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

Journal of Bacteriology

Volumn 183, Issue 10, 2001, Pages 3211-3223

  Bahn, Yong Sun ^a   Sundstrom, Paula ^a,b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; FUNGUS GROWTH; GENE DISRUPTION; GENE EXPRESSION; MOLECULAR CLONING; MORPHOGENESIS; MOUSE; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; CANDIDA ALBICANS; CANDIDIASIS; CELL CYCLE PROTEINS; CYCLIC AMP; CYTOSKELETAL PROTEINS; DROSOPHILA PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENETIC COMPLEMENTATION TEST; HUMANS; MALE; MICE; MICE, INBRED CBA; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; VIRULENCE;

ANIMALIA; CANDIDA ALBICANS; FUNGI;

EID: 0035033538     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.183.10.3211-3223.2001     Document Type: Article

References (87)

1. Alex, L. A., C. Korch, C. P. Selitrennikoff, and M. I. Simon. 1998. COS1, a two-component histidine kinase that is involved in hyphal development in the opportunistic pathogen Candida albicans. Proc. Natl. Acad. Sci. USA 95:7069-7073.
2. Alspaugh, J. A., J. R. Perfect, and J. Heitman. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev. 11:3206-3217.
3. Anderson, J. M., and D. R. Soll. 1486. Differences in actin localization during hud and hypha formation in the yeast Candida albicans. J. Gen. Microbiol. 132:2035-2047.
4. Barlow, A. J., T. Aldersley, and F. W. Chattaway. 1974. Factors present in scrum and seminal plasma which promote germ-tube formation and mycelial growth of Candida albicans. J. Gen. Microbiol. 82:261-272.
5. Baum, B., W. Li, and N. Perrimon. 2000. A cyclase-associated protein regulates actin and cell polarity during Drosophila oogenesis and in yeast. Curr. Biol. 10:964-973.
6. Birse, C. E., M. Y. Irwin, W. A. Fonzi, and P. S. Sypherd. 1993. Cloning and characterization of ECE1, a gene expressed in association with cell elongation of the dimorphic pathogen Candida albicans. Infect. Immun. 61:3648-3655.
7. Boeke, J. D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
8. Borges-Walmsley, M. I., and A. R. Walmsley. 2000. cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. Trends Microbiol. 8:133-141.
9. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
10. Bruno, K. S., R. Aramayo, P. F. Minke, R. L. Metzenberg, and M. Plamann. 1996. Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J. 15:5772-5782.
11. Calera, J. A., X. J. Zhao, and R. Calderone. 2000. Defective hyphal development and avirulence caused by a deletion of the SSK1 response regulator gene in Candida albicans. Infect. Immun. 68:518-525.
12. Calera, J. A., X. J. Zhao, F. De Bernardis, M. Sheridan, and R. Calderone. 1999. Avirulence of Candida albicans CaHK1 mutants in a murine model of hematogenously disseminated candidiasis. Infect. Immun. 67:4280-4284.
13. Castilla, R., S. Passeron, and M. L. Cantore. 1998. N-acetyl-D-glucosamine induces germination in Candida albicans through a mechanism sensitive to inhibitors of cAMP-dependent protein kinase. Cell. Signal. 10:713-719.
14. Chattaway, F. W., P. R. Wheeler, and J. O'Reilly. 1981. Involvement of adenosine 3′:5′-cyclic monophosphate in the germination of blastospores of Candida albicans. J. Gen. Microbiol. 123:233-240.
15. Chen, J., S. Zhou, Q. Wang, X. Chen, T. Pan, and H. Liu. 2000. Crk1, a novel Cdc2-related protein kinase, is required for hyphal development and virulence in Candida albicans. Mol. Cell. Biol. 20:8696-8708.
16. Cho, T., H. Hamatake, H. Kaminishi, Y. Hagihara, and K. Watanabe. 1992. The relationship between cyclic adenosine 3′,5′-monophosphate and morphology in exponential phase Candida albicans. J. Med. Vet. Mycol. 30:35-42.
