Meiotic actin rings are essential for proper sporulation in fission yeast

Journal of Cell Science

Volumn 125, Issue 6, 2012, Pages 1429-1439

  Yan, Hongyan ^a   Balasubramanian, Mohan K ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Fission yeast; Meiotic actin ring; Sincytokinesis

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; F ACTIN; FOR3 PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SCHIZOSACCHAROMYCES POMBE; SPINDLE POLE BODY; SPOROGENESIS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84861208407     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.jcs091561     Document Type: Article

References (81)

1. Ayscough, K. R., Stryker, J., Pokala, N., Sanders, M., Crews, P. and Drubin, D. G. (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137, 399-416.
2. 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.
3. Balasubramanian, M. K., Hirani, B. R., Burke, J. D. and Gould, K. L. (1994). The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125, 1289-1301.
4. 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.
5. Balasubramanian, M. K., Bi, E. and Glotzer, M. (2004). Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14, R806-R818.
6. Bardin, A. J. and Amon, A. (2001). Men and sin: what's the difference? Nat. Rev. Mol. Cell Biol. 2, 815-826.
7. Baum, B. and Kunda, P. (2005). Actin nucleation: spire - actin nucleator in a class of its own. Curr. Biol. 15, R305-R308.
8. Campellone, K. G. andWelch, M. D. (2010). A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251.
9. Castagnetti, S., Behrens, R. and Nurse, P. (2005). End4/Sla2 is involved in establishment of a new growth zone in Schizosaccharomyces pombe. J. Cell Sci. 118, 1843-1850.
10. 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.
11. Chesarone, M. A. and Goode, B. L. (2009). Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37.
12. Dobbelaere, J. and Barral, Y. (2004). Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305, 393-396.
13. Edamatsu, M. and Toyoshima, Y. Y. (2003). Fission yeast synaptobrevin is involved in cytokinesis and cell elongation. Biochem. Biophys. Res. Commun. 301, 641-645.
14. 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.
15. Evangelista, M., Zigmond, S. and Boone, C. (2003). Formins: signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116, 2603-2611.
16. 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.
17. 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.
18. Feierbach, B. and Chang, F. (2001). Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11, 1656-1665.
19. Fujiwara, K. and Pollard, T. D. (1976). Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J. Cell Biol. 71, 848-875.
20. Fujiwara, K., Porter, M. E. and Pollard, T. D. (1978). Alpha-actinin localization in the cleavage furrow during cytokinesis. J. Cell Biol. 79, 268-275.
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. Furge, K. A., Cheng, Q. C., Jwa, M., Shin, S., Song, K. and Albright, C. F. (1999). Regions of Byr4, a regulator of septation in fission yeast, that bind Spg1 or Cdc16 and form a two-component GTPase-activating protein with Cdc16. J. Biol. Chem. 274, 11339-11343.
23. Ge, W., Chew, T. G., Wachtler, V., Naqvi, S. N. and Balasubramanian, M. K. (2005). The novel fission yeast protein Pal1p interacts with Hip1-related Sla2p/End4p and is involved in cellular morphogenesis. Mol. Biol. Cell 16, 4124-4138.
24. Glotzer, M. (2001). Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351-386.
25. Glotzer, M. (2005). The molecular requirements for cytokinesis. Science 307, 1735-1739
26. Goley, E. D. and Welch, M. D. (2006). The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713-726.
27. Gotte, M. and von Mollard, G. F. (1998). A new beat for the SNARE drum. Trends Cell Biol. 8, 215-218.
28. Gould, K. L. and Simanis, V. (1997). The control of septum formation in fission yeast. Genes Dev. 11, 2939-2951.
