Efficient inhibition of cathepsin B by a secreted type 1 cystatin of Fasciola gigantica

Molecular and Biochemical Parasitology

Volumn 186, Issue 2, 2012, Pages 126-133

  Siricoon, Sinee ^a   Grams, Suksiri Vichasri ^b   Grams, Rudi ^a  

^a THAMMASAT UNIVERSITY   (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Cathepsin B; Cathepsin L; Cystatin; Fasciola gigantica; Intestinal epithelium; Platyhelminthes; Prostate gland

Indexed keywords

CATHEPSIN B; CATHEPSIN B INHIBITOR; CATHEPSIN L; CYSTATIN; CYSTATIN C; FASCIOLA GIGANTICA STEFIN 1; FASCIOLA GIGANTICA STEFIN 2; PARASITE ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FASCIOLA GIGANTICA; IMMUNE RESPONSE; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROSTATE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPERATURE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CATHEPSIN B; CATTLE; CYSTATIN C; CYSTATINS; CYSTEINE PROTEINASE INHIBITORS; ENZYME ACTIVATION; ENZYME INHIBITORS; FASCIOLA; FASCIOLIASIS; HELMINTH PROTEINS; HUMANS; INHIBITORY CONCENTRATION 50; KINETICS; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

FASCIOLA; FASCIOLA GIGANTICA; FASCIOLA HEPATICA; PLATYHELMINTHES;

EID: 84870457491     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2012.10.003     Document Type: Article

References (41)

