Cell wall stress induces alternative fungal cytokinesis and septation strategies

Journal of Cell Science

Volumn 126, Issue 12, 2013, Pages 2668-2677

  Walker, Louise A ^a   Lenardon, Megan D ^a   Preechasuth, Kanya ^a   Munro, Carol A ^a   Gow, Neil A R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Chitin; Cytokinesis; Fungal cell wall; Septum; Signal transduction; Stress response

Indexed keywords

BETA GLUCAN; CHITIN SYNTHASE; FUNGAL ENZYME;

ARTICLE; CANDIDA ALBICANS; CELL DIVISION; CELL MUTANT; CELL STRESS; CELL WALL; CONTROLLED STUDY; CYTOKINESIS; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SYNTHESIS; TIME LAPSE IMAGING; TIME-LAPSE VIDEO MICROSCOPY;

CHITIN; CYTOKINESIS; FUNGAL CELL WALL; SEPTUM; SIGNAL TRANSDUCTION; STRESS RESPONSE;

CANDIDA ALBICANS; CELL DIVISION; CELL WALL; CHITIN; CHITIN SYNTHASE; CYTOKINESIS; STRESS, PHYSIOLOGICAL;

CANDIDA ALBICANS; FUNGI;

EID: 84879980268     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.118885     Document Type: Article

References (57)

