Trypsin-specific inhibitors from the basidiomycete Clitocybe nebularis with regulatory and defensive functions

Microbiology

Volumn 155, Issue 12, 2009, Pages 3971-3981

  Avanzo, Petra ^a   Sabotič, Jerica ^a   Anžlovar, Sabina ^a,b   Popovič, Titjana ^a   Leonardi, Adrijana ^a   Pain, Roger H ^a   Kos, Janko ^a,b   Brzin, Jože ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; CNISPIN; KALLIKREIN; PROTEINASE INHIBITOR; SUBTILISIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; BASIDIOMYCETES; CLITOCYBE NEBULARIS; CONTROLLED STUDY; DNA SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN ISOLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

AGARICALES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; DNA, FUNGAL; DROSOPHILA MELANOGASTER; FUNGAL PROTEINS; GENES, FUNGAL; INSECTICIDES; KINETICS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRYPSIN INHIBITORS;

DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; HEXAPODA; LENTINULA EDODES; LEPISTA NEBULARIS;

EID: 71449102604     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.032805-0     Document Type: Article

References (44)

1. Blumberg, S., Schechter, I. & Berger, A. (1970). The purification of papain by affinity chromatography. Eur J Biochem 15, 97-102.
2. Bode, W. & Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. Eur J Biochem 204, 433-451.
3. Brzin, J., Mesško, P. & Kregar, I. (1995). Potato tubers protein inhibitors of cysteine, serine and aspartic proteinases. Acta Pharm 45, 181-186.
4. Brzin, J., Rogelj, B., Popovicč, T., Štrukelj, B. & Ritonja, A. (2000). Clitocypin, a new type of cysteine proteinase inhibitor from fruit bodies of mushroom Clitocybe nebularis. J Biol Chem 275, 20104-20109.
5. Burton, K. S., Partis, M. D., Wood, D. A. & Thurston, C. F. (1997). Accumulation of serine proteinase in senescent sporophores of the cultivated mushroom, Agaricus bisporus. Mycol Res 101, 146-152.
6. Chase, T., Jr & Shaw, E. (1969). Comparison of the esterase activities of trypsin, plasmin, and thrombin on guanidinobenzoate esters. Titration of the enzymes. Biochemistry 8, 2212-2224.
7. Coles, P. S., Barber, W., Beyer, D. M., Fleischer, S. J., Keil, C., Rinker, D. L., Romaine, C. P., Whitney, S. P. & Wuest, P. (2002). Mushroom Integrated Pest Management. PA, USA: Pennsylvania State University.
8. Dohmae, N., Takio, K., Tsumuraya, Y. & Hashimoto, Y. (1995). The complete amino acid sequences of two serine proteinase inhibitors from the fruiting bodies of a basidiomycete, Pleurotus ostreatus. Arch Biochem Biophys 316, 498-506.
9. Espin, J. C., van Leeuwen, J. & Wichers, H. J. (1999). Kinetic study of the activation process of a latent mushroom (Agaricus bisporus) tyrosinase by serine proteases. J Agric Food Chem 47, 3509-3517.
10. Faraco, V., Palmieri, G., Festa, G., Monti, M., Sannia, G. & Giardina, P. (2005). A new subfamily of fungal subtilases: structural and functional analysis of a Pleurotus ostreatus member. Microbiology 151, 457-466.
11. Gzogian, L. A., Proskuriakov, M. T., Ievleva, E. V. & Valueva, T. A. (2005). Trypsin-like proteinases and trypsin inhibitors in fruiting bodies of higher fungi. Prikl Biokhim Mikrobiol 41, 612-615 (in Russian).
12. Habib, H. & Fazili, K. M. (2007). Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2, 068-085.
13. Henderson, P. J. (1972). A linear equation that describes the steady-state kinetics of enzymes and subcellular particles interacting with tightly bound inhibitors. Biochem J 127, 321-333.
14. Heneghan, M. N., Porta, C., Zhang, C., Burton, K. S., Challen, M. P., Bailey, A. M. & Foster, G. D. (2009). Characterization of serine proteinase expression in Agaricus bisporus and Coprinopsis cinerea by using green fluorescent protein and the A. bisporus SPR1 promoter. Appl Environ Microbiol 75, 792-801.
15. Kidrič, M., Fabian, H., Brzin, J., Popovicč, T. & Pain, R. H. (2002). Folding, stability, and secondary structure of a new dimeric cysteine proteinase inhibitor. Biochem Biophys Res Commun 297, 962-967.
16. Krishnamoorthi, R., Gong, Y. X. & Richardson, M. (1990). A new protein inhibitor of trypsin and activated Hageman factor from pumpkin (Cucurbita maxima) seeds. FEBS Lett 273, 163-167.
17. Krivosheina, N. P. (2008). Macromycete fruit bodies as a habitat for dipterans (Insecta, Diptera). Entomol Rev (Engl Transl) 88, 778-792.
18. Kupfer, D. M., Drabenstot, S. D., Buchanan, K. L., Lai, H., Zhu, H., Dyer, D. W., Roe, B. A. & Murphy, J. W. (2004). Introns and splicing elements of five diverse fungi. Eukaryot Cell 3, 1088-1100.
