The yeast Candida albicans evades human complement attack by secretion of aspartic proteases

Molecular Immunology

Volumn 47, Issue 2-3, 2009, Pages 465-475

  Gropp, Katharina ^a   Schild, Lydia ^b   Schindler, Susann ^a   Hube, Bernhard ^b,c   Zipfel, Peter F ^a,c   Skerka, Christine ^a  

^a HANS KNÖLL INSTITUTE   (Germany)

^b Research and Infection Biology   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Candida albicans; Complement; Immune evasion; Secreted aspartic proteases

Indexed keywords

ASPARTIC PROTEINASE; COMPLEMENT; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C4B; COMPLEMENT COMPONENT C5; FUNGAL PROTEIN; PROTEIN SAP1; PROTEIN SAP2; PROTEIN SAP3; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CELL SURFACE; CONTROLLED STUDY; ENZYME RELEASE; ERYTHROCYTE; FUNGAL CELL; HEMOLYSIS; HUMAN; HUMAN CELL; IMMUNOREGULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; WILD TYPE; YEAST;

ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CANDIDA ALBICANS; COMPLEMENT MEMBRANE ATTACK COMPLEX; COMPLEMENT PATHWAY, ALTERNATIVE; COMPLEMENT PATHWAY, CLASSICAL; ERYTHROCYTES; HEMOLYSIS; HUMANS; IMMUNE EVASION; OPSONIN PROTEINS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RABBITS; RECEPTOR, ANAPHYLATOXIN C5A; RECOMBINANT PROTEINS; SUBCELLULAR FRACTIONS;

CANDIDA ALBICANS; ORYCTOLAGUS CUNICULUS;

EID: 70450225229     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.08.019     Document Type: Article

References (42)

