The inflammatory response induced by aspartic proteases of Candida albicans is independent of proteolytic activity

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4754-4762

  Pietrella, Donatella ^a   Rachini, Anna ^a   Pandey, Neelam ^a   Schild, Lydia ^b   Netea, Mihai ^c   Bistoni, Francesco ^a   Hube, Bernhard ^b,d   Vecchiarelli, Anna ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b HANS KNÖLL INSTITUTE   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC PROTEINASE; CALCIUM; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; PEPSTATIN; PROTEIN KINASE B; PROTEINASE ACTIVATED RECEPTOR; RECOMBINANT PROTEIN; SECRETION OF ASPARTIC PROTEASE 1; SECRETION OF ASPARTIC PROTEASE 2; SECRETION OF ASPARTIC PROTEASE 3; SECRETION OF ASPARTIC PROTEASE 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM TRANSPORT; CANDIDA ALBICANS; CELL INTERACTION; CELL NUCLEUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INFLAMMATION; MONOCYTE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

ASPARTIC ACID ENDOPEPTIDASES; CANDIDA ALBICANS; CYTOKINES; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; MONOCYTES; RECOMBINANT PROTEINS;

EID: 78049441695     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00789-10     Document Type: Article

References (64)

1. Albrecht, A., A. Felk, I. Pichova, J. R. Naglik, M. Schaller, P. de Groot, D. Maccallum, F. C. Odds, W. Schafer, F. Klis, M. Monod, and B. Hube. 2006. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281:688-694.
2. Borelli, C., E. Ruge, J. H. Lee, M. Schaller, A. Vogelsang, M. Monod, H. C. Korting, R. Huber, and K. Maskos. 2008. X-ray structures of Sap1 and Sap5: structural comparison of the secreted aspartic proteinases from Candida albicans. Proteins 72:1308-1319.
3. Borg-von Zepelin, M., S. Beggah, K. Boggian, D. Sanglard, and M. Monod. 1998. The expression of the secreted aspartyl proteinases Sap4 to Sap6 from Candida albicans in murine macrophages. Mol. Microbiol. 28:543-554.
4. Brunke, S., and B. Hube. 2006. MfLIP1, a gene encoding an extracellular lipase of the lipid-dependent fungus Malassezia furfur. Microbiology 152: 547-554.
5. Calderone, R. A., and W. A. Fonzi. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9:327-335.
6. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
7. Cheng, S. C., L. Y. Chai, L. A. Joosten, A. Vecchiarelli, B. Hube, J. W. Van Der Meer, B. J. Kullberg, and M. G. Netea. 2010. Candida albicans releases soluble factors that potentiate cytokine production by human cells through a protease-activated receptor 1- and 2-independent pathway. Infect. Immun. 78:393-399.
8. Dagia, N. M., G. Agarwal, D. V. Kamath, A. Chetrapal-Kunwar, R. D. Gupte, M. G. Jadhav, S. S. Dadarkar, J. Trivedi, A. A. Kulkarni-Almeida, F. Kharas, L. C. Fonseca, S. Kumar, and M. R. Bhonde. 2010. A preferential p110alpha/gamma PI3K inhibitor attenuates experimental inflammation by suppressing the production of proinflammatory mediators in NF-kappaB dependent manner. Am. J. Physiol. Cell. Physiol. 298:C929-C941.
9. Dalle, F., B. Wachtler, C. L'Ollivier, G. Holland, N. Bannert, D. Wilson, C. Labruere, A. Bonnin, and B. Hube. 2010. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell. Microbiol. 12:248-271.
10. De Bernardis, F., A. Cassone, J. Sturtevant, and R. Calderone. 1995. Expression of Candida albicans SAP1 and SAP2 in experimental vaginitis. Infect. Immun. 63:1887-1892.
11. Dillon, R. L., D. E. White, and W. J. Muller. 2007. The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer. Oncogene 26:1338-1345.
12. Fradin, C., and B. Hube. 2003. Tissue infection and site-specific gene expression in Candida albicans. Adv. Appl. Microbiol. 53:271-290.
13. Gropp, K., L. Schild, S. Schindler, B. Hube, P. F. Zipfel, and C. Skerka. 2009. The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol. Immunol. 47:465-475.
14. Hajishengallis, G., H. Sojar, R. J. Genco, and E. DeNardin. 2004. Intracellular signaling and cytokine induction upon interactions of Porphyromonas gingivalis fimbriae with pattern-recognition receptors. Immunol. Invest. 33: 157-172.
15. Hawkins, P. T., K. E. Anderson, K. Davidson, and L. R. Stephens. 2006. Signalling through class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34:647-662.
16. Hollenberg, M. D., and S. J. Compton. 2002. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol. Rev. 54:203-217.
