Identification of a Zds-like gene ZDS3 as a new mediator of stress resistance, capsule formation and virulence of the human pathogenic yeast Cryptococcus neoformans

FEMS Yeast Research

Volumn 11, Issue 7, 2011, Pages 529-539

  Li, Zhongming ^a   Sun, Zhixiong ^a   Li, Dong ^a   Pan, Jiao ^a   Zhu, Xudong ^a  

^a NANKAI UNIVERSITY   (China)

Author keywords

Capsule; Cryptococcus neoformans; Virulence factor; Zds

Indexed keywords

AGAR; GLUCOSE; HYDROGEN PEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL INVASION; CELL WALL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; FEMALE; GENE; GENE DISRUPTION; HIGH TEMPERATURE; MOUSE; NONHUMAN; OSMOTIC PRESSURE; VIRULENCE; ZDS3 GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; GLUCOSE; HYDROGEN PEROXIDE; MICE; MICE, INBRED BALB C; OSMOTIC PRESSURE; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; TEMPERATURE; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; MAMMALIA;

EID: 80053964368     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2011.00744.x     Document Type: Article

References (46)

1. Alspaugh JA, Pukkila-Worley R, Harashima Tet al. (2002) Adenylyl cyclase functions downstream of the G-alpha protein GPA1 and controls mating and pathogenicity. Eukaryot Cell1: 75-84.
2. Bahn YS, Kojima K, Cox GM & Heitman J (2005) Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol Biol Cell16: 2285-2300.
3. Banks IR, Specht CA, Donlin MJ, Gerik KJ, Levitz SM & Lodge JK (2005) A chitin synthase and its regulator protein are critical for chitosan production and growth of the fungal pathogen Cryptococcus neoformans. Eukaryot Cell4: 1902-1912.
4. Bose I, Reese AJ, Ory JJ, Janbon G & Doering TL (2003) A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryot Cell 2: 655-663.
5. Chang YC & Kwon-Chung KJ (1998) Isolation of the third capsule-associated gene, CAP60, required for virulence in Cryptococcusneoformans. Infect Immun66: 2230-2236.
6. Chun CD & Madhani HD (2010) Ctr2 links copper homeostasis to polysaccharide capsule formation and phagocytosis inhibition in the human fungal pathogen Cryptococcus neoformans. PLoS One5: e12503.
7. Cox GM, Harrison TS, McDade HCet al. (2003) Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun71: 173-180.
8. Doering TL (2007) Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol63: 1385-1398.
9. Doering TL (2009) How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans. Annu Rev Microbiol63: 223-247.
10. Estruch F, Hodge CA, Rodríguez-Navarro S & Cole CN (2005) Physical and genetic interactions link the yeast protein Zds1p with mRNA nuclear export. J Biol Chem280: 9691-9697.
11. Fuchs BB, Tegos GP, Hamblin MR & Mylonakis E (2007) Susceptibility of Cryptococcus neoformans to photodynamic inactivation is associated with cell wall integrity. Antimicrob Agents Ch51: 2929-2936.
12. Gates-Hollingsworth MA & Kozel TR (2009) Phenotypic heterogeneity in expression of epitopes in the Cryptococcus neoformans capsule. Mol Microbiol74: 126-138.
13. Gerik KJ, Bhimireddy SR, Ryerse JS, Specht CA & Lodge JK (2008) PKC1 is essential for protection against both oxidative and nitrosative stresses, cell integrity, and normal manifestation of virulence factors in the pathogenic fungus Cryptococcus neoformans. Eukaryot Cell7: 1685-1698.
14. Giles SS, Batinic-Haberle I, Perfect JR & Cox GM (2005) Cryptococcus neoformans mitochondrial superoxide dismutase: an essential link between antioxidant function and high-temperature growth. Eukaryot Cell 4: 46-54.
15. Griffioen G, Branduardi P, Ballarini Aet al. (2001) Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol Cell Biol21: 511-523.
16. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR & Casadevall A (eds) (2010) Cryptococcus: From Human Pathogen to Model Yeast. American Society for Microbiology, Washington, DC.
17. Idnurm A, Bahn YS, Nielsen K, Lin X, Fraser JA & Heitman J (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol3: 753-764.
18. Ingavale SS, Chang YC, Lee H, McClelland CM, Leong ML & Kwon-Chung KJ (2008) Importance of mitochondria in survival of Cryptococcusneoformans under low oxygen conditions and tolerance to cobalt chloride. PLoS Pathog4: e1000155.
19. Janbon G (2004) Cryptococcusneoformans capsule biosynthesis and regulation. FEMS Yeast Res4: 765-771.
20. Jiang N, Xiao D, Zhang D, Sun N, Yan B & Zhu X (2009) Negative roles of a novel nitrogen metabolite repression-related gene, TAR1, in laccase production and nitrate utilization by the basidiomycete Cryptococcusneoformans. Appl Environ Microb75: 6777-6782.
