Contractile Ring Stability in S.pombe Depends on F-BAR Protein Cdc15p and Bgs1p Transport from the Golgi Complex

Cell Reports

Volumn 8, Issue 5, 2014, Pages 1533-1544

  Arasada, Rajesh ^a   Pollard, Thomas D ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ENZYME; MYOSIN II; PHOSPHOPROTEIN; PROTEIN BGS1P; PROTEIN CDC15P; PROTEIN MYP2P; UNCLASSIFIED DRUG; 1,3-BETA-GLUCAN SYNTHASE; CDC15 PROTEIN; CELL CYCLE PROTEIN; GLUCOSYLTRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; MYOSIN HEAVY CHAIN; MYP2 PROTEIN, S POMBE; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CELL ANCHORAGE; CELL MEMBRANE; CONTRACTILE RING STABILITY; CONTROLLED STUDY; CYTOKINESIS; ENZYME ACTIVITY; FUNGAL CELL WALL; FUNGAL PHENOMENA AND FUNCTIONS; GOLGI COMPLEX; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES POMBE; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCETACEAE;

CELL CYCLE PROTEINS; CELL MEMBRANE; CYTOKINESIS; GLUCOSYLTRANSFERASES; GOLGI APPARATUS; GTP-BINDING PROTEINS; MYOSIN HEAVY CHAINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84922540928     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.048     Document Type: Article

References (52)

