Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Springer, Deborah J ^a,b,d   Ren, Ping ^a   Raina, Ramesh ^c   Dong, Yimin ^a   Behr, Melissa J ^a,e   McEwen, Bruce F ^a,b   Bowser, Samuel S ^a   Samsonoff, William A ^a   Chaturvedi, Sudha ^a,b   Chaturvedi, Vishnu ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c SYRACUSE UNIVERSITY   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARABIDOPSIS; ARTICLE; CELL COMMUNICATION; CELL ENCAPSULATION; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; ECOLOGICAL NICHE; EVOLUTIONARY ADAPTATION; FUNGAL COLONIZATION; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS MUTANT; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PARTICLE SIZE; PHAGOCYTE; PLANT LEAF; PULMONARY CRYPTOCOCCOSIS; SCANNING ELECTRON MICROSCOPY; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; ULTRASTRUCTURE; VIRULENCE;

ANIMALIA; ARABIDOPSIS THALIANA; CRYPTOCOCCUS GATTII; MAMMALIA; MURINAE;

ANIMALS; ARABIDOPSIS; CRYPTOCOCCUS GATTII; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, SCANNING; NEUTROPHILS; PLANT LEAVES; VIRULENCE;

EID: 77956210102     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010978     Document Type: Article

References (68)

