Toward an integrated model of capsule regulation in Cryptococcus neoformans

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Haynes, Brian C ^a   Skowyra, Michael L ^a   Spencer, Sarah J ^a   Gish, Stacey R ^a   Williams, Matthew ^a   Held, Elizabeth P ^a   Brent, Michael R ^a   Doering, Tamara L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADA2 PROTEIN; CIR1 PROTEIN; FUNGAL PROTEIN; HISTONE H3; NRG1 PROTEIN; UNCLASSIFIED DRUG; HISTONE ACETYLTRANSFERASE; POLYSACCHARIDE; VIRULENCE FACTOR;

ARTICLE; CRYPTOCOCCUS NEOFORMANS; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE SEQUENCE; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA SEQUENCE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRESS; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHROMATIN IMMUNOPRECIPITATION; CRYPTOCOCCOSIS; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; PATHOGENICITY; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

AMINO ACID SEQUENCE; ANIMALS; CHROMATIN IMMUNOPRECIPITATION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FEMALE; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HISTONE ACETYLTRANSFERASES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION, GENETIC; VIRULENCE; VIRULENCE FACTORS;

EID: 84855263768     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002411     Document Type: Article

References (68)

1. Heitman J, Kozel TR, Kwon-Chung J, Perfect J, Casadevall A, (2011) Cryptococcus, from human pathogen to model yeast. Washington, D.C. ASM Press.
2. Giles SS, Dagenais TR, Botts MR, Keller NP, Hull CM, (2009) Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect Immun 77: 3491-3500 doi: 10.1128/IAI.00334-09.
3. Garcia-Hermoso D, Janbon G, Dromer F, (1999) Epidemiological evidence for dormant Cryptococcus neoformans infection. J Clin Microbiol 37: 3204-9.
4. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, et al. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-30.
5. Gomez BL, Nosanchuk JD, (2003) Melanin and fungi. Curr Opin Infect Dis 16: 91-96.
6. Cox GM, Mukherjee J, Cole GT, Casadevall A, Perfect JR, (2000) Urease as a virulence factor in experimental cryptococcosis. Infect Immun 68: 443-8.
7. Cox GM, McDade HC, Chen SC, Tucker SC, Gottfredsson M, et al. (2001) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39: 166-175.
8. Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, et al. (2010) Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6: e1000953.
9. Zaragoza O, García-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodríguez-Tudela JL, et al. (2010) Fungal cell gigantism during mammalian infection. PLoS Pathog 6: e1000945.
10. Doering TL, (2009) How sweet it is! Capsule formation and cell wall biogenesis in Cryptococcus neoformans. Annu Rev Microbiol 63: 223-247.
11. Rivera J, Feldmesser M, Cammer M, Casadevall A, (1998) Organ-dependent variation of capsule thickness in Cryptococcus neoformans during experimental murine infection. Infect Immun 66: 5027-30.
12. Vartivarian SE, Anaissie EJ, Cowart RE, Sprigg HA, Tingler MJ, et al. (1993) Regulation of cryptococcal capsular polysaccharide by iron. J Infect Dis 167: 186-90.
13. Littman ML, (1958) Capsule synthesis by Cryptococcus neoformans. Trans N Y Acad Sci 20: 623-48.
14. Granger DL, Perfect JR, Durack DT, (1985) Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. J Clin Invest 76: 508-16.
15. Clancy CJ, Nguyen MH, Alandoerffer R, Cheng S, Iczkowski K, et al. (2006) Cryptococcus neoformans var. grubii isolates recovered from persons with AIDS demonstrate a wide range of virulence during murine meningoencephalitis that correlates with the expression of certain virulence factors. Microbiology 152: 2247-55.
16. Chang YC, Kwon-Chung KJ, (1994) Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 14: 4912-9.
17. Janbon G, Himmelreich U, Moyrand F, Improvisi L, Dromer F, (2001) Cas1p is a membrane protein necessary for the O-acetylation of the Cryptococcus neoformans capsular polysaccharide. Mol Microbiol 42: 453-67.