1. Antebi A., Fink G.R. The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell 1992, 3:633-654.
2. Arai R., Mabuchi I. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J.Cell Sci. 2002, 115:887-898.
3. Arasada R., Pollard T.D. Distinct roles for F-BAR proteins Cdc15p and Bzz1p in actin polymerization at sites of endocytosis in fission yeast. Curr. Biol. 2011, 21:1450-1459.
4. Balasubramanian M.K., McCollum D., Chang L., Wong K.C., Naqvi N.I., He X., Sazer S., Gould K.L. Isolation and characterization of new fission yeast cytokinesis mutants. Genetics 1998, 149:1265-1275.
5. Barrowman J., Bhandari D., Reinisch K., Ferro-Novick S. TRAPP complexes in membrane traffic: convergence through a common Rab. Nat. Rev. Mol. Cell Biol. 2010, 11:759-763.
6. Berro J., Sirotkin V., Pollard T.D. Mathematical modeling of endocytic actin patch kinetics in fission yeast: disassembly requires release of actin filament fragments. Mol. Biol. Cell 2010, 21:2905-2915.
7. Bezanilla M., Wilson J.M., Pollard T.D. Fission yeast myosin-II isoforms assemble into contractile rings at distinct times during mitosis. Curr. Biol. 2000, 10:397-400.
8. Brazer S.C., Williams H.P., Chappell T.G., Cande W.Z. A fission yeast kinesin affects Golgi membrane recycling. Yeast 2000, 16:149-166.
9. Carnahan R.H., Gould K.L. The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J.Cell Biol. 2003, 162:851-862.
10. Chen J.S., Broadus M.R., McLean J.R., Feoktistova A., Ren L., Gould K.L. Comprehensive proteomics analysis reveals new substrates and regulators of the fission yeast clp1/cdc14 phosphatase. Mol. Cell. Proteomics 2013, 12:1074-1086.
11. Clifford D.M., Wolfe B.A., Roberts-Galbraith R.H., McDonald W.H., Yates J.R., Gould K.L. The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J.Cell Biol. 2008, 181:79-88.
12. Cortés J.C., Ishiguro J., Durán A., Ribas J.C. 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. 2002, 115:4081-4096.
13. Cortés J.C., Carnero E., Ishiguro J., Sánchez Y., Durán A., Ribas J.C. The novel fission yeast (1,3)beta-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J.Cell Sci. 2005, 118:157-174.
14. Cortés J.C., Sato M., Muñoz J., Moreno M.B., Clemente-Ramos J.A., Ramos M., Okada H., Osumi M., Durán A., Ribas J.C. Fission yeast Ags1 confers the essential septum strength needed for safe gradual cell abscission. J.Cell Biol. 2012, 198:637-656.
15. Daga R.R., Lahoz A., Muñoz M.J., Moreno S., Jimenez J. Etd1p is a novel protein that links the SIN cascade with cytokinesis. EMBO J. 2005, 24:2436-2446.
16. De Matteis M.A., Luini A. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 2008, 9:273-284.
17. Fankhauser C., Reymond A., Cerutti L., Utzig S., Hofmann K., Simanis V. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 1995, 82:435-444.
18. Ge W., Balasubramanian M.K. Pxl1p, a paxillin-related protein, stabilizes the actomyosin ring during cytokinesis in fission yeast. Mol. Biol. Cell 2008, 19:1680-1692.
19. Hachet O., Simanis V. Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev. 2008, 22:3205-3216.
20. Jaulin F., Xue X., Rodriguez-Boulan E., Kreitzer G. Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev. Cell 2007, 13:511-522.
21. Laporte D., Coffman V.C., Lee I.J., Wu J.Q. Assembly and architecture of precursor nodes during fission yeast cytokinesis. J.Cell Biol. 2011, 192:1005-1021.
22. Le Goff X., Utzig S., Simanis V. Controlling septation in fission yeast: finding the middle, and timing it right. Curr. Genet. 1999, 35:571-584.
23. Le Goff X., Woollard A., Simanis V. Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe. Mol. Gen. Genet. 1999, 262:163-172.
24. Lee I.J., Wu J.Q. Characterization of Mid1 domains for targeting and scaffolding in fission yeast cytokinesis. J.Cell Sci. 2012, 125:2973-2985.
25. Liu J., Wang H., McCollum D., Balasubramanian M.K. Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. Genetics 1999, 153:1193-1203.
26. Liu J., Tang X., Wang H., Oliferenko S., Balasubramanian M.K. 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 2002, 13:989-1000.
27. Martin S.G., Berthelot-Grosjean M. Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 2009, 459:852-856.
28. Martín-García R., Valdivieso M.H. The fission yeast Chs2 protein interacts with the type-II myosin Myo3p and is required for the integrity of the actomyosin ring. J.Cell Sci. 2006, 119:2768-2779.
29. Mishra M., Karagiannis J., Sevugan M., Singh P., Balasubramanian M.K. The 14-3-3 protein rad24p modulates function of the cdc14p family phosphatase clp1p/flp1p in fission yeast. Curr. Biol. 2005, 15:1376-1383.
30. Moseley J.B., Mayeux A., Paoletti A., Nurse P. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 2009, 459:857-860.
31. Pardo M., Nurse P. Equatorial retention of the contractile actin ring by microtubules during cytokinesis. Science 2003, 300:1569-1574.
32. Park J.S., Steinbach S.K., Desautels M., Hemmingsen S.M. Essential role for Schizosaccharomyces pombe pik1 in septation. PLoS ONE 2009, 4:e6179.
33. Pinar M., Coll P.M., Rincón S.A., Pérez P. Schizosaccharomyces pombe Pxl1 is a paxillin homologue that modulates Rho1 activity and participates in cytokinesis. Mol. Biol. Cell 2008, 19:1727-1738.
34. Pollard T.D., Wu J.Q. Understanding cytokinesis: lessons from fission yeast. Nat. Rev. Mol. Cell Biol. 2010, 11:149-155.
35. Pollard L.W., Onishi M., Pringle J.R., Lord M. Fission yeast Cyk3p is a transglutaminase-like protein that participates in cytokinesis and cell morphogenesis. Mol. Biol. Cell 2012, 23:2433-2444.
36. Qualmann B., Kelly R.B. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J.Cell Biol. 2000, 148:1047-1062.
37. Roberts-Galbraith R.H., Chen J.S., Wang J., Gould K.L. The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J.Cell Biol. 2009, 184:113-127.
38. Roberts-Galbraith R.H., Ohi M.D., Ballif B.A., Chen J.S., McLeod I., McDonald W.H., Gygi S.P., Yates J.R., Gould K.L. Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol. Cell 2010, 39:86-99.
39. Samejima I., Miller V.J., Rincon S.A., Sawin K.E. Fission yeast Mto1 regulates diversity of cytoplasmic microtubule organizing centers. Curr. Biol. 2010, 20:1959-1965.
40. Sammons M.R., James M.L., Clayton J.E., Sladewski T.E., Sirotkin V., Lord M. A calmodulin-related light chain from fission yeast that functions with myosin-I and PI 4-kinase. J.Cell Sci. 2011, 124:2466-2477.
41. Sawin K.E., Lourenco P.C., Snaith H.A. Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr. Biol. 2004, 14:763-775.
42. Takeda T., Kawate T., Chang F. Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 2004, 6:1142-1144.
43. Trautmann S., Wolfe B.A., Jorgensen P., Tyers M., Gould K.L., McCollum D. Fission yeast Clp1p phosphatase regulates G2/M transition andcoordination of cytokinesis with cell cycle progression. Curr. Biol. 2001, 11:931-940.
44. Tsujita K., Suetsugu S., Sasaki N., Furutani M., Oikawa T., Takenawa T. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J.Cell Biol. 2006, 172:269-279.
45. Valente C., Turacchio G., Mariggiò S., Pagliuso A., Gaibisso R., Di Tullio G., Santoro M., Formiggini F., Spanò S., Piccini D., et al. A 14-3-3γ dimer-based scaffold bridges CtBP1-S/BARS to PI(4)KIIIβ to regulate post-Golgi carrier formation. Nat. Cell Biol. 2012, 14:343-354.
46. Venkatram S., Tasto J.J., Feoktistova A., Jennings J.L., Link A.J., Gould K.L. Identification and characterization of two novel proteins affecting fission yeast gamma-tubulin complex function. Mol. Biol. Cell 2004, 15:2287-2301.
47. Vjestica A., Tang X.Z., Oliferenko S. The actomyosin ring recruits early secretory compartments to the division site in fission yeast. Mol. Biol. Cell 2008, 19:1125-1138.
48. Wachtler V., Huang Y., Karagiannis J., Balasubramanian M.K. Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. Mol. Biol. Cell 2006, 17:3254-3266.
49. Walch-Solimena C., Novick P. The yeast phosphatidylinositol-4-OH kinase pik1 regulates secretion at the Golgi. Nat. Cell Biol. 1999, 1:523-525.
50. Wu J.Q., Pollard T.D. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005, 310:310-314.
51. Wu J.Q., Kuhn J.R., Kovar D.R., Pollard T.D. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 2003, 5:723-734.
52. Yamaguchi H., Hiratani T., Baba M., Osumi M. Effect of aculeacin A, a wall-active antibiotic, on synthesis of the yeast cell wall. Microbiol. Immunol. 1985, 29:609-623.