Complement plays a central role in Candida albicans-induced cytokine production by human PBMCs

European Journal of Immunology

Volumn 42, Issue 4, 2012, Pages 993-1004

  Cheng, Shih Chin ^a   Sprong, Tom ^a   Joosten, Leo A B ^a   van der Meer, Jos W M ^a   Kullberg, Bart Jan ^a   Hube, Bernhard ^b,c   Schejbel, Lone ^d   Garred, Peter ^d   van Deuren, Marcel ^a   Netea, Mihai G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b HANS KNÖLL INSTITUTE   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d University of Copenhagen   (Denmark)

Author keywords

C5a; Candida; Complement; IL 1 ; IL 6

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT COMPONENT C6; COMPLEMENT MEMBRANE ATTACK COMPLEX; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ARTICLE; CANDIDA ALBICANS; COMPLEMENT ACTIVATION; COMPLEMENT DEFICIENCY; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; HOST RESISTANCE; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL;

CANDIDA ALBICANS; CANDIDIASIS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MONOCYTES; SIGNAL TRANSDUCTION;

EID: 84860260355     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142057     Document Type: Article

References (55)

1. Ferwerda, B., Ferwerda, G., Plantinga, T. S., Willment, J. A., van Spriel, A. B., Venselaar, H., Elbers, C. C. et al., Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 2009. 361: 1760-1767.
2. Koh, A. Y., Kohler, J. R., Coggshall, K. T., Van, R. N. and Pier, G. B., Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 2008. 4: e35.
3. Perlroth, J., Choi, B. and Spellberg, B., Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 2007. 45: 321-346.
4. Netea, M. G., Gow, N. A., Munro, C. A., Bates, S., Collins, C., Ferwerda, G., Hobson, R. P. et al., Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 2006. 116: 1642-1650.
5. Heinsbroek, S. E., Taylor, P. R., Martinez, F. O., Martinez-Pomares, L., Brown, G. D. and Gordon, S., Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog. 2008. 4: e1000218.
6. Netea, M. G., Brown, G. D., Kullberg, B. J. and Gow, N. A. R., An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Micro. 2008. 6: 67-78.
7. Ricklin, D., Hajishengallis, G., Yang, K. and Lambris, J. D., Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010. 11: 785-797.
8. Zhang, M. X., Lupan, D. M. and Kozel, T. R., Mannan-specific immunoglobulin G antibodies in normal human serum mediate classical pathway initiation of C3 binding to Candida albicans. Infect. Immun. 1997. 65: 3822-3827.
9. Zhang, M. X. and Kozel, T. R., Mannan-specific immunoglobulin G antibodies in normal human serum accelerate binding of C3 to Candida albicans via the alternative complement pathway. Infect. Immun. 1998. 66: 4845-4850.
10. Sealy, P. I., Garner, B., Swiatlo, E., Chapman, S. W. and Cleary, J. D., The interaction of mannose binding lectin (MBL) with mannose containing glycopeptides and the resultant potential impact on invasive fungal infection. Med. Mycol. 2008. 1-9.
11. Marodi, L., Korchak, H. M. and Johnston, R. B., Jr., Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derived macrophages. J. Immunol. 1991. 146: 2783-2789.
12. Speth, C., Rambach, G., Wurzner, R. and Lass-Florl, C., Complement and fungal pathogens: an update. Mycoses 2008. 51: 477-496.
13. Kozel, T. R., Activation of the complement system by pathogenic fungi. Clin. Microbiol. Rev. 1996. 9: 34-46.
14. Klos, A., Tenner, A. J., Johswich, K. O., Ager, R. R., Reis, E. S. and Kohl, J., The role of the anaphylatoxins in health and disease. Mol. Immunol. 2009. 46: 2753-2766.
15. Sonesson, A., Ringstad, L., Nordahl, E. A., Malmsten, M., Morgelin, M. and Schmidtchen, A., Antifungal activity of C3a and C3a-derived peptides against Candida. Biochim. Biophys. Acta 2007. 1768: 346-353.
16. Mollnes, T. E., Brekke, O. L., Fung, M., Fure, H., Christiansen, D., Bergseth, G., Videm, V. et al., Essential role of the C5a receptor in E. coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 2002. 100: 1869-1877.
