DNA Mutations Mediate Microevolution between Host-Adapted Forms of the Pathogenic Fungus Cryptococcus neoformans

PLoS Pathogens

Volumn 8, Issue 10, 2012, Pages

  Magditch, Denise A ^a   Liu, Tong Bao ^b   Xue, Chaoyang ^b   Idnurm, Alexander ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; EPIGENETICS; FEMALE; FUNGAL STRUCTURES; FUNGUS ISOLATION; GENE MUTATION; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGEN CLEARANCE; PHENOTYPE; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMOEBA; ANIMALS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DNA, FUNGAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENES, FUNGAL; HOST-PATHOGEN INTERACTIONS; HYPHAE; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE PROTEINS; SELECTION, GENETIC;

FILOBASIDIELLA NEOFORMANS; FUNGI; MAMMALIA; MUS;

EID: 84868106286     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002936     Document Type: Article

References (83)

1. Casadevall A, Perfect J (1998) Cryptococcus neoformans. Washington, D.C.: American Society for Microbiology Press.
2. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A, et al. (2011) Cryptococcus: From Human Pathogen to Model Yeast. Washington, D.C.: American Society for Microbiology Press.
3. 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: 525-530.
4. Byrnes EJ 3rd, Bartlett KH, Perfect JR, Heitman J, (2011) Cryptococcus gattii: an emerging fungal pathogen infecting humans and animals. Microbes Infect 13: 895-907.
5. Bartlett KH, Cheng P-Y, Duncan C, Galanis E, Hoang L, et al. (2012) A decade of experience: Cryptococcus gattii in British Columbia. Mycopathologia 173: 311-319.
6. Harris JR, Lockhart SR, Debess E, Marsden-Haug N, Goldoft M, et al. (2011) Cryptococcus gattii in the United States: clinical aspects of infection with an emerging pathogen. Clin Infect Dis 53: 1188-1195.
7. Idnurm A, Bahn Y-S, Nielsen K, Lin X, Fraser JA, et al. (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 3: 753-764.
8. Kronstad JW, Attarian R, Cadieux B, Choi J, D'Souza CA, et al. (2011) Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat Rev Microbiol 9: 193-203.
9. Sullivan D, Haynes K, Moran G, Shanley D, Coleman D, (1996) Persistence, replacement, and microevolution of Cryptococcus neoformans strains in recurrent meningitis in AIDS patients. J Clin Microbiol 34: 1739-1744.
10. Fries BC, Casadevall A, (1998) Serial isolates of Cryptococcus neoformans from patients with AIDS differ in virulence for mice. J Infect Dis 178: 1761-1766.
11. Almeida AMF, Matsumoto MT, Baeza LC, de Oliveira e Silva RB, Kleiner AAP, et al. (2007) Molecular typing and antifungal susceptibility of clinical sequential isolates of Cryptococcus neoformans from Sao Paulo State, Brazil. FEMS Yeast Res 7: 152-164.
12. Blasi E, Brozzetti A, Francisci D, Neglia R, Cardinali G, et al. (2001) Evidence of microevolution in a clinical case of recurrent Cryptococcus neoformans meningoencephalitis. Eur J Clin Microbiol Infect Dis 20: 535-543.
13. Steenbergen JN, Shuman HA, Casadevall A, (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98: 15245-15250.
14. Steenbergen JN, Casadevall A, (2003) The origin and maintenance of virulence for the human pathogenic fungus Cryptococcus neoformans. Microbes Infect 5: 667-675.
15. Ruiz A, Neilson JB, Bulmer GS, (1982) Control of Cryptococcus neoformans in nature by biotic factors. Sabouraudia 20: 21-29.
16. Casadevall A, (2012) Amoeba provide insight into the origin of virulence in pathogenic fungi. Adv Exp Med Biol 710: 1-10.
17. Neilson JB, Ivey MH, Bulmer GS, (1978) Cryptococcus neoformans: pseudohyphal forms surviving culture with Acanthamoeba polyphaga. Infect Immun 20: 262-266.