17. Hornbach, A., A. Heyken, L. Schild, B. Hube, J. Loffler, and O. Kurzai. 2009. The glycosylphosphatidylinositol-anchored protease Sap9 modulates the interaction of Candida albicans with human neutrophils. Infect. Immun. 77: 5216-5224.
18. Hube, B. 1996. Candida albicans secreted aspartyl proteinases. Curr. Top. Med. Mycol. 7:55-69.
19. Hube, B. 2004. From commensal to pathogen: stage- and tissue-specific gene expression of Candida albicans. Curr. Opin. Microbiol. 7:336-341.
20. Hube, B., M. Monod, D. A. Schofield, A. J. Brown, and N. A. Gow. 1994. Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans. Mol. Microbiol. 14:87-99.
21. Ibrahim, A. S., S. G. Filler, D. Sanglard, J. E. Edwards, Jr., and B. Hube. 1998. Secreted aspartyl proteinases and interactions of Candida albicans with human endothelial cells. Infect. Immun. 66:3003-3005.
22. Karkowska-Kuleta, J., M. Rapala-Kozik, and A. Kozik. 2009. Fungi pathogenic to humans: molecular bases of virulence of Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus. Acta Biochim. Pol. 56:211-224.
23. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13:816-825.
24. Koelsch, G., J. Tang, J. A. Loy, M. Monod, K. Jackson, S. I. Foundling, and X. Lin. 2000. Enzymic characteristics of secreted aspartic proteases of Candida albicans. Biochim. Biophys. Acta 1480:117-131.
25. Koelsch, G., J. Tang, M. Monod, S. I. Foundling, and X. Lin. 1998. Primary substrate specificities of secreted aspartic proteases of Candida albicans. Adv. Exp. Med. Biol. 436:335-338.
26. Krishnan, J., G. Lee, and S. Choi. 2009. Drugs targeting Toll-like receptors. Arch. Pharm. Res. 32:1485-1502.
27. Lermann, U., and J. Morschhauser. 2008. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 154:3281-3295.
28. Lewis, R. E. 2009. Overview of the changing epidemiology of candidemia. Curr. Med. Res. Opin. 25:1732-1740.
29. Macdonald, F., and F. C. Odds. 1980. Inducible proteinase of Candida albicans in diagnostic serology and in the pathogenesis of systemic candidosis. J. Med. Microbiol. 13:423-435.
30. Martelli, A. M., F. Chiarini, C. Evangelisti, C. Grimaldi, A. Ognibene, L. Manzoli, A. M. Billi, and J. A. McCubrey. 2010. The phosphatidylinositol 3-kinase/AKT/mammalian target of rapamycin signaling network and the control of normal myelopoiesis. Histol. Histopathol. 25:669-680.
31. Mavor, A. L., S. Thewes, and B. Hube. 2005. Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr. Drug Targets 6:863-874. (Pubitemid 41672448)
32. Meiller, T. F., B. Hube, L. Schild, M. E. Shirtliff, M. A. Scheper, R. Winkler, A. Ton, and M. A. Jabra-Rizk. 2009. A novel immune evasion strategy of Candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS One 4:e5039.
33. Monod, M., and M. Borg-von Zepelin. 2002. Secreted aspartic proteases as virulence factors of Candida species. Biol. Chem. 383:1087-1093.
34. Naglik, J., A. Albrecht, O. Bader, and B. Hube. 2004. Candida albicans proteinases and host/pathogen interactions. Cell. Microbiol. 6:915-926.
35. Naglik, J. R., S. J. Challacombe, and B. Hube. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 67:400-428.
36. Naglik, J. R., D. Moyes, J. Makwana, P. Kanzaria, E. Tsichlaki, G. Weindl, A. R. Tappuni, C. A. Rodgers, A. J. Woodman, S. J. Challacombe, M. Schaller, and B. Hube. 2008. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 154:3266-3280.
37. Naglik, J. R., G. Newport, T. C. White, L. L. Fernandes-Naglik, J. S. Greenspan, D. Greenspan, S. P. Sweet, S. J. Challacombe, and N. Agabian. 1999. In vivo analysis of secreted aspartyl proteinase expression in human oral candidiasis. Infect. Immun. 67:2482-2490.
38. Okada, T., L. Sakuma, Y. Fukui, O. Hazeki, and M. Ui. 1994. Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:3563-3567.
39. Okkenhaug, K., and B. Vanhaesebroeck. 2003. PI3K in lymphocyte development, differentiation and activation. Nat. Rev. Immunol. 3:317-330.
40. Pagano, R. L., S. C. Sampaio, M. A. Juliano, L. Juliano, and R. Giorgi. 2010. Involvement of proteinase-activated receptors 1 and 2 in spreading and phagocytosis by murine adherent peritoneal cells: modulation by the Cterminal of S100A9 protein. Eur. J. Pharmacol. 628:240-246.
41. Palmerini, C. A., M. Mazzoni, C. Saccardi, and G. Arienti. 2008. The cytosolic calcium concentration is affected by S-nitrosocysteine in human lymphomonocytes. J. Biochem. Mol. Toxicol. 22:35-40.
42. Pietrella, D., P. Lupo, A. Rachini, S. Sandini, A. Ciervo, S. Perito, F. Bistoni, and A. Vecchiarelli. 2008. A Candida albicans mannoprotein deprived of its mannan moiety is efficiently taken up and processed by human dendritic cells and induces T-cell activation without stimulating proinflammatory cytokine production. Infect. Immun. 76:4359-4367.
