Characterization of the recombinant Candida albicans β-1,2- mannosyltransferase that initiates the β-mannosylation of cell wall phosphopeptidomannan

Biochemical Journal

Volumn 457, Issue 2, 2014, Pages 347-360

  Fabre, Emeline ^a   Sfihi Loualia, Ghenima ^a   Pourcelot, Marilyne ^b   Coddeville, Bernadette ^a   Krzewinski, Frédéric ^a   Bouckaert, Julie ^a   Maes, Emmanuel ^a   Hurtaux, Thomas ^a   Dubois, Romaric ^a   Fradin, Chantal ^c,d   Mallet, Jean Maurice ^b   Poulain, Daniel ^c,d   Delplace, Florence ^a   Guerardel, Yann ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c UNIV LILLE   (France)

^d UNIVERSITÉ DE LILLE   (France)

Author keywords

mannose; Cell wall; Glycosyltransferase; Synthesis; Yeast

Indexed keywords

ALPHA OLIGOMANNOSIDE; AMINO ACID; BETA 1,2 MANNOSYLTRANSFERASE; FUNGAL ENZYME; MANNOSE OLIGOSACCHARIDE; MANNOSYLTRANSFERASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CANDIDA ALBICANS; ENZYME ANALYSIS; ENZYME RELEASE; FUNGAL CELL WALL; FUNGAL STRAIN; METHYLOTROPHIC YEAST; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE;

EID: 84890933063     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131012     Document Type: Article

References (48)

