Induction of caspase-11 by aspartyl proteinases of Candida albicans and implication in promoting inflammatory response

Infection and Immunity

Volumn 83, Issue 5, 2015, Pages 1940-1948

  Gabrielli, Elena ^a   Pericolini, Eva ^a   Luciano, Eugenio ^a   Sabbatini, Samuele ^a   Roselletti, Elena ^a   Perito, Stefano ^a   Kasper, Lydia ^b   Hube, Bernhard ^b,c,d   Vecchiarelli, Anna ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b HANS KNÖLL INSTITUTE   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d Center for Sepsis Control and Care   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; ASPARTIC PROTEINASE; CASPASE 11; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; SECRETED ASPARTYL PROTEINASE 2; SECRETED ASPARTYL PROTEINASE 6; UNCLASSIFIED DRUG; CASP11 PROTEIN, MOUSE; CASPASE; FUNGAL PROTEIN; INTERFERON; SAP2 PROTEIN, CANDIDA; SAP6 PROTEIN, CANDIDA ALBICANS;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANDIDA ALBICANS; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOCYTOSIS; ENZYME ACTIVATION; FEMALE; IMMUNOCOMPETENT CELL; INFLAMMATION; INTERNALIZATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; ANIMAL; C57BL MOUSE; CELL LINE; ENZYMOLOGY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOLOGY;

ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CANDIDA ALBICANS; CASPASE 1; CASPASES; CELL LINE; ENDOCYTOSIS; FEMALE; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; INFLAMMASOMES; INFLAMMATION; INTERFERON TYPE I; MACROPHAGES; MICE, INBRED C57BL;

EID: 84928176611     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02895-14     Document Type: Article

References (35)