19. Martin, F., Aerts, A., Ahren, D., Brun, A., Danchin, E. G., Duchaussoy, F., Gibon, J., Kohler, A., Lindquist, E. & other authors (2008). The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88-92.
20. Matsumoto, I., Watanabe, H., Abe, K., Arai, S. & Emori, Y. (1995). A putative digestive cysteine proteinase from Drosophila melanogaster is predominantly expressed in the embryonic and larval midgut. Eur J Biochem 227, 582-587.
21. Moller, E. M., Bahnweg, G., Sandermann, H. & Geiger, H. H. (1992). A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res 20, 6115-6116.
22. Mondego, J. M., Carazzolle, M. F., Costa, G. G., Formighieri, E. F., Parizzi, L. P., Rincones, J., Cotomacci, C., Carraro, D. M., Cunha, A. F. & other authors (2008). A genome survey of Moniliophthora perniciosa gives new insights into Witches' Broom Disease of cacao. BMC Genomics 9, 548.
23. Morrison, J. F. (1982). The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions. Trends Biochem Sci 7, 102-105.
24. Muhlia-Almazan, A., Sanchez-Paz, A. & Garcia-Carreno, F. L. (2008). Invertebrate trypsins: a review. J Comp Physiol [B] 178, 655-672.
25. Nyberg, P., Ylipalosaari, M., Sorsa, T. & Salo, T. (2006). Trypsins and their role in carcinoma growth. Exp Cell Res 312, 1219-1228.
26. Odani, S., Tominaga, K., Kondou, S., Hori, H., Koide, T., Hara, S., Isemura, M. & Tsunasawa, S. (1999). The inhibitory properties and primary structure of a novel serine proteinase inhibitor from the fruiting body of the basidiomycete, Lentinus edodes. Eur J Biochem 262, 915-923.
27. Ortiz, M. L., Calero, M., Fernandez Patron, C., Patron, C. F., Castellanos, L. & Mendez, E. (1992). Imidazole-SDS-Zn reverse staining of proteins in gels containing or not SDS and microsequence of individual unmodified electroblotted proteins. FEBS Lett 296, 300-304.
28. Page, M. J. & Di Cera, E. (2008). Serine peptidases: classification, structure and function. Cell Mol Life Sci 65, 1220-1236.
29. Palmieri, G., Bianco, C., Cennamo, G., Giardina, P., Marino, G., Monti, M. & Sannia, G. (2001). Purification, characterization, and functional role of a novel extracellular protease from Pleurotus ostreatus. Appl Environ Microbiol 67, 2754-2759.
30. Pearce, G., Sy, L., Russell, C., Ryan, C. A. & Hass, G. M. (1982). Isolation and characterization from potato tubers of two polypeptide inhibitors of serine proteinases. Arch Biochem Biophys 213, 456-462.
31. Pohleven, J., Obermajer, N., Sabotič, J., Anžlovar, S., Sepčić, K., Kos, J., Kralj, B., Štrukelj, B. & Brzin, J. (2009). Purification, characterization and cloning of a ricin B-like lectin from mushroom Clitocybe nebularis with antiproliferative activity against human leukemic T cells. Biochim Biophys Acta 1790, 173-181.
32. Ramachandran, R. & Hollenberg, M. D. (2008). Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 153, S263-S282.
33. Rawlings, N. D., Morton, F. R., Kok, C. Y., Kong, J. & Barrett, A. J. (2008). MEROPS: the peptidase database. Nucleic Acids Res 36, D320-D325.
34. Sabotič, J., Gaser, D., Rogelj, B., Gruden, K., Štrukelj, B. & Brzin, J. (2006). Heterogeneity in the cysteine protease inhibitor clitocypin gene family. Biol Chem 387, 1559-1566.
35. Sabotič, J., Galeša, K., Popovič, T., Leonardi, A. & Brzin, J. (2007a). Comparison of natural and recombinant clitocypins, the fungal cysteine protease inhibitors. Protein Expr Purif 53, 104-111.
36. Sabotič, J., Trček, T., Popovič, T. & Brzin, J. (2007b). Basidiomycetes harbour a hidden treasure of proteolytic diversity. J Biotechnol 128, 297-307.
37. Sabotič, J., Popovič, T., Puizdar, V. & Brzin, J. (2009). Macrocypins, a family of cysteine protease inhibitors from the basidiomycete Macrolepiota procera. FEBS J 276, 4334-4345.
38. St Leger, R. J., Joshi, L. & Roberts, D. W. (1997). Adaptation of proteases and carbohydrates of saprophytic, phytopathogenic and entomopathogenic fungi to the requirements of their ecological niches. Microbiology 143, 1983-1992.
39. Terra, W. R. & Ferreira, C. (1994). Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109, 1-62.
40. Twining, S. S. (1984). Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes. Anal Biochem 143, 30-34.
41. Vandeputte-Rutten, L. & Gros, P. (2002). Novel proteases: common themes and surprising features. Curr Opin Struct Biol 12, 704-708.
42. Vetter, J. (2000). Trypsin inhibitor activity of basidiomycetous mushrooms. Eur Food Res Technol 211, 346-348.
43. Whitcomb, D. C. & Lowe, M. E. (2007). Human pancreatic digestive enzymes. Dig Dis Sci 52, 1-17.
44. Zuchowski, J. & Grzywnowicz, K. (2006). Partial purification of proteinase K inhibitors from liquid-cultured mycelia of the white rot basidiomycete Trametes versicolor. Curr Microbiol 53, 259-264.