1. Albrecht A., Felk A., Pichova I., Naglik J.R., Schaller M., de Groot P., Maccallum D., Odds F.C., Schafer W., Klis F., Monod M., and Hube B. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281 (2006) 688-694
2. Behnsen J., Hartmann A., Schmaler J., Gehrke A., Brakhage A.A., and Zipfel P.F. The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system. Infect. Immun. 76 (2008) 820-827
3. Borg-von Zepelin M., Beggah S., Boggian K., Sanglard D., and Monod M. The expression of the secreted aspartyl proteases Sap4 to Sap6 from Candida albicans in murine macrophages. Mol. Microbiol. 28 (1998) 543-554
4. Calderone, and San Blas G. Pathogenic fungi: host interactions and emerging strategies for control. In: Schaller M., Korting H.C., and Hube B. (Eds). Virulence Factors That Promote Invasion of Candida albicans (2004), Caister Academic Press 97-127 Chapter 3
5. Enfert C.D., and Hube B. Candida: comparative and functional genomics (2007), Caister Acedemic Press, Wymondham, Norfolk, U.K.
6. Faux J.A., Agbarakwe A.E., Misbah S.A., and Chapel H.M. A comparison of specific IgG antibody levels to the cell wall mannan of Candida albicans in normal individuals and in patients with primary antibody deficiency. J. Immunol. Methods 153 (1992) 167-172
7. Feilotter H.E., Hannon G.J., Ruddell C.J., and Beach D. Construction of an improved host strain for two hybrid screening. Nucleic Acids Res. 22 (1994) 1502-1503
8. Felk A., Kretschmar M., Albrecht A., Schaller M., Beinhauer S., Nichterlein T., Sanglard D., Korting H.C., Schafer W., and Hube B. Candida albicans hyphal formation and the expression of the Efg1-regulated proteases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect. Immun. 70 (2002) 3689-3700
9. Filler S.G., and Sheppard D.C. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2 (2006) e129
10. Frohner I.E., Bourgeois C., Yatsyk K., Majer O., and Kuchler K. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71 (2009) 240-252
11. Lambris J.D., Ricklin D., and Geisbrecht B.V. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6 (2008) 132-142 Review
12. Gillum A.M., Tsay E.Y., and Kirsch D.R. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198 (1984) 179-182
13. Heinen S., Hartmann A., Lauer N., Wiehl U., Dahse H.M., Schirmer S., Gropp K., Enghardt T., Wallich R., Hälbich S., Mihlan M., Schlötzer-Schrehardt U., Zipfel P.F., Skerka C., 2009. Factor H related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood, in press.
14. Hube B., and Naglik J. Candida albicans proteases: resolving the mystery of a gene family. Microbiology 147 (2001) 1997-2005
15. Hube B., Sanglard D., Odds F.C., Hess D., Monod M., Schafer W., Brown A.J., and Gow N.A. Disruption of each of the secreted aspartyl protease genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence. Infect. Immun. 65 (1997) 3529-3538
16. Kaminishi H., Miyaguchi H., Tamaki T., Suenaga N., Hisamatsu M., Mihashi I., Matsumoto H., Maeda H., and Hagihara Y. Degradation of humoral host defense by Candida albicans protease. Infect. Immun. 63 (1995) 984-988
17. Kraiczy P., Skerka C., Kirschfink M., Brade V., and Zipfel P.F. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H. Eur. J. Immunol. 31 (2001) 1674-1684
18. Kretschmar M., Felk A., Staib P., Schaller M., Hess D., Callapina M., Morschhauser J., Schafer W., Korting H.C., Hof H., Hube B., and Nichterlein T. Individual acid aspartic proteases (Saps) 1-6 of Candida albicans are not essential for invasion and colonization of the gastrointestinal tract in mice. Microb. Pathog. 32 (2002) 61-70
19. Kunert A., Losse J., Gruszin C., Hühn M., Kaendler K., Mikkat S., Volke D., Hoffmann R., Jokiranta T.S., Seeberger H., Moellmann U., Hellwage J., and Zipfel P.F. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a Factor H and plasminogen binding protein. J. Immunol. 179 (2007) 2979-2988
20. Luo S., Poltermann S., Kunert A., Rupp S., Zipfel P.F., 2009. Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a Factor H, FHL-1 and Plasminogen binding surface protein. Mol. Immunol., in press.
21. McCabe R.E., and Mullins B.T. Failure of Trypanosoma cruzi to trigger the respiratory burst of activated macrophages. Mechanism for immune evasion and importance of oxygen-independent killing. J. Immunol. 144 (1990) 2384-2388
22. 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. 72 (2004) 6633-6641
23. Meri T., Hartmann A., Lenk D., Eck R., Wurzner R., Hellwage J., Meri S., and Zipfel P.F. The yeast Candida albicans binds complement regulators Factor H and FHL-1. Infect. Immun. 70 (2002) 5185-5192
24. Nagl M., Gruber A., Fuchs A., Lell C.P., Lemberger E.M., Borg-Von Zepelin M., and Wurzner R. Impact of N-chlorotaurine on viability and production of secreted aspartyl proteases of Candida spp. Antimicrob. Agents Chemother. 46 (2002) 1996-1999
25. Naglik J., Albrecht A., Bader O., and Hube B. Candida albicans proteases and host/pathogen interactions. Cell Microbiol. 6 (2004) 915-926
26. Naglik J.R., Moyes D., Makwana J., Kanzaria P., Tsichlaki E., Weindl G., Tappuni A.R., Rodgers C.A., Woodman A.J., Challacombe S.J., Schaller M., and Hube B. Quantitative expression of the Candida albicans secreted aspartyl protease gene family in human oral and vaginal candidiasis. Microbiology 154 (2008) 3266-3280
27. Netea M.G., van der Meer J.W., and Kullberg B.J. Both TLR2 and TLR4 are involved in the recognition of Candida albicans. Reply to "TLR2, but not TLR4, triggers cytokine production by murine cells in response to Candida albicans yeasts and hyphae" by Gil and Gozalbo. Microb. Infect. 8 (2006) 2821-2822 author reply 2823-4
28. Perlroth J., Choi B., and Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45 (2007) 321-346
29. Pfaller M.A., and Diekema D.J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20 (2007) 133-163
30. Phan Q.T., Myers C.L., Fu Y., Sheppard D.C., Yeaman M.R., Welch W.H., Ibrahim A.S., Edwards Jr. J.E., and Filler S.G. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5 (2007) e64
31. Poltermann S., Kunert A., von der Heide 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. 282 (2007) 37537-37544
32. Quin L.R., Onwubiko C., Moore Q.C., Mills M.F., McDaniel L.S., and Carmicle S. Factor H binding to PspC of Streptococcus pneumoniae increases adherence to human cell lines in vitro and enhances invasion of mouse lungs in vivo. Infect. Immun. 75 (2007) 4082-4087
33. Jongerius I., Köhl J., Pandey M.K., Ruyken M., van Kessel K.P., van Strijp J.A., and Rooijakkers S.H. Staphylococcal complement evasion by various convertase-blocking molecules. J. Exp. Med. 204 (2007) 2461-2471
34. Schaller M., Borelli C., Korting H.C., and Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48 (2005) 365-377
35. Schenkein H.A., Fletcher H.M., Bodnar M., and Macrina F.L. Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J. Immunol. 154 (1995) 5331-5337
36. Tavanti A., Pardini G., Campa D., Davini P., Lupetti A., and Senesi S. Differential expression of secretory aspartyl proteinase genes (SAP1-10) in oral Candida albicans isolates with distinct karyotypes. J. Clin. Microbiol. 42 10 (2004) 4726-4734
37. Tronchin G., Pihet M., Lopes-Bezerra L.M., and Bouchara J.P. Adherence mechanisms in human pathogenic fungi. Med. Mycol. 46 (2008) 749-772
38. Walport M.J. Complement. First of two parts. N Engl. J. Med. 344 (2001) 1058-1066
39. Walport M.J. Complement. Second of two parts. N Engl. J. Med. 344 (2001) 1140-1144
40. Zipfel P.F., 2009. Complement and immune defense: from innate immunity to human diseases. Immunol. Lett., in press.
41. Zipfel P.F., Halström T., Hammerschmidt S., and Skerka C. The complement fitness Factor H: Role in human diseases and for immune escape of pathogenes, like pneumococci. Vaccine 265 (2008) 167-174
42. Zipfel P.F., Skerka C., 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. in press.