Striking a balance: Fungal commensalism versus pathogenesis

Current Opinion in Microbiology

Volumn 16, Issue 3, 2013, Pages 366-373

  Iliev, Iliyan D ^a   Underhill, David M ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ASPERGILLUS; CANDIDA; COMMENSALISM; CRYPTOCOCCUS; CYTOKINE PRODUCTION; IMMUNE RESPONSE; INVASIVE ASPERGILLOSIS; MUCOSAL IMMUNITY; MYCOSIS; NONHUMAN; PATHOGENESIS; PNEUMOCYSTIS; REVIEW; T LYMPHOCYTE;

FUNGI;

EID: 84881550589     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.05.004     Document Type: Review

References (72)

1. Brown G.D., Denning D.W., Gow N.A., Levitz S.M., Netea M.G., White T.C. Hidden killers: human fungal infections. Sci Transl Med 2012, 4:165rv113.
2. Hardison S.E., Brown G.D. C-type lectin receptors orchestrate antifungal immunity. Nat Immunol 2012, 13:817-822.
3. Romani L. Immunity to fungal infections. Nat Rev Immunol 2011, 11:275-288.
4. Steele C., Wormley F.L. Immunology of fungal infections: lessons learned from animal models. Curr Opin Microbiol 2012, 15:413-419.
5. Vinh D.C. Insights into human antifungal immunity from primary immunodeficiencies. Lancet Infect Dis 2011, 11:780-792.
6. Shapiro S., Beenhouwer D.O., Feldmesser M., Taborda C., Carroll M.C., Casadevall A., Scharff M.D. Immunoglobulin g monoclonal antibodies to Cryptococcus neoformans protect mice deficient in complement component c3. Infect Immun 2002, 70:2598-2604.
7. Held K., Thiel S., Loos M., Petry F. Increased susceptibility of complement factor b/c2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 2008, 45:3934-3941.
8. Babula O., Lazdane G., Kroica J., Ledger W.J., Witkin S.S. Relation between recurrent vulvovaginal candidiasis, vaginal concentrations of mannose-binding lectin, and a mannose-binding lectin gene polymorphism in latvian women. Clin Infect Dis 2003, 37:733-737.
9. Kaur S., Gupta V.K., Shah A., Thiel S., Sarma P.U., Madan T. Elevated levels of mannan-binding lectin (mbl) and eosinophilia in patients of bronchial asthma with allergic rhinitis and allergic bronchopulmonary aspergillosis associate with a novel intronic polymorphism in mbl. Clin Exp Immunol 2006, 143:414-419.
10. Steele C., Marrero L., Swain S., Harmsen A.G., Zheng M., Brown G.D., Gordon S., Shellito J.E., Kolls J.K. Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the dectin-1 beta-glucan receptor. J Exp Med 2003, 198:1677-1688.
11. Saijo S., Fujikado N., Furuta T., Chung S.H., Kotaki H., Seki K., Sudo K., Akira S., Adachi Y., Ohno N., Kinjo T., et al. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 2007, 8:39-46.
12. Rivera A., Hohl T.M., Collins N., Leiner I., Gallegos A., Saijo S., Coward J.W., Iwakura Y., Pamer E.G. Dectin-1 diversifies Aspergillus fumigatus-specific t cell responses by inhibiting t helper type 1 cd4 t cell differentiation. J Exp Med 2011, 208:369-381.
13. Gessner M.A., Werner J.L., Lilly L.M., Nelson M.P., Metz A.E., Dunaway C.W., Chan Y.R., Ouyang W., Brown G.D., Weaver C.T., Steele C. Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect Immun 2012, 80:410-417.
14. Iliev I.D., Funari V.A., Taylor K.D., Nguyen Q., Reyes C.N., Strom S.P., Brown J., Becker C.A., Fleshner P.R., Dubinsky M., Rotter J.I., et al. Interactions between commensal fungi and the c-type lectin receptor dectin-1 influence colitis. Science 2012, 336:1314-1317.
15. Ferwerda B., Ferwerda G., Plantinga T.S., Willment J.A., van Spriel A.B., Venselaar H., Elbers C.C., Johnson M.D., Cambi A., Huysamen C., Jacobs L., et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 2009, 361:1760-1767.
16. Cunha C., Di Ianni M., Bozza S., Giovannini G., Zagarella S., Zelante T., D'Angelo C., Pierini A., Pitzurra L., Falzetti F., Carotti A., et al. Dectin-1 y238x polymorphism associates with susceptibility to invasive aspergillosis in hematopoietic transplantation through impairment of both recipient-dependent and donor-dependent mechanisms of antifungal immunity. Blood 2010, 116:5394-5402.