1. M. Kasny, L. Mikes, V. Hampl, J. Dvorak, C.R. Caffrey, J.P. Dalton, and P. Horak Peptidases of trematodes Advances in Parasitology 69 2009 205 297
2. P.M. Smooker, R. Jayaraj, R.N. Pike, and T.W. Spithill Cathepsin B proteases of flukes: the key to facilitating parasite control? Trends in Parasitology 26 2010 506 514
3. C. Stack, J.P. Dalton, and M.W. Robinson The phylogeny, structure and function of trematode cysteine proteases, with particular emphasis on the Fasciola hepatica cathepsin L family Advances in Experimental Medicine and Biology 712 2011 116 135
4. S.A. Beckham, D. Piedrafita, C.I. Phillips, N. Samarawickrema, R.H. Law, P.M. Smooker, N.S. Quinsey, J.A. Irving, D. Greenwood, S.H. Verhelst, M. Bogyo, B. Turk, T.H. Coetzer, L.C. Wijeyewickrema, T.W. Spithill, and R.N. Pike A major cathepsin B protease from the liver fluke Fasciola hepatica has atypical active site features and a potential role in the digestive tract of newly excysted juvenile parasites International Journal of Biochemistry and Cell Biology 41 2009 1601 1612
5. L.J. Norbury, S. Beckham, R.N. Pike, R. Grams, T.W. Spithill, J.V. Fecondo, and P.M. Smooker Adult and juvenile Fasciola cathepsin L proteases: different enzymes for different roles Biochimie 93 2011 604 611
6. R.M. Morphew, H.A. Wright, E.J. Lacourse, J. Porter, J. Barrett, D.J. Woods, and P.M. Brophy Towards delineating functions within the Fasciola secreted cathepsin l protease family by integrating in vivo based sub-proteomics and phylogenetics PLoS Neglected Tropical Diseases 5 2011 e937
7. M.W. Robinson, I. Corvo, P.M. Jones, A.M. George, M.P. Padula, J. To, M. Cancela, G. Rinaldi, J.F. Tort, L. Roche, and J.P. Dalton Collagenolytic activities of the major secreted cathepsin l peptidases involved in the virulence of the helminth pathogen, Fasciola hepatica PLoS Neglected Tropical Diseases 5 2011 e1012
8. L.J. Norbury, A. Hung, S. Beckham, R.N. Pike, T.W. Spithill, C.S. Craik, Y. Choe, J.V. Fecondo, and P.M. Smooker Analysis of Fasciola cathepsin L5 by S(2) subsite substitutions and determination of the P(1)-P(4) specificity reveals an unusual preference Biochimie 94 2012 1119 1127
9. N.D. Rawlings, A.J. Barrett, and A. Bateman MEROPS: the database of proteolytic enzymes, their substrates and inhibitors Nucleic Acids Research 40 2012 D343 D350
10. V. Turk, V. Stoka, and D. Turk Cystatins: biochemical and structural properties, and medical relevance Frontiers in Bioscience 13 2008 5406 5420
11. M. Tarasuk, S. Vichasri Grams, V. Viyanant, and R. Grams Type I cystatin (stefin) is a major component of Fasciola gigantica excretion/secretion product Molecular and Biochemical Parasitology 167 2009 60 71
12. F.C. Morales, D.R. Furtado, and F.D. Rumjanek The N-terminus moiety of the cystatin SmCys from Schistosoma mansoni regulates its inhibitory activity in vitro and in vivo Molecular and Biochemical Parasitology 134 2004 65 73
13. J.M. Kang, K.H. Lee, W.M. Sohn, and B.K. Na Identification and functional characterization of CsStefin-1, a cysteine protease inhibitor of Clonorchis sinensis Molecular and Biochemical Parasitology 177 2011 126 134
14. E. Khaznadji, P. Collins, J.P. Dalton, Y. Bigot, and N. Moiré A new multi-domain member of the cystatin superfamily expressed by Fasciola hepatica International Journal for Parasitology 35 2005 1115 1125
15. L. McGonigle, A. Mousley, N.J. Marks, G.P. Brennan, J.P. Dalton, T.W. Spithill, T.A. Day, and A.G. Maule The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration International Journal for Parasitology 38 2008 149 155
16. M. Sethadavit, K. Meemon, A. Jardim, T.W. Spithill, and P. Sobhon Identification, expression and immunolocalization of cathepsin B3, a stage-specific antigen expressed by juvenile Fasciola gigantica Acta Tropica 112 2009 164 173
17. R. Jayaraj, D. Piedrafita, K. Dynon, R. Grams, T.W. Spithill, and P.M. Smooker Vaccination against fasciolosis by a multivalent vaccine of stage-specific antigens Veterinary Parasitology 160 2009 230 236
18. S. Vichasri-Grams, P. Subpipattana, P. Sobhon, V. Viyanant, and R. Grams An analysis of the calcium-binding protein 1 of Fasciola gigantica with a comparison to its homologs in the phylum Platyhelminthes Molecular and Biochemical Parasitology 146 2006 10 23
19. J. Ruangsittichai, V. Viyanant, S. Vichasri-Grams, P. Sobhon, S. Tesana, E.S. Upatham, A. Hofmann, G. Korge, and R. Grams Opisthorchis viverrini: Identification of a glycine-tyrosine rich eggshell protein and its potential as a diagnostic tool for human opisthorchiasis International Journal for Parasitology 36 2006 1329 1339