17. Csank, C., K. Schröppel, E. Leberer, D. Harcus, O. Mohamed, S. Meloche, D. Y. Thomas, and M. Whiteway. 1998. Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect. Immun. 66:2713-2721.
18. Dabrowa, N., and D. H. Howard. 1981. Proline uptake in Candida albicans. J. Gen. Microbiol. 127:391-397.
19. Egidy, G. A., M. C. Paveto, S. Passeron, and M. Galvagno. 1989. Relationship between cyclic adenosine 3′:5′-monophosphate and germination in Candida albicans. Exp. Mycol. 13:428-432.
20. 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.
21. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
22. Feinberg, A. P., and B. Vogelstein. 1984. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal. Biochem. 137:266-267.
23. Feng, Q., E. Summers, B. Guo, and G. Fink. 1999. Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J. Bacteriol. 181:6339-6346.
24. Field, J., A. Vojtek, R. Ballesler, G. Bolger, J. Colicelli, K. Ferguson, J. Gerst, T. Kataoka, T. Michaeli, S. Powers, et al. 1990. Cloning and characterization of CAP, the S. cerevisiae gene encoding the 70 kd adenylyl cyclase-associated protein. Cell 61:319-327.
25. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
26. Freeman, N. L., Z. Chen, J. Horenstein, A. Weber, and J. Field. 1995. An actin monomer binding activity localizes to the carboxyl-terminal half of the Saccharomyces cerevisiae cyclase-associated protein. J. Biol. Chem. 270: 5680-5685.
27. Freeman, N. L., T. Lila, K. A. Mintzer, Z. Chen, A. J. Pahk, R. Ren, D. G. Drubin, and J. Field. 1996. A conserved proline-rich region of the Saccharomyces cerevisiae cyclase-associated protein binds SH3 domains and modulates cytoskeletal localization. Mol. Cell. Biol. 16:548-556.
28. Gancedo, J. M. 2001. Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25:107-123.
29. Ghannoum, M. A., B. Spellberg, S. M. Saporito-Irwin, and W. A. Fonzi. 1995. Reduced virulence of Candida albicans PHR1 mutants. Infect. Immun. 63: 4528-4530.
30. Gillum, A. M., E. Y. H. 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.
31. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077-1090.
32. Griffioen, G., P. Anghileri, E. Imre, M. D. Baroni, and H. Ruis. 2000. Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae. J. Biol. Chem. 275:1449-1456.
33. Hall, D. D., D. D. Markwardt, F. Parviz, and W. Heideman. 1998. Regulation of the Cln3-Cdc28 kinase by cAMP in Saccharomyces cerevisiae. EMBO J. 17: 4370-4378.
34. Hazen, K. C., and J. E. Cutler. 1979. Autoregulation of germ tube formation by Candida albicans. Infect. Immun. 24:661-666.
35. Kawamukai, M., J. Gerst, J. Field, M. Riggs, L. Rodgers, M. Wigler, and D. Young. 1992. Genetic and biochemical analysis of the adenylyl cyclase-associated protein, cap, in Schizosaccharomyces pombe. Mol. Biol. Cell 3:167-180.
36. Kawarabayashi, T., T. Tsukamoto, T. Kishikawa, and H. Sugimori. 1989. Changes in serum calcium, magnesium, cyclic AMP and monoamine oxidase levels during pregnancy and under prolonged ritodrine treatment for preterm labor. Gynecol. Obstet. Investig. 28:132-137.
37. Kimura, L. H., and N. N. Pearsall. 1978. Adherence of Candida albicans to human buccal epithelial cells. Infect. Immun. 21:64-68.
38. Kinsman, O. S., K. Pitblado, and C. J. Coulson. 1988. Effect of mammalian steroid hormones and luteinizing hormone on the germination of Candida albicans and implications for vaginal candidosis. Mycoses 31:617-626.
39. Köhler, J. R., and G. R. Fink. 1996. Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc. Natl. Acad. Sci. USA 93:13223-13228.
40. Kronstad, J., A. De Maria, D. Funnell, R. D. Laidlaw, N. Lee, M. M. de Sá, and M. Ramesh. 1998. Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch. Microbiol. 170:395-404.
