Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis

Genes and Development

Volumn 22, Issue 22, 2008, Pages 3205-3216

  Hachet, Olivier ^a   Simanis, Viesturs ^a  

^a EPFL   (Switzerland)

Author keywords

Contractile actomyosin ring; Cytokinesis; Mid1p anillin; S. pombe; Septation initiation network

Indexed keywords

CDC15P PROTEIN; CELL CYCLE PROTEIN; CONTRACTILE PROTEIN; MID1P PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; CONTRACTILE RING ASSEMBLY; CYTOKINESIS; MOLECULAR IMAGING; MUTANT; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; SCHIZOSACCHAROMYCES POMBE; SEPTATION INITIATION NETWORK; SIGNAL TRANSDUCTION;

ACTOMYOSIN; CELL CYCLE; CELL CYCLE PROTEINS; CONTRACTILE PROTEINS; CYTOKINESIS; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEINS; MODELS, BIOLOGICAL; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

ANIMALIA; FUNGI; SCHIZOSACCHAROMYCES POMBE;

EID: 56549083997     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1697208     Document Type: Article

References (61)

1. Arai, R. and Mabuchi, I. 2002. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 115: 887-898.
2. Bahler, J. and Pringle, J.R. 1998. Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes & Dev. 12: 1356-1370.
3. Bahler, J., Steever, A.B., Wheatley, S., Wang, Y., Pringle, J.R., Gould, K.L., and McCollum, D. 1998. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J. Cell Biol. 143: 1603-1616.
4. Balasubramanian, M.K., Helfman, D.M., and Hemmingsen, S.M. 1992. A new tropomyosin essential for cytokinesis in the fission yeast S. pombe. Nature 360: 84-87.
5. Balasubramanian, M.K., McCollum, D., Chang, L., Wong, K.C., Naqvi, N.I., He, X., Sazer, S., and Gould, K.L. 1998. Isolation and characterization of new fission yeast cytokinesis mutants. Genetics 149: 1265-1275.
6. Bezanilla, M., Forsburg, S.L., and Pollard, T.D. 1997. Identification of a second myosin-II in Schizosaccharomyces pombe: Myp2p is conditionally required for cytokinesis. Mol. Biol. Cell 8: 2693-2705.
7. Bruno, K.S., Morrell, J.L., Hamer, J.E., and Staiger, C.J. 2001. SEPH, a Cdc7p orthologue from Aspergillus nidulans, functions upstream of actin ring formation during cytokinesis. Mol. Microbiol. 42: 3-12.
8. Carnahan, R.H. and Gould, K.L. 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.
9. Celton-Morizur, S., Racine, V., Sibarita, J.B., and Paoletti, A. 2006. Pom1 kinase links division plane position to cell polarity by regulating Mid1p cortical distribution. J. Cell Sci. 119: 4710-4718.
10. Cerutti, L. and Simanis, V. 1999. Asymmetry of the spindle pole bodies and spg1p GAP segregation during mitosis in fission yeast. J. Cell Sci. 112: 2313-2321.
11. Chang, L. and Gould, K.L. 2000. Sid4p is required to localize components of the septation initiation pathway to the spindle pole body in fission yeast. Proc. Natl. Acad. Sci. 97: 5249-5254.
12. Chang, F., Woollard, A., and Nurse, P. 1996. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J. Cell Sci. 109: 131-142.
13. Chang, F., Drubin, D., and Nurse, P. 1997. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137: 169-182.
14. Chitu, V., Pixley, F.J., Macaluso, F., Larson, D.R., Condeelis, J., Yeung, Y.G., and Stanley, E.R. 2005. The PCH family member MAYP/PSTPIP2 directly regulates F-actin bundling and enhances filopodia formation and motility in macrophages. Mol. Biol. Cell 16: 2947-2959.
15. Clifford, D.M., Wolfe, B.A., Roberts-Galbraith, R.H., McDonald, W.H., Yates III, J.R., and Gould, K.L. 2008. The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J. Cell Biol. 181: 79-88.
16. Daga, R.R. and Chang, F. 2005. Dynamic positioning of the fission yeast cell division plane. Proc. Natl. Acad. Sci. 102: 8228-8232.
