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Neutrophils with Human Candida Dubliniensis and Candida Albicans Differential Interaction of the Two Related Fungal Species Candida albicans and Candida dubliniensis with Human Neutrophils This information is current as of September 26, 2021. Eliska Svobodová, Peter Staib, Josephine Losse, Florian Hennicke, Dagmar Barz and Mihály Józsi J Immunol 2012; 189:2502-2511; Prepublished online 30 July 2012; doi: 10.4049/jimmunol.1200185 Downloaded from http://www.jimmunol.org/content/189/5/2502 Supplementary http://www.jimmunol.org/content/suppl/2012/07/30/jimmunol.120018 http://www.jimmunol.org/ Material 5.DC1 References This article cites 67 articles, 20 of which you can access for free at: http://www.jimmunol.org/content/189/5/2502.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 26, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2012 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Differential Interaction of the Two Related Fungal Species Candida albicans and Candida dubliniensis with Human Neutrophils Elisˇka Svobodova´,* Peter Staib,† Josephine Losse,* Florian Hennicke,† Dagmar Barz,‡ and Miha´ly Jo´zsi* Candida albicans, the most common facultative human pathogenic fungus is of major medical importance, whereas the closely related species Candida dubliniensis is less virulent and rarely causes life-threatening, systemic infections. Little is known, however, about the reasons for this difference in pathogenicity, and especially on the interactions of C. dubliniensis with the human immune system. Because innate immunity and, in particular, neutrophil granulocytes play a major role in host anti- fungal defense, we studied the responses of human neutrophils to clinical isolates of both C. albicans and C. dubliniensis. Downloaded from C. dubliniensis was found to support neutrophil migration and fungal cell uptake to a greater extent in comparison with C. albicans, whereas inducing less neutrophil damage and extracellular trap formation. The production of antimicrobial reactive oxygen species, myeloperoxidase, and lactoferrin, as well as the inflammatory chemokine IL-8 by neutrophils was increased when stimulated with C. dubliniensis as compared with C. albicans. However, most of the analyzed macrophage-derived inflammatory and regulatory cytokines and chemokines, such as IL-1a,IL-1b,IL-1ra,TNF-a,IL-10,G-CSF,andGM-CSF, were less induced by C. dubliniensis. Similarly, the amounts of the antifungal immunity-related IL-17A produced by PBMCs http://www.jimmunol.org/ was significantly lower when challenged with C. dubliniensis than with C. albicans. These data indicate that C. dubliniensis triggers stronger early neutrophil responses than C. albicans, thus providing insight into the differential virulence of these two closely related fungal species, and suggest that this is, in part, due to their differential capacity to form hyphae. The Journal of Immunology, 2012, 189: 2502–2511. ungi of the genus Candida are harmless commensals Despite their similarity, C. dubliniensis appears to be less virulent coexisting with humans. In the immunocompromised host, in animal and mucosal infection models (4–7) according to its in- F however, Candida spp. can cause superficial and even life- fection rate and the severity of disease. C. dubliniensis strains are by guest on September 26, 2021 threatening, systemic infections. Although Candida albicans is the more rapidly cleared form the site of infection and are less able to most common cause of candidiasis, the number of infections cause disseminated infections. The phylogenetic properties of C. caused by nonalbicans species such as Candida glabrata, Candida dubliniensis have been well described in the literature (2, 8). A DNA parapsilosis, and Candida dubliniensis, especially in HIV-infected hybridization array (9) and lately comparison of both genomes (10) and AIDS patients, is quite high (1). C. dubliniensis was first uncovered particular differences between C. dubliniensis and C. discovered in 1995 upon genetic characterization and is mainly albicans in regard to putative virulence genes, including those recovered from oral candidosis of HIV+ patients (2). C. dubliniensis encoding hyphae-associated factors such as specific secreted is the closest relative of C. albicans and is the only other Candida proteases or invasins. The ability of C. albicans to reversibly switch species able to form true hyphae and chlamydospores (3). between