18. Castellani A, (1930) An amoeba growing in cultures of a yeast: preliminary note. J Trop Med Hyg 33: 160.
19. Bunting LA, Neilson JB, Bulmer GS, (1979) Cryptococcus neoformans: gastronomic delight of a soil ameba. Sabouraudia 17: 225-232.
20. Castellani A, (1955) Action phagocytaire et destructrice de Hartmanella castellanii (Amoeba castellanii) sur un champignon levuriforme encapsulé pathogène Torulopsis neoformans (Cryptococcus neoformans). Ann Inst Pasteur 89: 1-7.
21. Mylonakis E, Ausubel FM, Perfect JR, Heitman J, Calderwood SB, (2002) Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci U S A 99: 15675-15680.
22. Mylonakis E, Idnurm A, Moreno R, El Khoury J, Rottman JB, et al. (2004) Cryptococcus neoformans Kin1 protein kinase homologue, identified through a Caenorhabditis elegans screen, promotes virulence in mammals. Mol Microbiol 54: 407-419.
23. Tang RJ, Breger J, Idnurm A, Gerik KJ, Lodge JK, et al. (2005) Cryptococcus neoformans gene involved in mammalian pathogenesis identified by a Caenorhabditis elegans progeny-based approach. Infect Immun 73: 8219-8225.
24. Steenbergen JN, Nosanchuk JD, Malliaris SD, Casadevall A, (2003) Cryptococcus neoformans virulence is enhanced after growth in the genetically malleable host Dictyostelium discoideum. Infect Immun 71: 4862-4872.
25. Neilson JB, Fromtling RA, Bulmer GS, (1981) Pseudohyphal forms of Cryptococcus neoformans: decreased survival in vivo. Mycopathologia 73: 57-59.
26. Fromtling RA, Blackstock R, Hall NK, Bulmer GS, (1979) Immunization of mice with an avirulent pseudohyphal form of Cryptococcus neoformans. Mycopathologia 68: 179-181.
27. Fries BC, Goldman DL, Cherniak R, Ju R, Casadevall A, (1999) Phenotypic switching in Cryptococcus neoformans results in changes in cellular morphology and glucuronoxylomannan structure. Infect Immun 67: 6076-6083.
28. Walton FJ, Heitman J, Idnurm A, (2006) Conserved elements of the RAM signaling pathway establish cell polarity in the basidiomycete Cryptococcus neoformans in a divergent fashion from other fungi. Mol Biol Cell 17: 3768-3780.
29. Nelson B, Kurischko C, Horecka J, Mody M, Nair P, et al. (2003) RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol Biol Cell 14: 3782-3803.
30. Maerz S, Seiler S, (2010) Tales of RAM and MOR: NDR kinase signaling in fungal morphogenesis. Curr Opin Microbiol 13: 663-671.
31. Du L-L, Novick P, (2002) Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae. Mol Biol Cell 13: 503-514.
32. Scheffer J, Ziv C, Yarden O, Tudzynski P, (2005) The COT1 homologue CPCOT1 regulates polar growth and branching and is essential for pathogenicity in Claviceps purpurea. Fungal Genet Biol 42: 107-118.
33. Dürrenberger F, Kronstad J, (1999) The ukc1 gene encodes a protein kinase involved in morphogenesis, pathogenicity and pigment formation in Ustilago maydis. Mol Gen Genet 261: 281-289.
34. Noble SM, French S, Kohn LA, Chen V, Johnson AD, (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
35. Saputo S, Chabrier-Rosello Y, Luca FC, Kumar A, Krysan DJ, (2012) The RAM network in pathogenic fungi. Eukaryot Cell 11: 708-717.
36. Muller LAH, Lucas JE, Georgianna DR, McCusker JH, (2011) Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Mol Ecol 20: 4085-4097.
37. Song Y, Cheon SA, Lee KE, Lee S-Y, Lee B-K, et al. (2008) Role of the RAM network in cell polarity and hyphal morphogenesis in Candida albicans. Mol Biol Cell 19: 5456-5477.
38. McNemar MD, Fonzi WA, (2002) Conserved serine/threonine kinase encoded by CBK1 regulates expression of several hypha-associated transcripts and genes encoding cell wall proteins in Candida albicans. J Bacteriol 184: 2058-2061.