17. Sprong, T., Brandtzaeg, P., Fung, M., Pharo, A. M., Hoiby, E. A., Michaelsen, T. E., Aase, A. et al., Inhibition of C5a-induced inflammation with preserved C5b-9-mediated bactericidal activity in a human whole blood model of meningococcal sepsis. Blood 2003. 102: 3702-3710.
18. Brouwer, N., Dolman, K. M., van, H. M., Sta, M., Roos, D. and Kuijpers, T. W., Mannose-binding lectin (MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J. Immunol. 2008. 180: 4124-4132.
19. Guo, R. F. and Ward, P. A., Role of C5a in inflammatory responses. Annu. Rev. Immunol. 2005. 23: 821-852.
20. Wetsel, R. A., Structure, function and cellular expression of complement anaphylatoxin receptors. Curr. Opin. Immunol. 1995. 7: 48-53.
21. Sumichika, H., Sakata, K., Sato, N., Takeshita, S., Ishibuchi, S., Nakamura, M., Kamahori, T. et al., Identification of a potent and orally active non-peptide C5a receptor antagonist. J. Biol. Chem. 2002. 277: 49403-49407.
22. Luo, S., Hartmann, A., Dahse, H. M., Skerka, C. and Zipfel, P. F., Secreted pH-regulated antigen 1 of Candida albicans blocks activation and conversion of complement C3. J. Immunol. 2010. 185: 2164-2173.
23. Luo, S., Blom, A. M., Rupp, S., Hipler, U. C., Hube, B., Skerka, C. and Zipfel, P. F., The pH-regulated antigen 1 of Candida albicans binds the human complement inhibitor C4b-binding protein and mediates fungal complement evasion. J. Biol. Chem. 2011. 286: 8021-8029.
24. Ip, W. K. and Lau, Y. L., Role of mannose-binding lectin in the innate defense against Candida albicans: enhancement of complement activation, but lack of opsonic function, in phagocytosis by human dendritic cells. J. Infect. Dis. 2004. 190: 632-640.
25. Kagaya, K. and Fukazawa, Y., Murine defense mechanism against Candida albicans infection. II. Opsonization, phagocytosis, and intracellular killing of C. albicans. Microbiol. Immunol. 1981. 25: 807-818.
26. Solomkin, J. S., Mills, E. L., Giebink, G. S., Nelson, R. D., Simmons, R. L. and Quie, P. G., Phagocytosis of Candida albicans by human leukocytes: opsonic requirements. J. Infect. Dis. 1978. 137: 30-37.
27. Gropp, K., Schild, L., Schindler, S., Hube, B., Zipfel, P. F. and Skerka, C., The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol. Immunol. 2009. 47: 465-475.
28. Meri, T., Blom, A. M., Hartmann, A., Lenk, D., Meri, S. and Zipfel, P. F., The hyphal and yeast forms of Candida albicans bind the complement regulator C4b-binding protein. Infect. Immun. 2004. 72: 6633-6641.
29. Meri, T., Hartmann, A., Lenk, D., Eck, R., Wurzner, R., Hellwage, J., Meri, S. et al., The yeast Candida albicans binds complement regulators factor H and FHL-1. Infect. Immun. 2002. 70: 5185-5192.
30. Poltermann, S., Kunert, A., von der, H. M., Eck, R., Hartmann, A. and Zipfel, P. F., Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 2007. 282: 37537-37544.
31. Lesiak-Markowicz, I., Vogl, G., Schwarzmuller, T., Speth, C., Lass-Florl, C., Dierich, M. P., Kuchler, K. et al., Candida albicans Hgt1p, a multifunctional evasion molecule: complement inhibitor, CR3 analogue, and human immunodeficiency virus-binding molecule. J. Infect. Dis. 2011. 204: 802-809.
32. Boxx, G. M., Kozel, T. R., Nishiya, C. T. and Zhang, M. X., Influence of mannan and glucan on complement activation and C3 binding by Candida albicans. Infect. Immun. 2010. 78: 1250-1259.
33. Hajishengallis, G. and Lambris, J. D., Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol. 2010. 31: 154-163.
34. Riedemann, N. C., Guo, R. F., Bernacki, K. D., Reuben, J. S., Laudes, I. J., Neff, T. A., Gao, H. et al., Regulation by C5a of neutrophil activation during sepsis. Immunity 2003. 19: 193-202.
35. Cavaillon, J. M., Fitting, C. and Haeffner-Cavaillon, N., Recombinant C5a enhances interleukin 1 and tumor necrosis factor release by lipopolysaccharide-stimulated monocytes and macrophages. Eur. J. Immunol. 1990. 20: 253-257.
36. Wang, M., Krauss, J. L., Domon, H., Hosur, K. B., Liang, S., Magotti, P., Triantafilou, M. et al., Microbial hijacking of complement-Toll-like receptor crosstalk. Sci. Signal. 2010. 3: ra11.