41. Kübler, E., H. U. Mösch, S. Rupp, and M. P. Lisanti. 1997. Gpa2p, a G-protein alpha-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. J. Biol. Chem. 272:20321-20323.
42. Kurtz, M. B., M. W. Cortelyou, and D. R. Kirsch. 1986. Integrative transformation of Candida albicans, using a cloned Candida ADE2 gene. Mol. Cell. Biol. 6:142-149.
43. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
44. Lambrechts, M. G., F. F. Bauer, J. Marmur, and I. S. Pretorius. 1996. Mucl, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc. Natl. Acad. Sci. USA 93:8419-8424.
45. Lee, K. L., H. R. Buckley, and C. C. Campbell. 1975. An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13:148-153.
46. Lengeler, K. B., R. C. Davidson, C. D'Souza, T. Harashima, W. C. Shen, P. Wang, X. Pan, M. Waugh, and J. Heitman. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746-785.
47. 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.
48. Liu, H., J. Köhler, and G. R. Fink. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723-1726. (Erratum, 267:17, 1995.)
49. Lo, H. J., J. R. Köhler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
50. Lo, W. S., and A. M. Dranginis. 1998. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9:161-171.
51. 1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol. Cell. Biol. 19:4019-4027.
52. Lorenz, M. C., and J. Heitman. 1997. Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog. EMBO J. 16:7008-7018.
53. Lorenz, M. C., X. Pan, T. Harashima, M. E. Cardenas, Y. Xue, J. P. Hirsch, and J. Heitman. 2000. The G protein-coupled receptor Gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154:609-622.
54. Makimura, K., S. Y. Murayama, and H. Yamaguchi. 1994. Detection of a wide range of medically important fungi by the polymerase chain reaction. J. Med. Microbiol. 40:358-364.
55. Matviw, H., G. Yu, and D. Young. 1992. Identification of a human cDNA encoding a protein that is structurally and functionally related to the yeast adenylyl cyclase-associated CAP proteins. Mol. Cell. Biol. 12:5033-5040.
56. Mitchell, T. K., and R. A. Dean. 1995. The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7:1869-1878.
57. Mösch, H. U., and G. R. Fink. 1997. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145:671-684.
58. Mösch, H. U., E. Kübler, S. Krappmann, G. R. Fink, and G. H. Braus. 1999. Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol. Biol. Cell 10:1325-1335.
59. Naglik, J. R., G. Newport, T. C. White, L. L. Fernandes-Naglik, J. S. Greenspan, D. Greenspan, S. P. Sweet, S. J. Challacombe, and N. Agabian. 1999. In vivo analysis of secreted aspartyl proteinase expression in human oral candidiasis. Infect. Immun. 67:2482-2490.
60. Navarro-Garcia, F., M. Sanchez, J. Pla, and C. Nombela. 1995. Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol. Cell. Biol. 15:2197-2206.
61. Niimi, M. 1996. Dibutyryl cyclic AMP-enhanced germ tube formation in exponentially growing Candida albicans cells. Fungal Genet. Biol. 20:79-83.
62. Niimi, M., K. Niimi, J. Tokunaga, and H. Nakayama. 1980. Changes in cyclic nucleotide levels and dimorphic transition in Candida albicans. J. Bacteriol. 142:1010-1014.
63. Pan, X., and J. Heitman. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:4874-4887.
64. Paravicini, G., A. Mendoza, B. Antonsson, M. Cooper, C. Losberger, and M. A. Payton. 1996. The Candida albicans PKC1 gene encodes a protein kinase C homolog necessary for cellular integrity hut not dimorphism. Yeast 12:741-756.
65. Postlethwait, P., and P. Sundstrom. 1995. Genetic organization and mRNA expression of enolase genes of Candida albicans. J. Bacteriol. 177:1772-1779.
66. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
67. Rupp, S., E. Summers, H. J. Lo, H. Madhani, and G. Fink. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18:1257-1269.
