Differential Adaptation of Candida albicans In Vivo Modulates Immune Recognition by Dectin-1

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Marakalala, Mohlopheni J ^a,g   Vautier, Simon ^b   Potrykus, Joanna ^b   Walker, Louise A ^b   Shepardson, Kelly M ^c   Hopke, Alex ^d   Mora Montes, Hector M ^b,h   Kerrigan, Ann ^b   Netea, Mihai G ^e   Murray, Graeme I ^f   MacCallum, Donna M ^b   Wheeler, Robert ^d   Munro, Carol A ^b   Gow, Neil A R ^b   Cramer, Robert A ^c   Brown, Alistair J P ^b   Brown, Gordon D ^a,b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MAINE   (United States)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

^g HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^h UNIVERSITY OF GUANAJUATO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; CASPOFUNGIN; CHITIN; CYTOKINE; DECTIN 1; IMMUNOGLOBULIN G;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL SUSCEPTIBILITY; ANTIGEN RECOGNITION; ARTICLE; BIOCHEMICAL COMPOSITION; CANDIDA ALBICANS; CANDIDIASIS; CONTROLLED STUDY; DRUG EXPOSURE; FUNGAL CELL WALL; GENE EXPRESSION; HYPOXIA; IMMUNE DYSREGULATION; IMMUNE SYSTEM; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PATHOGEN LOAD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIFUNGAL AGENTS; BETA-GLUCANS; CANDIDA ALBICANS; CELL WALL; CHITIN; ECHINOCANDINS; LECTINS, C-TYPE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, PATTERN RECOGNITION;

CANDIDA ALBICANS; FUNGI;

EID: 84876848564     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003315     Document Type: Article

References (48)