37. Boxx, G. M., Nishiya, C. T., Kozel, T. R. and Zhang, M. X., Characteristics of Fc-independent human antimannan antibody-mediated alternative pathway initiation of C3 deposition to Candida albicans. Mol. Immunol. 2009. 46: 473-480.
38. Raby, A. C., Holst, B., Davies, J., Colmont, C., Laumonnier, Y., Coles, B., Shah, S. et al., TLR activation enhances C5a-induced pro-inflammatory responses by negatively modulating the second C5a receptor, C5L2. Eur. J. Immunol. 2011. 41: 2741-2752.
39. Okada, N., Asai, S., Hotta, A., Miura, N., Ohno, N., Farkas, I., Hau, L. et al., Increased inhibitory capacity of an anti-C5a complementary peptide following acetylation of N-terminal alanine. Microbiol. Immunol. 2007. 51: 439-443.
40. Fulurija, A., Ashman, R. B. and Papadimitriou, J. M., Early inflammatory responses to Candida albicans infection in inbred and complement-deficient mice. FEMS Immunol. Med. Microbiol. 1996. 14: 83-94.
41. Mullick, A., Elias, M., Picard, S., Bourget, L., Jovcevski, O., Gauthier, S., Tuite, A. et al., Dysregulated inflammatory response to Candida albicans in a C5-deficient mouse strain. Infect. Immun. 2004. 72: 5868-5876.
42. Tsoni, S. V., Kerrigan, A. M., Marakalala, M. J., Srinivasan, N., Duffield, M., Taylor, P. R., Botto, M. et al., Complement C3 plays an essential role in the control of opportunistic fungal infections. Infect. Immun. 2009. 77: 3679-3685.
43. Netea, M. G., van der Meer, J. W., van, D. M. and Kullberg, B. J., Proinflammatory cytokines and sepsis syndrome: not enough, or too much of a good thing? Trends Immunol. 2003. 24: 254-258.
44. Gerard, C., Complement C5a in the sepsis syndrome-too much of a good thing? N. Engl. J. Med. 2003. 348: 167-169.
45. Hillmen, P., Young, N. S., Schubert, J., Brodsky, R. A., Socie, G., Muus, P., Roth, A. et al., The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. N. Engl. J. Med. 2006. 355: 1233-1243.
46. Gruppo, R. A. and Rother, R. P., Eculizumab for congenital atypical hemolytic-uremic syndrome. N. Engl. J. Med. 2009. 360: 544-546.
47. Luo, S., Poltermann, S., Kunert, A., Rupp, S. and Zipfel, P. F., Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a Factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 2009. 47: 541-550.
48. van der Graaf, C. A., Netea, M. G., Verschueren, I., Van der Meer, J. W. and Kullberg, B. J., Differential cytokine production and Toll-like receptor signaling pathways by Candida albicans blastoconidia and hyphae. Infect. Immun. 2005. 73: 7458-7464.
49. Murad, A. M., Lee, P. R., Broadbent, I. D., Barelle, C. J. and Brown, A. J., CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 2000. 16: 325-327.
50. Fradin, C., de Groot, P., Maccallum, D., Schaller, M., Klis, F., Odds, F. C. and Hube, B., Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 2005. 56: 397-415.
51. Marcil, A., Gadoury, C., Ash, J., Zhang, J., Nantel, A. and Whiteway, M., Analysis of PRA1 and its relationship to Candida albicans- macrophage interactions. Infect. Immun. 2008. 76: 4345-4358.
52. Lappegard, K. T., Christiansen, D., Pharo, A., Thorgersen, E. B., Hellerud, B. C., Lindstad, J., Nielsen, E. W. et al., Human genetic deficiencies reveal the roles of complement in the inflammatory network: lessons from nature. Proc. Natl. Acad. Sci. U.S.A. 2009. 106: 15861-15866.
53. Netea, M. G., Gow, N. A., Munro, C. A., Bates, S., Collins, C., Ferwerda, G., Hobson, R. P. et al., Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 2006. 116: 1642-1650.
54. Netea, M. G., Vonk, A. G., van den, H. M., Verschueren, I., Joosten, L. A., van Krieken, J. H., van den Berg, W. B. et al., Differential role of IL-18 and IL-12 in the host defense against disseminated Candida albicans infection. Eur. J. Immunol. 2003. 33: 3409-3417.
55. Cheng, S. C., Chai, L. Y., Joosten, L. A., Vecchiarelli, A., Hube, B., van der Meer, J. W., Kullberg, B. J. et al., Candida albicans releases soluble factors that potentiate cytokine production by human cells through a protease-activated receptor 1- and 2-independent pathway. Infect. Immun. 2010. 78: 393-399.