Targeting CBLB as a potential therapeutic approach for disseminated candidiasis

Nature Medicine

Volumn 22, Issue 8, 2016, Pages 906-914

  Xiao, Yun ^a,b,c   Tang, Juan ^a,b   Guo, Hui ^a   Zhao, Yixia ^a,b   Tang, Rong ^a,b   Ouyang, Song ^a,b,d   Zeng, Qiuming ^a,b   Rappleye, Chad A ^a   Rajaram, Murugesan V S ^a   Schlesinger, Larry S ^a   Tao, Lijian ^b   Brown, Gordon D ^e   Langdon, Wallace Y ^f   Li, Belinda T ^a   Zhang, Jian ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF SOUTH CHINA   (China)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CBLB ENZYME; CURDLAN; DECTIN 1; DECTIN 2; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; PATTERN RECOGNITION RECEPTOR; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ZYMOSAN; CBL PROTEIN; CBLB PROTEIN, HUMAN; CBLB PROTEIN, MOUSE; CYTOKINE; DECTIN-2, MOUSE; LECTIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SYK PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANDIDA ALBICANS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME INACTIVATION; FEMALE; FUNGUS HYPHAE; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; INNATE IMMUNITY; INTERNALIZATION; INTERSTITIAL NEPHRITIS; INVASIVE CANDIDIASIS; LYSOSOME; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTE; PHAGOCYTOSIS; POLYUBIQUITINATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; UBIQUITINATION; WILD TYPE; ANIMAL; CONFOCAL MICROSCOPY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SILENCING; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; METABOLISM; MONONUCLEAR CELL; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CANDIDA ALBICANS; CANDIDIASIS, INVASIVE; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNITY, INNATE; IMMUNOPRECIPITATION; INFLAMMASOMES; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MUTAGENESIS, SITE-DIRECTED; NEUTROPHILS; PHAGOCYTOSIS; PROTO-ONCOGENE PROTEINS C-CBL; REACTIVE OXYGEN SPECIES; SYK KINASE; UBIQUITINATION;

EID: 84978650005     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4141     Document Type: Article

References (49)