39. Finkel JS, Xu W, Huang D, Hill EM, Desai JV, et al. (2012) Portrait of Candida albicans adherence regulators. PLoS Pathog 8: e1002525.
40. Gutiérrez-Escribano P, González-Novo A, Suárez MB, Li C-R, Wang Y, et al. (2011) CDK-dependent phosphorylation of Mob2 is essential for hyphal development in Candida albicans. Mol Biol Cell 22: 2458-2469.
41. Bharucha N, Chabrier-Roselló Y, Xu T, Johnson C, Sobczynski S, et al. (2011) A large-scale complex haploinsufficiency-based genetic interaction screen in Candida albicans: analysis of the RAM network during morphogenesis. PLoS Genet 7: e1002058.
42. Gutiérrez-Escribano P, Zeidler U, Suarez MB, Bachellier-Bassi S, Clemente-Blanco A, et al. (2012) The NDR/LATS kinase Cbk1 controls the activity of the transcriptional regulator Bcr1 during biofilm formation in Candida albicans. PLoS Pathog 8: e1002683.
43. Odom A, Del Poeta M, Perfect J, Heitman J, (1997) The immunosuppressant FK506 and its nonimmunosuppressive analog L-685,818 are toxic to Cryptococcus neoformans by inhibition of a common target protein. Antimicrob Agents Chemother 41: 156-161.
44. Goldman DL, Fries BC, Franzot SP, Montella L, Casadevall A, (1998) Phenotypic switching in the human pathogenic fungus Cryptococcus neoformans is associated with changes in virulence and pulmonary inflammatory response in rodents. Proc Natl Acad Sci U S A 95: 14967-14972.
45. Franzot SP, Mukherjee J, Cherniak R, Chen LC, Hamdan JS, et al. (1998) Microevolution of a standard strain of Cryptococcus neoformans resulting in differences in virulence and other phenotypes. Infect Immun 66: 89-97.
46. Kwon-Chung KJ, Varma A, Edman JC, Bennett JE, (1992) Selection of ura5 and ura3 mutants from the two varieties of Cryptococcus neoformans on 5-fluoroorotic acid medium. J Med Vet Mycol 30: 61-69.
47. Nielsen K, De Obaldia AL, Heitman J, (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6: 949-959.
48. Paliwal DK, Randhawa HS, (1978) Evaluation of a simplified Guizotia abyssinica seed medium for differentiation of Cryptococcus neoformans. J Clin Microbiol 7: 346-348.
49. Staib F, (1962) Cryptococcus neoformans und Guizotia abyssinica (syn. G. oleifera D.C.) (Farbreaktion für Cr. neoformans). Z Hyg 148: 466-475.
50. Sionov E, Lee H, Chang YC, Kwon-Chung KJ, (2010) Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog 6: e1000848.
51. Hu G, Liu I, Sham A, Stajich JE, Dietrich FS, et al. (2008) Comparative hybridization reveals extensive genome variation in the AIDS-associated pathogen Cryptococcus neoformans. Genome Biol 9: R41.
52. Jain N, Fries BC, (2008) Phenotypic switching of Cryptococcus neoformans and Cryptococcus gattii. Mycopathologia 166: 181-188.
53. Guerrero A, Jain N, Goldman DL, Fries BC, (2006) Phenotypic switching in Cryptococcus neoformans. Microbiology 152: 3-9.
54. Panozzo C, Bourens M, Nowacka A, Herbert CJ, (2010) Mutations in the C-terminus of the conserved NDR kinase, Cbk1p of Saccharomyces cerevisiae, make the protein independent of upstream activators. Mol Genet Genomics 283: 111-122.
55. Bruno KS, Tinsley JH, Minke PF, Plamann M, (1996) Genetic interactions among cytoplasmic dynein, dynactin, and nuclear distribution mutants of Neurospora crassa. Proc Natl Acad Sci U S A 93: 4775-4780.
56. Plamann M, Minke PF, Tinsley JH, Bruno KS, (1994) Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J Cell Biol 127: 139-149.
57. 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.
58. 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.
59. Wang L, Zhai B, Lin X, (2012) The link between morphotype transition and virulence in Cryptococcus neoformans. PLoS Pathog 8: e1002765.