29. Gourlay, C. W., Dewar, H., Warren, D. T., Costa, R., Satish, N. and Ayscough, K. R. (2003). An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast. J. Cell Sci. 116, 2551-2564.
30. 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.
31. Hachet, O. and Simanis, V. (2008). Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev. 22, 3205-3216.
32. Hirata, A. and Shimoda, C. (1992). Electron microscopic examination of sporulationdeficient mutants of the fission yeast Schizosaccharomyces pombe. Arch. Microbiol. 158, 249-255.
33. Holtzman, D. A., Yang, S. and Drubin, D. G. (1993). Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J. Cell Biol. 122, 635-644.
34. 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.
35. Itadani, A., Nakamura, T. and Shimoda, C. (2006). Localization of type I myosin and F-actin to the leading edge region of the forespore membrane in Schizosaccharomyces pombe. Cell Struct. Funct. 31, 181-195.
36. 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.
37. Karagiannis, J., Bimbo, A., Rajagopalan, S., Liu, J. and Balasubramanian, M. K. (2005). The nuclear kinase Lsk1p positively regulates the septation initiation network and promotes the successful completion of cytokinesis in response to perturbation of the actomyosin ring in Schizosaccharomyces pombe. Mol. Biol. Cell 16, 358-371.
38. Krapp, A. and Simanis, V. (2008). An overview of the fission yeast septation initiation network (SIN). Biochem. Soc. Trans. 36, 411-415.
39. 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.
40. Krapp, A., Gulli, M. P. and Simanis, V. (2004). SIN and the art of splitting the fission yeast cell. Curr. Biol. 14, R722-R730.
41. Krapp, A., Collin, P., Cokoja, A., Dischinger, S., Cano, E. and Simanis, V. (2006). The Schizosaccharomyces pombe septation initiation network (SIN) is required for spore formation in meiosis. J. Cell Sci. 119, 2882-2891.
42. 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.
43. Lee, W. L., Bezanilla, M. and Pollard, T. D. (2000). Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J. Cell Biol. 151, 789-800.
44. Li, C., Furge, K. A., Cheng, Q. C. and Albright, C. F. (2000). Byr4 localizes to spindle-pole bodies in a cell cycle-regulated manner to control Cdc7 localization and septation in fission yeast. J. Biol. Chem. 275, 14381-14387.
45. Maeda, Y., Kashiwazaki, J., Shimoda, C. and Nakamura, T. (2009). The Schizosaccharomyces pombe syntaxin 1 homolog, Psy1, is essential in the development of the forespore membrane. Biosci. Biotechnol. Biochem. 73, 339-345.
46. 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.
47. McCollum, D. and Gould, K. L. (2001). Timing is everything: regulation of mitotic exit and cytokinesis by the MEN and SIN. Trends Cell Biol. 11, 89-95.
48. McCollum, D., Balasubramanian, M. K., Pelcher, L. E., Hemmingsen, S. M. and Gould, K. L. (1995). Schizosaccharomyces pombe cdc4+ gene encodes a novel EFhand protein essential for cytokinesis. J. Cell Biol. 130, 651-660.
49. McCollum, D., Feoktistova, A., Morphew, M., Balasubramanian, M. and Gould, K. L. (1996). The Schizosaccharomyces pombe actin-related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. EMBO J. 15, 6438-6446.
50. 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.
51. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
52. Motegi, F., Nakano, K. and Mabuchi, I. (2000). Molecular mechanism of myosin-II assembly at the division site in Schizosaccharomyces pombe. J. Cell Sci. 113, 1813-1825.
53. 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.
54. Nakamura, T., Nakamura-Kubo, M., Hirata, A. and Shimoda, C. (2001). The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1(+)-encoding syntaxin-like protein. Mol. Biol. Cell 12, 3955-3972.
55. Nakamura, T., Kashiwazaki, J. and Shimoda, C. (2005). A fission yeast SNAP-25 homologue, SpSec9, is essential for cytokinesis and sporulation. Cell Struct. Funct. 30, 15-24.
