for normal cell morphology and cytokinesis in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell 8 : 790–799.
65. StreiblovaE, MalekI, BeranK (1966) Structural changes in the cell wall of Schizosaccharomyces pombe during cell division. J Bacteriol 91 : 428–435.
66. MullinsJM, BieseleJJ (1973) Cytokinetic activities in a human cell line: the midbody and intercellular bridge. Tissue Cell 5 : 47–61.
67. HuCK, CoughlinM, FieldCM, MitchisonTJ (2008) Cell polarization during monopolar cytokinesis. J Cell Biol 181 : 195–202.
68. WeberGF, BjerkeMA, DeSimoneDW (2012) A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22 : 104–115.
69. WhiteJG, BorisyGG (1983) On the mechanisms of cytokinesis in animal cells. J Theor Biol 101 : 289–316.
70. PanterisE, GalatisB (2005) The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments. New Phytol 167 : 721–732.
71. O'ConnellCB, WheatleySP, AhmedS, WangYL (1999) The small GTP-binding protein rho regulates cortical activities in cultured cells during division. J Cell Biol 144 : 305–313.
72. NeujahrR, HeizerC, GerischG (1997) Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow. J Cell Sci 110 (Pt 2) 123–137.
73. KingJS, VeltmanDM, GeorgiouM, BaumB, InsallRH (2010) SCAR/WAVE is activated at mitosis and drives myosin-independent cytokinesis. J Cell Sci 123 : 2246–2255.
74. TullyGH, NishihamaR, PringleJR, MorganDO (2009) The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol Biol Cell 20 : 1201–1212.
75. EmotoK, UmedaM (2000) An essential role for a membrane lipid in cytokinesis. Regulation of contractile ring disassembly by redistribution of phosphatidylethanolamine. J Cell Biol 149 : 1215–1224.
76. BraceJ, HsuJ, WeissEL (2011) Mitotic exit control of the Saccharomyces cerevisiae Ndr/LATS kinase Cbk1 regulates daughter cell separation after cytokinesis. Mol Cell Biol 31 : 721–735.
77. Colman-LernerA, ChinTE, BrentR (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107 : 739–750.
78. Gonzalez-NovoA, Correa-BordesJ, LabradorL, SanchezM, Vazquez de AldanaCR, et al. (2008) Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol Biol Cell 19 : 1509–1518.
79. WangA, RanigaPP, LaneS, LuY, LiuH (2009) Hyphal chain formation in Candida albicans: Cdc28-Hgc1 phosphorylation of Efg1 represses cell separation genes. Mol Cell Biol 29 : 4406–4416.
80. ErnstJF (2000) Regulation of dimorphism in Candida albicans. Contrib Microbiol 5 : 98–111.
81. BahlerJ, WuJQ, LongtineMS, ShahNG, McKenzieA3rd, et al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14 : 943–951.
82. KeeneyJB, BoekeJD (1994) Efficient targeted integration at leu1-32 and ura4-294 in Schizosaccharomyces pombe. Genetics 136 : 849–856.
83. TakedaT, KawateT, ChangF (2004) Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat Cell Biol 6 : 1142–1144.
84. MaundrellK (1990) nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J Biol Chem 265 : 10857–10864.
85. MaundrellK (1993) Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123 : 127–130.
86. RiedlJ, CrevennaAH, KessenbrockK, YuJH, NeukirchenD, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5 : 605–607.
87. BasiG, SchmidE, MaundrellK (1993) TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene 123 : 131–136.
88. BohnertKA, ChenJS, CliffordDM, Vander KooiCW, GouldKL (2009) A link between aurora kinase and Clp1/Cdc14 regulation uncovered by the identification of a fission yeast borealin-like protein. Mol Biol Cell 20 : 3646–3659.
89. RosenbergJA, TomlinGC, McDonaldWH, SnydsmanBE, MullerEG, et al. (2006) Ppc89 links multiple proteins, including the septation initiation network, to the core of the fission yeast spindle-pole body. Mol Biol Cell 17 : 3793–3805.
90. GouldKL, MorenoS, OwenDJ, SazerS, NurseP (1991) Phosphorylation at Thr167 is required for Schizosaccharomyces pombe p34cdc2 function. EMBO J 10 : 3297–3309.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
