Identification of novel secreted proteases during extracellular proteolysis by dermatophytes at acidic pH

Proteomics

Volumn 11, Issue 22, 2011, Pages 4422-4433

  Sriranganadane, Dev ^a   Waridel, Patrice ^b   Salamin, Karine ^a   Feuermann, Marc ^c   Mignon, Bernard ^d   Staib, Peter ^e   Neuhaus, Jean Marc ^f   Quadroni, Manfredo ^b   Monod, Michel ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e HANS KNÖLL INSTITUTE   (Germany)

^f UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Arthroderma benhamiae; Dermatophytes; Microbiology; Microsporum canis; Secreted proteases; Shotgun mass spectrometry

Indexed keywords

CARBOXYPEPTIDASE; PEPSIN A; PROTEINASE; SEDOLISIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACIDITY; ARTHRODERMA; ARTICLE; ASPERGILLUS; CULTURE MEDIUM; DERMATOPHYTE; ENZYME ANALYSIS; EXTRACELLULAR SPACE; FUNGAL VIRULENCE; MASS SPECTROMETRY; MICROSPORUM CANIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ARTHRODERMATACEAE; CULTURE MEDIA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXTRACELLULAR SPACE; HYDROGEN-ION CONCENTRATION; MASS SPECTROMETRY; MICROSPORUM; PEPSTATINS; PEPTIDE HYDROLASES; PEPTIDE MAPPING; PROTEOLYSIS; SOYBEAN PROTEINS;

ANIMALIA; ARTHRODERMA BENHAMIAE; ARTHRODERMATACEAE; ASPERGILLUS; FUNGI; MICROSPORUM CANIS;

EID: 80055122116     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100234     Document Type: Article

References (48)

