Cryptococcus gattii infection dampens Th1 and Th17 responses by attenuating dendritic cell function and pulmonary chemokine expression in the immunocompetent hosts

Infection and Immunity

Volumn 82, Issue 9, 2014, Pages 3880-3890

  Angkasekwinai, Pornpimon ^a   Sringkarin, Nuntarat ^a   Supasorn, Oratai ^a   Fungkrajai, Madtika ^a   Wang, Yui Hsi ^b   Chayakulkeeree, Methee ^c   Ngamskulrungroj, Popchai ^d   Angkasekwinai, Nasikarn ^c   Pattanapanyasat, Kovit ^d  

^a THAMMASAT UNIVERSITY   (Thailand)

^b UNIVERSITY OF CINCINNATI   (United States)

^c MAHIDOL UNIVERSITY   (Thailand)

^d MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 23;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; COCULTURE; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; DENDRITIC CELL; DOWN REGULATION; FUNGAL STRAIN; FUNGAL VIRULENCE; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; TH17 CELL;

ANIMALS; CHEMOKINES; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; DENDRITIC CELLS; DOWN-REGULATION; FEMALE; LUNG; MICE; MICE, INBRED C57BL; TH1 CELLS; TH17 CELLS;

EID: 84906070895     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01773-14     Document Type: Article

References (35)

