The functional expression and characterisation of a cysteine peptidase from the invasive stage of the neuropathogenic schistosome Trichobilharzia regenti

International Journal for Parasitology

Volumn 39, Issue 2, 2009, Pages 201-211

  Dolečková, Kateřina ^a   Kašný, Martin ^a   Mikeš, Libor ^a   Cartwright, Jared ^b   Jedelský, Petr ^a   Schneider, Eric L ^c   Dvořák, Jan ^c   Mountford, Adrian P ^b   Craik, Charles S ^c   Horák, Petr ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cathepsin B; Cercaria; Histolysis; Penetration gland; Protease; Schistosoma; Skin; Trematoda

Indexed keywords

CATHEPSIN B; CATHEPSIN B2 ENZYME; COMPLEMENTARY DNA; CYSTEINE; CYSTEINE PEPTIDASE; ENZYME PRECURSOR; PEPTIDASE; PROCATHEPSIN B2; RECOMBINANT PROTEIN; TRCB2 ENZYME; UNCLASSIFIED DRUG;

ANTIBODY; ENZYME; GENE EXPRESSION; INVASIVE SPECIES; PATHOGEN; YEAST;

ARTICLE; CONTROLLED STUDY; ENZYME ASSAY; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; PHYSICAL CHEMISTRY; PICHIA PASTORIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION; SCHISTOSOMA; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS; TRICHOBILHARZIA REGENTI; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CATHEPSIN B; CATTLE; CYSTEINE; CYSTEINE PROTEASES; DUCKS; HUMANS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PICHIA; RABBITS; SCHISTOSOMA; SCHISTOSOMA MANSONI; SNAILS; SUBSTRATE SPECIFICITY; TURKEYS;

AVES; CERCARIA (TREMATODE GENUS); PICHIA PASTORIS; SCHISTOSOMA; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; TREMATODA; TRICHOBILHARZIA REGENTI;

EID: 57449101334     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.06.010     Document Type: Article

References (51)