68. Schaller, M., H. C. Korting, W. Schafer, J. Bastert, W. Chen, and B. Hube. 1999. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol. Microbiol. 34:169-180.
69. Scherer, S., and D. A. Stevens. 1987. Application of DNA typing methods to epidemiology and taxonomy of Candida species. J. Clin. Microbiol. 25:675-679.
70. Schweizer, A., S. Rupp, B. N. Taylor, M. Rollinghoff, and K. Schroppel. 2000. The TEA/ATTS transcription factor CaTeclp regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38:435-445.
71. Shepherd, M. G., C. Y. Yin, S. P. Ram, and P. A. Sullivan. 1980. Germ tube induction in Candida albicans. Can. J. Microbiol. 26:21-26.
72. Shima, F., T. Okada, M. Kido, H. Sen, Y. Tanaka, M. Tamada, C. D. Hu, Y. Yamawaki-Kataoka, K. Kariya, and T. Kataoka. 2000. Association of yeast adenylyl cyclase with cyclase-associated protein CAP forms a second Ras-binding site which mediates its Ras-dependent activation. Mol. Cell. Biol. 20: 25-33.
73. Sobel, J. D., G. Muller, and H. R. Buckley. 1984. Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect. Immon. 44:576-580.
74. Sonneborn, A., D. P. Bockmühl, M. Gerads, K. Kurpanek, D. Sanglard, and J. F. Ernst. 2000. Protein kinase A encoded by TPK2 regulates dimorphism of Candida albicans. Mol. Microbiol. 35:386-396.
75. Staab, J. F., S. D. Bradway, P. L. Fidel, and P. Sundstrom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283:1535-1538.
76. 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.
77. Staib, P., M. Kretschmar, T. Nichterlein, H. Hof, and J. Morschhäuser. 2000. Differential activation of a Candida albicans virulence gene family during infection. Proc. Natl. Acad. Sci. USA 97:6102-6107.
78. Sundstrom, P., and G. R. Aliaga. 1992. Molecular cloning of cDNA and analysis of protein secondary structure of Candida albicans enolase, an abundant, immunodominant glycolytic enzyme. J. Bacteriol. 174:6789-6799.
79. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
80. Toda, T., I. Uno, T. Ishikawa, S. Powers, T. Kataoka, D. Broek, S. Cameron, J. Broach, K. Matsumoto, and M. Wigler. 1985. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27-36.
81. van Zeijl, C. M. J., E. H. M. van de Kamp, P. J. Punt, G. C. M. Selten, B. Hauer, R. F. M. van Gorcom, and C. A. M. J. J. van den Hondel. 1998. An improved colony-PCR method for filamentous fungi for amplification of PCR-fragments of several kilobases. J. Biotechnol. 59:221-224.
82. Vojtek, A. B., and J. A. Cooper. 1993. Identification and characterization of a cDNA encoding mouse CAP: a homolog of the yeast adenylyl cyclase associated protein. J. Cell Sci. 105:777-785.
83. Wright, F. 1990. The 'effective number of codons' used in a gene. Gene 87: 23-29.
84. Yamada-Okabe, T., T. Mio, N. Ono, Y. Kashima, M. Matsui, M. Arisawa, and H. Yamada-Okabe. 1999. Roles of three histidine kinase genes in hyphal development and virulence of the pathogenic fungus Candida albicans. J. Bacteriol. 181:7243-7247.
85. Yu, J., C. Wang, S. J. Palmieri, B. K. Haarer, and J. Field. 1999. A cytoskeletal localizing domain in the cyclase-associated protein, CAP/Srv2p. regulates access to a distant SH3-binding site. J. Biol. Chem. 274:19985-19991.
86. Zelada, A., R. Castilla, S. Passeron, and M. L. Cantore. 1996. Reassessment of the effect of glucagon and nucleotides on Candida atbicans germ tube formation. Cell. Mol. Biol. (Noisy-le-grand) 42:567-576.
87. Zelicof, A., V. Protopopov, D. David, X. Y. Lin, V. Lustgarten, and J. E. Gerst. 1996. Two separate functions are encoded by the carboxyl-terminal domains of the yeast cyclase-associated protein and its mammalian homologs. Dimerization and actin binding. J. Biol. Chem. 271:18243-18252.