1. Bi, E., Maddox, P., Lew, D. J., Salmon, E. D., McMillan, J. N., Yeh, E. and Pringle, J. R. (1998). Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142, 1301-1312.
2. Bulawa, C. E. (1993). Genetics molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47 505-534.
3. Bulawa, C. E. and Osmond, B. C. (1990). Chitin synthase I and chitin synthase II are not required for chitin synthesis in vivo in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 87, 7424-7428.
4. Bulawa, C. E., Miller, D. W., Henry, L. K. and Becker, J. M. (1995). Attenuated virulence of chitin-deficient mutants of Candida albicans. Proc. Natl. Acad. Sci. USA 92, 10570-10574.
5. Cabib, E. (2004). The septation apparatus, a chitin-requiring machine in budding yeast. Arch. Biochem. Biophys. 426, 201-207.
6. Cabib, E. and Schmidt, M. (2003). Chitin synthase III activity, but not the chitin ring, is required for remedial septa formation in budding yeast. FEMS Microbiol. Lett. 224, 299-305.
7. 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.
8. 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.
9. Cid, V. J., Adamiková, L., Sánchez, M., Molina, M. and Nombela, C. (2001). Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147, 1437-1450.
10. DeMarini, D. J., Adams, A. E., Fares, H., De Virgilio, C., Valle, G., Chuang, J. S. and Pringle, J. R. (1997). A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 139, 75-93.
11. Denning, D. W. (2003). Echinocandin antifungal drugs. Lancet 362, 1142-1151.
12. Douglas, C. M., D'Ippolito, J. A., Shei, G. J., Meinz, M., Onishi, J., Marrinan, J. A., Li, W., Abruzzo, G. K., Flattery, A., Bartizal, K. et al. (1997). Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob. Agents Chemother. 41, 2471-2479.
13. Fonzi, W. A. and Irwin, M. Y. (1993). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
14. Gaughran, J. P., Lai, M. H., Kirsch, D. R. and Silverman, S. J. (1994). Nikkomycin Z is a specific inhibitor of Saccharomyces cerevisiae chitin synthase isozyme Chs3 in vitro and in vivo. J. Bacteriol. 176, 5857-5860.
15. Gladfelter, A. S. and Sudbery, P. E. (2008). Septins in four model fungal systems: diversity in form and function. In The Septins (ed. P. A. Hall, S. E. H. Russell and J. R. Pringle), pp. 125-146. West Sussex: Wiley-Blackwell.
16. Gladfelter, A. S., Pringle, J. R. and Lew, D. J. (2001). The septin cortex at the yeast mother-bud neck. Curr. Opin. Microbiol. 4, 681-689.
17. Gow, N. A. R. and Gooday, G. W. (1982). Growth kinetics and morphology of colonies of the filamentous form of Candida albicans. J. Gen. Microbiol. 128, 2187-2194.
18. Gow, N. A. R., Gooday, G. W., Newsam, R. J. and Gull, K. (1980). Ultrastructure of the septum in Candida albicans. Microbiology 4, 357-359.
19. Gow, N. A. R., Robbins, P. W., Lester, J. W., Brown, A. J. P., Fonzi, W. A., Chapman, T. and Kinsman, O. S. (1994). A hyphal-specific chitin synthase gene (CHS2) is not essential for growth, dimorphism, or virulence of Candida albicans. Proc. Natl. Acad. Sci. USA 91, 6216-6220.
20. Gow, N. A. R., van de Veerdonk, F. L., Brown, A. J. P. and Netea, M. G. (2012). Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat. Rev. Microbiol. 10, 112-122.
21. Hilenski, L. L., Naider, F. and Becker, J. M. (1986). Polyoxin D inhibits colloidal gold-wheat germ agglutinin labelling of chitin in dimorphic forms of Candida albicans. J. Gen. Microbiol. 132, 1441-1451.
22. Ichinomiya, M., Yamada, E., Yamashita, S., Ohta, A. and Horiuchi, H. (2005). Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot. Cell 4, 1125-1136.
23. Klis, F. M., Mol, P., Hellingwerf, K. and Brul, S. (2002). Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 26, 239-256.
24. Klis, F. M., Boorsma, A. and De Groot, P. W. (2006). Cell wall construction in Saccharomyces cerevisiae. Yeast 23, 185-202.
25. Larson, J. R., Bharucha, J. P., Ceaser, S., Salamon, J., Richardson, C. J., Rivera, S. M. and Tatchell, K. (2008). Protein phosphatase type 1 directs chitin synthesis at the bud neck in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 3040-3051.
26. Lee, K. K., Maccallum, D. M., Jacobsen, M. D., Walker, L. A., Odds, F. C., Gow, N. A. R. and Munro, C. A. (2012). Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob. Agents Chemother. 56, 208-217.
27. Lenardon, M. D., Whitton, R. K., Munro, C. A., Marshall, D. and Gow, N. A. R. (2007). Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol. Microbiol. 66, 1164-1173.
28. Lenardon, M. D., Munro, C. A. and Gow, N. A. R. (2010). Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol. 13, 416-423.
29. Lippincott, J., Shannon, K. B., Shou, W., Deshaies, R. J. and Li, R. (2001). The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J. Cell Sci. 114, 1379-1386.
