Cryptococcus neoformans capsular enlargement and cellular gigantism during Galleria mellonella infection

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  García Rodas, Rocío ^a   Casadevall, Arturo ^b   Rodríguez Tudela, Juan Luís ^a   Cuenca Estrella, Manuel ^a   Zaragoza, Oscar ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CELL; CATERPILLAR; CELL COUNT; CELL DENSITY; CELL ENLARGEMENT; CELL GROWTH; CELL KILLING; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; CRYPTOCOCCOSIS; FUNGAL VIRULENCE; GALLERIA MELLONELLA; GIANT CELL; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TEMPERATURE; INOCULATION; LEPIDOPTERA; NONHUMAN; PHAGOCYTOSIS; TEMPERATURE DEPENDENCE; THERMAL STIMULATION; ANIMAL; BACTERIAL MEMBRANE; BAGG ALBINO MOUSE; CRYPTOCOCCUS NEOFORMANS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY;

ANIMALIA; FILOBASIDIELLA NEOFORMANS; FUNGI; GALLERIA MELLONELLA; MAMMALIA; MUS; VERTEBRATA;

ANIMALS; BACTERIAL CAPSULES; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; GIANT CELLS; LEPIDOPTERA; MICE; MICE, INBRED BALB C; PHAGOCYTOSIS;

EID: 84857099099     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024485     Document Type: Article

References (64)

