The meiosis-specific Sid2p-related protein Slk1p regulates forespore membrane assembly in fission yeast

Molecular Biology of the Cell

Volumn 19, Issue 9, 2008, Pages 3676-3690

  Yan, Hongyan ^a   Ge, Wanzhong ^a   Ting, Gang Chew ^a   Jeng, Yeong Chow ^a   McCollum, Dannel ^b   Neiman, Aaron M ^c   Balasubramanian, Mohan K ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PROTEIN KINASE; PROTEIN PSY1P; PROTEIN SID2P; PROTEIN SLK1P; PROTEIN SPO3; SYNTAXIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINESIS; GENE MUTATION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SPINDLE POLE BODY; SPOROGENESIS;

AMINO ACID SEQUENCE; CELL MEMBRANE; CYTOKINESIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GREEN FLUORESCENT PROTEINS; MEIOSIS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN KINASES; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

SCHIZOSACCHAROMYCETACEAE;

EID: 55549134338     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-10-1060     Document Type: Article

References (66)

1. 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.
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. Baluska, F., Menzel, D., and Barlow, P. W. (2006). Cytokinesis in plant and animal cells: endosomes 'shut the door.' Dev. Biol. 294, 1-10.
6. Basi, G., Schmid, E., and Maundrell, K. (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.
7. Bimbo, A. et al. (2005). Systematic deletion analysis of fission yeast protein kinases. Eukaryot. Cell 4, 799-813.
8. 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.
9. 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. USA 97, 5249-5254.
10. 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.
11. 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.
12. 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.
13. Flory, M. R., Morphew, M., Joseph, J. D., Means, A. R., and Davis, T. N. (2002). Pcp1p, an Spc110p-related calmodulin target at the centrosome of the fission yeast Schizosaccharomyces pombe. Cell Growth Differ. 13, 47-58.
14. Glotzer, M. (2001). Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351-386.
15. Glotzer, M. (2005). The molecular requirements for cytokinesis. Science 307, 1735-1739.
16. Gould, K. L., and Simanis, V. (1997). The control of septum formation in fission yeast. Genes Dev. 11, 2939-2951.
17. Gromley, A., Yeaman, C., Rosa, J., Redick, S., Chen, C. T., Mirabelle, S., Guha, M., Sillibourne, J., and Doxsey, S. J. (2005). Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle- mediated abscission. Cell 123, 75-87.
18. 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.
19. Guertin, D. A., Trautmann, S., and McCollum, D. (2002). Cytokinesis in eukaryotes. Microbiol. Mol. Biol. Rev. 66, 155-178.
20. Hagan, I. M., and Hyams, J. S. (1988). The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 89(Pt 3), 343-357.
21. Hochstenbach, F., Klis, F. M., van den Ende, H., van Donselaar, E., Peters, P. J., and Klausner, R. D. (1998). Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc. Natl. Acad. Sci. USA 95, 9161-9166.
22. Hou, M. C., Guertin, D. A., and McCollum, D. (2004). Initiation of cytokinesis is controlled through multiple modes of regulation of the Sid2p-Mob1p kinase complex. Mol. Cell. Biol. 24, 3262-3276.
23. 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.
24. Ikemoto, S., Nakamura, T., Kubo, M., and Shimoda, C. (2000). S. pombe sporulation-specific coiled-coil protein Spo15p is localized to the spindle pole body and essential for its modification. J. Cell Sci. 113(Pt 3), 545-554.
25. Jurgens, G. (2005). Plant cytokinesis: fission by fusion. Trends Cell Biol. 15, 277-283.
26. Kitajima, T. S., Kawashima, S. A., and Watanabe, Y. (2004). The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427, 510-517.
27. Komarnitsky, S. I., Chiang, Y. C., Luca, F. C., Chen, J., Toyn, J. H., Winey, M., Johnston, L. H., and Denis, C. L. (1998). DBF2 protein kinase binds to and acts through the cell cycle-regulated MOB1 protein. Mol. Cell. Biol. 18, 2100-2107.
28. 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.
29. Krapp, A., Gulli, M. P., and Simanis, V. (2004). SIN and the art of splitting the fission yeast cell. Curr. Biol. 14, R722-730.
30. 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.
31. 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(23), 4157-4163.
