Role of actin cytoskeletal dynamics in activation of the cyclic AMP pathway and HWP1 gene expression in Candida albicans

Eukaryotic Cell

Volumn 6, Issue 10, 2007, Pages 1824-1840

  Wolyniak, Michael J ^a   Sundstrom, Paula ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYCLIC AMP; CYTOCHALASIN; CYTOCHALASIN A; DEPSIPEPTIDE; FUNGAL PROTEIN; FUSED HETEROCYCLIC RINGS; HWP1 PROTEIN, CANDIDA ALBICANS; JASPAMIDE; LATRUNCULIN A; MEMBRANE PROTEIN; THIAZOLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL MODEL; CANDIDA ALBICANS; CELL POLARITY; CYTOLOGY; CYTOSKELETON; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; FUNGUS HYPHAE; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT;

ACTINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CANDIDA ALBICANS; CELL POLARITY; CYCLIC AMP; CYTOCHALASINS; CYTOSKELETON; DEPSIPEPTIDES; FLUORESCENT ANTIBODY TECHNIQUE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; KINETICS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; MUTATION; PROTEIN TRANSPORT; THIAZOLIDINES;

CANDIDA ALBICANS; FUNGI;

EID: 35348813868     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00188-07     Document Type: Article

References (79)

1. Akashi, T., T. Kanbe, and K. Tanaka. 1994. The role of the cytoskeleton in the polarized growth of the germ tube in Candida albicans. Microbiology 140:271-280.
2. Anderson, J. M., and D. R. Soll. 1986. Differences in actin localization during bud and hypha formation in the yeast Candida albicans. J. Gen. Microbiol. 132:2035-2047.
3. Argimon, S., J. A. Wishart, R. Leng, S. Macaskill, A. Mavor, T. Alexandris, S. Nicholls, A. W. Knight, B. Enjalbert, R. Walmsley, F. C. Odds, N. A. Gow, and A. J. Brown. 2007. Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans. Eukaryot. Cell 6:682-692.
4. Arnaud, M. B., M. C. Costanzo, M. S. Skrzypek, G. Binkley, C. Lane, S. R. Miyasato, and G. Sherlock. 2005. The Candida Genome Database (CGD), a community resource for Candida albicans gene and protein information. Nucleic Acids Res. 33:D358-D363.
5. Ayscough, K. R. 2000. Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton. Curr. Biol. 10:1587-1590.
6. Bahn, Y. S., J. Staab, and P. Sundstrom. 2003. Increased high-affinity phosphodiesterase PDE2 gene expression in germ tubes counteracts CAP1-dependent synthesis of cyclic AMP, limits hypha production and promotes virulence of Candida albicans. Mol. Microbiol. 50:391-409.
7. Bahn, Y. S., and P. Sundstrom. 2001. CAP1, an adenylate cyclase-associated protein gene, regulates bud-hypha transitions, filamentous growth, and cyclic AMP levels and is required for virulence of Candida albicans. J. Bacteriol. 183:3211-3223.
8. Baker, C. A., K. Desrosiers, and J. W. Dolan. 2002. Propranolol inhibits hyphal development in Candida albicans. Antimicrob. Agents Chemother. 46:3617-3620.
9. Bershadsky, A. D., and A. H. Futerman. 1994. Disruption of the Golgi apparatus by brefeldin A blocks cell polarization and inhibits directed cell migration. Proc. Natl. Acad. Sci. USA 91:5686-5689.
10. Bubb, M. R., A. M. Senderowicz, E. A. Sausville, K. L. Duncan, and E. D. Korn. 1994. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J. Biol. Chem. 269:14869-14871.
11. Cao, F., S. Lane, P. P. Raniga, Y. Lu, Z. Zhou, K. Ramon, J. Chen, and H. Liu. 2006. The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17:295-307.
12. Crampin, H., K. Finley, M. Gerami-Nejad, H. Court, C. Gale, J. Berman, and P. Sudbery. 2005. Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae. J. Cell Sci. 118:2935-2947.
13. de Oliveira, C. A., and B. Mantovani. 1988. Latrunculin A is a potent inhibitor of phagocytosis by macrophages. Life Sci. 43:1825-1830.
14. Evangelista, M., K. Blundell, M. S. Longtine, C. J. Chow, N. Adames, J. R. Pringle, M. Peter, and C. Boone. 1997. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276:118-122.