1. Brown, G.D. et al. Hidden killers: human fungal infections. Sci. Transl. Med. 4, 165rv13 (2012).
2. Taylor, P.R. et al. Dectin-1 is required for β-glucan recognition and control of fungal infection. Nat. Immunol. 8, 31-38 (2007).
3. H17 cell differentiation is essential for host defense against Candida albicans. Immunity 32, 681-691 (2010).
4. Zhu, L.L. et al. C-type lectin receptors dectin-3 and dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity 39, 324-334 (2013).
5. H17 cells in immunity to Candida albicans. Cell Host Microbe 11, 425-435 (2012).
6. Liu, Q., Zhou, H., Langdon, W.Y. & Zhang, J. E3 ubiquitin ligase Cblb in innate and adaptive immunity. Cell Cycle 13, 1875-1884 (2014).
7. Bachmaier, K. et al. Negative regulation of lymphocyte activation and autoimmunity by the molecular adaptor Cblb. Nature 403, 211-216 (2000).
8. Jeon, M.S. et al. Essential role of the E3 ubiquitin ligase Cblb in T cell anergy induction. Immunity 21, 167-177 (2004).
9. Qiao, G. et al. T cell receptor-induced NF-κB activation is negatively regulated by E3 ubiquitin ligase Cblb. Mol. Cell. Biol. 28, 2470-2480 (2008).
10. Li, D. et al. Cutting edge: Cblb: one of the key molecules tuning CD28- and CTLA-4-mediated T cell co-stimulation. J. Immunol. 173, 7135-7139 (2004).
11. Zhang, J. et al. Cutting edge: regulation of T cell activation threshold by CD28 co-stimulation through targeting Cblb for ubiquitination. J. Immunol. 169, 2236-2240 (2002).
12. Guo, H. et al. E3 ubiquitin ligase Cblb regulates Pten via Nedd4 in T cells independently of its ubiquitin ligase activity. Cell Rep. 1, 472-482 (2012).
13. Qiao, G. et al. T cell activation threshold regulated by E3 ubiquitin ligase Cblb determines fate of inducible regulatory T cells. J. Immunol. 191, 632-639 (2013).
14. Qiao, G. et al. E3 ubiquitin ligase Cblb suppresses proallergic T cell development and allergic airway inflammation. Cell Rep. 6, 709-723 (2014).
15. Brown, G.D. Dectin-1: a signaling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 6, 33-43 (2006).
16. Yoshitomi, H. et al. A role for fungal β-glucans and their receptor dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J. Exp. Med. 201, 949-960 (2005).
17. Bahn, Y.S. & Sundstrom, P. CAP1, an adenylate cyclase-associated protein gene, regulates bud-hypha transitions, filamentous growth, and cyclic AMP levels and is required for virulence of Candida albicans. J. Bacteriol. 183, 3211-3223 (2001).
18. Hohl, T.M. & Feldmesser, M. Aspergillus fumigatus: principles of pathogenesis and host defense. Eukaryot. Cell 6, 1953-1963 (2007).
19. Steele, C. et al. The β-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog. 1, e42 (2005).
20. 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. 176, 3717-3724 (2006).
21. Rivera, A. et al. Dectin-1 diversifies Aspergillus fumigatus-specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J. Exp. Med. 208, 369-381 (2011).
22. Hise, A.G. et al. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5, 487-497 (2009).
23. Gringhuis, S.I. et al. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a noncanonical caspase-8 inflammasome. Nat. Immunol. 13, 246-254 (2012).
24. Smeekens, S.P. et al. An anti-inflammatory property of Candida albicans β-glucan: induction of high levels of interleukin-1 receptor antagonist via a dectin-1-CR3 independent mechanism. Cytokine 71, 215-222 (2015).
25. Kang, P.B. et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J. Exp. Med. 202, 987-999 (2005).
26. Rajaram, M.V. et al. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc. Natl. Acad. Sci. USA 108, 17408-17413 (2011).
27. Brown, G.D. Innate antifungal immunity: the key role of phagocytes. Annu. Rev. Immunol. 29, 1-21 (2011).
28. Hardison, S.E. & Brown, G.D. C-type lectin receptors orchestrate antifungal immunity. Nat. Immunol. 13, 817-822 (2012).
29. Osorio, F. & Reis e Sousa, C. Myeloid C-type lectin receptors in pathogen recognition and host defense. Immunity 34, 651-664 (2011).
30. Kerscher, B., Willment, J.A. & Brown, G.D. The dectin-2 family of C-type lectin-like receptors: an update. Int. Immunol. 25, 271-277 (2013).
31. Miyake, Y. et al. C-type lectin MCL is an FcR-γ-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38, 1050-1062 (2013).
32. Sato, K. et al. Dectin-2 is a pattern-recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J. Biol. Chem. 281, 38854-38866 (2006).
33. Sohn, H.W., Gu, H. & Pierce, S.K. Cblb negatively regulates B cell antigen receptor signaling in mature B cells through ubiquitination of the tyrosine kinase Syk. J. Exp. Med. 197, 1511-1524 (2003).
34. Kojo, S. et al. Mechanisms of NKT cell anergy induction involve Cblb-promoted monoubiquitination of CARMA1. Proc. Natl. Acad. Sci. USA 106, 17847-17851 (2009).
35. Oksvold, M.P., Dagger, S.A., Thien, C.B. & Langdon, W.Y. The Cblb RING finger domain has a limited role in regulating inflammatory cytokine production by IgE-activated mast cells. Mol. Immunol. 45, 925-936 (2008).
36. Sorkin, A. & Von Zastrow, M. Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3, 600-614 (2002).
37. Haglund, K. et al. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466 (2003).
38. Lin, Q. et al. HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Mol. Cell. Biol. 30, 1541-1554 (2010).
39. Hernanz-Falcón, P., Joffre, O., Williams, D.L. & Reis e Sousa, C. Internalization of dectin-1 terminates induction of inflammatory responses. Eur. J. Immunol. 39, 507-513 (2009).
40. Nicola, A.M., Casadevall, A. & Goldman, D.L. Fungal killing by mammalian phagocytic cells. Curr. Opin. Microbiol. 11, 313-317 (2008).
41. Brown, A.J., Haynes, K. & Quinn, J. Nitrosative and oxidative stress responses in fungal pathogenicity. Curr. Opin. Microbiol. 12, 384-391 (2009).
42. Wells, C.A. et al. The macrophage-inducible C-type lectin, Mincle, is an essential component of the innate immune response to Candida albicans. J. Immunol. 180, 7404-7413 (2008).
43. van de Veerdonk, F.L. et al. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5, 329-340 (2009).
44. Cambi, A. et al. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33, 532-538 (2003).
45. Goodridge, H.S., Underhill, D.M. & Touret, N. Mechanisms of Fc receptor and dectin-1 activation for phagocytosis. Traffic 13, 1062-1071 (2012).
46. Dupré-Crochet, S., Erard, M. & Nüße, O. ROS production in phagocytes: why, when, and where? J. Leukoc. Biol. 94, 657-670 (2013).
47. Underhill, D.M., Rossnagle, E., Lowell, C.A. & Simmons, R.M. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106, 2543-2550 (2005).
48. Swamydas, M., Luo, Y., Dorf, M.E. & Lionakis, M.S. Isolation of mouse neutrophils. Curr. Protoc. Immunol. 110, 3.20 (2015).
49. Wirnsberger, G. et al. Jagunal homolog 1 is a critical regulator of neutrophil function in fungal host defense. Nat. Genet. 46, 1028-1033 (2014).