60. Williamson JD, Silverman JF, Mallak CT, Christie JD, (1996) Atypical cytomorphologic appearance of Cryptococcus neoformans: a report of five cases. Acta Cytol 40: 363-370.
61. Gazzoni AF, Oliveira FdM, Salles EF, Mayayo E, Guarro J, et al. (2010) Unusual morphologies of Cryptococcus spp. in tissue specimens: report of 10 cases. Rev Inst Med Trop Sao Paulo 52: 145-149.
62. Alvarez M, Casadevall A, (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16: 2161-2165.
63. Ma H, Croudace JE, Lammas DA, May RC, (2006) Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160.
64. Chrisman CJ, Alvarez M, Casadevall A, (2010) Phagocytosis and non-lytic exocytosis of Cryptococcus noformans by and from Acanthamoeba castellanii. Appl Environ Microbiol 76: 6056-6062.
65. Goldman DL, Khine H, Abadi J, Lindenberg DJ, Pirofski L-a, et al. (2001) Serologic evidence for Cryptococcus neoformans infection in early childhood. Pediatrics 107: E66.
66. Saha DC, Goldman DL, Shao X, Casadevall A, Husain S, et al. (2007) Serologic evidence for reactivation of cryptococcosis in solid-organ transplant recipients. Clin Vaccine Immunol 14: 1550-1554.
67. Litvintseva AP, Mitchell TG, (2009) Most environmental isolates of Cryptococcus neoformans var. grubii (serotype A) are not lethal for mice. Infect Immun 77: 3188-3195.
68. da Silva EG, de Assis Baroni F, Viani FC, da Silva Ruiz L, Gandra RF, et al. (2006) Virulence profile of strains of Cryptococcus neoformans var. grubii evaluated by experimental infection in BALB/c mice and correlation with exoenzyme activity. J Med Microbiol 55: 139-142.
69. Fromtling RA, Abruzzo GK, Ruiz A, (1989) Virulence and antifungal susceptibility of environmental and clinical isolates of Cryptococcus neoformans from Puerto Rico. Mycopathologia 106: 163-166.
70. Hasenclever HF, Emmons CW, (1963) The prevalence and mouse virulence of Cryptococcus neoformans strains isolated from urban aeas. Am J Hyg 78: 227-231.
71. Boothroyd CE, Dreesen O, Leonova T, Ly KI, Figueiredo LM, et al. (2009) A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 459: 278-281.
72. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1254.
73. Denamur E, Bonacorsi S, Giraud A, Duriez P, Hilali F, et al. (2002) High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J Bacteriol 184: 605-609.
74. Picard B, Duriez P, Gouriou S, Matic I, Denamur E, et al. (2001) Mutator natural Escherichia coli isolates have an unusual virulence phenotype. Infect Immun 69: 9-14.
75. 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: 174-188.
76. Axelsson-Olsson D, Olofsson J, Ellström P, Waldenström J, Olsen B, (2009) A simple method for long-term storage of Acanthamoeba species. Parasitol Res 104: 935-937.
77. Xue C, Tada Y, Dong X, Heitman J, (2007) The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1: 263-273.
78. Pitkin JW, Panaccione DG, Walton JD, (1996) A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology 142: 1557-1565.
79. Idnurm A, Reedy JL, Nussbaum JC, Heitman J, (2004) Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell 3: 420-429.
80. Toffaletti DL, Rude TH, Johnston SA, Durack DT, Perfect JR, (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol 175: 1405-1411.
81. Hall BM, Ma C-X, Liang P, Singh KK, (2009) Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbrück fluctuation analysis. Bioinformatics 25: 1564-1565.
82. Mylonakis E, Moreno R, El Khoury JB, Idnurm A, Heitman J, et al. (2005) Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73: 3842-3850.
83. Cox GM, Mukherjee J, Cole GT, Casadevall A, Perfect JR, (2000) Urease as a virulence factor in experimental cryptococcosis. Infect Immun 68: 443-448.