15. Evangelista, M., D. Pruyne, D. C. Amberg, C. Boone, and A. Bretscher. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:260-269.
16. Fedor-Chaiken, M., R. J. Deschenes, and J. R. Broach. 1990. SRV2, a gene required for RAS activation of adenylate cyclase in yeast. Cell 61:329-340.
17. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
18. Freed, B. M., N. Lempert, and D. A. Lawrence. 1989. The inhibitory effects of N-ethylmaleimide, colchicine and cytochalasins on human T-cell functions. Int. J. Immonupharmacol. 11:459-465.
19. Gillum, A. M., E. Y. Tsay, and D. R. Kirsch. 1984. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198:179-182.
20. Gourlay, C. W., and K. R. Ayscough. 2005. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J. Cell Sci. 118:2119-2132.
21. Gourlay, C. W., and K. R. Ayscough. 2006. Actin-induced hyperactivation of the Ras signaling pathway leads to apoptosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:6487-6501.
22. Gupta, K., J. Bishop, A. Peck, J. Brown, L. Wilson, and D. Panda. 2004. Antimitotic antifungal compound benomyl inhibits brain microtubule polymerization and dynamics and cancer cell proliferation at mitosis, by binding to a novel site in tubulin. Biochemistry 43:6645-6655.
23. Ha, K. S., and J. H. Exton. 1993. Activation of actin polymerization by phosphatidic acid derived from phosphatidylcholine in IIC9 fibroblasts. J. Cell Biol. 123:1789-1796.
24. Hazan, I., M. Sepulveda-Becerra, and H. Liu. 2002. Hyphal elongation is regulated independently of cell cycle in Candida albicans. Mol. Biol. Cell 13:134-145.
25. Jamsa, E., M. Simonen, and M. Makarow. 1994. Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent. Yeast 10:355-370.
26. Johnson, D. I. 1999. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63:54-105.
27. Kadosh, D., and A. D. Johnson. 2005. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16:2903-2912.
28. Karpova, T. S., J. G. McNally, S. L. Moltz, and J. A. Cooper. 1998. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches. J. Cell Biol. 142:1501-1517.
29. Kim, S., M. J. Wolyniak, J. F. Staab, and P. Sundstrom. 2007. A 368-base-pair cis-acting HWP1 promoter region, HCR, of Candida albicans confers hypha-specific gene regulation and binds architectural transcription factors Nhp6 and Gcf1p. Eukaryot. Cell 6:693-709.
30. Klausner, R. D., J. G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
31. Kumamoto, C. A., and M. D. Vinces. 2005. Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence Cell. Microbiol. 7:1546-1554.
32. Kuo, S. C., and J. O. Lampen. 1975. Action of cytochalasin A, a sulfhydryl-reactive agent, on sugar metabolism and membrane-bound adenosine triphosphatase of yeast. Biochim. Biophys. Acta 389:143-153.
33. Kurzai, O., C. Schmitt, E. Brocker, M. Frosch, and A Kolb-Maurer. 2005. Polymorphism of Candida albicans is a major factor in the interaction with human dendritic cells. Int. J. Med. Microbiol. 295:121-127.
34. Kusner, D. J., J. A. Barton, K. K. Wen, X. Wang, P. A. Rubenstein, and S. S. Iyer. 2002. Regulation of phospholipase D activity by actin. Actin exerts bidirectional modulation of mammalian phospholipase D activity in a polymerization-dependent, isoform-specific manner. J. Biol. Chem. 277:50683-50692.
35. Lagunoff, D. 1976. The reaction of cytochalasin A with sulfhydryl groups. Biochem. Biophys. Res. Commun. 73:727-732.
36. Lamb, N. J., A. Fernandez, M. A. Conti, R. Adelstein, D. B. Glass, W. J. Welch, and J. R. Feramisco. 1988. Regulation of actin microfilament integrity in living nonmuscle cells by the cAMP-dependent protein kinase and the myosin light chain kinase. J. Cell Biol. 106:1955-1971.
37. Land, G. A., W. C. McDonald, R. L. Stjernholm, and T. L. Friedman. 1975. Factors affecting filamentation in Candida albicans: relationship of the uptake and distribution of proline to morphogenesis. Infect. Immun. 11:1014-1023.
38. Lane, S., C. Birse, S. Zhou, R. Matson, and H. Liu. 2001. DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J. Biol. Chem. 276:48988- 48996.
