MNN5 encodes an iron-regulated α-1,2-mannosyltransferase important for protein glycosylation, cell wall integrity, morphogenesis, and virulence in Candida albicans

Eukaryotic Cell

Volumn 5, Issue 2, 2006, Pages 238-247

  Bai, Chen ^a   Xu, Xiao Li ^a   Chan, Fong Yee ^a   Lee, Raymond Teck Ho ^a   Wang, Yue ^a  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALCIAN BLUE; IRON; LACTOFERRIN; MANGANESE; MANNOSYLTRANSFERASE;

ANIMAL; ARTICLE; CANDIDA ALBICANS; CELL WALL; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FUNGAL GENE; FUNGUS HYPHAE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MORPHOGENESIS; MOUSE; PATHOGENICITY; SACCHAROMYCES CEREVISIAE; VIRULENCE;

ALCIAN BLUE; ANIMALS; CANDIDA ALBICANS; CELL WALL; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, FUNGAL; GLYCOSYLATION; HYPHAE; IRON; LACTOFERRIN; MANGANESE; MANNOSYLTRANSFERASES; MICE; MORPHOGENESIS; SACCHAROMYCES CEREVISIAE; VIRULENCE;

CANDIDA ALBICANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 32944479485     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.5.2.238-247.2006     Document Type: Article

References (57)