1. Naglik JR, Challacombe SJ, Hube B. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67:400-428. http://dx.doi.org/10.1128/MMBR.67.3.400-428.2003.
2. Vecchiarelli A, Pericolini E, Gabrielli E, Pietrella D. 2012. New approaches in the development of a vaccine for mucosal candidiasis: progress and challenges. Front Microbiol 3:294. http://dx.doi.org/10.3389/fmicb.2012.00294.
3. Pfaller MA, Diekema DJ. 2010. Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36:1-53. http://dx.doi.org/10.3109/10408410903241444.
4. Mayer FL, Wilson D, Hube B. 2013. Candida albicans pathogenicity mechanisms. Virulence 4:119-128. http://dx.doi.org/10.4161/viru.22913.
5. Sudbery P, Gow N, Berman J. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol 12:317-324. http://dx.doi.org/10.1016/j.tim.2004.05.008.
6. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737-748. http://dx.doi.org/10.1038/nrmicro2636.
7. Gow NA, Brown AJ, Odds FC. 2002. Fungal morphogenesis and host invasion. Curr Opin Microbiol 5:366-371. http://dx.doi.org/10.1016/S1369-5274(02)00338-7.
8. Jacobsen ID, Wilson D, Wachtler B, Brunke S, Naglik JR, Hube B. 2012. Candida albicans dimorphism as a therapeutic target. Expert Rev Anti Infect Ther 10:85-93. http://dx.doi.org/10.1586/eri.11.152.
9. de Viragh PA, Sanglard D, Togni G, Falchetto R, Monod M. 1993. Cloning and sequencing of two Candida parapsilosis genes encoding acid proteases. J Gen Microbiol 139:335-342. http://dx.doi.org/10.1099/00221287-139-2-335.
10. Monod M, Togni G, Hube B, Sanglard D. 1994. Multiplicity of genes encoding secreted aspartic proteinases in Candida species. Mol Microbiol 13:357-368. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00429.x.
11. Pietrella D, Rachini A, Pandey N, Schild L, Netea M, Bistoni F, Hube B, Vecchiarelli A. 2010. The inflammatory response induced by aspartic proteases of Candida albicans is independent of proteolytic activity. Infect Immun 78:4754-4762. http://dx.doi.org/10.1128/IAI.00789-10.
12. Pietrella D, Pandey N, Gabrielli E, Pericolini E, Perito S, Kasper L, Bistoni F, Cassone A, Hube B, Vecchiarelli A. 2013. Secreted aspartic proteases of Candida albicans activate the NLRP3 inflammasome. Eur J Immunol 43:679-692. http://dx.doi.org/10.1002/eji.201242691.
13. Schroder K, Zhou R, Tschopp J. 2010. The NLRP3 inflammasome: a sensor for metabolic danger? Science 327:296-300. http://dx.doi.org/10.1126/science.1184003.
14. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, Leong JM, Fitzgerald KA. 2012. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by Gram-negative bacteria. Cell 150:606-619. http://dx.doi.org/10.1016/j.cell.2012.07.007.
15. Vigano E, Mortellaro A. 2013. Caspase-11: the driving factor for noncanonical inflammasomes. Eur J Immunol 43:2240-2245. http://dx.doi.org/10.1002/eji.201343800.
16. Broz P, Monack DM. 2013. Noncanonical inflammasomes: caspase-11 activation and effector mechanisms. PLoS Pathog 9:e1003144. http://dx.doi.org/10.1371/journal.ppat.1003144.
17. Borg-von Zepelin M, Beggah S, Boggian K, Sanglard D, Monod M. 1998. The expression of the secreted aspartyl proteinases Sap4 to Sap6 from Candida albicans in murine macrophages. Mol Microbiol 28:543-554. http://dx.doi.org/10.1046/j.1365-2958.1998.00815.x.
18. Gabrielli E, Pericolini E, Cenci E, Ortelli F, Magliani W, Ciociola T, Bistoni F, Conti S, Vecchiarelli A, Polonelli L. 2009. Antibody complementarity-determining regions (CDRs): a bridge between adaptive and innate immunity. PLoS One 4:e8187. http://dx.doi.org/10.1371/journal.pone.0008187.
19. Kobori M, Yang Z, Gong D, Heissmeyer V, Zhu H, Jung YK, Gakidis MA, Rao A, Sekine T, Ikegami F, Yuan C, Yuan J. 2004. Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ 11:123-130. http://dx.doi.org/10.1038/sj.cdd.4401325.
20. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, Heutel JD, Dungo-Arthur C, Carrero JA, White JM, Hertzog PJ, Schreiber RD. 2006. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res 26:804-819. http://dx.doi.org/10.1089/jir.2006.26.804.
21. Pericolini E, Gabrielli E, Bistoni G, Cenci E, Perito S, Chow SK, Riuzzi F, Donato R, Casadevall A, Vecchiarelli A. 2010. Role of CD45 signaling pathway in galactoxylomannan-induced T cell damage. PLoS One 5:e12720. http://dx.doi.org/10.1371/journal.pone.0012720.
22. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM. 2011. Non-canonical inflammasome activation targets caspase-11. Nature 479:117-121. http://dx.doi.org/10.1038/nature10558.
23. Broz P, Ruby T, Belhocine K, Bouley DM, Kayagaki N, Dixit VM, Monack DM. 2012. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490:288-291. http://dx.doi.org/10.1038/nature11419.
24. Fang R, Hara H, Sakai S, Hernandez-Cuellar E, Mitsuyama M, Kawamura I, Tsuchiya K. 2014. Type I interferon signaling regulates activation of the absent in melanoma 2 inflammasome during Streptococcus pneumoniae infection. Infect Immun 82:2310-2317. http://dx.doi.org/10.1128/IAI.01572-14.
25. Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. 2013. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341:1250-1253. http://dx.doi.org/10.1126/science.1240988.
26. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM. 2013. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341:1246-1249. http://dx.doi.org/10.1126/science.1240248.
27. Mogensen TH. 2009. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240-273. http://dx.doi.org/10.1128/CMR.00046-08.
28. del Fresno C, Soulat D, Roth S, Blazek K, Udalova I, Sancho D, Ruland J, Ardavin C. 2013. Interferon-beta production via Dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 38:1176-1186. http://dx.doi.org/10.1016/j.immuni.2013.05.010.
29. Inglis DO, Berkes CA, Hocking Murray DR, Sil A. 2010. Conidia but not yeast cells of the fungal pathogen Histoplasma capsulatum trigger a type I interferon innate immune response in murine macrophages. Infect Immun 78:3871-3882. http://dx.doi.org/10.1128/IAI.00204-10.
30. Majer O, Bourgeois C, Zwolanek F, Lassnig C, Kerjaschki D, Mack M, Muller M, Kuchler K. 2012. Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog 8:e1002811. http://dx.doi.org/10.1371/journal.ppat.1002811.
31. Biondo C, Signorino G, Costa A, Midiri A, Gerace E, Galbo R, Bellantoni A, Malara A, Beninati C, Teti G, Mancuso G. 2011. Recognition of yeast nucleic acids triggers a host-protective type I interferon response. Eur J Immunol 41:1969-1979. http://dx.doi.org/10.1002/eji.201141490.
32. Mahieu T, Park JM, Revets H, Pasche B, Lengeling A, Staelens J, Wullaert A, Vanlaere I, Hochepied T, van Roy F, Karin M, Libert C. 2006. The wild-derived inbred mouse strain SPRET/Ei is resistant to LPS and defective in IFN-beta production. Proc Natl Acad Sci USA 103:2292-2297. http://dx.doi.org/10.1073/pnas.0510874103.
33. Huys L, Van Hauwermeiren F, Dejager L, Dejonckheere E, Lienenklaus S, Weiss S, Leclercq G, Libert C. 2009. Type I interferon drives tumor necrosis factor-induced lethal shock. J Exp Med 206:1873-1882. http://dx.doi.org/10.1084/jem.20090213.
34. Latz E, Xiao TS, Stutz A. 2013. Activation and regulation of the inflammasomes. Nat Rev Immunol 13:397-411. http://dx.doi.org/10.1038/nri3452.
35. Cassone A. 23 July 2014. Vulvovaginal Candida albicans infections: pathogenesis, immunity and vaccine prospects. BJOG http://dx.doi.org/10.1111/1471-0528.12994.