Aspergillus protein degradation pathways with different secreted protease sets at neutral and acidic pH

Journal of Proteome Research

Volumn 9, Issue 7, 2010, Pages 3511-3519

  Sriranganadane, Dev ^a   Waridel, Patrice ^b   Salamin, Karine ^a   Reichard, Utz ^c   Grouzmann, Eric ^a   Neuhaus, Jean Marc ^d   Quadroni, Manfredo ^b   Monod, Michel ^b  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Aspergillus fumigatus; enzyme synergy; prolylpeptidase; protein acidic hydrolysis; protein degradation mechanism; secretome; sedolisin

Indexed keywords

FUNGAL PROTEIN; PEPSIN A; PROTEINASE; PEPTIDE FRAGMENT; PEPTIDE HYDROLASE;

AMINO ACID SEQUENCE; ARTICLE; ASPERGILLUS FUMIGATUS; FUNGUS GROWTH; NONHUMAN; PEPTIDE ANALYSIS; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; ASPERGILLUS; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; SECRETION (PROCESS);

ASPERGILLUS; ASPERGILLUS FUMIGATUS;

AMINO ACID SEQUENCE; ASPERGILLUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FUNGAL PROTEINS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES;

EID: 77954366190     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr901202z     Document Type: Article

References (41)

