Kinetic studies of Candida parapsilosis phagocytosis by macrophages and detection of intracellular survival mechanisms

Frontiers in Microbiology

Volumn 5, Issue NOV, 2014, Pages

  Tóth, Renáta ^a   Tóth, Adél ^a   Papp, Csaba ^a   Jankovics, Ferenc ^b   Vágvölgyi, Csaba ^a   Alonso, Maria F ^c   Bain, Judith M ^c   Erwig, Lars Peter ^c   Gácser, Attila ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Candida parapsilosis; Intracellular survival mechanisms; Phagocytic stages; Pseudohypha uptake; Video microscopy

Indexed keywords

ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; CANDIDA PARAPSILOSIS; CELL KILLING; CELL PHAGOCYTOSIS; CONFOCAL MICROSCOPY; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; KINETIC PARAMETERS; MACROPHAGE; MACROPHAGE MIGRATION; MITOSIS; MOUSE; NONHUMAN; NORMAL HUMAN; STAINING; SURVIVAL RATE; ULTRAVIOLET IRRADIATION; VIDEO MICROSCOPY; YEAST CELL;

EID: 84987806912     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00633     Document Type: Article

References (39)

1. Bain, J. M., Lewis, L. E., Okai, B., Quinn, J., Gow, N. A., and Erwig, L. P. (2012). Non-lytic expulsion/exocytosis of Candida albicans from macrophages. Fungal Genet. Biol. 49, 677-678. doi: 10.1016/j.fgb.2012.01.008
2. Barelle, C. J., Manson, C. L., Maccallum, D. M., Odds, F. C., Gow, N. A., and Brown, A. J. (2004). GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 21, 333-340. doi: 10.1002/yea.1099
3. Benjamin, D. K., Delong, E., Cotten, C. M., Garges, H. P., Steinbach, W. J., and Clark, R. H. (2004). Mortality following blood culture in premature infants: increased with Gram-negative bacteremia and candidemia, but not Gram-positive bacteremia. J. Perinatol. 24, 175-180. doi: 10.1038/sj.jp.7211068
4. Brown, G. D. (2011). Innate antifungal immunity: the key role of phagocytes. Annu. Rev. Immunol. 29, 1-21. doi: 10.1146/annurev-immunol-030409-101229
5. Brunke, S., and Hube, B. (2013). Two unlike cousins: Candida albicans and C. glabrata infection strategies. Cell. Microbiol. 15, 701-708. doi: 10.1111/cmi.12091
6. Chow, B. D., Linden, J. R., and Bliss, J. M. (2012). Candida parapsilosis and the neonate: epidemiology, virulence and host defense in a unique patient setting. Expert Rev. Anti Infect. Ther. 10, 935-946. doi: 10.1586/eri.12.74
7. Csank, C., and Haynes, K. (2000). Candida glabrata displays pseudohyphal growth. FEMS Microbiol. Lett. 189, 115-120. doi: 10.1111/j.1574-6968.2000.tb09216.x
8. Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., et al. (2004). Genome evolution in yeasts. Nature 430, 35-44. doi: 10.1038/nature02579
9. Fidel, P. L. Jr., Vazquez, J. A., and Sobel, J. D. (1999). Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin. Microbiol. Rev. 12, 80-96.
10. Foster, N., Symes, C., Barton, R., and Hobson, R. (2007). Rapid identification of Candida glabrata in Candida bloodstream infections. J. Med. Microbiol. 56, 1639-1643. doi: 10.1099/jmm.0.47406-0
11. Gillum, A. M., Tsay, E. Y., and Kirsch, D. R. (1984). Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198, 179-182. doi: 10.1007/BF00328721
12. Guinea, J. (2014). Global trends in the distribution of Candida species causing candidemia. Clin. Microbiol. Infect. 20(Suppl. 6), 5-10. doi: 10.1111/1469-0691.12539
13. Hays, C., Duhamel, C., Cattoir, V., and Bonhomme, J. (2011). Rapid and accurate identification of species belonging to the Candida parapsilosis complex by real-time PCR and melting curve analysis. J. Med. Microbiol. 60, 477-480. doi: 10.1099/jmm.0.026633-0
14. Holland, L. M., Schroder, M. S., Turner, S. A., Taff, H., Andes, D., Grozer, Z., et al. (2014). Comparative phenotypic analysis of the major fungal pathogens Candida parapsilosis and Candida albicans. PLoS Pathog. 10:e1004365. doi: 10.1371/journal.ppat.1004365
15. Hummert, S., Hummert, C., Schroter, A., Hube, B., and Schuster, S. (2010). Game theoretical modelling of survival strategies of Candida albicans inside macrophages. J. Theor. Biol. 264, 312-318. doi: 10.1016/j.jtbi.2010.01.022
16. Jong, A. Y., Stins, M. F., Huang, S. H., Chen, S. H., and Kim, K. S. (2001). Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immun. 69, 4536-4544. doi: 10.1128/IAI.69.7.4536-4544.2001
17. Laffey, S. F., and Butler, G. (2005). Phenotype switching affects biofilm formation by Candida parapsilosis. Microbiology 151, 1073-1081. doi: 10.1099/mic.0.27739-0
18. Lewis, L. E., Bain, J. M., Lowes, C., Gillespie, C., Rudkin, F. M., Gow, N. A., et al. (2012a). Stage specific assessment of Candida albicans phagocytosis by macrophages identifies cell wall composition and morphogenesis as key determinants. PLoS Pathog. 8:e1002578. doi: 10.1371/journal.ppat.1002578
