A flucytosine-responsive mbp1/swi4-like protein, mbs1, plays pleiotropic roles in antifungal drug resistance, stress response, and virulence of cryptococcus neoformans

Eukaryotic Cell

Volumn 11, Issue 1, 2012, Pages 53-67

  Song, Min Hee ^a   Lee, Jang Won ^a   Kim, Min Su ^a   Yoon, Ja Kyung ^a   White, Theodore C ^b   Floyd, Anna ^c   Heitman, Joseph ^c   Strain, Anna K ^d   Nielsen, Judith N ^e   Nielsen, Kirsten ^d   Bahn, Yong Sun ^a  

^a Yonsei University   (South Korea)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; ERGOSTEROL; FLUCYTOSINE; FUNGAL PROTEIN; PROTEIN KINASE; TRANSCRIPTION FACTOR; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ANIMAL; ANTIFUNGAL RESISTANCE; ARTICLE; BACTERIAL COUNT; BIOSYNTHESIS; CELL MEMBRANE; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DNA DAMAGE; DNA MICROARRAY; DRUG EFFECT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOGENICITY; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PLEIOTROPY; VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; ANTIFUNGAL AGENTS; CELL MEMBRANE; COLONY COUNT, MICROBIAL; CONSERVED SEQUENCE; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DNA DAMAGE; DRUG RESISTANCE, FUNGAL; ERGOSTEROL; FEMALE; FLUCYTOSINE; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; GENETIC PLEIOTROPY; LUNG; MICE; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN KINASES; TRANSCRIPTION FACTORS; VIRULENCE; VIRULENCE FACTORS;

FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 84855215088     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05236-11     Document Type: Article

References (58)