1. Bai, C., F. Y. Chan, and Y. Wang. 2005. Identification and functional characterization of a novel Candida albicans gene CaMNN5 that suppresses the iron-dependent growth defect of Saccharomyces cerevisiae aft1Δ mutant. Biochem. J. 389:27-35.
2. 2+-ATPase, is required for glycosylation and virulence. J. Biol. Chem. 280:23408-23415.
3. Beck-Sague, C., and W. R. Jarvis. 1993. Secular trends in the epidemiology of nosocomial fungal infections in the United States, 1980-1990. National Nosocomial Infections Surveillance System. J. Infect. Dis. 167:1247-1251.
4. Bockmuhl, D. P., S. Krishnamurthy, M. Gerads, A. Sonneborn, and J. F. Ernst. 2001. Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol. Microbiol. 42:1243-1257.
5. Brock, J. 1995. Lactoferrin: a multifunctional immunoregulatory protein? Immunol. Today 16:417-419.
6. Bullen, J. J. 1981. The significance of iron in infection. Rev. Infect. Dis. 3:1127-1138.
7. Burda, P., and M. Aebi. 1999. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426:239-257.
8. Buurman, E. T., C. Westwater, B. Hube, A. J. Brown, F. C. Odds, and N. A. Gow. 1998. Molecular analysis of CaMntlp, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc. Natl. Acad. Sci. USA 95:7670-7675.
9. Calderone, R. A., and P. C. Braun. 1991. Adherence and receptor relationships of Candida albicans. Microbiol. Rev. 55:1-20.
10. Calderone, R. A. 1993. Recognition between Candida albicans and host cells. Trends Microbiol. 1:55-58.
11. Casanova, M., J. L. Lopez-Ribot, C. Monteagudo, A. Llombart-Bosch, R. Sentandreu, and J. P. Martinez. 1992. Identification of a 58-kilodalton cell surface fibrinogen-binding mannoprotein from Candida albicans. Infect. Immun. 60:4221-4229.
12. Cohen, R. E., L. Ballou, and C. E. Ballou. 1980. Saccharomyces cerevisiae mannoprotein mutants. Isolation of the mnn5 mutant and comparison with the mnn3 strain. J. Biol. Chem. 255:7700-7707.
13. Dean, N. 1999. Asparagine-linked glycosylation in the yeast Golgi. Biochim. Biophys. Acta 1426:309-322.
14. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
15. Frangloni, J. V., and B. G. Neel. 1993. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210:179-187.
16. Gemmill, T. R., and R. B. Trimble. 1999. Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta 1426:227-237.
17. Gillum, A. M., E. Y. Tsay, and D. R. Kirscb. 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.
18. Haselbeck, A., and W. Tanner. 1983. O-glycosylation in Saccharomyces cerevisiae is initiated at the endoplasmic reticulum. FEBS Lett. 158:335-338.
19. Herrero, A. B., D. Uccelletti, C. B. Hirschberg, A. Dominguez, and C. Abeijon. 2002. The Golgi GDPase of the fungal pathogen Candida albicans affects morphogenesis, glycosylation, and cell wall properties. Eukaryot. Cell 1:420-431.
20. Hobson, R. P., C. A. Munro, S. Bates, D. M. MacCallum, J. E. Cutler, S. E. Heinsbroek, G. D. Brown, F. C. Odds, and N. A. Gow. 2004. Loss of cell wall mannosylphosphate in Candida albicans does not influence macrophage recognition. J. Biol. Chem. 279:39628-39635.
21. Hoek, K. S., J. M. Milne, P. A. Grieve, D. A. Dionysius, and R. Smith. 1997. Antibacterial activity in bovine lactoferrin-derived peptides. Antimicrob. Agents Chemother. 41:54-59.
22. Hu, C. J., C. Bai, X. D. Zheng, Y. M. Wang, and Y. Wang. 2002. Characterization and functional analysis of the siderophore-iron transporter CaArn1p in Candida albicans. J. Biol. Chem. 277:30598-30605.
23. Ibrahim, A. S., F. Mirbod, S. G. Filler, Y. Banno, G. T. Cole, Y. Kitajima, J. E. Edwards, Jr., Y. Nozawa, and M. A. Ghannoum. 1995. Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect. Immun. 63:1993-1998.
24. Kaufman, R. J., M. Swaroop, and P. Murtha-Riel. 1994. Depletion of manganese within the secretory pathway inhibits O-linked glycosylation in mammalian cells. Biochemistry 33:9813-9819.
25. Klis, F. M., P. de Groot, and K. Hellingwerf. 2001. Molecular organization of the cell wall of Candida albicans. Med. Mycol. 39(Suppl. 1):1-8.
26. Knauer, R., and L. Lehle. 1999. The oligosaccharyltransferase complex from yeast. Biochim. Biophys. Acta 1426:259-273.
27. Kuipers, M. E., H. G. de Vries, M. C. Eikelboom, D. K. Meijer, and P. J. Swart. 1999. Synergistic fungistatic effects of lactoferrin in combination with antifungal drugs against clinical Candida isolates. Antimicrob. Agents Chemother. 43:2635-2641.
28. Lo, H. J., J. R. Kohler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink. 1997. Nonfilamentous Candida albicans mutants are avirulent. Cell 90:939-949.
29. Lupetti, A., A. Paulusma-Annema, S. Senesi, M. Campa, J. T. Van Dissel, and P. H. Nibbering. 2002. Internal thiols and reactive oxygen species in candidacidal activity exerted by an N-terminal peptide of human lactoferrin. Antimicrob. Agents Chemother. 46:1634-1639.
