Molecular analysis of the Candida albicans homolog of Saccharomyces cerevisiae MNN9, required for glycosylation of cell wall mannoproteins

Journal of Bacteriology

Volumn 181, Issue 24, 1999, Pages 7439-7448

  Southard, Susan B ^a,b   Specht, Charles A ^a,b   Mishra, Chitra ^b   Chen Weiner, Joan ^b   Robbins, Phillips W ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HYGROMYCIN B; MANNOSE; VANADATE SODIUM;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCATION; GENE LOSS; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

CANDIDA ALBICANS; SACCHAROMYCES CEREVISIAE;

EID: 0032786422     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.24.7439-7448.1999     Document Type: Article

References (65)

1. Alani, E., L. Cao, and N. Kleckner. 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116:541-545.
2. Ballou, C. E. 1982. Yeast cell wall and cell surface, p. 335-360. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces. Metabolism and gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
3. Ballou, C. E. 1990. Isolation, characterization and properties of Saccharomyces mnn mutants with non-conditional protein glycosylation defects. Methods Enzymol. 185:440-476.
4. Ballou, L., R. E. Cohen, and C. E. Ballou. 1980. Saccharomyces cerevisiae mannoprotein mutants that make mannoproteins with a truncated outer chain. J. Biol. Chem. 255:5986-5991.
5. Ballou, L., R. A. Hitzeman, M. S. Lewis, and C. E. Ballou. 1991. Vanadate-resistant yeast are defective in protein glycosylation. Proc. Natl. Acad. Sci. USA 88:3209-3212.
6. Bulawa, C. E., D. W. Miller, L. K. Henry, and J. W. Becker. 1995. Attenuated virulence of chitin-deficient mutants of Candida albicans. Proc. Natl. Acad. Sci. USA 92:10570-10574.
7. Buurman, E. T., C. Westwater, B. Hube, A. J. Brown, F. C. Odds, and N. A. Gow. 1998. Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc. Natl. Acad. Sci. USA 95:7670-7675.
8. Calderone, R. A., and P. C. Braun. 1991. Adherence and receptor relationships of Candida albicans. Microbiol. Rev. 55:1-20.
9. Calderone, R. A., and M. Fukayama. 1992. Virulence-associated mannoproteins of Candida albicans, p. 524-545. In J. A. Sutcliffe and N. H. Georgeopapadakou (ed.), Emerging targets in antibacterial and antifungal chemotherapy. Chapman and Hall, New York, N.Y.
10. Calderone, R. A. 1994. The recognition of host cells by the pathogenic yeast, Candida albicans. Jpn. J. Med. Mycol. 35:9-18.
11. Castro, C., J. C. Ribas, M. H. Valdivieso, R. Varona, F. Del Rey, and A. Duran. 1995. Papulacandin B resistance in budding and fission yeast: isolation and characterization of a gene involved in (1,3)ß-D-glucan synthesis in Saccharomyces cerevisiae. J. Bacteriol. 177:5732-5739.
12. Chapman, R. E., and S. Munro. 1994. The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANPI, a member of a new family of genes affecting the secretory pathway. EMBO J. 13:4896-4907.
13. Chappell, T., N. Hajibagheri, K. Ayscough, M. Pierce, and G. Warren. 1994. Localization of an α-1,2 galactosyltransferase activity to the Golgi apparatus of Schizosaccharomyces pombe. Mol. Biol. Cell 5:519-528.
14. Cutler, J. E. 1991. Putative virulence factors of Candida albicans. Annu. Rev. Microbiol. 45:187-218.
15. Dean, N. 1995. Yeast glycosylation mutants are sensitive to aminoglycosides. Proc. Natl. Acad. Sci. USA 92:1287-1291.
16. Dean, N., and J. B. Poster. 1996. Molecular and phenotypic analysis of the S. cerevisiae MNN10 gene identifies a family of related glycosyltransferases. Glycobiology 6:73-81.
17. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
18. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
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. Gow, N. A. R., P. W. Robbins, J. W. Lester, A. J. P. Brown, W. A. Fonzi, T. Chapman, and O. Kinsman. 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.
21. Guthrie, C., and G. R. Fink. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:169-182.