17. Saijo S., Ikeda S., Yamabe K., Kakuta S., Ishigame H., Akitsu A., Fujikado N., Kusaka T., Kubo S., Chung S.H., Komatsu R., et al. Dectin-2 recognition of alpha-mannans and induction of th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010, 32:681-691.
18. Wells C.A., Salvage-Jones J.A., Li X., Hitchens K., Butcher S., Murray R.Z., Beckhouse A.G., Lo Y.L., Manzanero S., Cobbold C., Schroder K., et al. The macrophage-inducible c-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 2008, 180:7404-7413.
19. van de Veerdonk F.L., Kullberg B.J., van der Meer J.W., Gow N.A., Netea M.G. Host-microbe interactions: innate pattern recognition of fungal pathogens. Curr Opin Microbiol 2008, 11:305-312.
20. Bellocchio S., Montagnoli C., Bozza S., Gaziano R., Rossi G., Mambula S.S., Vecchi A., Mantovani A., Levitz S.M., Romani L. The contribution of the toll-like/il-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 2004, 172:3059-3069.
21. Bochud P.Y., Chien J.W., Marr K.A., Leisenring W.M., Upton A., Janer M., Rodrigues S.D., Li S., Hansen J.A., Zhao L.P., Aderem A., et al. Toll-like receptor 4 polymorphisms and aspergillosis in stem-cell transplantation. N Engl J Med 2008, 359:1766-1777.
22. Carvalho A., Pasqualotto A.C., Pitzurra L., Romani L., Denning D.W., Rodrigues F. Polymorphisms in toll-like receptor genes and susceptibility to pulmonary aspergillosis. J Infect Dis 2008, 197:618-621.
23. Kesh S., Mensah N.Y., Peterlongo P., Jaffe D., Hsu K.M., O'Reilly V.D.B., Pamer R., Satagopan E., Papanicolaou J.G.A. Tlr1 and tlr6 polymorphisms are associated with susceptibility to invasive aspergillosis after allogeneic stem cell transplantation. Ann N Y Acad Sci 2005, 1062:95-103.
24. Picard C., von Bernuth H., Ghandil P., Chrabieh M., Levy O., Arkwright P.D., McDonald D., Geha R.S., Takada H., Krause J.C., Creech C.B., et al. Clinical features and outcome of patients with irak-4 and myd88 deficiency. Medicine (Baltimore) 2010, 89:403-425.
25. Gross O., Gewies A., Finger K., Schafer M., Sparwasser T., Peschel C., Forster I., Ruland J. Card9 controls a non-tlr signalling pathway for innate anti-fungal immunity. Nature 2006, 442:651-656.
26. LeibundGut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., Schweighoffer E., Tybulewicz V., Brown G.D., Ruland J., Reis e Sousa C. Syk- and card9-dependent coupling of innate immunity to the induction of t helper cells that produce interleukin 17. Nat Immunol 2007, 8:630-638.
27. Glocker E.O., Hennigs A., Nabavi M., Schaffer A.A., Woellner C., Salzer U., Pfeifer D., Veelken H., Warnatz K., Tahami F., Jamal S., et al. A homozygous card9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009, 361:1727-1735.
28. Aratani Y., Koyama H., Nyui S., Suzuki K., Kura F., Maeda N. Severe impairment in early host defense against Candida albicans in mice deficient in myeloperoxidase. Infect Immun 1999, 67:1828-1836.
29. Pollock J.D., Williams D.A., Gifford M.A., Li L.L., Du X., Fisherman J., Orkin S.H., Doerschuk C.M., Dinauer M.C. Mouse model of x-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 1995, 9:202-209.
30. Dinauer M.C., Orkin S.H. Chronic granulomatous disease. Annu Rev Med 1992, 43:117-124.
31. Gross O., Poeck H., Bscheider M., Dostert C., Hannesschlager N., Endres S., Hartmann G., Tardivel A., Schweighoffer E., Tybulewicz V., Mocsai A., et al. Syk kinase signalling couples to the nlrp3 inflammasome for anti-fungal host defence. Nature 2009, 459:433-436.
32. Hise A.G., Tomalka J., Ganesan S., Patel K., Hall B.A., Brown G.D., Fitzgerald K.A. An essential role for the nlrp3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 2009, 5:487-497.
33. Lev-Sagie A., Prus D., Linhares I.M., Lavy Y., Ledger W.J., Witkin S.S. Polymorphism in a gene coding for the inflammasome component nalp3 and recurrent vulvovaginal candidiasis in women with vulvar vestibulitis syndrome. Am J Obstet Gynecol 2009, 200:303.e301-303.e306.