18. Pukkila-Worley R, Alspaugh JA, (2004) Cyclic AMP signaling in Cryptococcus neoformans. FEMS Yeast Res 4: 361-7.
19. D'Souza CA, Alspaugh JA, Yue C, Harashima T, Cox GM, et al. (2001) Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol Cell Biol 21: 3179-91.
20. Cramer KL, Gerrald QD, Nichols CB, Price MS, Alspaugh JA, (2006) Transcription factor Nrg1 mediates capsule formation, stress response, and pathogenesis in Cryptococcus neoformans. Eukaryot Cell 5: 1147-56.
21. ÒMeara TR, Norton D, Price MS, Hay C, Clements MF, et al. (2010) Interaction of Cryptococcus neoformans Rim101 and protein kinase A regulates capsule. PLoS Pathog 6: e1000776.
22. Jung WH, Saikia S, Hu G, Wang J, Fung CK-Y, et al. (2010) HapX positively and negatively regulates the transcriptional response to iron deprivation in Cryptococcus neoformans. PLoS Pathog 6: e1001209.
23. Jung WH, Sham A, White R, Kronstad JW, (2006) Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biol 4: e410.
24. Chun CD, Brown JCS, Madhani HD, (2011) A major role for capsule-independent phagocytosis-inhibitory mechanisms in mammalian infection by Cryptococcus neoformans. Cell Host Microbe 9: 243-51.
25. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, et al. (2008) Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-88.
26. Bahn Y-S, 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: 2285-300.
27. Zhang S, Hacham M, Panepinto J, Hu G, Shin S, et al. (2006) The Hsp70 member, Ssa1, acts as a DNA-binding transcriptional co-activator of laccase in Cryptococcus neoformans. Mol Microbiol 62: 1090-101.
28. Chang YC, Miller GF, Kwon-Chung KJ, (2003) Importance of a developmentally regulated pheromone receptor of Cryptococcus neoformans for virulence. Infect Immun 71: 4953-60.
29. Gerik KJ, Donlin MJ, Soto CE, Banks AM, Banks IR, et al. (2005) Cell wall integrity is dependent on the PKC1 signal transduction pathway in Cryptococcus neoformans. Mol Microbiol 58: 393-408.
30. 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 Cell 7: 1685-1698.
31. ÒMeara TR, Hay C, Price MS, Giles S, Alspaugh JA, (2010) Cryptococcus neoformans histone acetyltransferase Gcn5 regulates fungal adaptation to the host. Eukaryot Cell 9: 1193-202.
32. Koutelou E, Hirsch CL, Dent SYR, (2010) Multiple faces of the SAGA complex. Curr Opin Cell Biol 22: 374-82.
33. Wang P, Nichols CB, Lengeler KB, Cardenas ME, Cox GM, et al. (2002) Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot Cell 1: 257-72.
34. Hicks JK, Bahn Y-S, Heitman J, (2005) Pde1 phosphodiesterase modulates cyclic AMP levels through a protein kinase A-mediated negative feedback loop in Cryptococcus neoformans. Eukaryot Cell 4: 1971-81.
35. Grant PA, Duggan L, Côté J, Roberts SM, Brownell JE, et al. (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11: 1640-50.
36. Balasubramanian R, Pray-Grant MG, Selleck W, Grant PA, Tan S, (2002) Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J Biol Chem 277: 7989-95.
37. Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, et al. (2003) Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and alpha isolates. Infect Immun 71: 4831-41.
38. Grant PA, Eberharter A, John S, Cook RG, Turner BM, et al. (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274: 5895-900.
39. Huisinga KL, Pugh BF, (2004) A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 13: 573-85.
40. Sellam A, Askew C, Epp E, Lavoie H, Whiteway M, et al. (2009) Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol Biol Cell 20: 2389-400.
41. Johnsson A, Xue-Franzén Y, Lundin M, Wright APH, (2006) Stress-specific role of fission yeast Gcn5 histone acetyltransferase in programming a subset of stress response genes. Eukaryot Cell 5: 1337-46.
42. Xue-Franzén Y, Johnsson A, Brodin D, Henriksson J, Bürglin TR, et al. (2010) Genome-wide characterisation of the Gcn5 histone acetyltransferase in budding yeast during stress adaptation reveals evolutionarily conserved and diverged roles. BMC Genomics 11: 200.