21. Kozubowski L, Lee SC & Heitman J (2009) Signaling pathways in the pathogenesis of Cryptococcus. Cell Microbiol11: 370-380.
22. Klutts JS & Doering TL (2008) Cryptococcal xylosyltransferase 1 (Cxt1p) from Cryptococcus neoformans plays a direct role in the synthesis of capsule polysaccharides. J Biol Chem.283: 14327-14334.
23. Kwon-Chung KJ, Edman JC & Wickes BL (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun60: 602-605.
24. Lin X, Jackson JC, Feretzaki M, Xue C & Heitman J (2010) Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and same-sex mating in Cryptococcus neoformans. PLoS Genet6: e1000953.
25. Missall TA, Pusateri ME & Lodge JK (2004) Thiol peroxidase is critical for virulence and resistance to nitric oxide and peroxide in the fungal pathogen, Cryptococcusneoformans. Mol Microbiol51: 1447-1458.
26. Mizunuma M, Hirata D, Miyahara K, Tsuchiya E & Miyakawa T (1998) Role of calcineurin and Mpk1 in regulating the onset of mitosis in budding yeast. Nature392: 303-306.
27. Nichols CB, Perfect ZH & Alspaugh JA (2007) A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcusneoformans. Mol Microbiol63: 1118-1130.
28. Panepinto J, Komperda K, Frases Set al. (2009) Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcusneoformans. Mol Microbiol71: 1165-1176.
29. Pukkila-Worley R, Gerrald QD, Kraus PRet al. (2005) Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcusneoformans cyclic AMP cascade. Eukaryot Cell4: 190-201.
30. Queralt E & Uhlmann F (2008) Separase cooperates with Zds1 and Zds2 to activate Cdc14 phosphatase in early anaphase. J Cell Biol182: 873-883.
31. Reese AJ, Yoneda A, Breger JAet al. (1999) The ZDS1 and ZDS2 proteins require the Sir3p component of yeast silent chromatin to enhance the stability of short linear centromeric plasmids. Chromosoma108: 146-161.
32. Roy N & Runge KW (2000) Two paralogs involved in transcriptional silencing that antagonistically control yeast life span. Curr Biol10: 111-114.
33. Rutherford JC, Lin X, Nielsen K & Heitman J (2008) Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcusneoformans. Eukaryot Cell7: 237-246.
34. Salas SD, Bennett JE, Kwon-Chung KJ, Perfect JR & Williamson PR (1996) Effect of the laccase gene LAC1 on virulence of Cryptococcus neoformans. J Exp Med184: 377-386.
35. Schwer B & Shuman S (1996) Multicopy suppressors of temperature-sensitive mutations of yeast mRNA capping enzyme. Gene Expression5: 331-344.
36. Sekiya-Kawasaki M, Abe M, Saka Aet al. (2002) Dissection of upstream regulatory components of the Rho1p effector, 1, 3-beta-glucan synthase, in Saccharomycescerevisiae. Genetics162: 663-676.
37. Walton FJ, Idnurm A & Heitman J (2005) Novel gene functions required for melanization of the human pathogen Cryptococcusneoformans. Mol Microbiol57: 1381-1396.
38. Wicky S, Tjandra H, Schieltz D, Yates JIII & Kellogg DR (2011) The Zds proteins control entry into mitosis and target protein phosphatase 2A to the Cdc25 phosphatase. Mol Biol Cell22: 20-32.
39. Williamson PR (1994) Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 176: 656-664.
40. Yakura M, Ozoe F, Ishida Het al. (2006) zds1, a novel gene encoding an ortholog of Zds1 and Zds2, controls sexual differentiation, cell wall integrity and cell morphology in fission yeast. Genetics172: 811-825.
41. Yang J, Li D, Liu X, Pan J, Yan B & Zhu X (2010) Regulation of virulence factors, carbon utilization and virulence by SNF1 in Cryptococcus neoformans JEC21 and divergent actions of SNF1 between cryptococcal strains. Fungal Genet Biol.47: 994-1000.
42. Yasutis K, Vignali M, Ryder Met al. (2010) Zds2p regulates Swe1p-dependent polarized cell growth in Saccharomycescerevisiae via a novel Cdc55p interaction domain. Mol Biol Cell21: 4373-4386.
43. Yu Y, Jiang YW, Wellinger RJ, Carlson K, Roberts JM & Stillman DJ (1996) Mutations in the homologous ZDS1 and ZDS2 genes affect cell cycle progression. Mol Cell Biol16: 5254-5263.
44. Zaragoza O, Rodrigues ML, De Jesus M, Frases S, Dadachova E & Casadevall A (2009) The capsule of the fungal pathogen Cryptococcusneoformans. Adv Appl Microbiol68: 133-216.
45. Zhu X & Williamson PR (2003) A CLC-type chloride channel gene is required for laccase activity and virulence in Cryptococcus neoformans. Mol Microbiol50: 1271-1281.
46. Zhu X & Williamson PR (2004) Role of laccase in the biology and virulence of Cryptococcusneoformans. FEMS Yeast Res5: 1-10.