34. Conti H.R., Shen F., Nayyar N., Stocum E., Sun J.N., Lindemann M.J., Ho A.W., Hai J.H., Yu J.J., Jung J.W., Filler S.G., et al. Th17 cells and il-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 2009, 206:299-311.
35. Kagami S., Rizzo H.L., Kurtz S.E., Miller L.S., Blauvelt A. Il-23 and il-17a, but not il-12 and il-22, are required for optimal skin host defense against Candida albicans. J Immunol 2010, 185:5453-5462.
36. Gladiator A., Wangler N., Trautwein-Weidner K., LeibundGut-Landmann S. Cutting edge: Il-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol 2012, 190:521-525.
37. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M., Gumbleton M., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332:65-68.
38. Puel A., Doffinger R., Natividad A., Chrabieh M., Barcenas-Morales G., Picard C., Cobat A., Ouachee-Chardin M., Toulon A., Bustamante J., Al-Muhsen S., et al. Autoantibodies against il-17a, il-17f, and il-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type i. J Exp Med 2010, 207:291-297.
39. De Luca A., Zelante T., D'Angelo C., Zagarella S., Fallarino F., Spreca A., Iannitti R.G., Bonifazi P., Renauld J.C., Bistoni F., Puccetti P., et al. Il-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol 2010, 3:361-373.
40. Vonk A.G., Netea M.G., van Krieken J.H., Iwakura Y., van der Meer J.W., Kullberg B.J. Endogenous interleukin (il)-1 alpha and il-1 beta are crucial for host defense against disseminated candidiasis. J Infect Dis 2006, 193:1419-1426.
41. Denning D.W., O'Driscoll B.R., Hogaboam C.M., Bowyer P., Niven R.M. The link between fungi and severe asthma: a summary of the evidence. Eur Respir J 2006, 27:615-626.
42. Pearlman E., Sun Y., Roy S., Karmakar M., Hise A.G., Szczotka-Flynn L., Ghannoum M., Chinnery H.R., McMenamin P.G., Rietsch A. Host defense at the ocular surface. Int Rev Immunol 2013, 32:4-18.
43. Hohl T.M., Van Epps H.L., Rivera A., Morgan L.A., Chen P.L., Feldmesser M., Pamer E.G. Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 2005, 1:e30.
44. Gersuk G.M., Underhill D.M., Zhu L., Marr K.A. Dectin-1 and tlrs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J Immunol 2006, 176:3717-3724.
45. Faro-Trindade I., Willment J.A., Kerrigan A.M., Redelinghuys P., Hadebe S., Reid D.M., Srinivasan N., Wainwright H., Lang D.M., Steele C., Brown G.D. Characterisation of innate fungal recognition in the lung. PLoS ONE 2012, 7:e35675.
46. Grimm M.J., Vethanayagam R.R., Almyroudis N.G., Dennis C.G., Khan A.N., D'Auria A.C., Singel K.L., Davidson B.A., Knight P.R., Blackwell T.S., Hohl T.M., et al. Monocyte- and macrophage-targeted nadph oxidase mediates antifungal host defense and regulation of acute inflammation in mice. J Immunol 2013, 190:4175-4184.
47. Lass-Florl C., Roilides E., Loffler J., Wilflingseder D., Romani L. Minireview: host defence in invasive aspergillosis. Mycoses 2013, 10.1111/myc.12052.
48. Lilly L.M., Gessner M.A., Dunaway C.W., Metz A.E., Schwiebert L., Weaver C.T., Brown G.D., Steele C. The beta-glucan receptor dectin-1 promotes lung immunopathology during fungal allergy via il-22. J Immunol 2012, 189:3653-3660.
49. Rohatgi S., Pirofski L.A. Molecular characterization of the early b cell response to pulmonary Cryptococcus neoformans infection. J Immunol 2012, 189:5820-5830.
50. Cordero R.J., Pontes B., Frases S., Nakouzi A.S., Nimrichter L., Rodrigues M.L., Viana N.B., Casadevall A. Antibody binding to Cryptococcus neoformans impairs budding by altering capsular mechanical properties. J Immunol 2013, 190:317-323.
51. Manoloff E.S., Francioli P., Taffe P., Van Melle G., Bille J., Hauser P.M. Risk for Pneumocystis carinii transmission among patients with pneumonia: a molecular epidemiology study. Emerg Infect Dis 2003, 9:132-134.
52. Thomas C.F., Limper A.H. Current insights into the biology and pathogenesis of pneumocystis pneumonia. Nat Rev Microbiol 2007, 5:298-308.