1. de Hoog GS, Guarro J, Gene J, Figueras (2009) Atlas of Clinical Fungi. Utrecht: CBS/Universitat Rovira i Virgli.
2. Mylonakis E, Casadevall A, Ausubel FM (2007) Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog 3: e101.
3. Casadevall A, Steenbergen JN, Nosanchuk JD (2003) 'Ready made' virulence and 'dual use' virulence factors in pathogenic environmental fungi-the Cryptococcus neoformans paradigm. Curr Opin Microbiol 6: 332-337.
4. Brandl MT (2006) Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44: 367-392.
5. van Baarlen P, van Belkum A, Thomma BP (2007) Disease induction by human microbial pathogens in plant-model systems: potential, problems and prospects. Drug Discov Today 12: 167-173.
6. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, et al. (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97: 8815-8821.
7. Springer DJ, Chaturvedi V (2010) Projecting global occurrence of Cryptococcus gattii Emerg Infect Dis 16: 14-20.
8. Kwon-Chung KJ, Boekhout T, Fell JW, Diaz M (2002) (1557) Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. bacillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae). Taxon 51: 804-806.
9. Huerfano S, Castaneda A, Castaneda E (2001) Experimental infection of almond trees seedlings (Terminalia catappa) with an environmental isolate of Cryptococcus neoformans var. gattii, serotype C. Rev Iberoam Micol 18: 131-132.
10. Ren P, Springer DJ, Behr MJ, Samsonoff WA, Chaturvedi S, et al. (2006) Transcription factor STE12alpha has distinct roles in morphogenesis, virulence, and ecological fitness of the primary pathogenic yeast Cryptococcus gattii. Eukaryot Cell 5: 1065-1080.
11. 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.
12. Chaturvedi S, Ren P, Narasipura SD, Chaturvedi V (2005) Selection of optimal host strain for molecular pathogenesis studies on Cryptococcus gattii. Mycopathologia 160: 207-215.
13. Okabayashi K, Hasegawa A, Watanabe T (2007) Microreview: capsule-associated genes of Cryptococcus neoformans. Mycopathologia 163: 1-8.
14. Chang YC, Kwon-Chung KJ (1994) Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 14: 4912-4919.
15. Hu G, Kronstad JW (2006) Gene disruption in Cryptococcus neoformans and Cryptococcus gattii by in vitro transposition. Curr Genet 49: 341-350.
16. Yu JH, Hamari Z, Han KH, Seo JA, Dominguez YR, et al. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Gen Biol 41: 973-981.
17. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, et al. (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250.
18. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592.
19. Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, et al. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA 96: 3292-3297.
20. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, et al. (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.
21. Fullner KJ (1998) Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J Bacteriol 180: 430-434.
22. Polizzi G, Vitale A (2006) Dasylirion serratifolium as a new host of Botrytis cinerea, the causal agent of leaf spots and blight in Italy. Plant Dis 90: 114-114.
23. Mithofer A, Wanner G, Boland W (2005) Effects of Feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137: 1160-1168.
24. Chaturvedi V, Fan J, Stein B, Behr MJ, Samsonoff WA, et al. (2002) Molecular genetic analyses of mating pheromones reveal intervariety mating or hybridization in Cryptococcus neoformans. Infect Immun 70: 5225-5235.
25. Chen X, Steed A, Harden C, Nicholson P (2006) Characterization of Arabidopsis thaliana-Fusarium graminearum interactions and identification of variation in resistance among ecotypes. Molecular Plant Pathol 7: 391-403.
26. Rieder CL, Rupp G, Bowser SS (1985) Electron microscopy of semithick sections: Advantages for biomedical research. J Electron Micro Tech 2: 11-28.
27. Gao L, Bretscher A (2009) Polarized growth in budding yeast in the absence of a localized formin. Mol Biol Cell 20: 2540-2548.
28. Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422: 766-774.
29. Narasipura SD, Ault JG, Behr MJ, Chaturvedi V, Chaturvedi S (2003) Characterization of Cu,Zn superoxide dismutase (SOD1) gene knock-out mutant of Cryptococcus neoformans var. gattii: role in biology and virulence. Mol Microbiol 47: 1681-1694.
30. Wright LC, Chen SC, Wilson CF, Simpanya MF, Blackstock R, et al. (2002) Strain-dependent effects of environmental signals on the production of extracellular phospholipase by Cryptococcus neoformans. FEMS Microbiol Lett 209: 175-181.
31. Chaturvedi V, Wong B, Newman SL (1996) Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J Immunol 156: 3836-3840.
32. Bohman S, Staal J, Thomma BP, Wang M, Dixelius C (2004) Characterisation of an Arabidopsis-Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 37: 9-20.
33. Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28: 293-305.
34. Urban CF, Reichard U, Brinkmann V, Zychlinsky A (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 8: 668-676.
35. Jarrell K (2009) Pili and Flagella: Current Research and Future Trends: Caister Academic Press, Norfolk, UK.
36. Dworkin M (1999) Fibrils as extracellular appendages of bacteria: their role in contact-mediated cell-cell interactions in Myxococcus xanthus. Bioessays 21: 590-595.
