Inn1 and Cyk3 regulate chitin synthase during cytokinesis in budding yeasts

Journal of Cell Science

Volumn 125, Issue 22, 2012, Pages 5453-5466

  Devrekanli, Asli ^a   Foltman, Magdalena ^b   Roncero, Cesar ^c   Sanchez Diaz, Alberto ^b   Labib, Karim ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF CANTABRIA   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Budding yeasts; Chs2; Cyk3; Cytokinesis; Inn1

Indexed keywords

CHITIN SYNTHASE; CHITIN SYNTHASE II; CYK3 PROTEIN; FUNGAL PROTEIN; INN1 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CELL DIVISION; CYTOKINESIS; ENZYME ACTIVITY; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ALLELES; AMINO ACID SEQUENCE; BIOCATALYSIS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CHITIN SYNTHASE; CYTOKINESIS; GENES, DOMINANT; GENES, FUNGAL; GENES, SUPPRESSOR; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC;

EID: 84873532860     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.109157     Document Type: Article

References (53)

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. Cabib, E. (2004). The septation apparatus, a chitin-requiring machine in budding yeast. Arch. Biochem. Biophys. 426, 201-207.
3. Cabib, E., Sburlati, A., Bowers, B. and Silverman, S. J. (1989). Chitin synthase 1, an auxiliary enzyme for chitin synthesis in Saccharomyces cerevisiae. J. Cell Biol. 108, 1665-1672.
4. Calugi, C., Trabocchi, A. and Guarna, A. (2011). Novel small molecules for the treatment of infections caused by Candida albicans: a patent review (2002-2010). Expert Opin. Ther. Pat. 21, 381-397.
5. Charnock, S. J. and Davies, G. J. (1999). Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38, 6380-6385.
6. Chin, C. F., Bennett, A. M., Ma, W. K., Hall, M. C. and Yeong, F. M. (2012). Dependence of Chs2 ER export on dephosphorylation by cytoplasmic Cdc14 ensures that septum formation follows mitosis. Mol. Biol. Cell 23, 45-58.
7. Cho, W. and Stahelin, R. V. (2005). Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34, 119-151.
8. Cho, W. and Stahelin, R. V. (2006). Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 1761, 838-849.
9. Choi, W. J. and Cabib, E. (1994). The use of divalent cations and pH for the determination of specific yeast chitin synthetases. Anal. Biochem. 219, 368-372.
10. Dohmen, R. J., Wu, P. and Varshavsky, A. (1994). Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science 263, 1273-1276.
11. Foiani, M., Marini, F., Gamba, D., Lucchini, G. and Plevani, P. (1994). The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol. Cell. Biol. 14, 923-933.
12. Fox, D. S., Cox, G. M. and Heitman, J. (2003). Phospholipid-binding protein Cts1 controls septation and functions coordinately with calcineurin in Cryptococcus neoformans. Eukaryot. Cell 2, 1025-1035.
13. Gambus, A., van Deursen, F., Polychronopoulos, D., Foltman, M., Jones, R. C., Edmondson, R. D., Calzada, A. and Labib, K. (2009). A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J. 28, 2992-3004.
14. Hurley, J. H. (2006). Membrane binding domains. Biochim. Biophys. Acta 1761, 805-811.
15. Jendretzki, A., Ciklic, I., Rodicio, R., Schmitz, H. P. and Heinisch, J. J. (2009). Cyk3 acts in actomyosin ring independent cytokinesis by recruiting Inn1 to the yeast bud neck. Mol. Genet. Genomics 282, 437-451.
16. Kamei, T., Tanaka, K., Hihara, T., Umikawa, M., Imamura, H., Kikyo, M., Ozaki, K. and Takai, Y. (1998). Interaction of Bnr1p with a novel Src homology 3 domaincontaining Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273, 28341-28345.
17. Kanemaki, M., Sanchez-Diaz, A., Gambus, A. and Labib, K. (2003). Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 423, 720-724.
18. Kelley, L. A. and Sternberg, M. J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371.
19. Kim, J. and Sudbery, P. (2011). Candida albicans, a major human fungal pathogen. J. Microbiol. 49, 171-177.
20. Ko, N., Nishihama, R., Tully, G. H., Ostapenko, D., Solomon, M. J., Morgan, D. O. and Pringle, J. R. (2007). Identification of yeast IQGAP (Iqg1p) as an anaphasepromoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol. Biol. Cell 18, 5139-5153.
21. Korinek, W. S., Bi, E., Epp, J. A., Wang, L., Ho, J. and Chant, J. (2000). Cyk3, a novel SH3-domain protein, affects cytokinesis in yeast. Curr. Biol. 10, 947-950.
22. Kronstad, J. W., Attarian, R., Cadieux, B., Choi, J., D'Souza, C. A., Griffiths, E. J., Geddes, J. M., Hu, G., Jung, W. H., Kretschmer, M. et al. (2011). Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat. Rev. Microbiol. 9, 193-203.
23. Kubota, T., Shiba, T., Sugioka, S., Furukawa, S., Sawaki, H., Kato, R., Wakatsuki, S. and Narimatsu, H. (2006). Structural basis of carbohydrate transfer activity by human UDP-GalNAc: polypeptide alpha-N-acetylgalactosaminyltransferase (pp-GalNAc-T10). J. Mol. Biol. 359, 708-727.