1. Latgé, J. P. Aspergillus fumigatus and aspergillosis Clin. Microbiol. Rev. 1999, 12 (2) 310-50
2. 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 (4) 243-51
3. Monod, M.; Togni, G.; Rahalison, L.; Frenk, E. Isolation and characterisation of an extracellular alkaline protease of Aspergillus fumigatus J. Med. Microbiol. 1991, 35 (1) 23-8
4. Perry, J. R.; Basrai, M. A.; Steiner, H. Y.; Naider, F.; Becker, J. M. Isolation and characterization of a Saccharomyces cerevisiae peptide transport gene Mol. Cell. Biol. 1994, 14 (1) 104-15
5. Basrai, M. A.; Lubkowitz, M. A.; Perry, J. R.; Miller, D.; Krainer, E.; Naider, F.; Becker, J. M. Cloning of a Candida albicans peptide transport gene Microbiology 1995, 141 (Pt5) 1147-56
6. Hauser, M.; Narita, V.; Donhardt, A. M.; Naider, F.; Becker, J. M. Multiplicity and regulation of genes encoding peptide transporters in Saccharomyces cerevisiae Mol. Membr. Biol. 2001, 18 (1) 105-12
7. Koh, S.; Wiles, A. M.; Sharp, J. S.; Naider, F. R.; Becker, J. M.; Stacey, G. An oligopeptide transporter gene family in Arabidopsis Plant. Physiol. 2002, 128 (1) 21-9
8. Lubkowitz, M. A.; Hauser, L.; Breslav, M.; Naider, F.; Becker, J. M. An oligopeptide transport gene from Candida albicans Microbiology 1997, 143 (Pt2) 387-96
9. Reuss, O.; Morschhäuser, J. A family of oligopeptide transporters is required for growth of Candida albicans on proteins Mol. Microbiol. 2006, 60 (3) 795-812
10. Erratum in: Reuss, O.; Morschhäuser, J. Mol. Microbiol. 2006, 62 (3) 916
11. Monod, M.; Paris, S.; Sanglard, D.; Jaton-Ogay, K.; Bille, J.; Latgé, J. P. Isolation and characterization of a secreted metalloprotease of Aspergillus fumigatus Infect. Immun. 1993, 61 (10) 4099-104
12. Jaton-Ogay, K.; Paris, S.; Huerre, M.; Quadroni, M.; Falchetto, R.; Togni, G.; Latgé, J. P.; Monod, M. Cloning and disruption of the gene encoding an extracellular metalloprotease of Aspergillus fumigatus Mol. Microbiol. 1994, 14 (5) 917-28
13. Monod, M.; Lechenne, B.; Jousson, O.; Grand, D.; Zaugg, C.; Stocklin, R.; Grouzmann, E. Aminopeptidases and dipeptidyl-peptidases secreted by the dermatophyte Trichophyton rubrum Microbiology 2005, 151 (Pt 1) 145-55
14. Beauvais, A.; Monod, M.; Debeaupuis, J. P.; Diaquin, M.; Kobayashi, H.; Latgé, J. P. Biochemical and antigenic characterization of a new dipeptidyl-peptidase isolated from Aspergillus fumigatus J. Biol. Chem. 1997, 272 (10) 6238-44
15. Beauvais, A.; Monod, M.; Wyniger, J.; Debeaupuis, J. P.; Grouzmann, E.; Brakch, N.; Svab, J.; Hovanessian, A. G.; Latge, J. P. Dipeptidyl-peptidase IV secreted by Aspergillus fumigatus, a fungus pathogenic to humans Infect. Immun. 1997, 65 (8) 3042-7
16. Doumas, A.; van den Broek, P.; Affolter, M.; Monod, M. Characterization of the prolyl dipeptidyl peptidase gene (dppIV) from the koji mold Aspergillus oryzae Appl. Environ. Microbiol. 1998, 64 (12) 4809-15
17. Doumas, A.; Crameri, R.; Léchenne, B.; Monod., M. Cloning of the gene encoding neutral protease I of the koji mold Aspergillus oryzae and its expression in Pichia pastoris J. Food Mycol. 1999, 2 (1) 271-9
18. Blinkowsky, A. M.; Byun, T.; Brown, K. M.; Golightly, E. J.; Klotz, A. V. A non- specific aminopeptidase from Aspergillus Biochim. Biophys. Acta 2000, 1480 (1-2) 171-81
19. Chien, H. C.; Lin, S. H.; Chao, S. H.; Chen, C. C.; Wang, W. C.; Shaw, C. Y.; Tsai, Y. C.; Hu, H. Y.; Hsu, W. H. Purification, characterisation, and genetic analysis of a leucine aminopepeptidase from Aspergillus sojae Biochim. Biophys. Acta 2002, 1576 (1-2) 119-26
20. 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 (4) 2061-3
21. Reichard, U.; Léchenne, B.; Asif, A. R.; Streit, F.; Grouzmann, E.; Jousson, O.; Monod, M. Sedolisins, as new class of secreted proteases from Aspergillus fumigatus with endoprotease or tripeptidyl-peptidase activity at acidic pH Appl. Environ. Microbiol. 2006, 72 (3) 1739-48
22. Borg-von Zepelin, M.; Beggah, S.; Boggian, K.; Sanglard, D.; Monod, M. The expression of the secreted aspartyl proteinases Sap4 to Sap6 from Candida albicans in murine macrophages Mol. Microbiol. 1998, 28 (3) 543-54
23. Jousson, O.; Léchenne, B.; Bontems, O.; Capoccia, S.; Mignon, B.; Barblan, J.; Quadroni, M.; Monod, M. Multiplication of an ancestral gene encoding secreted fungalysin preceded species differentiation in the dermatophytes Trichophyton and Microsporum Microbiology 2004, 150 (Pt 2) 301-10
24. Jousson, O.; Léchenne, B.; Bontems, O.; Mignon, B.; Reichard, U.; Barblan, J.; Quadroni, M.; Monod, M. Secreted subtilisin gene family in Trichophyton rubrum Gene 2004, 339, 79-88
25. Sarfati, J.; Monod, M.; Recco, P.; Sulahian, A.; Pinel, C.; Candolfi, E.; Fontaine, T.; Debeaupuis, J. P.; Tabouret, M.; Latgé, J. P. Recombinant antigens as diagnostic markers for aspergillosis Diagn. Microbiol. Infect. Dis. 2006, 55 (4) 279-91
26. Chevallet, M.; Luche, S.; Rabilloud, T. Silver staining of proteins in polyacrylamide gels Nat. Protocols 2006, 1 (4) 1852-8
27. Wilm, M.; Shevchenko, A.; Houthaeve, T.; Breit, S.; Schweigerer, L.; Fotsis, T.; Mann, M. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry Nature 1996, 379 (6564) 466-9
28. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68 (5) 850-8
29. 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 (20) 5383-92
30. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-58
31. Liu, H.; Sadygov, R. G.; Yates, J. R. 3rd. A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 2004, 76 (14) 4193-201
32. Edens, L.; Dekker, P.; van der Hoeven, R.; Deen, F.; de Roos, A.; Floris, R. Extracellular prolyl endoprotease from Aspergillus niger and its use in the debittering of protein hydrolysates J. Agric. Food Chem. 2005, 53 (20) 7950-7
33. 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 (1) 69-74
34. Zaugg, C.; Jousson, O.; Léchenne, B.; Staib, P.; Monod, M. Trichophyton rubrum secreted and membrane-associated carboxypeptidases Int. J. Med. Microbiol. 2008, 298 (7-8) 669-82
35. Monod, M.; Jousson, O.; Reichard, U. Aspergillus fumigatus secreted proteases. In Aspergillus fumigatus and aspergillosis; Latgé, J.-P.; Steinbach, W. J., Eds.; ASM Press: Washington, D.C., 2009; pp 87 - 106.
36. von Heijne, G. A new method for predicting signal sequence cleavage sites Nucleic Acids Res. 1986, 14 (11) 4683-90
37. Bendtsen, J. D.; Nielsen, H.; von Heijne, G.; Brunak, S. Improved prediction of signal peptides: SignalP 3.0 J. Mol. Biol. 2004, 340 (4) 783-95
38. Kubota, K.; Tanokura, M.; Takahashi, K. Purification and characterization of a novel prolyl endopeptidase from Aspergillus niger Proc. Jpn. Acad. 2005, 81 (10) 447-53
39. Sebela, M.; Rehulka, P.; Kábrt, J.; Rehulková, H.; Ozdian, T.; Raus, M.; Franc, V.; Chmelík, J. Identification of N-glycosylation in prolyl endoprotease from Aspergillus niger and evaluation of the enzyme for its possible application in proteomics J. Mass Spectrom. 2009, 44 (11) 1587-95
40. Naglik, J. R.; Challacombe, S. J.; Hube, B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis Microbiol. Mol. Biol. Rev. 2003, 67 (3) 400-28
41. Biguet, J.; Tran, Van Ky, P.; Fruit, J.; Andrieu, S. Identification of chymotryptic activity in remarkable fractions of an antigenic extract of Aspergillus fumigatus. Significance for the immunologic diagnosis of aspergillosis Rev. Immunol. Ther. Antimicrob. 1967, 31 (4) 317-28