17. Eng, K., Naqvi, N.I., Wong, K.C., and Balasubramanian, M.K. 1998. Rng2p, a protein required for cytokinesis in fission yeast, is a component of the actomyosin ring and the spindle pole body. Curr. Biol. 8: 611-621.
18. Fankhauser, C. and Simanis, V. 1994. The cdc7 protein kinase is a dosage dependent regulator of septum formation in fission yeast. EMBO J. 13: 3011-3019.
19. Fankhauser, C., Marks, J., Reymond, A., and Simanis, V. 1993. The S. pombe cdc16 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: A link between mitosis and cytokinesis? EMBO J. 12: 2697-2704.
20. Fankhauser, C., Reymond, A., Cerutti, L., Utzig, S., Hofmann, K., and Simanis, V. 1995. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 82: 435-444.
21. Furge, K.A., Wong, K., Armstrong, J., Balasubramanian, M., and Albright, C.F. 1998. Byr4 and Cdc16 form a two-component GTPase-activating protein for the Spg1 GTPase that controls septation in fission yeast. Curr. Biol. 8: 947-954.
22. Gould, K.L. and Simanis, V. 1997. The control of septum formation in fission yeast. Genes & Dev. 11: 2939-2951.
23. Guertin, D.A., Chang, L., Irshad, F., Gould, K.L., and McCollum, D. 2000. The role of the sid1p kinase and cdc14p in regulating the onset of cytokinesis in fission yeast. EMBO J. 19: 1803-1815.
24. Heitz, M.J., Petersen, J., Valovin, S., and Hagan, I.M. 2001. MTOC formation during mitotic exit in fission yeast. J. Cell Sci. 114: 4521-4532.
25. Hou, M.C., Salek, J., and McCollum, D. 2000. Mob1p interacts with the Sid2p kinase and is required for cytokinesis in fission yeast. Curr. Biol. 10: 619-622.
26. Jin, Q.W., Zhou, M., Bimbo, A., Balasubramanian, M.K., and McCollum, D. 2006. A role for the septation initiation network in septum assembly revealed by genetic analysis of sid2-250 suppressors. Genetics 172: 2101-2112.
27. Kamasaki, T., Osumi, M., and Mabuchi, I. 2007. Three-dimensional arrangement of F-actin in the contractile ring of fission yeast. J. Cell Biol. 178: 765-771.
28. Kitayama, C., Sugimoto, A., and Yamamoto, M. 1997. Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe. J. Cell Biol. 137: 1309-1319.
29. Krapp, A., Schmidt, S., Cano, E., and Simanis, V. 2001. S. pombe cdc11p, together with sid4p, provides an anchor for septation initiation network proteins on the spindle pole body. Curr. Biol. 11: 1559-1568.
30. Krapp, A., Gulli, M.P., and Simanis, V. 2004. SIN and the art of splitting the fission yeast cell. Curr. Biol. 14: R722-R730. doi: 10.1016/j.cub.2004.08.049.
31. Le Goff, X., Woollard, A., and Simanis, V. 1999. Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe. Mol. Gen. Genet. 262: 163-172.
32. Le Goff, X., Motegi, F., Salimova, E., Mabuchi, I., and Simanis, V. 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: 4157-4163.
33. Liu, J., Wang, H., McCollum, D., and Balasubramanian, M.K. 1999. Drc1p/Cps1p, a 1,3-β-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. Genetics 153: 1193-1203.
34. MacIver, F.H., Glover, D.M., and Hagan, I.M. 2003a. A 'marker switch' approach for targeted mutagenesis of genes in Schizosaccharomyces pombe. Yeast 20: 587-594.
35. MacIver, F.H., Tanaka, K., Robertson, A.M., and Hagan, I.M. 2003b. Physical and functional interactions between polo kinase and the spindle pole component Cut12 regulate mitotic commitment in S. pombe. Genes & Dev. 17: 1507-1523.
36. Marks, J., Hagan, I.M., and Hyams, J.S. 1986. Growth polarity and cytokinesis in fission yeast: The role of the cytoskeleton. J. Cell Sci. Suppl. 5: 229-241.
37. + gene encodes a novel EF-hand protein essential for cytokinesis. J. Cell Biol. 130: 651-660.
38. Minet, M., Nurse, P., Thuriaux, P., and Mitchison, J.M. 1979. Uncontrolled septation in a cell division cycle mutant of the fission yeast Schizosaccharomyces pombe. J. Bacteriol. 137: 440-446.
39. Mishra, M. and Oliferenko, S. 2008. Cytokinesis: Catch and drag. Curr. Biol. 18: R247-R250. doi: 10.1016/j.cub.2008. 01.029.