39. Lane, S., S. Zhou, T. Pan, Q. Dai, and H. Liu. 2001. The basic helix-loop-helix transcription factor Cph2 regulates hyphal development in Candida albicans partly via TEC1. Mol. Cell. Biol. 21:6418-6428.
40. Lassing, I., F. Schmitzberger, M. Bjornstedt, A. Holmgren, P. Nordlund, C. E. Schutt, and U. Lindberg. 2007. Molecular and structural basis for redox regulation of beta-actin. J. Mol. Biol. 370:331-348.
41. Li, C. R., Y. M. Wang, X. De Zheng, H. Y. Liang, J. C. Tang, and Y. Wang. 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.
42. Lila, T., and D. G. Drubin. 1997. Evidence for physical and functional interactions among two Saccharomyces cerevisiae SH3 domain proteins, an adenylyl cyclase-associated protein and the actin cytoskeleton. Mol. Biol. Cell 8:367-385.
43. Lippincott-Schwartz, J., L. C. Yuan, J. S. Bonifacino, and R. D. Klausner. 1989. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56:801-813.
44. Liu, H. 2001. Transcriptional control of dimorphism in Candida albicans. Curr. Opin. Microbiol. 4:728-735.
45. Makishima, M., Y. Honma, M. Hozumi, K. Sampi, M. Hattori, and K. Motoyoshi. 1991. Induction of differentiation of human leukemia cells by inhibitors of myosin light chain kinase. FEBS Lett. 287:175-177.
46. Martin, R., A. Walther, and J. Wendland. 2005. Ras1-induced hyphal development in Candida albicans requires the formin Bni1. Eukaryot. Cell 4:1712-1724.
47. Mateus, C., and S. V. Avery. 2000. Destabilized green fluorescent protein for monitoring dynamic changes in yeast gene expression with flow cytometry. Yeast 16:1313-1323.
48. Mattila, P. K., O. Quintero-Monzon, J. Kugler, J. B. Moseley, S. C. Almo, P. Lappalainen, and B. L. Goode. 2004. A high-affinity interaction with ADP-actin monomers underlies the mechanism and in vivo function of Srv2/cyclase-associated protein. Mol. Biol. Cell 15:5158-5171.
49. Menon, V., D. Li, N. Chauhan, R. Rajnarayanan, A. Dubrovska, A. H. West, and R. Calderone. 2006. Functional studies of the Ssk1p response regulator protein of Candida albicans as determined by phenotypic analysis of receiver domain point mutants. Mol. Microbiol. 62:997-1013.
50. Michel, S., S. Ushinsky, B. Klebl, E. Leberer, D. Thomas, M. Whiteway, and J. Morschhäuser. 2002. Generation of conditional lethal Candida albicans mutants by inducible deletion of essential genes. Mol. Microbiol. 46:269-280.
51. Mösch, H. U., T. Kohler, and G. H. Braus. 2001. Different domains of the essential GTPase Cdc42p required for growth and development of Saccharomyces cerevisiae. Mol. Cell. Biol. 21:235-248.
52. Moseley, J. B., and B. L. Goode. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605-645.
53. Murthy, K., and P. Wadsworth. 2005. Myosin-II-dependent localization and dynamics of F-actin during cytokinesis. Curr. Biol. 15:724-731.
54. Nantel, A., D. Dignard, C. Bachewich, D. Harcus, A. Marcil, A. P. Bouin, C. W. Sensen, H. Hogues, M. van het Hoog, P. Gordon, T. Rigby, F. Benoit, D. C. Tessier, D. Y. Thomas, and M. Whiteway. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13:3452-3465.
55. Nicotra, A., and G. Schatten. 1990. Propranolol, a beta-adrenergic receptor blocker, affects microfilament organization, but not microtubules, during the first division in sea urchin eggs. Cell Motil. Cytoskel. 16:182-189.
56. Nobile, C. J., and A. P. Mitchell. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15:1150-1155.
57. Oberholzer, U., A. Marcil, E. Leberer, D. Y. Thomas, and M. Whiteway. 2002. Myosin I is required for hypha formation in Candida albicans. Eukaryot. Cell 1:213-238.
58. Oberholzer, U., A. Nantel, J. Berman, and M. Whiteway. 2006. Transcript profiles of Candida albicans cortical actin patch mutants reflect their cellular defects: contribution of the Hog1p and Mkc1p signaling pathways. Eukaryot. Cell 5:1252-1265.