1. Weitzman, I., Summerbell, R. C., The dermatophytes. Clin. Microbiol. Rev. 1995, 8, 240-259.
2. Taplin, D., Zaias, N., Rebell, G., Blank, H., Isolation and recognition of dermatophytes on a new medium (DTM). Arch. Derm. 1969, 99, 203-209.
3. Li, X. F., Shen, Y. N., Chen, W., Chen, H. et al., A new medium for diagnosis of dermatophyte infection. Eur. J. Dermatol. 2009, 19, 34-37.
4. Jousson, O., Léchenne, B., Bontems, O., Capoccia, S. et al., Multiplication of an ancestral gene encoding secreted fungalysin preceded species differentiation in the dermatophytes Trichophyton and Microsporum. Microbiology 2004, 150, 301-310.
5. Jousson, O., Léchenne, B., Bontems, O., Mignon, B. et al., Secreted subtilisin gene family in Trichophyton rubrum. Gene 2004, 339, 79-88.
6. Giddey, K., Favre, B., Quadroni, M., Monod, M., Closely related dermatophyte species produce different patterns of secreted proteins. FEMS Microbiol. Lett. 2007, 267, 95-101.
7. Giddey, K., Monod, M., Barblan, J., Potts, A. et al., Comprehensive analysis of proteins secreted by Trichophyton rubrum and Trichophyton violaceum under in vitro conditions. J. Proteome Res. 2007, 6, 3081-3092.
8. Monod, M., Léchenne, B., Jousson, O., Grand, D. et al., Aminopeptidases and dipeptidyl-peptidases secreted by the dermatophyte Trichophyton rubrum. Microbiology 2005, 151, 145-155.
9. Zaugg, C., Jousson, O., Léchenne, B., Staib, P., Monod, M., Trichophyton rubrum secreted and membrane-associated carboxypeptidases. Int. J. Med. Microbiol. 2008, 298, 669-682.
10. Vermout, S., Baldo, A., Tabart, J., Losson, B., Mignon, B., Secreted dipeptidyl peptidases as potential virulence factors for Microsporum canis. FEMS Immunol. Med. Microbiol. 2008, 54, 299-308.
11. Staib, Zaugg, C., Mignon, B., Weber, J. et al., Differential gene expression in the pathogenic dermatophyte Arthroderma benhamiae in vitro versus during infection. Microbiology 2010, 156, 884-895.
12. Woodfolk, J. A., Wheatley, L. M., Piyasena, R. V., Benjamin, D. C., Platts-Mills, T. A. E., Trichophyton antigens associated with IgE antibodies and delayed type hypersensitivity - sequence homology to two families of serine proteinases. J. Biol. Chem. 1998, 273, 29489-29496.
13. Burmester, A., Shelest, E., Glöckner, G., Heddergott, C. et al., Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol. 2011, 12, R7.
14. Reichard, U., Monod, M., Rüchel, R., Molecular cloning and sequencing of the gene encoding an extracellular aspartic proteinase from Aspergillus fumigatus. FEMS Microbiol. Lett. 1995, 130, 69-74.
15. Reichard, U., Léchenne, B., Asif, A. R., Streit, F. et al., Sedolisins, as new class of secreted proteases from Aspergillus fumigatus with endoprotease or tripeptidyl-peptidase activity at acidic pH. Appl. Environ. Microbiol. 2006, 72, 1739-1748.
16. Tsuboi, R., Ko, I. J., Takamori, K., Ogawa, H., Isolation of a keratinolytic proteinase from Trichophyton mentagrophytes with enzymatic activity at acidic pH. Infect. Immun. 1989, 57, 3479-3483.
17. Mathy, A., Baldo, A., Schoofs, L., Cambier, L. et al., Fungalysin and dipeptidyl-peptidase gene transcription in Microsporum canis strains isolated from symptomatic and asymptomatic cats. Vet. Microbiol. 2010, 146, 179-182.
18. Fumeaux, J., Mock, M., Ninet, B., Jan, I. et al., First report of Arthroderma benhamiae in Switzerland. Dermatology 2004, 208, 244-250.
19. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S. et al., Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 1996, 379, 466-469.
20. Shevchenko, A., Wilm, M., Vorm, O., Jensen, O. N. et al., A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem. Soc. Trans. 1996, 24, 893-896.
21. Keller, A., Nesvizhskii, A. I., Kolker, E., Aebersold, R., Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383-5392.
22. Nesvizhskii, A. I., Keller, A., Kolker, E., Aebersold, R., A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75, 4646-4658.
23. Lundgren, D. H., Hwang, S.-I., Wu, L., Han, D. K., Role of spectral counting in quantitative proteomics. Exp. Rev. Proteomics 2010, 7, 39-53.
24. Zaugg, C., Monod, M., Weber, J., Harshman, K. et al., Gene expression profiling in the human pathogenic dermatophyte Trichophyton rubrum during growth on proteins. Eukaryot. Cell 2009, 8, 241-250.
25. Fang, Y., Robinson, D. P., Foster, L. J., Quantitative analysis of proteome coverage and recovery rates for upstream fractionation methods in proteomics. J. Proteome Res. 2010, 9, 1902-1912.