1. Lin X, Heitman J. 2006. The biology of the Cryptococcus neoformans species complex. Annu. Rev. Microbiol. 60:69-105. http://dx.doi.org/10.1146/annurev.micro.60.080805.142102.
2. Speed B, Dunt D. 1995. Clinical and host differences between infections with the two varieties of Cryptococcus neoformans. Clin. Infect. Dis. 21:28-34, 35-26. http://dx.doi.org/10.1093/clinids/21.1.28.
3. Chen S, Sorrell T, Nimmo G, Speed B, Currie B, Ellis D, Marriott D, Pfeiffer T, Parr D, Byth K. 2000. Epidemiology and host-and varietydependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Australasian Cryptococcal Study Group. Clin. Infect. Dis. 31:499-508.
4. Ngamskulrungroj P, Chang Y, Sionov E, Kwon-Chung KJ. 2012. The primary target organ of Cryptococcus gattii is different from that of Cryptococcus neoformans in a murine model. mBio 3:e00103-12. http://dx.doi.org/10.1128/mBio.00103-12.
5. Cheng PY, Sham A, Kronstad JW. 2009. Cryptococcus gattii isolates from the British Columbia cryptococcosis outbreak induce less protective inflammation in a murine model of infection than Cryptococcus neoformans. Infect. Immun. 77:4284-4294. http://dx.doi.org/10.1128/IAI.00628-09.
6. Wright L, Bubb W, Davidson J, Santangelo R, Krockenberger M, Himmelreich U, Sorrell T. 2002. Metabolites released by Cryptococcus neoformans var. neoformans and var. gattii differentially affect human neutrophil function. Microbes Infect. 4:1427-1438. http://dx.doi.org/10.1016/S1286-4579(02)00024-2.
7. Brouwer AE, Siddiqui AA, Kester MI, SigaloffKC, Rajanuwong A, Wannapasni S, Chierakul W, Harrison TS. 2007. Immune dysfunction in HIV-seronegative, Cryptococcus gattii meningitis. J. Infect. 54:e165-168. http://dx.doi.org/10.1016/j.jinf.2006.10.002.
8. 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.
9. Pappu BP, Angkasekwinai P, Dong C. 2008. Regulatory mechanisms of helper T cell differentiation: new lessons learned from interleukin 17 family cytokines. Pharmacol. Ther. 117:374-384. http://dx.doi.org/10.1016/j.pharmthera.2007.12.003.
10. Herring AC, Lee J, McDonald RA, Toews GB, Huffnagle GB. 2002. Induction of interleukin-12 and gamma interferon requires tumor necrosis factor alpha for protective T1-cell-mediated immunity to pulmonary Cryptococcus neoformans infection. Infect. Immun. 70:2959-2964. http://dx.doi.org/10.1128/IAI.70.6.2959-2964.2002.
11. Decken K, Kohler G, Palmer-Lehmann K, Wunderlin A, Mattner F, Magram J, Gately MK, Alber G. 1998. Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans. Infect. Immun. 66:4994-5000.
12. Kawakami K, Tohyama M, Teruya K, Kudeken N, Xie Q, Saito A. 1996. Contribution of interferon-gamma in protecting mice during pulmonary and disseminated infection with Cryptococcus neoformans. FEMS Immunol. Med. Microbiol. 13:123-130. http://dx.doi.org/10.1111/j.1574-695X.1996.tb00225.x.
13. Kawakami K, Tohyama M, Xie Q, Saito A. 1996. IL-12 protects mice against pulmonary and disseminated infection caused by Cryptococcus neoformans. Clin. Exp. Immunol. 104:208-214. http://dx.doi.org/10.1046/j.1365-2249.1996.14723.x.
14. Kawakami K, Hossain Qureshi M, Zhang T, Koguchi Y, Xie Q, Kurimoto M, Saito A. 1999. Interleukin-4 weakens host resistance to pulmonary and disseminated cryptococcal infection caused by combined treatment with interferon-gamma-inducing cytokines. Cell Immunol. 197:55-61. http://dx.doi.org/10.1006/cimm.1999.1557.
15. Muller U, Stenzel W, Kohler G, Werner C, Polte T, Hansen G, Schutze N, Straubinger RK, Blessing M, McKenzie AN, Brombacher F, Alber G. 2007. IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J. Immunol. 179:5367-5377. http://dx.doi.org/10.4049/jimmunol.179.8.5367.
16. Voelz K, Lammas DA, May RC. 2009. Cytokine signaling regulates the outcome of intracellular macrophage parasitism by Cryptococcus neoformans. Infect. Immun. 77:3450-3457. http://dx.doi.org/10.1128/IAI.00297-09.
17. Voelz K, May RC. 2010. Cryptococcal interactions with the host immune system. Eukaryot. Cell 9:835-846. http://dx.doi.org/10.1128/EC.00039-10.
18. Kleinschek MA, Muller U, Brodie SJ, Stenzel W, Kohler G, Blumenschein WM, Straubinger RK, McClanahan T, Kastelein RA, Alber G. 2006. IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J. Immunol. 176:1098-1106. http://dx.doi.org/10.4049/jimmunol.176.2.1098.
19. Zhang Y, Wang F, Tompkins KC, McNamara A, Jain AV, Moore BB, Toews GB, Huffnagle GB, Olszewski MA. 2009. Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dis-semination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 175:2489-2500. http://dx.doi.org/10.2353/ajpath.2009.090530.
20. Angkasekwinai P, Park H, Wang YH, Chang SH, Corry DB, Liu YJ, Zhu Z, Dong C. 2007. Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 204:1509-1517. http://dx.doi.org/10.1084/jem.20061675.
21. De Filippo K, Henderson RB, Laschinger M, Hogg N. 2008. Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J. Immunol. 180:4308-4315. http://dx.doi.org/10.4049/jimmunol.180.6.4308.
22. Angkasekwinai P, Srimanote P, Wang YH, Pootong A, Sakolvaree Y, Pattanapanyasat K, Chaicumpa W, Chaiyaroj S, Dong C. 2013. Interleukin-25 (IL-25) promotes efficient protective immunity against Trichinella spiralis infection by enhancing the antigen-specific IL-9 response. Infect. Immun. 81:3731-3741. http://dx.doi.org/10.1128/IAI.00646-13.
23. Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, Diezmann S, Allen A, Stajich JE, Dietrich FS, Perfect JR, Heitman J. 2005. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360-1364. http://dx.doi.org/10.1038/nature04220.
24. Meyer W, Castaneda A, Jackson S, Huynh M, Castaneda E. 2003. Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg. Infect. Dis. 9:189-195. http://dx.doi.org/10.3201/eid0902.020246.
25. Dong C. 2006. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat. Rev. Immunol. 6:329-334. http://dx.doi.org/10.1038/nri1807.
26. Bromley SK, Mempel TR, Luster AD. 2008. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat. Immunol. 9:970-980. http://dx.doi.org/10.1038/ni.f.213.
27. D'Ambrosio D, Mariani M, Panina-Bordignon P, Sinigaglia F. 2001. Chemokines and their receptors guiding T lymphocyte recruitment in lung inflammation. Am. J. Respir. Crit. Care Med. 164:1266-1275. http://dx.doi.org/10.1164/ajrccm.164.7.2103011.
28. Perfect JR, Dismukes WE, Dromer F, Goldman DL, Graybill JR, Hamill RJ, Harrison TS, Larsen RA, Lortholary O, Nguyen MH, Pappas PG, Powderly WG, Singh N, Sobel JD, Sorrell TC. 2010. Clinical practice guidelines for the management of cryptococcal disease: 2010 update by the infectious diseases society of America. Clin. Infect. Dis. 50:291-322. http://dx.doi.org/10.1086/649858.
29. Purvis HA, Stoop JN, Mann J, Woods S, Kozijn AE, Hambleton S, Robinson JH, Isaacs JD, Anderson AE, Hilkens CM. 2010. Low-strength T-cell activation promotes Th17 responses. Blood 116:4829-4837. http://dx.doi.org/10.1182/blood-2010-03-272153.
30. Hoag KA, Lipscomb MF, Izzo AA, Street NE. 1997. IL-12 and IFNgamma are required for initiating the protective Th1 response to pulmonary cryptococcosis in resistant C.B-17 mice. Am. J. Respir. Cell Mol. Biol. 17:733-739. http://dx.doi.org/10.1165/ajrcmb.17.6.2879.
31. Kleinschek MA, Muller U, Schutze N, Sabat R, Straubinger RK, Blumenschein WM, McClanahan T, Kastelein RA, Alber G. 2010. Administration of IL-23 engages innate and adaptive immune mechanisms during fungal infection. Int. Immunol. 22:81-90. http://dx.doi.org/10.1093/intimm/dxp117.
32. Huston SM, Li SS, Stack D, Timm-McCann M, Jones GJ, Islam A, Berenger BM, Xiang RF, Colarusso P, Mody CH. 2013. Cryptococcus gattii is killed by dendritic cells, but evades adaptive immunity by failing to induce dendritic cell maturation. J. Immunol. 191:249-261. http://dx.doi.org/10.4049/jimmunol.1202707.
33. Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, Koch AE, Moser B, Mackay CR. 1998. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101:746-754. http://dx.doi.org/10.1172/JCI1422.
34. Huffnagle GB, McNeil LK, McDonald RA, Murphy JW, Toews GB, Maeda N, Kuziel WA. 1999. Cutting edge: role of C-C chemokine receptor 5 in organ-specific and innate immunity to Cryptococcus neoformans. J. Immunol. 163:4642-4646.
35. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K, von Andrian UH, Moon JJ, Mempel TR, Luster AD. 2012. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 37:1091-1103. http://dx.doi.org/10.1016/j.immuni.2012.08.016.