59. Ostrander, D. B., and J. A. Gorman. 1997. Isolation and characterization of the Candida albicans PFY1 gene for profilin. Yeast 13:871-880.
60. Pearson, C. L., K. Xu, K. E. Sharpless, and S. D. Harris. 2004. MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans. Mol. Biol. Cell 15:3658-3672.
61. Phillips, A. J., J. D. Crowe, and M. Ramsdale. 2006. Ras pathway signaling accelerates programmed cell death in the pathogenic fungus Candida albicans. Proc. Natl. Acad. Sci. USA 103:726-731.
62. Phillips, A. J., I. Sudbery, and M. Ramsdale. 2003. Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc. Natl. Acad. Sci. USA 100:14327-14332.
63. Reuß, O., A. Vik, R. Kolter, and J. Morschhäuser. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119-127.
64. Richard, M. L., C. J. Nobile, V. M. Bruno, and A. P. Mitchell. 2005. Candida albicans biofilm-defective mutants. Eukaryot. Cell 4:1493-1502.
65. Rida, P. C., A. Nishikawa, G. Y. Won, and N. Dean. 2006. Yeast-to-hyphal transition triggers formin-dependent Golgi localization to the growing tip in Candida albicans. Mol. Biol. Cell 17:4364-4378.
66. Sanz, M., L. Carrano, C. Jimenez, G. Candiani, J. A. Trilla, A. Duran, and C. Roncero. 2005. Candida albicans strains deficient in CHS7, a key regulator of chitin synthase III, exhibit morphogenetic alterations and attenuated virulence. Microbiology 151:2623-2636.
67. Schröter, C., U. C. Hipler, A. Wilmer, W. Kunkel, and U. Wollina. 2000. Generation of reactive oxygen species by Candida albicans in relation to morphogenesis. Arch. Dermatol. Res. 292:260-264.
68. Scott, V. R., R. Boehme, and T. R. Matthews. 1988. New class of antifungal agents: jasplakinolide, a cyclodepsipeptide from the marine sponge, Jaspis species. Antimicrob. Agents Chemother. 32:1154-1157.
69. Sharkey, L. L., M. D. McNemar, S. M. Saporito-Irwin, P. S. Sypherd, and W. A. Fonzi. 1999. HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J. Bacteriol. 181:5273-5279.
70. Shen, J., W. Guo, and J. R. Köhler. 2005. CaNAT1, a heterologous dominant selectable marker for transformation of Candida albicans and other pathogenic Candida species. Infect. Immun. 73:1239-1242.
71. Snide, J. L., and P. Sundstrom. 2006. A characterization of HWP1 promoter activation in pseudohyphal cells in Candida albicans, abstr. C192, p. 103. Abstr. 8th Candida Candidiasis, Denver, CO. American Society for Microbiology, Washington, DC.
72. Staab, J. F., Y. S. Bahn, and P. Sundstrom. 2003. Integrative, multifunctional plasmids for hypha-specific or constitutive expression of green fluorescent protein in Candida albicans. Microbiology 149:2977-2986.
73. Staab, J. F., Y. S. Bahn, C. H. Tai, P. F. Cook, and P. Sundstrom. 2004. Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification. J. Biol. Chem. 279:40737-40747.
74. Staab, J. F., C. A. Ferrer, and P. Sundstrom. 1996. Developmental expression of a tandemly repeated, proline- and glutamine-rich amino acid motif on hyphal surfaces on Candida albicans. J. Biol. Chem. 271:6298-6305.
75. Sundstrom, P. M., and G. E. Kenny. 1984. Characterization of antigens specific to the surface of germ tubes of Candida albicans by immunofluorescence. Infect. Immun. 43:850-855.
76. Svitkina, T. M., E. A. Bulanova, O. Y. Chaga, D. M. Vignjevic, S. Kojima, J. M. Vasiliev, and G. G. Borisy. 2003. Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160:409-421.
77. Ushinsky, S. C., D. Harcus, J. Ash, D. Dignard, A. Marcil, J. Morchhäuser, D. Y. Thomas, M. Whiteway, and E. Leberer. 2002. CDC42 is required for polarized growth in the human pathogen Candida albicans. Eukaryot. Cell 1:95-104.
78. vandenBerg, A. L., A. S. Ibrahim, J. E. Edwards, Jr., K. A. Toenjes, and D. I. Johnson. 2004. Cdc42p GTPase regulates the budded-to-hyphal-form transition and expression of hypha-specific transcripts in Candida albicans. Eukaryot. Cell 3:724-734.
79. Whiteway, M. 2000. Transcriptional control of cell type and morphogenesis in Candida albicans. Curr. Opin. Microbiol. 3:582-588.