22. Hanahan, D. 1988. Techniques for transformation of E. coli, p. 109-135. In D. M. Glover (ed.), DNA cloning. IRL Press, Oxford. United Kingdom.
23. Herscovics, A., and P. Orlean. 1993. Glycoprotein synthesis in yeast. FASEB J. 7:540-548.
24. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells with alkali cations. J. Bacteriol. 153:163-168.
25. Jiang, Y., A. Scarpa, L. Zhang, S. Stone, E. Feliciano, and S. Ferro-Novick. 1998. A high-copy suppressor screen reveals genetic interactions between BET3 and a new gene: evidence for a novel complex in ER-to-Golgi transport. Genetics 49:833-841.
26. Jungmann, J., and S. Munro. 1998. Multi-protein complexes in the cis Golgi of S. cerevisiae with α-1,6 mannosyltransferase activity. EMBO J. 17:423-434.
27. Kanbe, T., Y. Han, B. Redgrave, M. Rieselman, and J. Cutler. 1993. Evidence that mannans of Candida albicans are responsible for adherence of yeast forms to spleen and lymph node tissue. Infect. Immun. 61:2578-2584.
28. Kanik-Ennulat, C., and N. Neff. 1990. Vanadate-resistant mutants of Saccharomyces cerevisiae show alterations in protein phosphorylation and growth control. Mol. Cell. Biol. 10:898-909.
29. Kanik-Ennulat, C., E. Montalvo, and N. Neff. 1995. Sodium orthovanadate-resistant mutants of Saccharomyces cerevisiae show defects in Golgi-mediated protein glycosylation, sporulation and detergent resistance. Genetics 140:933-943.
30. Kapteyn, J. C., R. C. Montijn, E. Vink, J. de la Cruz, H. Shimoi, P. N. Lipke, and F. M. Klis. 1996. Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked β-1,3-/β-1,6-glucan heteropolymer. Glycobiology 6:337-345.
31. Kurtz, M. B., R. Kelly, and D. R. Kirsch. 1990. Molecular biology of Candida albicans, p. 21-74. In D. R. Kirsch, R. Kelly, and M. B. Kurtz (ed.), The genetics of Candida albicans. CRC Press, Inc., Boca Raton, Fla.
32. Kwon-Chung, K. J., D. Lehman, C. Good, and P. T. Magee. 1985 Genetic evidence for role of extracellular proteinase in virulence of Candida albicans. Infect. Immun. 49:571-575.
33. Kwon-Chung, K. J., and J. E. Bennett. 1992. Medical mycology, p. 280-336. Lea and Febiger, Philadelphia, Pa.
34. Lee, K. L., H. R. Buckley, and C. C. Campbell. 1975. An amino acid liquid synthetic medium for development of mycelial and yeast forms of Candida albicans. Sabouraudia 13:148-153.
35. Lussier, M., A. M. White, J. Sheraton, T. diPaolo, J. Treadwell, S. B. Southard, C. I. Horenstein, J. Chen-Weiner, A. R. J. Ram, J. C. Kapteyn, T. Roemer, D. H. Vo, D. C. Bondoc, J. Hall, W. W. Zhong, A. M. Sidcu, J. Davies, F. M. Klis, P. W. Robbins, and H. Bussey. 1997. Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147:435-450.
36. Lussier, M., A. M. Sidcu, S. Shahinian, and H. Bussey. 1998. The Candida albicans KRE9 gene is required for cell wall β-1,6-glucan synthesis and is essential for growth on glucose. Proc. Natl. Acad. Sci. USA 95:9825-9830.
37. Magee, B. B., Y. Koltin, J. A. Gorman, and P. T. Magee. 1988. Assignment of cloned genes to the seven electrophoretically separated Candida albicans chromosomes. Mol. Cell. Biol. 8:4721-4726.
38. McCreath, K. J., C. A. Specht, and P. W. Robbins. 1995. Molecular cloning and characterization of chitinase genes from Candida albicans. Proc. Natl. Acad. Sci. USA 92:2544-2548.
39. McKnight, G. L., T. S. Cardillo, and F. Sherman. 1981. An extensive deletion causing overproduction of yeast iso-2-cytochrome c. Cell 25:409-419.
40. Mio, T., M. Adachi-Shimizu, Y. Tachibana, H. Tabuchi, S. B. Inoue, T. Yabe, T. Yamada-Okabe, M. Arisawa, T. Watanabe, and H. Yamada-Okabe. 1997. Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSCI/ FKS1 and its involvement in β-1,3-glucan synthesis. J. Bacteriol. 179:4096-4105.
41. Mondesert, G., D. J. Clarke, and S. I. Reed. 1997. Identification of genes controlling growth polarity in the budding yeast Saccharomyces cerevisiae: a possible role of N-glycosylation and involvement of the exocyst complex. Genetics 147:421-434.