19. Lewis, L. E., Bain, J. M., Lowes, C., Gow, N. A., and Erwig, L. P. (2012b). Candida albicans infection inhibits macrophage cell division and proliferation. Fungal Genet. Biol. 49, 679-680. doi: 10.1016/j.fgb.2012.05.007
20. Lewis, L. E., Bain, J. M., Okai, B., Gow, N. A., and Erwig, L. P. (2013). Live-cell video microscopy of fungal pathogen phagocytosis. J. Vis. Exp. 71:e50196. doi: 10.3791/50196
21. Lo, H. J., Kohler, J. R., Didomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G. R. (1997). Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949. doi: 10.1016/S0092-8674(00)80358-X
22. Malani, A., Hmoud, J., Chiu, L., Carver, P. L., Bielaczyc, A., and Kauffman, C. A. (2005). Candida glabrata fungemia: experience in a tertiary care center. Clin. Infect. Dis. 41, 975-981. doi: 10.1086/432939
23. Mckenzie, C. G., Koser, U., Lewis, L. E., Bain, J. M., Mora-Montes, H. M., Barker, R. N., et al. (2010). Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect. Immun. 78, 1650-1658. doi: 10.1128/IAI.00001-10
24. Nemeth, T., Toth, A., Hamari, Z., Falus, A., Eder, K., Vagvolgyi, C., et al. (2014). Transcriptome profile of the murine macrophage cell response to Candida parapsilosis. Fungal Genet. Biol. 65, 48-56. doi: 10.1016/j.fgb.2014.01.006
25. Nemeth, T., Toth, A., Szenzenstein, J., Horvath, P., Nosanchuk, J. D., Grozer, Z., et al. (2013). Characterization of virulence properties in the C. parapsilosis sensu lato species. PLoS ONE 8:e68704. doi: 10.1371/journal.pone.0068704
26. Pfaller, M. A., and Diekema, D. J. (2007). Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163. doi: 10.1128/CMR.00029-06
27. Quindos, G. (2014). Epidemiology of candidaemia and invasive candidiasis. A changing face. Rev. Iberoam. Micol. 31, 42-48. doi: 10.1016/j.riam.2013.10.001
28. Reuss, O., Vik, A., Kolter, R., and Morschhauser, J. (2004). The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341, 119-127. doi: 10.1016/j.gene.2004.06.021
29. Roetzer, A., Gratz, N., Kovarik, P., and Schuller, C. (2010). Autophagy supports Candida glabrata survival during phagocytosis. Cell. Microbiol. 12, 199-216. doi: 10.1111/j.1462-5822.2009.01391.x
30. Rudkin, F. M., Bain, J. M., Walls, C., Lewis, L. E., Gow, N. A., and Erwig, L. P. (2013). Altered dynamics of Candida albicans phagocytosis by macrophages and PMNs when both phagocyte subsets are present. MBio 4, e00810-00813. doi: 10.1128/mBio.00810-13
31. Schafer, K., Bain, J. M., Di Pietro, A., Gow, N. A., and Erwig, L. P. (2014). Hyphal growth of phagocytosed Fusarium oxysporum causes cell lysis and death of murine macrophages. PLoS ONE 9:e101999. doi: 10.1371/journal.pone.0101999
32. Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., et al. (2011). The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J. Immunol. 187, 3072-3086. doi: 10.4049/jimmunol.1003730
33. Seider, K., Gerwien, F., Kasper, L., Allert, S., Brunke, S., Jablonowski, N., et al. (2014). Immune evasion, stress resistance, and efficient nutrient acquisition are crucial for intracellular survival of Candida glabrata within macrophages. Eukaryotic Cell 13, 170-183. doi: 10.1128/EC.00262-13
34. Toth, A., Csonka, K., Jacobs, C., Vagvolgyi, C., Nosanchuk, J. D., Netea, M. G., et al. (2013). Candida albicans and Candida parapsilosis induce different T-cell responses in human peripheral blood mononuclear cells. J. Infect. Dis. 208, 690-698. doi: 10.1093/infdis/jit188
35. Toth, A., Nemeth, T., Csonka, K., Horvath, P., Vagvolgyi, C., Vizler, C., et al. (2014). Secreted Candida parapsilosis lipase modulates the immune response of primary human macrophages. Virulence 5, 555-562. doi: 10.4161/viru.28509
36. Trofa, D., Gacser, A., and Nosanchuk, J. D. (2008). Candida parapsilosis, an emerging fungal pathogen. Clin. Microbiol. Rev. 21, 606-625. doi: 10.1128/CMR.00013-08
37. Vylkova, S., and Lorenz, M. C. (2014). Modulation of phagosomal pH by Candida albicans promotes hyphal morphogenesis and requires Stp2p, a regulator of amino acid transport. PLoS Pathog. 10:e1003995. doi: 10.1371/journal.ppat.1003995
38. Wellington, M., Koselny, K., and Krysan, D. J. (2012). Candida albicans morphogenesis is not required for macrophage interleukin 1beta production. MBio 4, e00433-e00412. doi: 10.1128/mBio.00433-12
39. Wellington, M., Koselny, K., Sutterwala, F. S., and Krysan, D. J. (2014). Candida albicans triggers NLRP3-mediated pyroptosis in macrophages. Eukaryotic Cell 13, 329-340. doi: 10.1128/EC.00336-13