Candida albicans possesses Sap7 as a pepstatin A-insensitive secreted aspartic protease

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Aoki, Wataru ^a,b   Kitahara, Nao ^b   Miura, Natsuko ^a,b   Morisaka, Hironobu ^b   Yamamoto, Yoshihiro ^c   Kuroda, Kouichi ^b   Ueda, Mitsuyoshi ^b  

^a JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c Kyoto Municipal Institute of Industrial Technology and Culture   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC PROTEINASE; METHIONINE; PEPSTATIN; PROTEIN SAP7; THREONINE; UNCLASSIFIED DRUG; ISOPROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; ENZYME ACTIVE SITE; FUNGAL GENE; MOLECULAR CLONING; MUTANT; NONHUMAN; PICHIA PASTORIS; PROTEIN DEGRADATION; SAP7 GENE; WILD TYPE; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MUTATION; PICHIA; PLASMID; PROTEIN TERTIARY STRUCTURE; SEQUENCE ANALYSIS; VIRULENCE;

CANDIDA ALBICANS; PICHIA PASTORIS;

AMINO ACID SEQUENCE; ASPARTIC ACID PROTEASES; CANDIDA ALBICANS; CATALYTIC DOMAIN; CLONING, MOLECULAR; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; PEPSTATINS; PICHIA; PLASMIDS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, PROTEIN; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE;

EID: 84857604682     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032513     Document Type: Article

References (48)

