Deletion of the CAP10 gene of Cryptococcus neoformans results in a pleiotropic phenotype with changes in expression of virulence factors

Research in Microbiology

Volumn 165, Issue 6, 2014, Pages 399-410

  Tefsen, Boris ^a,c   Grijpstra, Jan ^b,d   Ordonez, Soledad ^a,b   Lammers, Menno ^b   van Die, Irma ^a   De Cock, Hans ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c INSTITUTE OF MICROBIOLOGY   (China)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acid phosphatase; Capsule; Cryptococcus; Laccase; Polysaccharide; Virulence

Indexed keywords

POLYSACCHARIDE; TRANSCRIPTOME; VIRULENCE FACTOR; CAP10 PROTEIN, CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEIN;

ARTICLE; BIOGENESIS; CAP10 GENE; CELL MATURATION; CELL MUTANT; CELL SIZE; CELL SURFACE; CELL WALL; CRYPTOCOCCUS NEOFORMANS; DENDRITIC CELL; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; UNINDEXED SEQUENCE; WILD TYPE; BIOSYNTHESIS; CYTOLOGY; EXOSOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ULTRASTRUCTURE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

CRYPTOCOCCUS NEOFORMANS; EXOSOMES; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENETIC PLEIOTROPY; PHENOTYPE; VIRULENCE FACTORS;

EID: 84904762012     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2014.04.001     Document Type: Article

References (43)