1. Alspaugh JA, Perfect JR, Heitman J. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein subunit GPA1 and cAMP. Genes Dev. 11:3206-3217.
2. Aramayo R, Peleg Y, Addison R, Metzenberg R. 1996. Asm-1, a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics 144:991-1003.
3. Baddley JW, Pappas PG. 2005. Antifungal combination therapy: clinical potential. Drugs 65:1461-1480.
4. Baginski M, Czub J. 2009. Amphotericin B and its new derivatives- mode of action. Curr. Drug Metab. 10:459-469.
5. Bahn YS, Hicks JK, Giles SS, Cox GM, Heitman J. 2004. Adenylyl cyclase-associated protein AcaI regulates virulence and differentiation of Cryptococcus neoformans via the cyclic AMP-protein kinase A cascade. ukaryot. Cell 3:1476-1491.
6. 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. Cell 16:2285-2300.
7. Bahn YS, Kojima K, Cox GM, Heitman J. 2006. A unique fungal twocomponent system regulates stress responses, drug sensitivity, sexual development, and virulence of Cryptococcus neoformans. Mol. Biol. Cell 17: 3122-3135.
8. Bean JM, Siggia ED, Cross FR. 2005. High functional overlap between MluI cell-cycle box binding factor and Swi4/6 cell-cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171:49-61.
9. Black KE, Baden LR. 2007. Fungal infections of the CNS: treatment strategies for the immunocompromised patient. CNS Drugs 21:293-318.
10. Blackstock R, Buchanan KL, Adesina AM, Murphy JW. 1999. Differential regulation of immune responses by highly and weakly virulent Cryptococcus neoformans isolates. Infect. Immun. 67:3601-3609.
11. Block ER, Jennings AE, Bennett JE. 1973. 5-Fluorocytosine resistance in Cryptococcus neoformans. Antimicrob. Agents Chemother. 3:649-656.
12. Bouquin N, Johnson AL, Morgan BA, Johnston LH. 1999. Association of the cell cycle transcription factor Mbp1 with the Skn7 response regulator in budding yeast. Mol. Biol. Cell 10:3389-3400.
13. Carroll SF, Guillot L, Qureshi ST. 2007. Mammalian model hosts of cryptococcal infection. Comp. Med. 57:9-17.
14. Chang YC, Bien CM, Lee H, Espenshade PJ, Kwon-Chung KJ. 2007. Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans. Mol. Microbiol. 64:614-629.
15. Chen GH, et al. 2008. Inheritance of immune polarization patterns is linked to resistance versus susceptibility to Cryptococcus neoformans in a mouse model. Infect. Immun. 76:2379-2391.
16. Datta K, et al. 2009. Spread of Cryptococcus gattii into Pacific Northwest region of the United States. Emerg. Infect. Dis. 15:1185-1191.
17. Davidson RC, et al. 2002. A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148: 2607-2615.
18. Del Poeta M, Cruz MC, Cardenas ME, Perfect JR, Heitman J. 2000. Synergistic antifungal activities of bafilomycin A(1), fluconazole, and the pneumocandin MK-0991/caspofungin acetate (L-743,873) with calcineurin inhibitors FK506 and L-685,818 against Cryptococcus neoformans. Antimicrob. Agents Chemother. 44:739-746.
19. Dutton JR, Johns S, Miller BL. 1997. StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J. 16:5710-5721.
20. Garcia-Pedrajas MD, Baeza-Montanez L, Gold SE. 2010. Regulation of Ustilago maydis dimorphism, sporulation, and pathogenic development by a transcription factor with a highly conserved APSES domain. Mol. Plant Microbe Interact. 23:211-222.
21. Gimeno CJ, Fink GR. 1994. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol. 14:2100-2112.
22. Granger DL, Perfect JR, Durack DT. 1985. Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. J. Clin. Invest. 76:508-516.
23. Hossack JA, Rose AH. 1976. Fragility of plasma membranes in Saccharomyces cerevisiae enriched with different sterols. J. Bacteriol. 127:67-75.
24. Idnurm A, et al. 2005. Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat. Rev. Microbiol. 3:753-764.
25. Iyer VR, et al. 2001. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409:533-538.
26. Jung KW, Kim SY, Okagaki LH, Nielsen K, Bahn YS. 2011. Ste50 adaptor protein governs sexual differentiation of Cryptococcus neoformans via the pheromone-response MAPK signaling pathway. Fungal Genet. Biol. 48:154-165.
27. Jung WH, Hu G, Kuo W, Kronstad JW. 2009. Role of ferroxidases in iron uptake and virulence of Cryptococcus neoformans. Eukaryot. Cell 8:1511-1520.
28. Kim MS, et al. 2010. Comparative transcriptome analysis of the CO2 sensing pathway via differential expression of carbonic anhydrase in Cryptococcus neoformans. Genetics 185:1207-1219.
29. Ko YJ, et al. 2009. Remodeling of global transcription patterns of Cryptococcus neoformans genes mediated by the stress-activated HOG signaling pathways. Eukaryot. Cell 8:1197-1217.
30. Koc A, Wheeler LJ, Mathews CK, Merrill GF. 2004. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J. Biol. Chem. 279:223-230.
31. Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K. 1993. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261:1551-1557.
32. Kojima K, Bahn YS, Heitman J. 2006. Calcineurin, Mpk1 and Hog1 MAPK pathways independently control fludioxonil antifungal sensitivity in Cryptococcus neoformans. Microbiology 152:591604.
33. Lee JW, Ko YJ, Kim SY, Bahn YS. 2011. Multiple roles of Ypd1 phosphotransfer protein in viability, stress response, and virulence factor regulation in Cryptococcus neoformans. Eukaryot. Cell 10:998-1002.
34. Lin X, Heitman J. 2006. The biology of the Cryptococcus neoformans species complex. Annu. Rev. Microbiol. 60:69-105.
35. CT method. Methods 25: 402-408.
36. Lo HJ, et al. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
37. Lopez-Mirabal HR, Winther JR. 2008. Redox characteristics of the eukaryotic cytosol. Biochim. Biophys. Acta 1783:629-640.
38. Lundin C, et al. 2005. Methyl methanesulfonate (MMS) produces heatlabile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res. 33:3799-3811.
39. Lupetti A, Nibbering PH, Campa M, Del Tacca M, Danesi R. 2003. Molecular targeted treatments for fungal infections: the role of drug combinations. Trends Mol. Med. 9:269-276.
40. Maeng S, et al. 2010. Comparative transcriptome analysis reveals novel roles of the Ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryot. Cell 9:360-378.
41. McLean-Bowen CA, Parks LW. 1982. Effect of altered sterol composition on the osmotic behavior of sphaeroplasts and mitochondria of Saccharomyces cerevisiae. Lipids 17:662-665.
42. Miller KY, Toennis TM, Adams TH, Miller BL. 1991. Isolation and transcriptional characterization of a morphological modifier: the Aspergillus nidulans stunted (stuA) gene. Mol. Gen. Genet. 227:285-292.
43. Miller KY, Wu J, Miller BL. 1992. StuA is required for cell pattern formation in Aspergillus. Genes Dev. 6:1770-1782.
44. Nichols CB, Ferreyra J, Ballou ER, Alspaugh JA. 2009. Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryot. Cell 8:181-189.
45. Okagaki LH, et al. 2010. Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog. 6:e1000953.
46. Park BJ, et al. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
47. Prasad T, et al. 2010. Morphogenic regulator EFG1 affects the drug susceptibilities of pathogenic Candida albicans. FEMS Yeast Res. 10: 587-596.
48. Ramirez-Zavala B, Dominguez A. 2008. Evolution and phylogenetic relationships of APSES proteins from Hemiascomycetes. FEMS Yeast Res. 8:511-519.
49. Segal BH, Steinbach WJ. 2007. Combination antifungals: an update. Expert Rev. Anti Infect. Ther. 5:883-892.
50. Sloan D, Dlamini S, Paul N, Dedicoat M. 2008. Treatment of acute cryptococcal meningitis in HIV infected adults, with an emphasis on resource-limited settings. Cochrane Database Syst. Rev. 4:CD005647.
51. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 16:1982-1991
52. Vermes A, Guchelaar HJ, Dankert J. 2000. Flucytosine: a review of its pharmacology, clinical indications, pharmacokinetics, toxicity and drug interactions. J. Antimicrob. Chemother. 46:171-179.
53. Walsh L, et al. 2002. DNA-damage induction of RAD54 can be regulated independently of the RAD9- and DDC1-dependent checkpoints that regulate RNR2. Curr. Genet. 41:232-240.
54. Ward MP, Gimeno CJ, Fink GR, Garrett S. 1995. SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol. Cell. Biol. 15: 6854-6863.
55. Whelan WL. 1987. The genetic basis of resistance to 5-fluorocytosine in Candida species and Cryptococcus neoformans. Crit. Rev. Microbiol. 15: 45-56.
56. Zaragoza O, et al. 2010. Fungal cell gigantism during mammalian infection. PLoS Pathog. 6:e1000945.
57. Zhang L, Zhang Y, Zhou Y, Zhao Y, Cheng J. 2002. Expression profiling of the response of Saccharomyces cerevisiae to 5-fluorocytosine using a DNA microarray. Int. J. Antimicrob. Agents 20:444-450.
58. Zhang Y, et al. 2009. Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 175:2489-2500.