30. Lussier, M., A. M. Sdicu, and H. Bussey. 1999. The KTR and MNN1 mannosyltransferase families of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1426:323-334.
31. Manas, P., I. Olivero, M. Avalos, and L. M. Hernandez. 1997. Isolation of new nonconditional Saccharomyces cerevisiae mutants defective in asparagine-linked glycosylation. Glycobiology 7:487-497.
32. Munro, C. A., S. Bates, E. T. Buurman, H. B. Hughes, D. M. Maccallum, G. Bertram, A. Atrih, M. A. Ferguson, J. M. Bain, A. Brand, S. Hamilton, C. Westwater, L. M. Thomson, A. J. Brown, F. C. Odds, and N. A. Gow. 2004. Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1,2- mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J. Biol. Chem. 280:1051-1060.
33. Nishikawa, A., J. B. Poster, Y. Jigami, and N. Dean. 2002. Molecular and phenotypic analysis of CaVRG4, encoding an essential Golgi apparatus GDP-mannose transporter. J. Bacteriol. 184:29-42.
34. Odani, T., Y. Shimma, X. H. Wang, and Y. Jigami. 1997. Mannosylphosphate transfer to cell wall mannan is regulated by the transcriptional level of the MNN4 gene in Saccharomyces cerevisiae. FEBS Lett. 420:186-190.
35. Odds, F. C. 1996. Resistance of clinically important yeasts to antifungal agents. Int. J. Antimicrob. Agents 6:145-147.
36. Prill, S. K., B. Klinkert, C. Timpel, C. A. Gale, K. Schroppel, and J. F. Ernst. 2005. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol. Microbiol. 55:546-560.
37. Ramanan, N., and Y. Wang. 2000. A high-affinity iron permease essential for Candida albicans virulence. Science 288:1062-1064.
38. 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.
39. Rouabhia, M., M. Schaller, C. Corbucci, A. Vecchiarelli, S. K. Prill, L. Giasson, and J. F. Ernst. 2005. Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect. Immun. 73:4571-4580.
40. Sanchez, L., M. Calvo, and J. H. Brock. 1992. Biological role of lactoferrin. Arch. Dis. Child. 67:657-661.
41. Sobel, J. D., G. Muller, and H. R. Buckley. 1984. Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect. Immun. 44:576-580.
42. Soll, D. R., C. J. Langtimm, J. McDowell, J. Hicks, and R. Galask. 1987. High-frequency switching in Candida strains isolated from vaginitis patients. J. Clin. Microbiol. 25:1611-1622.
43. Soukka, T., J. Tenovuo, and M. Lenander-Lumikari. 1992. Fungicidal effect of human lactoferrin against Candida albicans. FEMS Microbiol. Lett. 90:223-228.
44. Southard, S. B., C. A. Specht, C. Mishra, J. Chen-Weiner, and P. W. Robbins. 1999. Molecular analysis of the Candida albicans homolog of Saccharomyces cerevisiae MNN9, required for glycosylation of cell wall mannoproteins. J. Bacteriol. 181:7439-7448.
45. Strabl-Bolsinger, S., M. Gentzscb, and W. Tanner. 1999. Protein O-mannosylation. Biochim. Biophys. Acta 1426:297-307.
46. Sundstrom, P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4:461-469.
47. Sundstrom, P. 1999. Adhesins in Candida albicans. Curr. Opin. Microbiol. 2:353-357.
48. Timpel, C., S. Zink, S. Strahl-Bolsinger, K. Schroppel, and J. Ernst. 2000. Morphogenesis, adhesive properties, and antifungal resistance depend on the Pmt6 protein mannosyltransferase in the fungal pathogen Candida albicans. J. Bacteriol. 182:3063-3071.
49. Timpel, C., S. Strahl-Bolsinger, K. Ziegelbauer, and J. F. Ernst. 1998. Multiple functions of Pmt1p-mediated protein O-mannosylation in the fungal pathogen Candida albicans. J. Biol. Chem. 273:20837-20846.
50. 14C-labeled mannolipid with properties of dolichyl mannopyranosyl phosphate. J. Biol. Chem. 249:6372-6381.
51. Tomita, M., H. Wakabayashi, K. Yamauchi, S. Teraguchi, and H. Hayasawa. 2002. Bovine lactoferrin and lactoferricin derived from milk: production and applications. Biochem. Cell Biol. 80:109-112.
52. Vorland, L. H. 1999. Lactoferrin: a multifunctional glycoprotein. APMIS 107:971-981.
53. Wakabayashi, H., S. Abe, T. Okutomi, S. Tansho, K. Kawase, and H. Yamaguchi. 1996. Cooperative anti-Candida effects of lactoferrin or its peptides in combination with azole antifungal agents. Microbiol. Immunol. 40:821-825.
54. Wang, Y., S. P. Li, S. A. Moser, K. L. Best, and J. E. Domer. 1998. Cytokine involvement in immunomodulatory activity affected by Candida albicans mannan. Infect. Immun. 66:1384-1391.
55. Warit, S., N. Zhang, A. Short, R. M. Walmsley, S. G. Oliver, and L. I. Stateva. 2000. Glycosylation deficiency phenotypes resulting from depletion of GDP-mannose pyrophosphorylase in two yeast species. Mol. Microbiol. 36:1156-1166.
56. Wiggins, C. A., and S. Munro. 1998. Activity of the yeast MNN1 alpha-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl. Acad. Sci. USA 95:7945-7950.
57. Zheng, X., Y. Wang, and Y. Wang. 2004. Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 23:1845-1856.