30. Meitinger, F., Petrova, B., Lombardi, I. M., Bertazzi, D. T., Hub, B., Zentgraf, H. and Pereira, G. (2010). Targeted localization of Inn1, Cyk3 and Chs2 by the mitotic-exit network regulates cytokinesis in budding yeast. J. Cell Sci. 123, 1851-1861.
31. 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.
32. Motoyama, T., Kojima, N., Horiuchi, H., Ohta, A. and Takagi, M. (1994). Isolation of a chitin synthase gene (chsC) of Aspergillus nidulans. Biosci. Biotechnol. Biochem. 58, 2254-2257.
33. Motoyama, T., Fujiwara, M., Kojima, N., Horiuchi, H., Ohta, A. and Takagi, M. (1997). The Aspergillus nidulans genes chsA and chsD encode chitin synthases which have redundant functions in conidia formation [corrected and republished article originally appeared in Mol Gen Genet 1996 Jun; 251(4):442-50]. Mol. Gen. Genet. 253, 520-528.
34. Munro, C. A. and Gow, N. A. R. (1995). Chitin biosynthesis as a target for antifungals. In Antifungal Agents: Discovery and Mode of Action (ed. G. K. Dixon, L. G. Copping, and D. W. Hollomon), pp. 161-171. Oxford: Bios Scientific.
35. Munro, C. A. and Gow, N. A. R. (2001). Chitin synthesis in human pathogenic fungi. Med. Mycol. 39 Suppl. 1, 41-53.
36. Munro, C. A., Schofield, D. A., Gooday, G. W. and Gow, N. A. R. (1998). Regulation of chitin synthesis during dimorphic growth of Candida albicans. Microbiology 144, 391-401.
37. Munro, C. A., Winter, K., Buchan, A., Henry, K., Becker, J. M., Brown, A. J. P., Bulawa, C. E. and Gow, N. A. R. (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.
38. Munro, C. A., Whitton, R. K., Hughes, H. B., Rella, M., Selvaggini, S. and Gow, N. A. R. (2003). CHS8-a fourth chitin synthase gene of Candida albicans contributes to in vitro chitin synthase activity, but is dispensable for growth. Fungal Genet. Biol. 40, 146-158.
39. Munro, C. A., Selvaggini, S., de Bruijn, I., Walker, L. A., Lenardon, M. D., Gerssen, B., Milne, S., Brown, A. J. P. and Gow, N. A. R. (2007). The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol. Microbiol. 63, 1399-1413.
40. Oh, Y. and Bi, E. (2011). Septin structure and function in yeast and beyond. Trends Cell Biol. 21, 141-148.
41. Popolo, L., Gilardelli, D., Bonfante, P. and Vai, M. (1997). Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1delta mutant of Saccharomyces cerevisiae. J. Bacteriol. 179, 463-469.
42. Rancati, G., Pavelka, N., Fleharty, B., Noll, A., Trimble, R., Walton, K., Perera, A., Staehling-Hampton, K., Seidel, C. W. and Li, R. (2008). Aneuploidy and polyploidy underlie rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135, 879-893.
43. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
44. Rodri'guez-Quiñones, J. F. and Rodri'guez-Medina, J. R. (2009). Differential gene expression signatures for cell wall integrity found in chitin synthase II (chs2Delta) and myosin II (myo1Delta) deficient cytokinesis mutants of Saccharomyces cerevisiae. BMC Res. Notes 2, 87.
45. Roncero, C. (2002). The genetic complexity of chitin synthesis in fungi. Curr. Genet. 41, 367-378.
46. Ruiz-Herrera, J., Gonza'lez-Prieto, J. M. and Ruiz-Medrano, R. (2002). Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res. 1, 247-256.
47. 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.
48. Shaw, J. A., Mol, P. C., Bowers, B., Silverman, S. J., Valdivieso, M. H., Dura'n, 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.
49. 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.
50. Sudoh, M., Yamazaki, T., Masubuchi, K., Taniguchi, M., Shimma, N., Arisawa, M. and Yamada-Okabe, H. (2000). Identification of a novel inhibitor specific to the fungal chitin synthase. Inhibition of chitin synthase 1 arrests the cell growth, but inhibition of chitin synthase 1 and 2 is lethal in the pathogenic fungus Candida albicans. J. Biol. Chem. 275, 32901-32905.
51. Tronchin, G., Poulain, D., Herbaut, J. and Biguet, J. (1981). Localization of chitin in the cell wall of Candida albicans by means of wheat germ agglutinin. Fluorescence and ultrastructural studies. Eur. J. Cell Biol. 26, 121-128.
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. Versele, M. and Thorner, J. (2004). Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J. Cell Biol. 164, 701-715.
54. Veses, V. and Gow, N. A. R. (2008). Vacuolar dynamics during the morphogenetic transition in Candida albicans. FEMS Yeast Res. 8, 1339-1348.
55. Walker, L. A., Munro, C. A., de Bruijn, I., Lenardon, M. D., McKinnon, A. and Gow, N. A. R. (2008). Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog. 4, e1000040.
56. 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.
57. Zheng, L., Mendoza, L., Wang, Z., Liu, H., Park, C., Kauffman, S., Becker, J. M. and Szaniszlo, P. J. (2006). WdChs1p, a class II chitin synthase, is more responsible than WdChs2p (Class I) for normal yeast reproductive growth in the polymorphic, pathogenic fungus Wangiella (Exophiala) dermatitidis. Arch. Microbiol. 185, 316-329.