53. Rapaka R.R., Ricks D.M., Alcorn J.F., Chen K., Khader S.A., Zheng M., Plevy S., Bengten E., Kolls J.K. Conserved natural igm antibodies mediate innate and adaptive immunity against the opportunistic fungus pneumocystis murina. J Exp Med 2010, 207:2907-2919.
54. Limper A.H., Hoyte J.S., Standing J.E. The role of alveolar macrophages in Pneumocystis carinii degradation and clearance from the lung. J Clin Invest 1997, 99:2110-2117.
55. Wachtler B., Wilson D., Haedicke K., Dalle F., Hube B. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS ONE 2011, 6:e17046.
56. Ghannoum M.A., Jurevic R.J., Mukherjee P.K., Cui F., Sikaroodi M., Naqvi A., Gillevet P.M. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 2010, 6:e1000713.
57. White S.J., Rosenbach A., Lephart P., Nguyen D., Benjamin A., Tzipori S., Whiteway M., Mecsas J., Kumamoto C.A. Self-regulation of Candida albicans population size during gi colonization. PLoS Pathog 2007, 3:e184.
58. Enoch D.A., Ludlam H.A., Brown N.M. Invasive fungal infections: a review of epidemiology and management options. J Med Microbiol 2006, 55:809-818.
59. Dwivedi P., Thompson A., Xie Z., Kashleva H., Ganguly S., Mitchell A.P., Dongari-Bagtzoglou A. Role of bcr1-activated genes hwp1 and hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE 2011, 6:e16218.
60. Bendel C.M., Hostetter M.K. Distinct mechanisms of epithelial adhesion for Candida albicans and Candida tropicalis. Identification of the participating ligands and development of inhibitory peptides. J Clin Invest 1993, 92:1840-1849.
61. Dongari-Bagtzoglou A., Kashleva H., Dwivedi P., Diaz P., Vasilakos J. Characterization of mucosal Candida albicans biofilms. PLoS ONE 2009, 4:e7967.
62. Zipfel P.F., Wurzner R., Skerka C. Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol Immunol 2007, 44:3850-3857.
63. Naglik J.R., Fidel P.L., Odds F.C. Animal models of mucosal candida infection. FEMS Microbiol Lett 2008, 283:129-139.
64. Mason K.L., Erb Downward J.R., Falkowski N.R., Young V.B., Kao J.Y., Huffnagle G.B. Interplay between the gastric bacterial microbiota and Candida albicans during postantibiotic recolonization and gastritis. Infect Immun 2011, 80:150-158.
65. Ott S.J., Kuhbacher T., Musfeldt M., Rosenstiel P., Hellmig S., Rehman A., Drews O., Weichert W., Timmis K.N., Schreiber S. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol 2008, 43:831-841.
66. Hamad I., Sokhna C., Raoult D., Bittar F. Molecular detection of eukaryotes in a single human stool sample from senegal. PLoS ONE 2012, 7:e40888.
67. Scanlan P.D., Marchesi J.R. Micro-eukaryotic diversity of the human distal gut microbiota: Qualitative assessment using culture-dependent and -independent analysis of faeces. ISME J 2008, 2:1183-1193.
68. McFarland L.V., Surawicz C.M., Greenberg R.N., Fekety R., Elmer G.W., Moyer K.A., Melcher S.A., Bowen K.E., Cox J.L., Noorani Z., et al. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA 1994, 271:1913-1918.
69. Castagliuolo I., LaMont J.T., Nikulasson S.T., Pothoulakis C. Saccharomyces boulardii protease inhibits Clostridium difficile toxin an effects in the rat ileum. Infect Immun 1996, 64:5225-5232.
70. Martins F.S., Dalmasso G., Arantes R.M., Doye A., Lemichez E., Lagadec P., Imbert V., Peyron J.F., Rampal P., Nicoli J.R., Czerucka D. Interaction of Saccharomyces boulardii with salmonella enterica serovar typhimurium protects mice and modifies t84 cell response to the infection. PLoS ONE 2010, 5:e8925.
71. Thomas S., Metzke D., Schmitz J., Dorffel Y., Baumgart D.C. Anti-inflammatory effects of Saccharomyces boulardii mediated by myeloid dendritic cells from patients with Crohn's disease and ulcerative colitis. Am J Physiol Gastrointest Liver Physiol 2011, 301:G1083-G1092.
72. Dalmasso G., Cottrez F., Imbert V., Lagadec P., Peyron J.F., Rampal P., Czerucka D., Groux H., Foussat A., Brun V. Saccharomyces boulardii inhibits inflammatory bowel disease by trapping t cells in mesenteric lymph nodes. Gastroenterology 2006, 131:1812-1825.