1. Naglik JR, Challacombe SJ, Hube B, (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400-428.
2. Sobel JD, (1992) Pathogenesis and treatment of recurrent vulvovaginal candidiasis. Clin Infect Dis 14: 148-153.
3. Sobel JD, (1988) Pathogenesis and epidemiology of vulvovaginal candidiasis. Ann N Y Acad Sci 544: 547-557.
4. Schaller M, Borelli C, Korting HC, Hube B, (2005) Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48: 365-377.
5. Calderone RA, Fonzi WA, (2001) Virulence factors of Candida albicans. Trends Microbiol 9: 327-335.
6. Naglik J, Albrecht A, Bader O, Hube B, (2004) Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 6: 915-926.
7. Schaller M, Januschke E, Schackert C, Woerle B, Korting HC, (2001) Different isoforms of secreted aspartyl proteinases (Sap) are expressed by Candida albicans during oral and cutaneous candidosis in vivo. J Med Microbiol 50: 743-747.
8. White TC, Miyasaki SH, Agabian N, (1993) Three distinct secreted aspartyl proteinases in Candida albicans. J Bacteriol 175: 6126-6133.
9. 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.
10. Taylor BN, Hannemann H, Sehnal M, Biesemeier A, Schweizer A, et al. (2005) Induction of SAP7 correlates with virulence in an intravenous infection model of candidiasis but not in a vaginal infection model in mice. Infect Immun 73: 7061-7063.
11. Naglik JR, Moyes D, Makwana J, Kanzaria P, Tsichlaki E, et al. (2008) Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 154: 3266-3280.
12. Monod M, Hube B, Hess D, Sanglard D, (1998) Differential regulation of SAP8 and SAP9, which encode two new members of the secreted aspartic proteinase family in Candida albicans. Microbiology 144: 2731-2737.
13. Albrecht A, Felk A, Pichova I, Naglik JR, Schaller M, et al. (2006) Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J Biol Chem 281: 688-694.
14. Schild L, Heyken A, de Groot PW, Hiller E, Mock M, et al. (2011) Proteolytic cleavage of covalently linked cell wall proteins by Candida albicans Sap9 and Sap10. Eukaryot Cell 10: 98-109.
15. Hornbach A, Heyken A, Schild L, Hube B, Loffler J, et al. (2009) The glycosylphosphatidylinositol-anchored protease Sap9 modulates the interaction of Candida albicans with human neutrophils. Infect Immun 77: 5216-5224.
16. Colina AR, Aumont F, Deslauriers N, Belhumeur P, de Repentigny L, (1996) Evidence for degradation of gastrointestinal mucin by Candida albicans secretory aspartyl proteinase. Infect Immun 64: 4514-4519.
17. Kaminishi H, Miyaguchi H, Tamaki T, Suenaga N, Hisamatsu M, et al. (1995) Degradation of humoral host defense by Candida albicans proteinase. Infect Immun 63: 984-988.
18. Ruchel R, (1986) Cleavage of immunoglobulins by pathogenic yeasts of the genus Candida. Microbiol Sci 3: 316-319.
19. Gropp K, Schild L, Schindler S, Hube B, Zipfel PF, et al. (2009) The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol Immunol 47: 465-475.
20. Villar CC, Kashleva H, Nobile CJ, Mitchell AP, Dongari-Bagtzoglou A, (2007) Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p. Infect Immun 75: 2126-2135.
21. Schaller M, Bein M, Korting HC, Baur S, Hamm G, et al. (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.
22. Aoki W, Kitahara N, Miura N, Morisaka H, Yamamoto Y, et al. (2011) Comprehensive characterization of secreted aspartic proteases encoded by a virulence gene family in Candida albicans. J Biochem 150: 431-438.
23. Berman J, Sudbery PE, (2002) Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3: 918-930.
24. Arnaud MB, Costanzo MC, Skrzypek MS, Binkley G, Lane C, et al. (2005) The Candida Genome Database (CGD), a community resource for Candida albicans gene and protein information. Nucleic Acids Res 33: 358-363.
25. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
26. Cutfield SM, Dodson EJ, Anderson BF, Moody PC, Marshall CJ, et al. (1995) The crystal structure of a major secreted aspartic proteinase from Candida albicans in complexes with two inhibitors. Structure 3: 1261-1271.
27. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
28. Laskowski RA, (2009) PDBsum new things. Nucleic Acids Res 37: 355-359.
29. Tanskul S, Oda K, Oyama H, Noparatnaraporn N, Tsunemi M, et al. (2003) Substrate specificity of alkaline serine proteinase isolated from photosynthetic bacterium, Rubrivivax gelatinosus KDDS1. Biochem Biophys Res Commun 309: 547-551.
30. Aoki W, Kitahara N, Miura N, Morisaka H, Yamamoto Y, et al. (2011) Comprehensive characterization of secreted aspartic proteases encoded by a virulence gene family in Candida albicans. J Biochem 150: 431-438.
31. Hube B, Sanglard D, Odds FC, Hess D, Monod M, et al. (1997) Disruption of each of the secreted aspartyl proteinase genes SAP1, SAP2, and SAP3 of Candida albicans attenuates virulence. Infect Immun 65: 3529-3538.
32. Naglik JR, Newport G, White TC, Fernandes-Naglik LL, Greenspan JS, et al. (1999) In vivo analysis of secreted aspartyl proteinase expression in human oral candidiasis. Infect Immun 67: 2482-2490.
33. Smolenski G, Sullivan PA, Cutfield SM, Cutfield JF, (1997) Analysis of secreted aspartic proteinases from Candida albicans: purification and characterization of individual Sap1, Sap2 and Sap3 isoenzymes. Microbiology 143: 349-356.
34. Marciniszyn J Jr, Hartsuck JA, Tang J, (1976) Mode of inhibition of acid proteases by pepstatin. J Biol Chem 251: 7088-7094.
35. Marciniszyn J Jr, Hartsuck JA, Tang J, (1977) Pepstatin inhibition mechanism. Adv Exp Med Biol 95: 199-210.
36. Fujinaga M, Cherney MM, Oyama H, Oda K, James MN, (2004) The molecular structure and catalytic mechanism of a novel carboxyl peptidase from Scytalidium lignicolum. Proc Natl Acad Sci U S A 101: 3364-3369.
37. Sims AH, Dunn-Coleman NS, Robson GD, Oliver SG, (2004) Glutamic protease distribution is limited to filamentous fungi. FEMS Microbiol Lett 239: 95-101.
38. Gemmill TR, Trimble RB, (1999) Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim Biophys Acta 1426: 227-237.
39. Chen YC, Wu CC, Chung WL, Lee FJ, (2002) Differential secretion of Sap4-6 proteins in Candida albicans during hyphae formation. Microbiology 148: 3743-3754.
40. Schild L, Heyken A, de Groot PW, Hiller E, Mock M, et al. (2011) Proteolytic cleavage of covalently linked cell wall proteins by Candida albicans Sap9 and Sap10. Eukaryot Cell 10: 98-109.
41. Fallon K, Bausch K, Noonan J, Huguenel E, Tamburini P, (1997) Role of aspartic proteases in disseminated Candida albicans infection in mice. Infect Immun 65: 551-556.
42. De Bernardis F, Boccanera M, Adriani D, Spreghini E, Santoni G, et al. (1997) Protective role of antimannan and anti-aspartyl proteinase antibodies in an experimental model of Candida albicans vaginitis in rats. Infect Immun 65: 3399-3405.
43. Hube B, (1998) Possible role of secreted proteinases in Candida albicans infections. Rev Iberoam Micol 15: 65-68.
44. Sanglard D, Hube B, Monod M, Odds FC, Gow NA, (1997) A triple deletion of the secreted aspartyl proteinase genes SAP4, SAP5, and SAP6 of Candida albicans causes attenuated virulence. Infect Immun 65: 3539-3546.
45. Odds FC, (2008) Secreted proteinases and Candida albicans virulence. Microbiology 154: 3245-3246.
46. Lermann U, Morschhauser J, (2008) Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 154: 3281-3295.
47. Kretschmar M, Felk A, Staib P, Schaller M, Hess D, et al. (2002) Individual acid aspartic proteinases (Saps) 1-6 of Candida albicans are not essential for invasion and colonization of the gastrointestinal tract in mice. Microb Pathog 32: 61-70.
48. Edison AM, Manning-Zweerink M, (1988) Comparison of the extracellular proteinase activity produced by a low-virulence mutant of Candida albicans and its wild-type parent. Infect Immun 56: 1388-1390.