1. Botts MR, Hull CM, (2010) Dueling in the lung: how Cryptococcus spores race the host for survival. Curr Opin Microbiol 13: 437-442.
2. Velagapudi R, Hsueh YP, Geunes-Boyer S, Wright JR, Heitman J, (2009) Spores as infectious propagules of Cryptococcus neoformans. Infect Immun 77: 4345-4355.
3. Casadevall A, Perfect JR, (1998) Cryptococcus neoformans; In: Press A, editors. Washington DC ASM Press.
4. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A, (2011) Cryptococcus. From human pathogen to model yeast; In: Press A, editors. Washington DC ASM Press.
5. Park BI, 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.
6. Goldman DL, Lee SC, Mednick AJ, Montella L, Casadevall A, (2000) Persistent Cryptococcus neoformans pulmonary infection in the rat is associated with intracellular parasitism, decreased inducible nitric oxide synthase expression, and altered antibody responsiveness to cryptococcal polysaccharide. Infect Immun 68: 832-838.
7. Grijpstra J, Tefsen B, van Die I, de Cock H, (2009) The Cryptococcus neoformans cap10 and cap59 mutant strains, affected in glucuronoxylomannan synthesis, differentially activate human dendritic cells. FEMS Immunol Med Microbiol 57: 142-150.
8. Fonseca FL, Nohara LL, Cordero RJ, Frases S, Casadevall A, et al. Immunomodulatory effects of serotype B glucuronoxylomannan from Cryptococcus gattii correlate with polysaccharide diameter. Infect Immun 78: 3861-3870.
9. Zaragoza O, Rodrigues ML, De Jesus M, Frases S, Dadachova E, et al. (2009) The Capsule of the Fungal Pathogen Cryptococcus neoformans. Adv Appl Microbiol 68: 133-216.
10. Monari C, Bistoni F, Vecchiarelli A, (2006) Glucuronoxylomannan exhibits potent immunosuppressive properties. FEMS Yeast Res 6: 537-542.
11. Monari C, Pericolini E, Bistoni G, Casadevall A, Kozel TR, et al. (2005) Cryptococcus neoformans capsular glucuronoxylomannan induces expression of fas ligand in macrophages. J Immunol 174: 3461-3468.
12. Retini C, Vecchiarelli A, Monari C, Tascini C, Bistoni F, et al. (1996) Capsular polysaccharide of Cryptococcus neoformans induces proinflammatory cytokine release by human neutrophils. Infect Immun 64: 2897-2903.
13. Vecchiarelli A, (2005) The cellular responses induced by the capsular polysaccharide of Cryptococcus neoformans differ depending on the presence or absence of specific protective antibodies. Curr Mol Med 5: 413-420.
14. Vecchiarelli A, Pietrella D, Lupo P, Bistoni F, McFadden DC, et al. (2003) The polysaccharide capsule of Cryptococcus neoformans interferes with human dendritic cell maturation and activation. J Leukoc Biol 74: 370-378.
15. Chaka W, Verheul AF, Vaishnav VV, Cherniak R, Scharringa J, et al. (1997) Cryptococcus neoformans and cryptococcal glucuronoxylomannan, galactoxylomannan, and mannoprotein induce different levels of tumor necrosis factor alpha in human peripheral blood mononuclear cells. Infect Immun 65: 272-278.
16. Dong ZM, Murphy JW, (1997) Cryptococcal polysaccharides bind to CD18 on human neutrophils. Infect Immun 65: 557-563.
17. McClelland EE, Bernhardt P, Casadevall A, (2006) Estimating the relative contributions of virulence factors for pathogenic microbes. Infect Immun 74: 1500-1504.
18. Feldmesser M, Kress Y, Casadevall A, (2001) Dynamic changes in the morphology of Cryptococcus neoformans during murine pulmonary infection. Microbiology 147: 2355-2365.
19. 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.
20. Zaragoza O, Garcia-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodriguez-Tudela JL, et al. (2010) Fungal cell gigantism during mammalian infection. PLoS Pathog 6: e1000945.
21. Apidianakis Y, Rahme LG, Heitman J, Ausubel FM, Calderwood SB, et al. (2004) Challenge of Drosophila melanogaster with Cryptococcus neoformans and role of the innate immune response. Eukaryot Cell 3: 413-419.
22. 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.
23. 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.
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. Steenbergen JN, Nosanchuk JD, Malliaris SD, Casadevall A, (2004) Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect Immun 72: 3478-3488.
26. 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.
27. 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.
28. Fuchs BB, O'Brien E, Khoury JB, Mylonakis E, (2010) Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1: 475-482.
29. 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.
30. Bergin D, Brennan M, Kavanagh K, (2003) Fluctuations in haemocyte density and microbial load may be used as indicators of fungal pathogenicity in larvae of Galleria mellonella. Microbes Infect 5: 1389-1395.
31. Brennan M, Thomas DY, Whiteway M, Kavanagh K, (2002) Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol 34: 153-157.
32. Chrisman CJ, Albuquerque P, Guimaraes AJ, Nieves E, Casadevall A, (2011) Phospholipids Trigger Cryptococcus neoformans Capsular Enlargement during Interactions with Amoebae and Macrophages. PLoS Pathog 7: e1002047.
33. Rodrigues ML, Alvarez M, Fonseca FL, Casadevall A, (2008) Binding of the wheat germ lectin to Cryptococcus neoformans suggests an association of chitinlike structures with yeast budding and capsular glucuronoxylomannan. Eukaryot Cell 7: 602-609.
34. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E, (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71: 2404-2413.
35. Jander G, Rahme LG, Ausubel FM, (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
36. Morton DB, Barnett RI, Chadwick JS, (1984) Structural alterations to Proteus mirabilis as a result of exposure to haemolymph from the larvae of Galleria mellonella. Microbios 39: 177-185.
37. Cytrynska M, Zdybicka-Barabas A, Jakubowicz T, (2007) The involvement of protein kinase A in the immune response of Galleria mellonella larvae to bacteria. Acta Biochim Pol 54: 167-174.
38. Hu K, Li J, Li B, Webster JM, Chen G, (2006) A novel antimicrobial epoxide isolated from larval Galleria mellonella infected by the nematode symbiont, Photorhabdus luminescens (Enterobacteriaceae). Bioorg Med Chem 14: 4677-4681.
39. Reeves EP, Messina CG, Doyle S, Kavanagh K, (2004) Correlation between gliotoxin production and virulence of Aspergillus fumigatus in Galleria mellonella. Mycopathologia 158: 73-79.
40. St Leger RJ, Screen SE, Shams-Pirzadeh B, (2000) Lack of host specialization in Aspergillus flavus. Appl Environ Microbiol 66: 320-324.
41. Tojo S, Naganuma F, Arakawa K, Yokoo S, (2000) Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. J Insect Physiol 46: 1129-1135.
42. Brivio MF, Mastore M, Nappi AJ, (2010) A pathogenic parasite interferes with phagocytosis of insect immunocompetent cells. Dev Comp Immunol 34: 991-998.
43. Dubovskiy IM, Krukova NA, Glupov VV, (2008) Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. J Invertebr Pathol 98: 360-362.
44. Bergin D, Reeves EP, Renwick J, Wientjes FB, Kavanagh K, (2005) Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73: 4161-4170.
45. Cerenius L, Lee BL, Soderhall K, (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29: 263-271.
46. Zaragoza O, Taborda CP, Casadevall A, (2003) The efficacy of complement-mediated phagocytosis of Cryptococcus neoformans is dependent on the location of C3 in the polysaccharide capsule and involves both direct and indirect C3-mediated interactions. Euro J Immnunol 33: 1957-1967.
47. Kozel TR, Gotschlich EC, (1982) The capsule of Cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J Immunol 129: 1675-1680.
48. Kozel TR, Pfrommer GS, Guerlain AS, Highison BA, Highison GJ, (1988) Role of the capsule in phagocytosis of Cryptococcus neoformans. Rev Infect Dis 10 (Suppl 2): S436-439.
49. Feldmesser M, Kress Y, Novikoff P, Casadevall A, (2000) Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect Immun 68: 4225-4237.
50. Zaragoza O, Telzak A, Bryan RA, Dadachova E, Casadevall A, (2006) The polysaccharide capsule of the pathogenic fungus Cryptococcus neoformans enlarges by distal growth and is rearranged during budding. Mol Microbiol 59: 67-83.
51. Charlier C, Chretien F, Baudrimont M, Mordelet E, Lortholary O, et al. (2005) Capsule structure changes associated with Cryptococcus neoformans crossing of the blood-brain barrier. Am J Pathol 166: 421-432.
52. Gates MA, Thorkildson P, Kozel TR, (2004) Molecular architecture of the Cryptococcus neoformans capsule. Mol Microbiol 52: 13-24.
53. Maxson ME, Dadachova E, Casadevall A, Zaragoza O, (2007) Radial mass density, charge, and epitope distribution in the Cryptococcus neoformans capsule. Eukaryot Cell 6: 95-109.
54. Pierini LM, Doering TL, (2001) Spatial and temporal sequence of capsule construction in Cryptococcus neoformans. Mol Microbiol 41: 105-115.
55. Fuchs BB, Mylonakis E, (2006) Using non-mammalian hosts to study fungal virulence and host defense. Curr Opin Microbiol 9: 346-351.
56. London R, Orozco BS, Mylonakis E, (2006) The pursuit of cryptococcal pathogenesis: heterologous hosts and the study of cryptococcal host-pathogen interactions. FEMS Yeast Res 6: 567-573.
57. Steenbergen JN, Casadevall A, (2003) The origin and maintenance of virulence for the human pathogenic fungus Cryptococcus neoformans. Microbes Infect 5: 667-675.
58. Perfect JR, Lang SDR, Durack DT, (1980) Chronic cryptococcal meningitis: a new experimental model in rabbits. Am J Pathol 101: 177-194.
59. 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.
60. Kwon-Chung KJ, (1976) Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68: 821-833.
61. Chang YC, Wickes BL, Kwon-Chung KJ, (1995) Further analysis of the CAP59 locus of Cryptococcus neoformans: structure defined by forced expression and description of a new ribosomal protein-encoding gene. Gene 167: 179-183.
62. Zaragoza O, Casadevall A, (2004) Experimental modulation of capsule size in Cryptococcus neoformans. Biol Proced Online 6: 10-15.
63. Casadevall A, Mukherjee J, Devi SJ, Schneerson R, Robbins JB, et al. (1992) Antibodies elicited by a Cryptococcus neoformans-tetanus toxoid conjugate vaccine have the same specificity as those elicited in infection. J Infect Dis 165: 1086-1093.
64. Zaragoza O, Alvarez M, Telzak A, Rivera J, Casadevall A, (2007) The relative susceptibility of mouse strains to pulmonary Cryptococcus neoformans infection is associated with pleiotropic differences in the immune response. Infect Immun 75: 2729-2739.