1. Sardi, J. C. O., Scorzoni, L., Bernardi, T., Fusco-Almeida, A. M. and Mendes Giannini, M. J. S. (2013) Candida species: Current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J. Med. Microbiol. 62, 10-24
2. Strahl-Bolsinger, S., Gentzsch, M. and Tanner, W. (1999) Protein O-mannosylation. Biochim. Biophys. Acta 1426, 297-307
3. Dean, N. (1999) Asparagine-linked glycosylation in the yeast Golgi. Biochim. Biophys. Acta 1426, 309-322
4. Shibata, N., Ichikawa, T., Tojo, M., Takahashi, M., Ito, N., Okubo, Y. and Suzuki, S. (1985) Immunochemical study on the mannans of Candida albicans NIH A-207, NIH B-792, and J-1012 strains prepared by fractional precipitation with cetyltrimethylammonium bromide. Arch. Biochem. Biophys. 243, 338-348
5. Kobayashi, H., Shibata, N. and Suzuki, S. (1992) Evidence for oligomannosyl residues containing both -1,2 and -1,2 linkages as a serotype A-specific epitope(s) in mannans of Candida albicans. Infect. Immun. 60, 2106-2109
6. Trinel, P.-A., Maes, E., Zanetta, J.-P., Delplace, F., Coddeville, B., Jouault, T., Strecker, G. and Poulain, D. (2002) Candida albicans phospholipomannan, a new member of the fungal mannose inositol phosphoceramide family. J. Biol. Chem. 277, 37260-37271
7. Fradin, C., Slomianny, M. C., Mille, C., Masset, A., Robert, R., Sendid, B., Ernst, J. F., Michalski, J. C. and Poulain, D. (2008) -1,2 Oligomannose adhesin epitopes are widely distributed over the different families of Candida albicans cell wall mannoproteins and are associated through both N-and O-glycosylation processes. Infect. Immun. 76, 4509-4517
8. Maes, E., Mille, C., Trivelli, X., Janbon, G., Poulain, D. and Gúerardel, Y. (2009) Molecular phenotyping of mannosyltransferases- deficient Candida albicans cells by high-resolution magic angle spinning NMR. J. Biochem. 145, 413-419
9. Dalle, F., Jouault, T., Trinel, P. A., Esnault, J., Mallet, J. M., d'Athis, P., Poulain, D. and Bonnin, A. (2003) -1,2-and -1,2-linked oligomannosides mediate adherence of Candida albicans blastospores to human enterocytes in vitro. Infect. Immun. 71, 7061-7068
10. Jouault, T., Fradin, C., Trinel, P. A. and Poulain, D. (2000) Candida albicans-derived -1,2-linked mannooligosaccharides induce desensitization of macrophages. Infect. Immun. 68, 965-968
11. Jouault, T., El Abed-El Behi, M., Mart́nez-Esparza, M., Breuilh, L., Trinel, P.-A., Chamaillard, M., Trottein, F. and Poulain, D. (2006) Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J. Immunol. 177, 4679-4687
12. Jouault, T., Lepage, G., Bernigaud, A., Trinel, P. A., Fradin, C., Wieruszeski, J. M., Strecker, G. and Poulain, D. (1995) -1,2-Linked oligomannosides from Candida albicans act as signals for tumor necrosis factor production. Infect. Immun. 63, 2378-2381
13. Fradin, C., Poulain, D. and Jouault, T. (2000) -1,2-Linked oligomannosides from Candida albicans bind to a 32-kilodalton macrophage membrane protein homologous to the mammalian lectin galectin-3. Infect. Immun. 68, 4391-4398
14. Han, Y., Kanbe, T., Cherniak, R. and Cutler, J. E. (1997) Biochemical characterization of Candida albicans epitopes that can elicit protective and nonprotective antibodies. Infect. Immun. 65, 4100-4107
15. Dromer, F., Chevalier, R., Sendid, B., Improvisi, L., Jouault, T., Robert, R., Mallet, J. M. and Poulain, D. (2002) Synthetic analogues of -1,2 oligomannosides prevent intestinal colonization by the pathogenic yeast Candida albicans. Antimicrob. Agents Chemother. 46, 3869-3876
16. Xin, H., Dziadek, S., Bundle, D. R. and Cutler, J. E. (2008) Synthetic glycopeptide vaccines combining -mannan and peptide epitopes induce protection against candidiasis. Proc. Natl. Acad. Sci. U.S.A. 105, 13526-13531
17. Xin, H., Cartmell, J., Bailey, J. J., Dziadek, S., Bundle, D. R. and Cutler, J. E. (2012) Self-adjuvanting glycopeptide conjugate vaccine against disseminated candidiasis. PLoS ONE 7, e35106
18. Lussier, M., Sdicu, A. M., Bussereau, F., Jacquet, M. and Bussey, H. (1997) The Ktr1p, Ktr3p, and Kre2p/Mnt1p mannosyltransferases participate in the elaboration of yeast Oand N-linked carbohydrate chains. J. Biol. Chem. 272, 15527-15531
19. Yip, C. L., Welch, S. K., Klebl, F., Gilbert, T., Seidel, P., Grant, F. J., O'Hara, P. J. and MacKay, V. L. (1994) Cloning and analysis of the Saccharomyces cerevisiae MNN9 and MNN1 genes required for complex glycosylation of secreted proteins. Proc. Natl. Acad. Sci. U.S.A. 91, 2723-2727
20. Rayner, J. C. and Munro, S. (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
21. Liu, B., Gong, X., Chang, S., Yang, Y., Song, M., Duan, D., Wang, L., Ma, Q. and Wu, J. (2009) Disruption of the OCH1 and MNN1 genes decrease N-glycosylation on glycoprotein expressed in Kluyveromyces lactis. J. Biotechnol. 143, 95-102
22. Mille, C., Bobrowicz, P., Trinel, P.-A., Li, H., Maes, E., Guerardel, Y., Fradin, C., Mart́nez-Esparza, M., Davidson, R. C., Janbon, G. et al. (2008) Identification of a new family of genes involved in -1,2-mannosylation of glycans in Pichia pastoris and Candida albicans. J. Biol. Chem. 283, 9724-9736
23. Lairson, L. L., Henrissat, B., Davies, G. J. and Withers, S. G. (2008) Glycosyltransferases: Structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
24. Mille, C., Fradin, C., Delplace, F., Trinel, P.-A., Masset, A., François, N., Coddeville, B., Bobrowicz, P., Jouault, T., Guerardel, Y. et al. (2012) Members and of the Candida albicans BMT family encode enzymes acting specifically on -mannosylation of the phospholipomannan cell-wall glycosphingolipid. Glycobiology 22, 1332-1342