1. Acar M., Jafar-Nejad H., Takeuchi H., Rajan A., Ibrani D., Rana N.A., et al. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 2008, 132:247-258.
2. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
3. Casadevall A., Rosas A.L., Nosanchuk J.D. Melanin and virulence in Cryptococcus neoformans. Curr Opin Microbiol 2000, 3:354-358.
4. Castle S.A., Owuor E.A., Thompson S.H., Garnsey M.R., Klutts J.S., Doering T.L., et al. Beta1,2-xylosyltransferase Cxt1p is solely responsible for xylose incorporation into Cryptococcus neoformans glycosphingolipids. Eukaryot Cell 2008, 7:1611-1615.
5. Chang Y.C., Kwon-Chung K.J. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 1994, 14:4912-4919.
6. Chang Y.C., Kwon-Chung K.J. Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J Bacteriol 1999, 181:5636-5643.
7. Chen L.C., Pirofski L.A., Casadevall A. Extracellular proteins of Cryptococcus neoformans and host antibody response. Infect Immun 1997, 65:2599-2605.
8. Cherniak R., Reiss E., Turner S.H. A galactoxylomannan antigen of Cryptococcus neoformans serotype A. Carbohydr Res 1982, 103:239-250.
9. Collopy-Junior I., Esteves F.F., Nimrichter L., Rodrigues M.L., Alviano C.S., Meyer-Fernandes J.R. An ectophosphatase activity in Cryptococcus neoformans. FEMS Yeast Res 2006, 6:1010-1017.
10. De Jesus M., Chow S.K., Cordero R.J., Frases S., Casadevall A. Galactoxylomannans from Cryptococcus neoformans varieties neoformans and grubii are structurally and antigenically variable. Eukaryot Cell 2010, 9:1018-1028.
11. de Vries R.P., van de Vondervoort P.J., Hendriks L., van de Belt M., Visser J. Regulation of the alpha-glucuronidase-encoding gene (aguA) from Aspergillus niger. Mol Genet Genomics 2002, 268:96-102.
12. Doering T.L. How does Cryptococcus get its coat?. Trends Microbiol 2000, 8:547-553.
13. Eisenman H.C., Chow S.K., Tse K.K., McClelland E.E., Casadevall A. The effect of L-DOPA on Cryptococcus neoformans growth and gene expression. Virulence 2011, 2:329-336.
14. Foster A.J. FITC-lectin avidity of Cryptococcus neoformans cell wall and capsular components. Mycologia 2004, 8.
15. Foster A.J., Bird R.A., Kelly S.L., Nishimura K., Poyner D., Taylor S., et al. FITC-lectin avidity of Cryptococcus neoformans cell wall and capsular components. Mycologia 2004, 96:1-8.
16. Franzot S.P., Salkin I.F., Casadevall A. Cryptococcus neoformans var. grubii: separate varietal status for Cryptococcus neoformans serotype A isolates. J Clin Microbiol 1999, 37:838-840.
17. Grijpstra J., Gerwig G.J., Wosten H., Kamerling J.P., de Cock H. Production of extracellular polysaccharides by CAP mutants of Cryptococcus neoformans. Eukaryot Cell 2009, 8:1165-1173.
18. Grijpstra J., Tefsen B., van Die I., de Cock H. The Cryptococcus neoformans cap10 and cap59 mutant strains, affected in glucuronoxylomannan synthesis, differentially activate human dendritic cells. FEMS Immunol Med Microbiol 2009, 57(2):142-150.
19. Harris J., Lockhart S., Chiller T. Cryptococcus gattii: where do we go from here?. Med Mycol 2012, 50:113-129.
20. Heiss C., Klutts J.S., Wang Z., Doering T.L., Azadi P. The structure of Cryptococcus neoformans galactoxylomannan contains beta-D-glucuronic acid. Carbohydr Res 2009, 344:915-920.
21. Klutts J.S., Levery S.B., Doering T.L. A beta-1,2-xylosyltransferase from Cryptococcus neoformans defines a new family of glycosyltransferases. J Biol Chem 2007, 282:17890-17899.
22. Levitz S.M. The ecology of Cryptococcus neoformans and the epidemiology of cryptococcosis. Rev Infect Dis 1991, 13:1163-1169.
23. Liu L., Tewari R.P., Williamson P.R. Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect Immun 1999, 67:6034-6039.
24. Missall T.A., Moran J.M., Corbett J.A., Lodge J.K. Distinct stress responses of two functional laccases in Cryptococcus neoformans are revealed in the absence of the thiol-specific antioxidant Tsa1. Eukaryot Cell 2005, 4:202-208.
25. Moyrand F., Fontaine T., Janbon G. Systematic capsule gene disruption reveals the central role of galactose metabolism on Cryptococcus neoformans virulence. Mol Microbiol 2007, 64:771-781.
26. Moyrand F., Janbon G. UGD1, encoding the Cryptococcus neoformans UDP-glucose dehydrogenase, is essential for growth at 37 degrees C and for capsule biosynthesis. Eukaryot Cell 2004, 3:1601-1608.
27. Murphy J.W. Immunological down-regulation of host defenses in fungal infections. Mycoses 1999, 42(Suppl. 2):37-43.
28. Nakamura Y., Kano R., Watanabe S., Hasegawa A. Molecular analysis of CAP59 gene sequences from five serotypes of Cryptococcus neoformans. J Clin Microbiol 2000, 38:992-995.
29. Noverr M.C., Williamson P.R., Fajardo R.S., Huffnagle G.B. CNLAC1 is required for extrapulmonary dissemination of Cryptococcus neoformans but not pulmonary persistence. Infect Immun 2004, 72:1693-1699.
30. Panepinto J.C., Komperda K.W., Hacham M., Shin S., Liu X., Williamson P.R. Binding of serum mannan binding lectin to a cell integrity-defective Cryptococcus neoformans ccr4Delta mutant. Infect Immun 2007, 75:4769-4779.
31. Perfect J.R., Wong B., Chang Y.C., Kwon-Chung K.J., Williamson P.R. Cryptococcus neoformans: virulence and host defences. Med Mycol 1998, 36(Suppl. 1):79-86.
32. Rodrigues M.L., Nakayasu E.S., Oliveira D.L., Nimrichter L., Nosanchuk J.D., Almeida I.C., et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 2008, 7:58-67.
33. Rodrigues M.L., Nimrichter L., Oliveira D.L., Frases S., Miranda K., Zaragoza O., et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 2007, 6:48-59.
34. Rodrigues M.L., Nimrichter L., Oliveira D.L., Nosanchuk J.D., Casadevall A. Vesicular trans-cell wall transport in fungi: a mechanism for the delivery of virulence-associated macromolecules?. Lipid Insights 2008, 2:27-40.
35. Salas S.D., Bennett J.E., Kwon-Chung K.J., Perfect J.R., Williamson P.R. Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J Exp Med 1996, 184:377-386.
36. Schein J.E., Tangen K.L., Chiu R., Shin H., Lengeler K.B., MacDonald W.K., et al. Physical maps for genome analysis of serotype A and D strains of the fungal pathogen Cryptococcus neoformans. Genome Res 2002, 12:1445-1453.
37. Srinivasan C., Dsouza T.M., Boominathan K., Reddy C.A. Demonstration of laccase in the white rot basidiomycete Phanerochaete chrysosporium BKM-F1767. Appl Environ Microbiol 1995, 61:4274-4277.
38. Takeuchi H., Fernandez-Valdivia R.C., Caswell D.S., Nita-Lazar A., Rana N.A., Garner T.P., et al. Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc Natl Acad Sci U S A 2011, 108:16600-16605.
39. Thompson J.R., Douglas C.M., Li W., Jue C.K., Pramanik B., Yuan X., et al. A glucan synthase FKS1 homolog in Cryptococcus neoformans is single copy and encodes an essential function. J Bacteriol 1999, 181:444-453.
40. Vecchiarelli A., Pietrella D., Lupo P., Bistoni F., McFadden D.C., Casadevall A. The polysaccharide capsule of Cryptococcus neoformans interferes with human dendritic cell maturation and activation. J Leukoc Biol 2003, 74:370-378.
41. Voorhout W.F., Leunissen-Bijvelt J.J., Leunissen J.L., Verkleij A.J. Steric hindrance in immunolabelling. J Microsc 1986, 141:303-310.
42. Williamson P.R. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 1994, 176:656-664.
43. Zhu X., Gibbons J., Garcia-Rivera J., Casadevall A., Williamson P.R. Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 2001, 69:5589-5596.