1. Brown GD, Denning DW, Gow NA, Netea MG, White T, (2012) Human fungal infections: The Hidden Killers. Sci Transl Med 4: 165rv113.
2. Hernandez-Santos N, Gaffen SL, (2012) Th17 cells in immunity to Candida albicans. Cell Host and Microbe 11: 425-435.
3. Hardison SE, Brown GD, (2012) C-type lectin receptors orchestrate antifungal immunity. Nat Immunol 13: 817-822.
4. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, et al. (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336: 1314-1317.
5. Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, et al. (2009) Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361: 1760-1767.
6. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, et al. (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8: 31-38.
7. Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, et al. (2009) An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5: 487-497.
8. Gales A, Conduche A, Bernad J, Lefevre L, Olagnier D, et al. (2010) PPARgamma controls dectin-1 expression required for host antifungal defense against Candida albicans. PLoS Pathog 6: e1000714.
9. Carvalho A, Giovannini G, De Luca A, D'Angelo C, Casagrande A, et al. (2012) Dectin-1 isoforms contribute to distinct Th1/Th17 cell activation in mucosal candidiasis. Cell Mol Immunol 9: 276-286.
10. Werner JL, Metz AE, Horn D, Schoeb TR, Hewitt MM, et al. (2009) Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182: 4938-4946.
11. Saijo S, Fujikado N, Furuta T, Chung SH, Kotaki H, et al. (2007) Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 8: 39-46.
12. Netea MG, Gow NA, Joosten LA, Verschueren I, van der Meer JW, et al. (2010) Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 48: 897-903.
13. Heinsbroek SE, taylor PR, Rosas M, Willment JA, Williams DL, et al. (2006) Expression of functionally different Dectin-1 isoforms by murine macrophages. J Immunol 176: 5513-5518.
14. Whiley RA, Cruchley AT, Gore C, Hagi-Pavli E, (2012) Candida albicans strain-dependent modulation of pro-inflammatory cytokine release by in vitro oral and vaginal mucosal models. Cytokine 57: 89-97.
15. Odds FC, Bougnoux ME, Shaw DJ, Bain JM, Davidson AD, et al. (2007) Molecular phylogenetics of Candida albicans. Eukaryot Cell 6: 1041-1052.
16. Gantner BN, Simmons RM, Underhill DM, (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. Embo J 24: 1277-1286.
17. Wheeler RT, Kombe D, Agarwala SD, Fink GR, (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4: e1000227.
18. Shepardson KM, Ngo LY, Aimanianda V, Latge JP, Barker BM, et al. (2012) Hypoxia enhances innate immune activation to Aspergillus fumigatus through cell wall modulation. Microbes Infect In Press.
19. Netea MG, Brown GD, Kullberg BJ, Gow NA, (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6: 67-78.
20. Mora-Montes HM, Netea MG, Ferwerda G, Lenardon MD, Brown GD, et al. (2011) Recognition and blocking of innate immunity cells by Candida albicans chitin. Infect Immun 79: 1961-1970.
21. Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, et al. (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45: 1404-1414.
22. Lee KK, Maccallum DM, Jacobsen MD, Walker LA, Odds FC, et al. (2012) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56: 208-217.
23. Hector RF, Domer JE, Carrow EW, (1982) Immune responses to Candida albicans in genetically distinct mice. Infect Immun 38: 1020-1028.
24. Ashman RB, Fulurija A, Papadimitriou JM, (1996) Strain-dependent differences in host response to Candida albicans infection in mice are related to organ susceptibility and infectious load. Infect Immun 64: 1866-1869.
25. Del Pilar Jimenez AM, Viriyakosol S, Walls L, Datta SK, Kirkland T, et al. (2008) Susceptibility to Coccidioides species in C57BL/6 mice is associated with expression of a truncated splice variant of Dectin-1 (Clec7a). Genes Immun 9: 338-348.
26. MacCallum DM, Castillo L, Nather K, Munro CA, Brown AJ, et al. (2009) Property differences among the four major Candida albicans strain clades. Eukaryot Cell 8: 373-387.
27. Odds FC, (2010) Molecular phylogenetics and epidemiology of Candida albicans. Future Microbiol 5: 67-79.
28. Synnott JM, Guida A, Mulhern-Haughey S, Higgins DG, Butler G, (2010) Regulation of the hypoxic response in Candida albicans. Eukaryot Cell 9: 1734-1746.
29. Grahl N, Shepardson KM, Chung D, Cramer RA, (2012) Hypoxia and fungal pathogenesis: to air or not to air? Eukaryot Cell 11: 560-570.
30. Sosinska GJ, de Groot PW, Teixeira de Mattos MJ, Dekker HL, de Koster CG, et al. (2008) Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154: 510-520.
31. Murciano C, Villamon E, Gozalbo D, Roig P, O'Connor JE, et al. (2006) Toll-like receptor 4 defective mice carrying point or null mutations do not show increased susceptibility to Candida albicans in a model of hematogenously disseminated infection. Med Mycol 44: 149-157.
32. Netea MG, Van Der Graaf CA, Vonk AG, Verschueren I, Van Der Meer JW, et al. (2002) The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J Infect Dis 185: 1483-1489.
33. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, et al. (2004) The contribution of the toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 172: 3059-3069.
34. Adams EL, Rice PJ, Graves B, Ensley HE, Yu H, et al. (2008) Differential high affinity interaction of Dectin-1 with natural or synthetic glucans is dependent upon primary structure and is influenced by polymer chain length and side chain branching. J Pharmacol Exp Ther 325: 115-123.
35. Palma AS, Feizi T, Zhang Y, Stoll MS, Lawson AM, et al. (2006) Ligands for the beta-glucan receptor, Dectin-1, assigned using "designer" microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J Biol Chem 281: 5771-5779.
36. Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, et al. (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4: e1000040.
37. Staib P, Kretschmar M, Nichterlein T, Hof H, Morschhauser J, (2000) Differential activation of a Candida albicans virulence gene family during infection. Proc Natl Acad Sci U S A 97: 6102-6107.
38. Lorenz MC, Bender JA, Fink GR, (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087.
39. Thewes S, Kretschmar M, Park H, Schaller M, Filler SG, et al. (2007) In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol Microbiol 63: 1606-1628.
40. Walker LA, Maccallum DM, Bertram G, Gow NA, Odds FC, et al. (2009) Genome-wide analysis of Candida albicans gene expression patterns during infection of the mammalian kidney. Fungal Genet Biol 46: 210-219.
41. Andes D, Lepak A, Pitula A, Marchillo K, Clark J, (2005) A simple approach for estimating gene expression in Candida albicans directly from a systemic infection site. J Infect Dis 192: 893-900.
42. Arroyo J, Sarfati J, Baixench MT, Ragni E, Guillen M, et al. (2007) The GPI-anchored Gas and Crh families are fungal antigens. Yeast 24: 289-296.
43. Liu TT, Lee RE, Barker KS, Wei L, Homayouni R, et al. (2005) Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Chemother 49: 2226-2236.
44. Garcia R, Bermejo C, Grau C, Perez R, Rodriguez-Pena JM, et al. (2004) The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 279: 15183-15195.
45. Lenardon MD, Whitton RK, Munro CA, Marshall D, Gow NA, (2007) Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol Microbiol 66: 1164-1173.
46. Drakulovski P, Dunyach C, Bertout S, Reynes J, Mallie M, (2011) A Candida albicans strain with high MIC for caspofungin and no FKS1 mutations exhibits a high chitin content and mutations in two chitinase genes. Med Mycol 49: 467-474.
47. Mora-Montes HM, Bates S, Netea MG, Diaz-Jimenez DF, Lopez-Romero E, et al. (2007) Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal host-fungus interaction. Eukaryot Cell 6: 2184-2193.
48. Graham LM, Tsoni SV, Willment JA, Williams DL, Taylor PR, et al. (2006) Soluble Dectin-1 as a tool to detect beta-glucans. J Immunol Methods 314: 164-169.