43. Missall TA, Pusateri ME, Donlin MJ, Chambers KT, Corbett JA, et al. (2006) Posttranslational, translational, and transcriptional responses to nitric oxide stress in Cryptococcus neoformans: implications for virulence. Eukaryot Cell 5: 518-529.
44. Brown SM, Campbell LT, Lodge JK, (2007) Cryptococcus neoformans, a fungus under stress. Curr Opin Microbiol 10: 320-325.
45. Cryptococcus neoformans var. grubii H99 Sequencing Project, (n.d.) Broad Institute of Harvard and MIT. Available:http://www.broadinstitute.org/.
46. Lee H, Chang YC, Varma A, Kwon-Chung KJ, (2009) Regulatory diversity of TUP1 in Cryptococcus neoformans. Eukaryot Cell 8: 1901-8.
47. Ko Y-J, Yu YM, Kim G-B, Lee G-W, Maeng PJ, et al. (2009) Remodeling of global transcription patterns of Cryptococcus neoformans genes mediated by the stress-activated HOG signaling pathways. Eukaryot Cell 8: 1197-217.
48. T-young Roh, Ngau WC, Cui K, Landsman D, Zhao K, (2004) High-resolution genome-wide mapping of histone modifications. Nat Biotechnol 22: 1013-6.
49. Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, et al. (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3: e328.
50. Ma P, Wera S, Van Dijck P, Thevelein JM, (1999) The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell 10: 91-104.
51. Serrano R, Bernal D, Simón E, Ariño J, (2004) Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J Biol Chem 279: 19698-704.
52. Helmlinger D, Marguerat S, Villén J, Gygi SP, Bähler J, et al. (2008) The S. pombe SAGA complex controls the switch from proliferation to sexual differentiation through the opposing roles of its subunits Gcn5 and Spt8. Genes Dev 22: 3184-95.
53. Jacobson S, Pillus L, (2009) The SAGA subunit Ada2 functions in transcriptional silencing. Mol Cell Biol 29: 6033-45 doi:10.1128/MCB.00542-09.
54. Robert F, Pokholok DK, Hannett NM, Rinaldi NJ, Chandy M, et al. (2004) Global position and recruitment of HATs and HDACs in the yeast genome. Mol Cell 16: 199-209.
55. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-27.
56. Chikamori M, Fukushima K, (2005) A new hexose transporter from Cryptococcus neoformans: molecular cloning and structural and functional characterization. Fungal Genet Biol 42: 646-55.
57. Moyrand F, Fontaine T, Janbon G, (2007) Systematic capsule gene disruption reveals the central role of galactose metabolism on Cryptococcus neoformans virulence. Mol Microbiol 64: 771-81.
58. Dromer F, Mathoulin S, Dupont B, Brugiere O, Letenneur L, (1996) Comparison of the efficacy of amphotericin B and fluconazole in the treatment of cryptococcosis in human immunodeficiency virus-negative patients: retrospective analysis of 83 cases. French Cryptococcosis Study Group. Clin Infect Dis 22 (Suppl 2): S154-60.
59. Cottrell TR, Griffith CL, Liu H, Nenninger AA, Doering TL, (2007) The pathogenic fungus Cryptococcus neoformans expresses two functional GDP-mannose transporters with distinct expression patterns and roles in capsule synthesis. Eukaryot Cell 6: 776-785.
60. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
61. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-21.
62. Nelson RT, Hua J, Pryor B, Lodge JK, (2001) Identification of virulence mutants of the fungal pathogen Cryptococcus neoformans using signature-tagged mutagenesis. Genetics 157: 935-947.
63. Fu J, Hettler E, Wickes BL, (2006) Split marker transformation increases homologous integration frequency in Cryptococcus neoformans. Fungal Genet Biol 43: 200-212 doi:10.1016/j.fgb.2005.09.007.
64. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-11.
65. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-5.
66. Lo K, Gottardo R, (2007) Flexible empirical Bayes models for differential gene expression. Bioinformatics 23: 328-35.
67. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
68. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.