24. Labib, K., Tercero, J. A. and Diffley, J. F. X. (2000). Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288, 1643-1647.
25. Lippincott, J. and Li, R. (1998). Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143, 1947-1960.
26. Martín-García, R. and Valdivieso, M. H. (2006). 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. 119, 2768-2779.
27. Martín-García, R., Durán, A. and Valdivieso, M. H. (2003). In Schizosaccharomyces pombe chs2p has no chitin synthase activity but is related to septum formation. FEBS Lett. 549, 176-180.
28. Merzendorfer, H. (2011). The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur. J. Cell Biol. 90, 759-769.
29. Mio, T., Yabe, T., Sudoh, M., Satoh, Y., Nakajima, T., Arisawa, M. and Yamada-Okabe, H. (1996). Role of three chitin synthase genes in the growth of Candida albicans. J. Bacteriol. 178, 2416-2419.
30. 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.
31. Morohashi, H., Maculins, T. and Labib, K. (2009). The amino-terminal TPR domain of Dia2 tethers SCF(Dia2) to the replisome progression complex. Curr. Biol. 19, 1943-1949.
32. Munro, C. A., Winter, K., Buchan, A., Henry, K., Becker, J. M., Brown, A. J., Bulawa, C. E. and Gow, N. A. (2001). Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Mol. Microbiol. 39, 1414-1426.
33. Nagahashi, S., Sudoh, M., Ono, N., Sawada, R., Yamaguchi, E., Uchida, Y., Mio, T., Takagi, M., Arisawa, M. and Yamada-Okabe, H. (1995). Characterization of chitin synthase 2 of Saccharomyces cerevisiae. Implication of two highly conserved domains as possible catalytic sites. J. Biol. Chem. 270, 13961-13967.
34. Nishihama, R., Schreiter, J. H., Onishi, M., Vallen, E. A., Hanna, J., Moravcevic, K., Lippincott, M. F., Han, H., Lemmon, M. A., Pringle, J. R. 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.
35. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T. and Kanemaki, M. (2009). An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922.
36. Oliferenko, S., Chew, T. G. and Balasubramanian, M. K. (2009). Positioning cytokinesis. Genes Dev. 23, 660-674.
37. Pollard, T. D. (2010). Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50-56.
38. Pollard, L. W., Onishi, M., Pringle, J. R. and Lord, M. (2012). Fission yeast Cyk3p is a transglutaminase-like protein that participates in cytokinesis and cell morphogenesis. Mol. Biol. Cell 23, 2433-2444.
39. Reijnst, P., Jorde, S. and Wendland, J. (2010). Candida albicans SH3-domain proteins involved in hyphal growth, cytokinesis, and vacuolar morphology. Curr. Genet. 56, 309-319.
40. Roberts-Galbraith, R. H., Chen, J. S., Wang, J. and Gould, K. L. (2009). The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 184, 113-127.
41. Roncero, C. and Sánchez, Y. (2010). Cell separation and the maintenance of cell integrity during cytokinesis in yeast: the assembly of a septum. Yeast 27, 521-530. Sable, C. A., Strohmaier, K. M. and Chodakewitz, J. A. (2008). Advances in antifungal therapy. Annu. Rev. Med. 59, 361-379.
42. Sable, C. A., Strohmaier, K. M. and Chodakewitz, J. A. (2008). Advances in antifungal therapy. Annu. Rev. Med. 59, 361-379.
43. Sanchez-Diaz, A., Marchesi, V., Murray, S., Jones, R., Pereira, G., Edmondson, R., Allen, T. and Labib, K. (2008). Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat. Cell Biol. 10, 395-406.
44. Sburlati, A. and Cabib, E. (1986). Chitin synthetase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J. Biol. Chem. 261, 15147-15152.
45. Schmidt, M., Bowers, B., Varma, A., Roh, D. H. and Cabib, E. (2002). In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J. Cell Sci. 115, 293-302.
46. Shaw, J. A., Mol, P. C., Bowers, B., Silverman, S. J., Valdivieso, M. H., Durán, A. and Cabib, E. (1991). The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 114, 111-123.
47. Sikorski, R. S. and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
48. Silverman, S. J., Sburlati, A., Slater, M. L. and Cabib, E. (1988). Chitin synthase 2 is essential for septum formation and cell division in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 85, 4735-4739.
49. Teh, E. M., Chai, C. C. and Yeong, F. M. (2009). Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 8, 2964-2974.
50. Tolliday, N., Bouquin, N. and Li, R. (2001). Assembly and regulation of the cytokinetic apparatus in budding yeast. Curr. Opin. Microbiol. 4, 690-695.
51. Valdivieso, M. H., Mol, P. C., Shaw, J. A., Cabib, E. and Durán, A. (1991). CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J. Cell Biol. 114, 101-109.
52. VerPlank, L. and Li, R. (2005). Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. Mol. Biol. Cell 16, 2529-2543.
53. Zhang, G., Kashimshetty, R., Ng, K. E., Tan, H. B. and Yeong, F. M. (2006). Exit from mitosis triggers Chs2p transport from the endoplasmic reticulum to motherdaughter neck via the secretory pathway in budding yeast. J. Cell Biol. 174, 207-220.