32. Liu, J., Tang, X., Wang, H., and Balasubramanian, M. (2000). Bgs2p, a 1,3-beta-glucan synthase subunit, is essential for maturation of ascospore wall in Schizosaccharomyces pombe. FEBS Lett. 478, 105-108.
33. Marash, M., and Gerst, J. E. (2001). t-SNARE dephosphorylation promotes SNARE assembly and exocytosis in yeast. EMBO J. 20, 411-421.
34. 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.
35. Martin-Castellanos, C. et al. (2005). A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events. Curr. Biol. 15, 2056-2062.
36. Martin, V., Ribas, J. C., Carnero, E., Duran, A., and Sanchez, Y. (2000). bgs2+, a sporulation-specific glucan synthase homologue is required for proper ascospore wall maturation in fission yeast. Mol. Microbiol. 38, 308-321.
37. Mata, J., Lyne, R., Burns, G., and Bahler, J. (2002). The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32, 143-147.
38. Matheson, J., Yu, X., Fielding, A. B., and Gould, G. W. (2005). Membrane traffic in cytokinesis. Biochem. Soc. Trans. 33, 1290-1294.
39. McCollum, D., Balasubramanian, M. K., Pelcher, L. E., Hemmingsen, S. M., and Gould, K. L. (1995). Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis. J. Cell Biol. 130, 651-660.
40. 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.
41. Mishra, M., Karagiannis, J., Sevugan, M., Singh, P., and Balasubramanian, M. K. (2005). The 14-3-3 protein rad24p modulates function of the cdc14p family phosphatase clp1p/flp1p in fission yeast. Curr. Biol. 15, 1376-1383.
42. Moreno, S., Klar, A., and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
43. Morrell, J. L., Tomlin, G. C., Rajagopalan, S., Venkatram, S., Feoktistova, A. S., Tasto, J. J., Mehta, S., Jennings, J. L., Link, A., Balasubramanian, M. K., and Gould, K. L. (2004). Sid4p-Cdc11p assembles the septation initiation network and its regulators at the S. pombe SPB. Curr. Biol. 14, 579-584.
44. 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.
45. Nakamura, T., Nakamura-Kubo, M., Hirata, A., and Shimoda, C. (2001). The Schizosaccharomyces pombe spo3+ gene is required for assembly of the fore-spore membrane and genetically interacts with psy1(+)-encoding syntaxin-like protein. Mol. Biol. Cell 12, 3955-3972.
46. Nakase, Y., Nakamura-Kubo, M., Ye, Y., Hirata, A., Shimoda, C., and Nakamura, T. (2008). Meiotic spindle pole bodies acquire the ability to assemble the spore plasma membrane by sequential recruitment of sporulation-specific components in fission yeast. Mol. Biol. Cell 19, 2476-2487.
47. 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.
48. Neiman, A. M. (2005). Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 565-584.
49. 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.
50. 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.
51. 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.
52. 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.
53. Rajagopalan, S., Wachtler, V., and Balasubramanian, M. (2003). Cytokinesis in fission yeast: a story of rings, rafts and walls. Trends Genet. 19, 403-408.
54. Salimova, E., Sohrmann, M., Fournier, N., and Simanis, V. (2000). The S. pombe orthologue of the S. cerevisiae mob1 gene is essential and functions in signalling the onset of septum formation. J. Cell Sci. 113(Pt 10), 1695-1704.
55. 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.
56. Shimoda, C. (2004). Forespore membrane assembly in yeast: coordinating SPBs and membrane trafficking. J. Cell Sci. 117, 389-396.
57. Simanis, V. (2003). Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116, 4263-4275.
58. 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.
59. 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.
60. 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.
61. Toyn, J. H., and Johnston, L. H. (1994). The Dbf2 and Dbf20 protein kinases of budding yeast are activated after the metaphase to anaphase cell cycle transition. EMBO J. 13, 1103-1113.
62. Vos, A., Dekker, N., Distel, B., Leunissen, J. A., and Hochstenbach, F. (2007). Role of the synthase domain of Ags1p in cell wall alpha-glucan biosynthesis in fission yeast. J. Biol. Chem. 282, 18969-18979.
63. 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(Pt 13), 2421-2432.
64. 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.
65. Wu, J. Q., and Pollard, T. D. (2005). Counting cytokinesis proteins globally and locally in fission yeast. Science 310, 310-314.
66. 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.