42. Montijn, R. C., J. van Rinsum, F. A. van Schagen, and F. M. Klis. 1994. Glucomannoproteins in the cell wall of Saccharomyces cerevisiae contain a novel type of carbohydrate side chain. J. Biol. Chem. 269:19338-19342.
43. Nakayama, K., T. Nagusa, Y. Shimma, J. Kuromitu, and Y. Jigami. 1992. OCHI encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagine-linked oligosaccharides. EMBO J. 11:2511-2519.
44. Navarro-Garcia, F., M. Sanchez, J. Pla, and C. Nombela. 1995. Functional characterization of the MKCI gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol. Cell. Biol. 15:2197-2206.
45. Neiman, A. M., V. Mhaiskar, V. Manus, F. Galibert, and N. Dean. 1997. Saccharomyces cerevisiae HOCI, a suppressor of pkc1, encodes a putative glycosyltransferase. Genetics 145:637-645.
46. Nothwehr, S. F., N. J. Bryant, and T. H. Stevens. 1996. The newly identified yeast GRD genes are required for retention of late-Golgi membrane proteins. Mol. Cell. Biol. 16:2700-2707.
47. Odds, F. C. 1994. Candida species and virulence. ASM News 60:313-318.
48. Paravicini, G., A. Mendiza, B. Antonsson, M. Cooper, C. Losberger, and M. Payton. 1996. The Candida albicans PKC1 gene encodes a protein kinase C homolog necessary for cellular integrity, but not for dimorphism. Yeast 12:741-756.
49. Ram, A. F. J., A. Wolters, R. T. Hoopen, and F. M. Klis. 1994. A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to Calcofluor white. Yeast 10:1019-1030.
50. Rayner, J. C., and S. Munro. 1998. Identification of the MNN2 and MNN5 mannosyltransferases required for forming and extending the mannose branches of the outer chain mannans of Saccharomyces cerevisiae. J. Biol. Chem. 273:26836-26843.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
53. Sarthy, A. V., T. McGonigal, M. Coen, D. J. Frost, J. A. Meulbroek, and R. C. Goldman. 1997. Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-β-glucosyltransferase. Microbiology 143:367-376.
54. Sekiya-Kawasaki, M., D. Botstein, and Y. Ohya. 1998. Identification of functional connections between calmodulin and the yeast actin cytoskeleton. Genetics 150:43-48.
55. Sherman, F., G. R. Fink, and J. B. Hicks. 1986. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
56. Sobel, J. D., G. Muller, and H. R. Buckley. 1984. Clinical role of germ-tube formation in the pathogenesis of candidal vaginitis. Infect. Immun. 44:576-580.
57. Soll, D. R., C. J. Langtimm, J. McDowell, J. Hicks, and R. Galask. 1987. High-frequency switching in Candida strains from vaginitis patients. J. Clin. Microbiol. 25:1611-1622.
58. Southard, S. Unpublished data.
59. Thompson, J. R., C. M. Douglas, W. Li, C. K. Jue, B. Premanik, X. Yuan, T. H. Rude, D. L. Tofaletti, J. R. Perfect, and M. Kurtz. 1999. A glucan synthase FKS1 homolog in Cryptococcus neoformans is single copy and encodes an essential function. J. Bacteriol. 181:444-453.
60. Timpel, C., S. Strahl-Bolsinger, S. Ziegelbauer, and J. F. Ernst. 1998. Multiple functions of Pmt1p-mediated O-mannosylation in the fungal pathogen Candida albicans. J. Biol. Chem. 273:20837-20846.
61. Tsai, P. K., P. Frevert, and C. E. Ballou. 1984. Carbohydrate structure of Saccharomyces cerevisiae mnn9 mannoprotein. J. Biol. Chem. 259:3805-3811.
62. van der Vaart, J. M., L. H. P. Caro, J. W. Chapman, F. M. Klis, and C. T. Verrips, 1995. Identification of three mannoproteins in the cell wall of Saccharomyces cerevisiae. J. Bacteriol. 177:3104-3110.
63. Wang, X. H., K. Nakayama, Y. Shimma, A. Tanaka, and Y. Jigami. 1997. MNN6, a member of the KRE2/MNT1 family, is the gene responsible for mannosylphosphate transfer in Saccharomyces cerevisiae. J. Biol. Chem. 272: 18117-18124.
64. Wickes, B. L., J. E. Golin, and K. J. Kwon-Chung. 1991. Chromosomal rearrangement in Candida stellatoidea results in a positive effect on phenotype. Infect. Immun. 59:1762-1771.
65. Yip, C. L., S. K. Welch, F. Klebel, T. Gilbert, P. Seidel, F. J. Grant, P. J. O'Hara, and V. L. MacKay. 1994. Cloning and analysis of the S. cerevisiae MNN9 and MNN1 genes required for complex glycosylation of secreted proteins. Proc. Natl. Acad. Sci. USA 91:2723-2727.