Yeast-to-hyphal transition triggers formin-dependent Golgi localization to the growing tip in Candida albicans

Molecular Biology of the Cell

Volumn 17, Issue 10, 2006, Pages 4364-4378

  Rida, Padmashree C G ^a   Nishikawa, Akiko ^a   Won, Gena Y ^a   Dean, Neta ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; METHENAMINE; PROTEIN BNI1; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CELL SECRETION; CELL VACUOLE; CONTROLLED STUDY; CYTOSKELETON; ENDOPLASMIC RETICULUM; FUNGUS HYPHAE; GOLGI COMPLEX; MICROTUBULE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEDIMENTATION; YEAST;

ACTINS; CANDIDA ALBICANS; CELL POLARITY; CELLS, CULTURED; ENDOPLASMIC RETICULUM; EPITOPES; FLUORESCENT ANTIBODY TECHNIQUE; FUNGAL PROTEINS; GENES, REPORTER; GOLGI APPARATUS; HYPHAE; MICROFILAMENT PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; VACUOLES; YEASTS;

CANDIDA ALBICANS; FUNGI;

EID: 33749456481     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-02-0143     Document Type: Article

References (58)

1. Akashi, T., Kanbe, T., and Tanaka, K. (1994). The role of the cytoskeleton in the polarized growth of the germ tube in Candida albicans. Microbiology 140, 271-280.
2. Bates, S., et al. (2006). Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans J. Biol. Chem. 281, 90-98.
3. Cole, L., Orlovich, D. A., and Ashford, A. E. (1998). Structure, function and motility of vacuoles in filamentous fungi. Fungal Genet. Biol. 24, 86-100.
4. Cooper, J. A. (1987). Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105, 1473-1478.
5. Cormack, B. P., Bertram, G., Egerton, M., Gow, N. A., Falkow, S., and Brown, A. J. (1997). Yeast-enhanced green fluorescent protein (yEGFP)a reporter of gene expression in Candida albicans. Microbiology 143, 303-311.
6. Crampin, H., Finley, K., Gerami-Nejad, M., Court, H., Gale, C., Berman, J., and Sudbery, P. (2005). Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae. J. Cell Sci. 118, 2935-2947.
7. Dean, N., Zhang, Y. B., and Poster, J. B. (1997). The VRG4 gene is required for GDP-mannose transport into the lumen of the Golgi in the yeast, Saccharomyces cerevisiae. J. Biol. Chem, 272, 31908-31914.
8. Fratti, R. A., Jun, Y. Merz, A. J., Margolis, N., and Wickner, W. (2004). Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J. Cell Biol. 167, 1087-1098.
9. Evangelista, M., Blundell, K., Longtine, M. S., Chow, C. J., Adames, N., Pringle, J. R., Peter, M., and Boone, C. (1997). Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118-122.
10. Evangelista, M., Pruyne, D., Amberg, D. C., Boone, C., and Bretscher, A. (2002). Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4, 260-269.
11. Evangelista, M., Zigmond, S., and Boone, C. (2003). Formins: signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116, 2603-2611.
12. Finger, F. P., and Novick, P. (1998). Spatial regulation of exocytosis: lessons from yeast. J. Cell Biol. 142, 609-612.
13. Fonzi, W. A., and Irwin, M. Y. (1993). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
14. Fujiwara, T., Tanaka, K., Mino, A., Kikyo, M., Takahashi, K., Shimizu, K., and Takai, Y. (1998). Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1221-1233.
15. Gao, X. D., and Dean, N. (2000). Distinct protein domains of the yeast Golgi GDP-mannose transporter mediate oligomer assembly and export from the endoplasmic reticulum. J. Biol. Chem. 275, 17718-17727.
16. Gow, N. A., Brown, A. J., and Odds, F. C. (2002). Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5, 366-371.
17. Harris, S. D., Read, N. D., Roberson, R. W., Shaw, B., Seiler, S., Plamann, M., and Momany, M. (2005). Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryot. Cell 4, 225-229.
18. Hazan, I., Sepulveda-Becerra, M., and Liu, H. (2002). Hyphal elongation is regulated independently of cell cycle in Candida albicans. Mol. Biol. Cell 13, 134-145.
19. Herrero, A. B., Uccelletti, D., Hirschberg, C. B., Dominguez, A., and Abeijon, C. (2002). The Golgi GDPase of the fungal pathogen Candida albicans affects morphogenesis, glycosylation, and cell wall properties. Eukaryot. Cell 1, 420-431.
20. Higgs, H. N. (2005). Formin proteins: a domain-based approach. Trends Biochem. Sci. 30, 342-353.
21. Howard, R. J. (1981). Ultrastructural analysis of hyphal tip cell growth in fungi: Spitzenkörper, cytoskeleton and endomembranes after freeze-substitution. J. Cell Sci. 48, 89-103.
22. Howard, R. J., and Aist, J. R. (1977). Effects of MBC on hyphal tip organization, growth, and mitosis of Fusarium acuminatum, and their antagonism by D2O. Protoplasma 92, 195-210.
23. Kohno, H., et al, (1996). Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15, 6060-6068.
24. Koning, A. J., Lum, P. Y., Williams, J. M., and Wright, R. (1993). DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil. Cytoskeleton 25, 111-128.
25. Lew, D. J., and Reed, S. I. (1995). Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5, 17-23.
26. Li, C. R., Wang, Y. M., De Zheng, X., Liang, H. Y., Tang, J. C., and Wang, Y. (2005). The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J. Cell Sci. 118, 2637-2648.
27. Lo, H. J., Kohler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G. R. (1997). 'Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949.
28. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, F., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
29. Losev, E., Reinke, C. A., Jellen, J., Strongin, D. E., Bevis, B. J., and Glick, B. S. (2006). Golgi maturation visualized in living yeast. Nature 441, 1002-1006.
30. Martin, R., Walther, A., and Wendland, J. (2005). Ras1-induced hyphal development in Candida albicans requires the formin Bni1. Eukaryot. Cell 4, 1712-1724.
31. Murad, A. M., Lee, P. R., Broadbent, I. D., Barelle, C. J., and Brown, A. J. (2000). CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16, 325-327.
32. Nantel, A., et al. (2002). Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13, 3452-3465.
33. Neiman, A. M., Mhaiskar, V., Manus, V., Galibert, P., and Dean, N. (1997). Saccharomyces cerevisiae HOC1, a suppressor of pkc1, encodes a putative glycosyltransferase. Genetics 145, 637-645.
34. Nishikawa, A., Poster, J. B., Jigami, Y., and Dean, N. (2002). Molecular and phenotypic analysis of CaVRG4, encoding an essential Golgi apparatus GDP-mannose transporter. J. Bacteriol. 184, 29-42.
35. Pannunzio, V. G., Burgos, H. I., Alonso, M., Mattoon, J. R., Ramos, E. H., and Stella, C. A. (2004). A simple chemical method for rendering wild-type yeast permeable to brefeldin a that does not require the presence of an erge mutation. J. Biomed. Biotechnol. 2004, 150-155.
36. Pringle, J. R., Preston, R. A., Adams, A. E., Stearns, T., Drubin, D. G., Haarer, B. K., and Jones, E. W. (1989). Fluorescence microscope methods for yeast. Methods Cell Biol. 31, 357-435.
37. 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.
38. Pruyne, D., Gao, L., Bi, E., and Bretscher, A. (2004). Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15, 4971-4989.
39. Pruyne, D., Legesse-Miller, A., Gao, L., Dong, Y., and Bretscher, A. (2004). Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 20, 559-591.
40. Rambourg, A., Jackson, C. L., and Clermont, Y. (2001). Three dimensional configuration of the secretory pathway and segregation of secretion granules in the yeast Saccharomyces cerevisiae. J. Cell Sci. 114, 2231-2239.
41. Raudaskoski, M., Mao, W. Z., and Yli-Mattila, T. (1994). Microtubule cytoskeleton in hyphal growth. Response to nocodazole in a sensitive and a tolerant strain of the homobasidiomycete Schizophyllum commune. Eur. J. Cell Biol. 64, 131-141.
42. Reynaga-Pena, C. G., Gierz, G., and Bartnicki-Garcia. (1997). Analysis of the role of the Spitzenkörper in fungal morphogenesis by computer simulation of apical branching in Aspergillus niger Proc. Natl. Acad. Sci. USA 94, 9096-9101.
43. Sagot, I., Rodal, A. A., Moseley, J., Goode, B. L., and Pellman, D. (2002). An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4, 626-631.
44. Sharpless, K. E., and Harris, S. D. (2002). Functional characterization and localization of the Aspergillus nidulans formin SEPA. Mol. Biol. Cell 13, 469-479.
45. Sheu, Y. J., Santos, B., Fortin, N., Costigan, C., and Snyder, M. (1998). Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell Biol. 18, 4053-4069.
46. Steinberg, G., Wedlich-Soldner, R., Brill, M., and Schulz, I. (2001). Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci. 114, 609-622.
47. Sudbery, P., Gow, N., and Berman, J. (2004). The distinct morphogenic states of Candida albicans. Trends Microbiol. 12, 317-324.
48. Temperli, E., Roos, U. P., and Hohl, H. R. (1990). Actin and tubulin cytoskeletons in germlings of the oomycete fungus Phytophthora infestans. Eur. J. Cell Biol. 53, 75-88.
49. That, T. C., Rossier, C., Barja, F., Turian, G., and Roos, U. P. (1988). Induction of multiple germ tubes in Neurospora crassa by antitubulin agents. Eur. J. Cell Biol. 46, 68-79.
50. Tominaga, T., Sahai, E., Chardin, P., McCormick, F., Courtneidge, S. A., and Alberts, A. S. (2000). Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 5, 13-25.
51. Vida, T. A., Graham, T. R., and Emr, S. D. (1990). In vitro reconstitution of intercompartmental protein transport to the yeast vacuole. J. Cell Biol. 111, 2871-2884.
52. Walther, A., and Wendland, J. (2003). An improved transformation protocol for the human fungal pathogen Candida albicans. Curr. Genet. 42, 339-343.
53. Walther, A., and Wendland, J. (2004). Apical localization of actin patches and vacuolar dynamics in Ashbya gossypii depend on the WASP homolog Wal1p. J. Cell Sci. 117, 4947-4958.
54. Weisman, L. S., Emr, S. D., and Wickner, W. T. (1990). Mutants of Saccharomyces cerevisiae that block intervacuole vesicular traffic and vacuole division and segregation. Proc. Natl. Acad. USA 87, 1076-1080.
55. Wilson, R. B., Davis, D., and Mitchell, A. P. (1999). Rapid hypothesis testing with Candida albican through gene disruption with short homology regions. J. Bacteriol. 181, 1868-1874.
56. Yang, H. C., and Pon, L. A. (2002). Actin cable dynamics in budding yeast. Proc. Natl. Acad. USA 99, 751-756.
57. Yokoyama, K., Kaji, H., Nishimura, K., and Miyaji, M. (1990). The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans. J. Gen. Microbiol. 136, 1067-1075.
58. Zheng, X. D., Wang, Y. M., and Wang, Y. (2003). CaSPA2 is important for polarity establishment and maintenance in Candida albicans. Mol. Microbiol. 49, 1391-1405.