20. P. Rice, I. Longden, and A. Bleasby EMBOSS: the European Molecular Biology Open Software Suite Trends in Genetics 16 2000 276 277
21. T.N. Petersen, S. Brunak, G. von Heijne, and H. Nielsen SignalP 4.0: discriminating signal peptides from transmembrane regions Nature Methods 8 2011 785 786
22. F. Sievers, A. Wilm, D. Dineen, T.J. Gibson, K. Karplus, W. Li, R. Lopez, H. McWilliam, M. Remmert, J. Soding, J.D. Thompson, and D.G. Higgins Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega Molecular Systems Biology 7 2011 539
23. E. Beitz TEXshade: shading and labeling of multiple sequence alignments using LATEX2 epsilon Bioinformatics 16 2000 135 139
24. P. Adisakwattana, V. Viyanant, W. Chaicumpa, S. Vichasri-Grams, A. Hofmann, G. Korge, P. Sobhon, and R. Grams Comparative molecular analysis of two asparaginyl endopeptidases and encoding genes from Fasciola gigantica Molecular and Biochemical Parasitology 156 2007 102 116
25. A.J. Barrett, and H. Kirschke Cathepsin B, Cathepsin H, and cathepsin L Methods in Enzymology 80 Pt C 1981 535 561
26. R.A. Copeland Tight binding inhibitors R.A. Copeland, Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis 2000 Wiley-VCH New York 305 317
27. J.R. Martin, C.J. Craven, R. Jerala, L. Kroon-Zitko, E. Zerovnik, V. Turk, and J.P. Waltho The three-dimensional solution structure of human stefin A Journal of Molecular Biology 246 1995 331 343
28. M.T. Stubbs, B. Laber, W. Bode, R. Huber, R. Jerala, B. Lenarčič, and V. Turk The refined 2.4 A X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction EMBO Journal 9 1990 1939 1947
29. D. Musil, D. Zucic, D. Turk, R.A. Engh, I. Mayr, R. Huber, T. Popovic, V. Turk, T. Towatari, and N. Katunuma The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity EMBO Journal 10 1991 2321 2330
30. B. Lenarcic, I. Krizaj, P. Zunec, and V. Turk Differences in specificity for the interactions of stefins A, B and D with cysteine proteinases FEBS Letters 395 1996 113 118
31. M. Renko, U. Pozgan, D. Majera, and D. Turk Stefin A displaces the occluding loop of cathepsin B only by as much as required to bind to the active site cleft FEBS Journal 277 2010 4338 4345
32. C. Naudin, F. Lecaille, S. Chowdhury, J.C. Krupa, E. Purisima, J.S. Mort, and G. Lalmanach The occluding loop of cathepsin B prevents its effective inhibition by human kininogens Journal of Molecular Biology 400 2010 1022 1035
33. V. Turk, V. Stoka, O. Vasiljeva, M. Renko, T. Sun, B. Turk, and D. Turk Cysteine cathepsins: from structure, function and regulation to new frontiers Biochimica et Biophysica Acta 1824 2012 68 88
34. L.R. Wilson, R.T. Good, M. Panaccio, G.L. Wijffels, R.M. Sandeman, and T.W. Spithill Fasciola hepatica: characterization and cloning of the major cathepsin B protease secreted by newly excysted juvenile liver fluke Experimental Parasitology 88 1998 85 94
35. R.H. Law, P.M. Smooker, J.A. Irving, D. Piedrafita, R. Ponting, N.J. Kennedy, J.C. Whisstock, R.N. Pike, and T.W. Spithill Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection Infection and Immunity 71 2003 6921 6932
36. K. Meemon, R. Grams, S. Vichasri-Grams, A. Hofmann, G. Korge, V. Viyanant, E.S. Upatham, S. Habe, and P. Sobhon Molecular cloning and analysis of stage and tissue-specific expression of cathepsin B encoding genes from Fasciola gigantica Molecular and Biochemical Parasitology 136 2004 1 10
37. M. Cancela, D. Acosta, G. Rinaldi, E. Silva, R. Duran, L. Roche, A. Zaha, C. Carmona, and J.F. Tort A distinctive repertoire of cathepsins is expressed by juvenile invasive Fasciola hepatica Biochimie 90 2008 1461 1475
38. E. Pol, and I. Björk Importance of the second binding loop and the C-terminal end of cystatin B (stefin B) for inhibition of cysteine proteinases Biochemistry 38 1999 10519 10526
39. G.A. Cornwall, and N. Hsia A new subgroup of the family 2 cystatins Molecular and Cellular Endocrinology 200 2003 1 8
40. W.F. Gregory, and R.M. Maizels Cystatins from filarial parasites: evolution, adaptation and function in the host-parasite relationship International Journal of Biochemistry and Cell Biology 40 2008 1389 1398
41. C. Klotz, T. Ziegler, E. Danilowicz-Luebert, and S. Hartmann Cystatins of parasitic organisms Advances in Experimental Medicine and Biology 712 2011 208 221