25. Faille, C., Wieruszeski, J. M., Michalski, J. C., Poulain, D. and Strecker, G. (1992) Complete 1H-and 13C-resonance assignments for D-mannooligosaccharides of the -D-(12)-linked series released from the phosphopeptidomannan of Candida albicans VW.32 (serotype A). Carbohydr. Res. 236, 17-27
26. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A. and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38, 16424-16431
27. Stewart, T. S., Mendershausen, P. B. and Ballou, C. E. (1968) Preparation of a mannopentaose, mannohexaose, and mannoheptaose from Saccharomyces cerevisiae mannan. Biochemistry 7, 1843-1854
28. Faille, C., Wieruszeski, J. M., Lepage, G., Michalski, J. C., Poulain, D. and Strecker, G. (1991) 1H-NMR spectroscopy of manno-oligosaccharides of the -1,2-linked series released from the phosphopeptidomannan of Candida albicans VW-32 (serotype A). Biochem. Biophys. Res. Commun. 181, 1251-1258
29. Hase, S. (1994) High-performance liquid chromatography of pyridylaminated saccharides. Methods Enzymol. 230, 225-237
30. Pourcelot, M., Cattiaux, L., Sfihi-Loualia, G., Fabre, E., Krzewinski, F., Fradin, C., Poulain, D., Delplace, F., Guerardel, Y. and Mallet, J.-M. (2013) Mantyl tagged oligo (1-2) mannosides as Candida albicans -mannosyltransferases substrates: A comparison between synthetic strategies. RSC Adv. 3, 22560-22571
31. Gomes, A. C., Miranda, I., Silva, R. M., Moura, G. R., Thomas, B., Akoulitchev, A. and Santos, M. A. S. (2007) A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol. 8, R206
32. Yuan, Z. and Teasdale, R. D. (2002) Prediction of Golgi Type II membrane proteins based on their transmembrane domains. Bioinformatics 18, 1109-1115
33. Claros, M. G. and von Heijne, G. (1994) TopPred II: An improved software for membrane protein structure predictions. CABIOS, Comput. Appl. Biosci. 10, 685-686
34. Miyatake, N., Kamo, M., Satake, K., Uchiyama, Y. and Tsugita, A. (1993) Removal of N-terminal formyl groups and deblocking of pyrrolidone carboxylic acid of proteins with anhydrous hydrazine vapor. Eur. J. Biochem. 212, 785-789
35. Shibata, N., Suzuki, A., Kobayashi, H. and Okawa, Y. (2007) Chemical structure of the cell-wall mannan of Candida albicans serotype A and its difference in yeast and hyphal forms. Biochem. J. 404, 365-372
36. Vinogradov, E., Petersen, B. and Bock, K. (1998) Structural analysis of the intact polysaccharide mannan from Saccharomyces cerevisiae yeast using 1H and 13C NMR spectroscopy at 750 MHz. Carbohydr. Res. 307, 177-183
37. Suzuki, A., Takata, Y., Oshie, A., Tezuka, A., Shibata, N., Kobayashi, H., Okawa, Y. and Suzuki, S. (1995) Detection of -1,2-mannosyltransferase in Candida albicans cells. FEBS Lett. 373, 275-279
38. Shibata, N., Kobayashi, H. and Suzuki, S. (2012) Immunochemistry of pathogenic yeast, Candida species, focusing on mannan. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 88, 250-265
39. Kobayashi, H., Shibata, N., Nakada, M., Chaki, S., Mizugami, K., Ohkubo, Y. and Suzuki, S. (1990) Structural study of cell wall phosphomannan of Candida albicans NIH B-792 (serotype B) strain, with special reference to 1H and 13C NMR analyses of acid-labile oligomannosyl residues. Arch. Biochem. Biophys. 278, 195-204
40. Miyakawa, Y., Kuribayashi, T., Kagaya, K., Suzuki, M., Nakase, T. and Fukazawa, Y. (1992) Role of specific determinants in mannan of Candida albicans serotype A in adherence to human buccal epithelial cells. Infect. Immun. 60, 2493-2499
41. Han, Y., Morrison, R. P. and Cutler, J. E. (1998) A vaccine and monoclonal antibodies that enhance mouse resistance to Candida albicans vaginal infection. Infect. Immun. 66, 5771-5776
42. Han, Y., Riesselman, M. H. and Cutler, J. E. (2000) Protection against candidiasis by an immunoglobulin G3 (IgG3) monoclonal antibody specific for the same mannotriose as an IgM protective antibody. Infect. Immun. 68, 1649-1654
43. Lee, J.-H., Jang, E.-C. and Han, Y. (2011) Combination immunotherapy of MAb B6.1 with fluconazole augments therapeutic effect to disseminated candidiasis. Arch. Pharm. Res. 34, 399-405
44. Lobsanov, Y. D., Romero, P. A., Sleno, B., Yu, B., Yip, P., Herscovics, A. and Howell, P. L. (2004) Structure of Kre2p/Mnt1p: A yeast 1,2-mannosyltransferase involved in mannoprotein biosynthesis. J. Biol. Chem. 279, 17921-17931
45. Shibata, N., Ikuta, K., Imai, T., Satoh, Y., Satoh, R., Suzuki, A., Kojima, C., Kobayashi, H., Hisamichi, K. and Suzuki, S. (1995) Existence of branched side chains in the cell wall mannan of pathogenic yeast, Candida albicans: Structure-antigenicity relationship between the cell wall mannans of Candida albicans and Candida parapsilosis. J. Biol. Chem. 270, 1113-1122
46. Shibata, N., Akagi, R., Hosoya, T., Kawahara, K., Suzuki, A., Ikuta, K., Kobayashi, H., Hisamichi, K., Okawa, Y. and Suzuki, S. (1996) Existence of novel branched side chains containing -1,2 and -1,6 linkages corresponding to antigenic factor in the mannan of Candida guilliermondii. J. Biol. Chem. 271, 9259-9266
47. Suzuki, A., Shibata, N., Suzuki, M., Saitoh, F., Oyamada, H., Kobayashi, H., Suzuki, S. and Okawa, Y. (1997) Characterization of -1,2-mannosyltransferase in Candida guilliermondii and its utilization in the synthesis of novel oligosaccharides. J. Biol. Chem. 272, 16822-16828
48. Pak, J. E., Arnoux, P., Zhou, S., Sivarajah, P., Satkunarajah, M., Xing, X. and Rini, J. M. (2006) X-ray crystal structure of leukocyte type core 2 1,6-N-acetylglucosaminyltransferase: Evidence for a convergence of metal ion-independent glycosyltransferase mechanism. J. Biol. Chem. 281, 26693-26701