56. Nakamura, T., Asakawa, H., Nakase, Y., Kashiwazaki, J., Hiraoka, Y. and Shimoda, C. (2008). Live observation of forespore membrane formation in fission yeast. Mol. Biol. Cell. 19, 3544-3553.
57. Nakano, K., Satoh, K., Morimatsu, A., Ohnuma, M. and Mabuchi, I. (2001). Interactions among a fimbrin, a capping protein, and an actin-depolymerizing factor in organization of the fission yeast actin cytoskeleton. Mol. Biol. Cell. 12, 3515-3526.
58. Naqvi, N. I., Wong, K. C., Tang, X. and Balasubramanian, M. K. (2000). Type II myosin regulatory light chain relieves auto-inhibition of myosin-heavy-chain function. Nat. Cell Biol. 2, 855-858.
59. Neiman, A. M. (2005). Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 565-584.
60. Ohtaka, A., Okuzaki, D., Saito, T. T. and Nojima, H. (2007). Mcp4, a meiotic coiledcoil protein, plays a role in F-actin positioning during Schizosaccharomyces pombe meiosis. Eukaryot. Cell 6, 971-983.
61. Ohtaka, A., Okuzaki, D. and Nojima, H. (2008). Mug27 is a meiosis-specific protein kinase that functions in fission yeast meiosis II and sporulation. J. Cell Sci. 121, 1547-1558.
62. Okazaki, K., Okazaki, N., Kume, K., Jinno, S., Tanaka, K. and Okayama, H. (1990). High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 18, 6485-6489.
63. Okuzaki, D., Satake, W., Hirata, A. and Nojima, H. (2003). Fission yeast meu14+ is required for proper nuclear division and accurate forespore membrane formation during meiosis II. J. Cell Sci. 116, 2721-2735.
64. Perez-Hidalgo, L., Rozalen, A. E., Martin-Castellanos, C. and Moreno, S. (2008). Slk1 is a meiosis-specific Sid2-related kinase that coordinates meiotic nuclear division with growth of the forespore membrane. J. Cell Sci. 121, 1383-1392.
65. Petersen, J., Nielsen, O., Egel, R. and Hagan, I. M. (1998). F-actin distribution and function during sexual differentiation in Schizosaccharomyces pombe. J. Cell Sci. 111, 867-876.
66. Pruyne, D., Evangelista, M., Yang, C., Bi, E., Zigmond, S., Bretscher, A. and Boone, C. (2002). Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612-615.
67. Schmidt, S., Hofmann, K. and Simanis, V. (1997). Sce3, a suppressor of the Schizosaccharomyces pombe septation mutant cdc11, encodes a putative RNAbinding protein. Nucleic Acids Res. 25, 3433-3439.
68. Schroeder, T. E. (1968). Cytokinesis: filaments in the cleavage furrow. Exp. Cell Res. 53, 272-276.
69. Schroeder, T. E. (1973). Actin in dividing cells: contractile ring filaments bind heavy meromyosin. Proc. Natl. Acad. Sci. USA 70, 1688-1692.
70. Shimoda, C. (2004). Forespore membrane assembly in yeast: coordinating SPBs and membrane trafficking. J. Cell Sci. 117, 389-396.
71. Simanis, V. (2003). Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116, 4263-4275.
72. 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.
73. 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.
74. Toya, M., Motegi, F., Nakano, K., Mabuchi, I. and Yamamoto, M. (2001). Identification and functional analysis of the gene for type I myosin in fission yeast. Genes Cells 6, 187-199.
75. Wong, K. C., Naqvi, N. I., Iino, Y., Yamamoto, M. and Balasubramanian, M. K. (2000). Fission yeast Rng3p: an UCS-domain protein that mediates myosin II assembly during cytokinesis. J. Cell Sci. 113, 2421-2432.
76. Wu, J. Q. and Pollard, T. D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
77. Wu, J. Q., Bahler, J. and Pringle, J. R. (2001). Roles of a fimbrin and an alpha-actininlike protein in fission yeast cell polarization and cytokinesis. Mol. Biol. Cell 12, 1061-1077.
78. 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.
79. 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.
80. Yamamoto, M. (1996). Regulation of meiosis in fission yeast. Cell Struct. Funct. 21, 431-436.
81. Yan, H., Ge, W., Chew, T. G., Chow, J. Y., McCollum, D., Neiman, A. M. and Balasubramanian, M. K. (2008). The meiosis-specific Sid2p-related protein Slk1p regulates forespore membrane assembly in fission yeast. Mol. Biol. Cell 19, 3676-3690.