40. Mishra, M., Karagiannis, J., Trautmann, S., Wang, H., McCollum, D., and Balasubramanian, M.K. 2004. The Clp1p/Flp1p phosphatase ensures completion of cytokinesis in response to minor perturbation of the cell division machinery in Schizosaccharomyces pombe. J. Cell Sci. 117: 3897-3910.
41. Moreno, S., Klar, A., and Nurse, P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194: 795-823.
42. Motegi, F., Mishra, M., Balasubramanian, M.K., and Mabuchi, I. 2004. Myosin-II reorganization during mitosis is controlled temporally by its dephosphorylation and spatially by Mid1 in fission yeast. J. Cell Biol. 165: 685-695.
43. Ohkura, H., Hagan, I.M., and Glover, D.M. 1995. The conserved Schizosaccharomyces pombe kinase plo1, required to form a bipolar spindle, the actin ring, and septum, can drive septum formation in G1 and G2 cells. Genes & Dev. 9: 1059-1073.
44. Padte, N.N., Martin, S.G., Howard, M., and Chang, F. 2006. The cell-end factor pom1p inhibits mid1p in specification of the cell division plane in fission yeast. Curr. Biol. 16: 2480-2487.
45. Paoletti, A. and Chang, F. 2000. Analysis of mid1p, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast. Mol. Biol. Cell 11: 2757-2773.
46. Petronczki, M., Lenart, P., and Peters, J.M. 2008. Polo on the rise - From mitotic entry to cytokinesis with Plk1. Dev. Cell 14: 646-659.
47. Rosenberg, J.A., Tomlin, G.C., McDonald, W.H., Snydsman, B.E., Muller, E.G., Yates III, J.R., and Gould, K.L. 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.
48. Schmidt, S., Sohrmann, M., Hofmann, K., Woollard, A., and Simanis, V. 1997. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes & Dev. 11: 1519-1534.
49. Simanis, V. 2003. Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116: 4263-4275.
50. Sohrmann, M., Fankhauser, C., Brodbeck, C., and Simanis, V. 1996. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes & Dev. 10: 2707-2719.
51. Sohrmann, M., Schmidt, S., Hagan, I., and Simanis, V. 1998. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septum-inducing protein kinase Cdc7p. Genes & Dev. 12: 84-94.
52. Sparks, C.A., Morphew, M., and McCollum, D. 1999. Sid2p, a spindle pole body kinase that regulates the onset of cytokinesis. J. Cell Biol. 146: 777-790.
53. Spencer, S., Dowbenko, D., Cheng, J., Li, W., Brush, J., Utzig, S., Simanis, V., and Lasky, L.A. 1997. PSTPIP: A tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 138: 845-860.
54. Tanaka, K., Petersen, J., MacIver, F., Mulvihill, D.P., Glover, D.M., and Hagan, I.M. 2001. The role of Plo1 kinase in mitotic commitment and septation in Schizosaccharomyces pombe. EMBO J. 20: 1259-1270.
55. Tomlin, G.C., Morrell, J.L., and Gould, K.L. 2002. The spindle pole body protein Cdc11p links Sid4p to the fission yeast septation initiation network. Mol. Biol. Cell 13: 1203-1214.
56. Vavylonis, D., Wu, J.Q., Hao, S., O'Shaughnessy, B., and Pollard, T.D. 2008. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319: 97-100.
57. Wachtler, V., Huang, Y., Karagiannis, J., and Balasubramanian, M.K. 2006. Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. Mol. Biol. Cell 17: 3254-3266.
58. Wolfe, B.A. and Gould, K.L. 2005. Split decisions: Coordinating cytokinesis in yeast. Trends Cell Biol. 15: 10-18.
59. Wu, J.Q., Bahler, J., and Pringle, J.R. 2001. Roles of a fimbrin and an α-actinin-like protein in fission yeast cell polarization and cytokinesis. Mol. Biol. Cell 12: 1061-1077.
60. Wu, J.Q., Kuhn, J.R., Kovar, D.R., and Pollard, T.D. 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 5: 723-734.
61. Wu, J.Q., Sirotkin, V., Kovar, D.R., Lord, M., Beltzner, C.C., Kuhn, J.R., and Pollard, T.D. 2006. Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 174: 391-402.