26. Liu, H., Sadygov, R. G., Yates, J. R., A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76, 4193-4201.
27. Reichard, U., Büttner, S., Eiffert, H., Staib, F., Rüchel, R., Purification and characterisation of an extracellular serine proteinase from Aspergillus fumigatus and its detection in tissue. J. Med. Microbiol. 1990, 33, 243-251.
28. Monod, M., Paris, S., Sanglard, D., Jaton-Ogay, K. et al., Isolation and characterization of a secreted metalloprotease of Aspergillus fumigatus. Infect. Immun. 1993, 61, 4099-4104.
29. Reichard, U., Eiffert, H., Rüchel, R., Purification and characterization of an extracellular aspartic proteinase from Aspergillus fumigatus. J. Med. Vet. Mycol. 1994, 32, 427-436.
30. Beauvais, A., Monod, M., Debeaupuis, J. P., Diaquin, M. et al., Biochemical and antigenic characterization of a new dipeptidyl-peptidase isolated from Aspergillus fumigatus. J. Biol. Chem. 1997, 272, 6238-6244.
31. Beauvais, A., Monod, M., Wyniger, J., Debeaupuis, J. P. et al., Dipeptidyl-peptidase IV secreted by Aspergillus fumigatus, a fungus pathogenic to humans. Infect. Immun. 1997, 65, 3042-3047.
32. Monod, M., Jousson, O., Reichard, U., Aspergillus fumigatus secreted proteases, in: Latgé, J. P., Steinbach, W. J. (Eds.), Aspergillus fumigatus and Aspergillosis, ASM Press, Washington, DC 2009, pp. 87-106.
33. Sriranganadane, D., Waridel, P., Salamin, K., Reichard, U. et al., Aspergillus protein degradation pathways with different secreted protease sets at neutral and acidic pH. J. Proteome Res. 2010, 9, 3511-3519.
34. Wartenberg, D., Lapp, K., Jacobsen, I. D., Dahse, H. M. et al., Secretome analysis of Aspergillus fumigatus reveals Asp-hemolysin as a major secreted protein. Int. J. Med. Microbiol. 2011 (in press, PMID 21658997).
35. Byun, T., Kofod, L., Blinkovsky, A., Synergistic action of an X-prolyl dipeptidyl aminopeptidase and a non-specific aminopeptidase in protein hydrolysis. J.Agric. Food Chem. 2001, 49, 2061-2063.
36. Wilson, R. A., Arst, H. N., Mutational analysis of AREA, a transcriptional activator mediating nitrogen metabolite repression in Aspergillus nidulans and a member of the "streetwise" GATA family of transcription factors. Microbiol. Mol. Biol. Rev. 1998, 62, 586-596.
37. Peñalva, M. A., Tilburn, J., Bignell E., Arst, H. N., Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 2008, 16, 291-300.
38. Yamada, T., Makimura, K., Abe, S., Isolation, characterization, and disruption of dnr1, the areA/nit-2-like nitrogen regulatory gene of the zoophilic dermatophyte Microsporum canis. Med. Mycol. 2006, 44, 243-252.
39. Ferreira-Nozawa, M. S., Silveira, H. C., Ono, C. J., Fachin, A. L. et al., The pH signaling transcription factor PacC mediates the growth of Trichophyton rubrum on human nail in vitro. Med. Mycol. 2006, 44, 641-645.
40. Punt, P. J., Schuren, F. H., Lehmbeck, J., Christensen, T. et al., Characterization of the Aspergillus niger prtT, a unique regulator of extracellular protease encoding genes. Fungal Genet. Biol. 2008, 45, 1591-1599.
41. Bergmann, A., Hartmann, T., Cairns, T., Bignell, E. M., Krappmann, S., A regulator of Aspergillus fumigatus extracellular proteolytic activity is dispensable for virulence. Infect. Immun. 2009, 77, 4041-4050.
42. Sharon, H., Hagag, S., Osherov, N., Transcription factor PrtT controls expression of multiple secreted proteases in the human pathogenic mold Aspergillus fumigatus. Infect. Immun. 2009, 77, 4051-4060.
43. Vanbreuseghem, R., De Vroey, C., Takashio, M., Guide pratique de mycologie médicale et vétérinaire. Masson, Paris, France, 1978, pp. 1-264.
44. Harmsen, D., Schwinn, A., Weig, M., Bröcker, E. B., Heesemann, J., Phylogeny and dating of some pathogenic keratinophilic fungi using small subunit ribosomal RNA. J. Med. Vet. Mycol. 1995, 33, 299-303.
45. Scott, D. W., Miller, W. H., Griffin, C. E., Fungal Skin Diseases. in: Muller, G. H. (Ed.), Small animal dermatology, 5th Edn, W. B. Saunders, Philadelphia, PA 1995, pp. 329-391.
46. Schmid-Wendtner, M. H., Korting, H. C., The pH of the skin surface and its impact on the barrier function. Skin Pharmacol. Physiol. 2006, 19, 296-302.
47. Sriranganadane, D., Reichard, U., Salamin, K., Fratti, M. et al., Secreted glutamic protease rescues aspartic protease Pep deficiency in Aspergillus fumigatus during growth in acidic protein medium. Microbiology 2011, 157, 1541-1550.
48. Nierman, W. C., Pain, A., Anderson, M. J., Wortman, J. R. et al., Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438, 1151-1156.