yeast and filamentous growth forms has widely been docu- mented as an important virulence attribute of C. albicans, facilitating host invasion and colonization. C. dubliniensis also produces true *Junior Research Group Cellular Immunobiology, Leibniz Institute for Natural Prod- hyphae, however, with a far lesser efficiency than C. albicans,which uct Research and Infection Biology–Hans Kno¨ll Institute, D-07745 Jena, Germany; putatively contributes to its comparatively poor virulence (6, 11). † Junior Research Group Fundamental Molecular Biology of Pathogenic Fungi, Leib- The control of fungal infection in the human host critically niz Institute for Natural Product Research and Infection Biology–Hans Kno¨ll Insti- tute, D-07745 Jena, Germany; and ‡Institute for Transfusion Medicine, University depends on cells of the innate immunity. Neutrophil granulocytes Hospital of Jena, D-07747 Jena, Germany are major phagocytic cells that are recruited early to the infection Received for publication January 13, 2012. Accepted for publication July 3, 2012. site, where they activate a large repertoire of antimicrobial This work was supported in part by the Deutsche Forschungsgemeinschaft (DFG mechanisms including phagocytosis, the generation of reactive Grant STA 1147/1-1 to P.S.). oxygen species (ROS), the release of granule enzymes and anti- Address correspondence and reprint requests to Dr. Miha´ly Jo´zsi, Junior Research microbial peptides, and the formation of neutrophil extracellular Group Cellular Immunobiology, Leibniz Institute for Natural Product Research and traps (NETs) (12–14). Attracted monocytes possess less micro- Infection Biology–Hans Kno¨ll Institute, Beutenbergstrasse 11a, D-07745 Jena, Germany. E-mail address: [email protected] bicidal capacity but are important in alerting cells of the innate The online version of this article contains supplemental material. and adaptive immune system, and give rise to macrophages, im- Abbreviations used in this article: CFW, calcofluor white; DPBS, Dulbecco’s portant phagocytic and APCs. These innate immune cells recog- phosphate-buffered saline; LDH, lactate dehydrogenase; MDM, monocyte-derived nize fungal pathogens via three major receptor families (i.e., the macrophage; MOI, multiplicity of infection; MPO, myeloperoxidase; NET, neutro- TLRs, the lectin receptors, and the NOD-like receptors), leading phil extracellular trap; ROS, reactive oxygen species. to activation of signaling pathways that result in tightly regulated Copyright Ó 2012 by The American Association of Immunologists, Inc. 0022-1767/12/$16.00 and complementary immune responses (15, 16). www.jimmunol.org/cgi/doi/10.4049/jimmunol.1200185 The Journal of Immunology 2503 To date, little is known about the Candida species-specific sites, respectively, to result in pCdADH1E2. A SalI-BglII GFP frag- responses of human innate immune cells. Because C. dubliniensis ment from pNIM1 (28) was cloned in the XhoI-BglII digested plasmid has a reduced ability to cause severe (i.e., systemic) infections, pCdADH1E2, resulting in pCdADH1GFP1. Flanked by CdADH1 upstream and downstream sequences, pCdADH1GFP1 contains a cassette with the which are usually brought in context with C. albicans, one would GFP gene under control of PCdADH1,followedbyTCaACT1 termination expect a better clearance of the former by host immune cells. A sequences, and the SAT1 marker for transformant selection after trans- previous report found no difference in the phagocytosis, oxidative formation. Transformation by electroporation of C. dubliniensis Wu¨284 burst, or killing induced by these two fungal species in whole by use of the linear ApaI-SacII DNA cassette from pCdADH1GFP1, transformant selection on nourseothricin (Werner Bioagents, Jena, Ger- blood (17). Nevertheless, it has been shown that even though both many),andSouthernanalysisofgenomic DNA with ECL-labeled (GE Candida species release a chemotactic factor for neutrophils, Healthcare, Freiburg, Germany) upstream and downstream CdADH1 the chemotaxis toward C. dubliniensis is enhanced compared with probes for proving correct insertion of the GFP construct in the CdADH1 C. albicans (18). Studies using epithelial cell infection mod- locus of the resulting transformant CdADH1GFP1A were performed by els demonstrated that C. dubliniensis causes minimal invasion standard procedures as described previously (29). (5, 19) and cytokine production (20, 21)
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