43. Powis, G., R. Bonjouklian, M. M. Berggren, A. Gallegos, R. Abraham, C. Ashendel, L. Zalkow, W. F. Matter, J. Dodge, G. Grindey, et al. 1994. Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res. 54:2419-2423.
44. Restani, P., A. Fiocchi, B. Beretta, T. Velonà, M. Giovannini, and C. L. Galli. 1997. Studies on the antigenic properties of serum albumins. Lett. Pept. Sci. 4:269-273.
45. Richardson, M. D. 2005. Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56(Suppl. 1):i5-i11.
46. Ripeau, J. S., M. Fiorillo, F. Aumont, P. Belhumeur, and L. de Repentigny. 2002. Evidence for differential expression of Candida albicans virulence genes during oral infection in intact and human immunodeficiency virus type 1-transgenic mice. J. Infect. Dis. 185:1094-1102.
47. Ruchel, R., F. Zimmermann, B. Boning-Stutzer, and U. Helmchen. 1991. Candidiasis visualised by proteinase-directed immunofluorescence. Virchows Arch. A Pathol. Anat. Histopathol. 419:199-202.
48. Sandini, S., R. La Valle, F. De Bernardis, C. Macri, and A. Cassone. 2007. The 65 kDa mannoprotein gene of Candida albicans encodes a putative beta-glucanase adhesin required for hyphal morphogenesis and experimental pathogenicity. Cell. Microbiol. 9:1223-1238.
49. Schaller, M., M. Bein, H. C. Korting, S. Baur, G. Hamm, M. Monod, S. Beinhauer, and B. Hube. 2003. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect. Immun. 71:3227-3234.
50. Schaller, M., C. Borelli, H. C. Korting, and B. Hube. 2005. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48:365-377. (Pubitemid 43942679)
51. Schaller, M., H. C. Korting, C. Borelli, G. Hamm, and B. Hube. 2005. Candida albicans-secreted aspartic proteinases modify the epithelial cytokine response in an in vitro model of vaginal candidiasis. Infect. Immun. 73:2758-2765.
52. Schaller, M., H. C. Korting, W. Schafer, J. Bastert, W. Chen, and B. Hube. 1999. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol. Microbiol. 34:169-180.
53. Shpacovitch, V., M. Feld, N. W. Bunnett, and M. Steinhoff. 2007. Protease-activated receptors: novel PARtners in innate immunity. Trends Immunol. 28:541-550. (Pubitemid 350101418)
54. Sigurdardottir, T., V. Bjorck, H. Herwald, M. Morgelin, S. Rutardottir, J. Tornebrant, and M. Bodelsson. 2010. M1 protein from Streptococcus pyogenes induces nitric oxide-mediated vascular hyporesponsiveness to phenylephrine: involvement of Toll-like receptor activation. Shock 34:98-104.
55. Smolenski, G., P. A. Sullivan, S. M. Cutfield, and J. F. Cutfield. 1997. Analysis of secreted aspartic proteinases from Candida albicans: purification and characterization of individual Sap1, Sap2 and Sap3 isoenzymes. Microbiology 143:349-356.
56. Staib, P., M. Kretschmar, T. Nichterlein, H. Hof, and J. Morschhauser. 2000. Differential activation of a Candida albicans virulence gene family during infection. Proc. Natl. Acad. Sci. U. S. A. 97:6102-6107.
57. Staib, P., M. Kretschmar, T. Nichterlein, G. Kohler, S. Michel, H. Hof, J. Hacker, and J. Morschhauser. 1999. Host-induced, stage-specific virulence gene activation in Candida albicans during infection. Mol. Microbiol. 32: 533-546.
58. Stringaro, A., P. Crateri, G. Pellegrini, G. Arancia, A. Cassone, and F. De Bernardis. 1997. Ultrastructural localization of the secretory aspartyl proteinase in Candida albicans cell wall in vitro and in experimentally infected rat vagina. Mycopathologia 137:95-105.
59. Takahashi, A., P. Camacho, J. D. Lechleiter, and B. Herman. 1999. Measurement of intracellular calcium. Physiol. Rev. 79:1089-1125.
60. Taylor, B. N., P. Staib, A. Binder, A. Biesemeier, M. Sehnal, M. Rollinghoff, J. Morschhauser, and K. Schroppel. 2005. Profile of Candida albicans-secreted aspartic proteinase elicited during vaginal infection. Infect. Immun. 73:1828-1835.
61. Verduyn Lunel, F. M., J. F. Meis, and A. Voss. 1999. Nosocomial fungal infections: candidemia. Diagn. Microbiol. Infect. Dis. 34:213-220.
62. Yang, Y. L. 2003. Virulence factors of Candida species. J. Microbiol. Immunol. Infect. 36:223-228.
63. Zhang, N., M. H. Ahsan, L. Zhu, L. C. Sambucetti, A. F. Purchio, and D. B. West. 2005. Regulation of IkappaBalpha expression involves both NFkappaB and the MAP kinase signaling pathways. J. Inflamm. (London) 2:10.
64. Zhu, W., and S. G. Filler. 2010. Interactions of Candida albicans with epithelial cells. Cell. Microbiol. 12:273-282.