37. Saarimaa C, Peltola M, Raulio M, Neu TR, Salkinoja-Salonen MS, et al. (2006) Characterization of adhesion threads of Deinococcus geothermalis as type IV pili. J Bacteriol 188: 7016-7021.
38. Clark ME, Edelmann RE, Duley ML, Wall JD, Fields MW (2007) Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments. Environ Microbiol 9: 2844-2854.
39. Walker JR, Gnanam AJ, Blinkova AL, Hermandson MJ, Karymov MA, et al. (2007) Clostridium taeniosporum spore ribbon-like appendage structure, composition and genes. Mol Microbiol 63: 629-643.
40. Machesky L, Jurdic P, Hinz B (2008) Grab, stick, pull and digest: the functional diversity of actin-associated matrix-adhesion structures. Workshop on invadopodia, podosomes and focal adhesions in tissue invasion. EMBO Rep 9: 139-143.
41. Machado CM, Schenka A, Vassallo J, Tamashiro WM, Goncalves EM, et al. (2005) Morphological characterization of a human glioma cell line. Cancer Cell Int 5: 13.
42. Rokusek D, Davitt C, Bandyopadhyay A, Bose S, Hosick HL (2005) Interaction of human osteoblasts with bioinert and bioactive ceramic substrates. J Biomed Mater Res A 75: 588-594.
43. Al-Nazhan S (2004) SEM observations of the attachment of human periodontal ligament fibroblasts to non-demineralized dentin surface in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97: 393-397.
44. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, et al. (2008) Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 10: 211-219.
45. Varon M, Choder M (2000) Organization and cell-cell interaction in starved Saccharomyces cerevisiae colonies. J Bacteriol 182: 3877-3880.
46. Sebolai OM, Pohl CH, Botes PJ, Strauss CJ, van Wyk PW, et al. (2007) 3-hydroxy fatty acids found in capsules of Cryptococcus neoformans. Can J Microbiol 53: 809-812.
47. Sebolai OM, Pohl CH, Botes PJ, van Wyk PW, Kock JL (2008) The influence of acetylsalicylic acid on oxylipin migration in Cryptococcus neoformans var. neoformans UOFS Y-1378. Can J Microbiol 54: 91-96.
48. Sebolai OM, Pohl CH, Botes PJ, van Wyk PW, Mzizi R, et al. (2008) Distribution of 3-hydroxy oxylipins and acetylsalicylic acid sensitivity in Cryptococcus species. Can J Microbiol 54: 111-118.
49. Panepinto J, Komperda K, Frases S, Park YD, Djordjevic JT, et al. (2009) Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 71: 1165-1176.
50. Rodrigues ML, Nakayasu ES, Oliveira DL, Nimrichter L, Nosanchuk JD, et al. (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7: 58-67.
51. Nicola AM, Frases S, Casadevall A (2009) Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryotic Cell 8: 1373-1380.
52. Frases S, Pontes B, Nimrichter L, Viana NB, Rodrigues ML, et al. (2009) Capsule of Cryptococcus neoformans grows by enlargement of polysaccharide molecules. Proc Natl Acad Sci USA 106: 1228-1233.
53. Garcia-Rivera J, Chang YC, Kwon-Chung KJ, Casadevall A (2004) Cryptococcus neoformans CAP59 (or Cap59p) is involved in the extracellular trafficking of capsular glucuronoxylomannan. Eukaryot Cell 3: 385-392.
54. Reese AJ, Doering TL (2003) Cell wall alpha-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol Microbiol 50: 1401-1409.
55. Reese AJ, Yoneda A, Breger JA, Beauvais A, Liu H, et al. (2007) Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol 63: 1385-1398.
56. Vardy L, Toda T (2000) The fission yeast gamma-tubulin complex is required in G(1) phase and is a component of the spindle assembly checkpoint. EMBO J 19: 6098-6111.
57. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, et al. (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55: 327-342.
58. Staib F (1981) The perfect state of Cryptococcus neoformans, Filobasidiella neoformans, on pigeon manure filtrate agar. Zentralbl Bakteriol A 248: 575-578.
59. 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.
60. Fonseca Á, Inácio J (2006) Phylloplane Yeasts. In: Péter G, Rosa C, editors. Biodiversity and Ecophysiology of Yeasts: Springer Berlin Heidelberg. pp. 263-301.
61. Inacio J, Portugal L, Spencer-Martins I, Fonseca A (2005) Phylloplane yeasts from Portugal: seven novel anamorphic species in the Tremellales lineage of the Hymenomycetes (Basidiomycota) producing orange-coloured colonies. FEMS Yeast Res 5: 1167-1183.
62. Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, et al. (2004) A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci U S A 101: 17258-17263.
63. Narasipura SD, Chaturvedi V, Chaturvedi S (2005) Characterization of Cryptococcus neoformans variety gattii SOD2 reveals distinct roles of the two superoxide dismutases in fungal biology and virulence. Mol Microbiol 55: 1782-1800.
64. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
65. Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, et al. (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16: 396-400.
66. Urban CF, Lourido S, Zychlinsky A (2006) How do microbes evade neutrophil killing? Cell Microbiol 8: 1687-1696.
67. Dong ZM, Murphy JW (1995) Effects of the two varieties of Cryptococcus neoformans cells and culture filtrate antigens on neutrophil locomotion. Infect Immun 63: 2632-2644.
68. Wartha F, Beiter K, Albiger B, Fernebro J, Zychlinsky A, et al. (2007) Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 9: 1162-1171.