1. Abdulla M.H., Lim K.C., Sajid M., McKerrow J.H., and Caffrey C.R. Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med. 4 (2007) e14
2. Baig S., Damian R.T., and Peterson D.S. A novel cathepsin B active site motif is shared by helminth bloodfeeders. Exp. Parasitol. 101 (2002) 83-89
3. Bharadwaj M., Bharadwaj D., and Hati R.N. Characterization of a membrane protease from rat submaxillary-gland mitochondria that possess thrombin-like activity. Biochem. J. 313 (1996) 193-199
4. Bieth J.G. Pancreatic elastase. In: Barrett A.J., Rawlings N.D., and Woessner J.F. (Eds). Handbook of Proteolytic Enzymes vol. 2 (2004), Elsevier, Amsterdam 504-1508
5. Bretthauer R.K., and Castellino F.J. Glycosylation of Pichia pastoris-derived proteins. Biotechnol. Appl. Biochem. 30 (1999) 193-200
6. Brown P.L., Mecham L., Tisdale C., and Mecham R.P. The cysteine residues in the carboxy terminal domain of tropoelastin form an intrachain disulfide bond that stabilizes a loop structure and positively charged pocket. Biochem. Biophys. Res. Commun. 186 (1992) 549-555
7. Caffrey C.R., Salter J.P., Lucas K.D., Khiem D., Hsieh I., Lim K.C., Ruppel A., McKerrow J.H., and Sajid M. SmCB2, a novel tegumental cathepsin B from adult Schistosoma mansoni. Mol. Biochem. Parasitol. 121 (2002) 49-61
8. Caffrey C.R., McKerrow J.H., Salter J.P., and Sajid M. Blood 'n' guts: an update on schistosome digestive peptidases. Trends Parasitol. 20 (2004) 241-248
9. Choe Y., Leonetti F., Greenbaum D.C., Lecaille F., Bogyo M., Brömme D., Ellman J.A., and Craik C.S. Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem. 281 (2006) 12824-12832
10. Cleland W.W. Dithiothreitol, a new protective agent for SH groups. Biochemistry 3 (1964) 480-482
11. Cocude C., Pierrot C., Cêtre C., Fontaine J., Godin C., Capron A., and Khalife J. Identification of a developmentally regulated Schistosoma mansoni serine protease homologous to mouse plasma kallikrein and human factor I. Parasitology 118 (1999) 389-396
12. Dalton J.P., Clough K.A., Jones M.K., and Brindley P.J. Characterization of the cathepsin-like cysteine proteinases of Schistosoma mansoni. Infect. Immun. 64 (1996) 1328-1334
13. Dalton J.P., Clough K.A., Jones M.K., and Brindley P.J. The cysteine proteinases of Schistosoma mansoni cercariae. Parasitology 114 (1997) 105-112
14. Delcroix M., Sajid M., Caffrey C.R., Lim K.C., Dvořák J., Hsieh I., Bahgat M., Dissous C., and McKerrow J.H. A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J. Biol Chem. 281 (2006) 39316-39329
15. Dolečková K., Kašný M., Mikeš L., Mutapi F., Stack C., Mountford A.P., and Horák P. Peptidases of Trichobilharzia regenti (Schistosomatidae) and its molluscan host Radix peregra s. lat. (Lymnaeidae): construction and screening of cDNA library from intramolluscan stages of the parasite. Folia Parasitol. 54 (2007) 94-98
16. Dvořák J., Delcroix M., Rossi A., Vopálenský V., Pospíšek M., Šedinová M., Mikeš L., Sajid M., Sali A., McKerrow J.H., Horák P., and Caffrey C.R. Multiple cathepsin B isoforms in schistosomula of Trichobilharzia regenti: identification, characterisation and putative role in migration and nutrition. Int. J. Parasitol. 35 (2005) 895-910
17. Dvořák J., Mashiyama S.T., Braschi S., Sajid M., Knudsen G.M., Hansell E., Lim K.C., Hsieh I., Bahgat M., Mackenzie B., Medzihradszky K.F., Babbitt P.C., Caffrey C.R., and McKerrow J.H. Differential use of protease families for invasion by schistosome cercariae. Biochimie 90 (2008) 345-358
18. Greenbaum D., Medzihradszky K.F., Burlingame A., and Bogyo M. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 7 (2000) 569-581
19. Horák P., Kolářová L., and Dvořák J. Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5 (1998) 349-357
20. Horák P., Dvořák J., Kolářová L., and Trefil L. Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119 (1999) 577-581
21. Horák P., and Kolářová L. Bird schistosomes: do they die in mammalian skin?. Trends Parasitol. 17 (2001) 66-69
22. Horák P., Kolářová L., and Adema C.M. Biology of the schistosome genus Trichobilharzia. Adv. Parasitol. 52 (2002) 155-233
23. Hrádková K., and Horák P. Neurotropic behaviour of Trichobilharzia regenti in ducks and mice. J. Helminthol. 76 (2002) 137-141
24. Kašný M., Mikeš L., Dalton J.P., Mountford A.P., and Horák P. Comparison of cysteine peptidase activities in Trichobilharzia regenti and Schistosoma mansoni cercariae. Parasitology 134 (2007) 1599-1609
25. Khersonsky O., Roodveldt C., and Tawfik D.S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 10 (2006) 498-508
26. Klose A., Zigrino P., Dennhöfer R., Mauch C., and Hunzelmann N. Identification and discrimination of extracellularly active cathepsins B and L in high-invasive melanoma cells. Anal. Biochem. 353 (2006) 57-62
27. Kolářová L., Horák P., and Čada F. Histopathology of CNS and nasal infections caused by Trichobilharzia regenti in vertebrates. Parasitol. Res. 87 (2001) 644-650
28. Kouřilová P., Hogg K.G., Kolářová L., and Mountford A.P. Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reactions. J. Immunol. 172 (2004) 3766-3774
29. Li Y.L., Idris M.A., Corachan M., Han J.J., Kirschfink M., and Ruppel A. Circulating antigens in schistosomiasis: detection of 31/32-kDa proteins in sera from patients infected with Schistosoma japonicum, S. mansoni, S. haematobium, or S. intercalatum. Parasitol. Res. 82 (1996) 14-18
30. Marikovsky M., Parizade M., Arnon R., and Fishelson Z. Complement regulation on the surface of cultured schistosomula and adult worms of Schistosoma mansoni. Eur. J. Immunol. 20 (1990) 221-227
31. Mason R.W., Johnson D.A., Barrett A.J., and Chapman H.A. Elastinolytic activity of human cathepsin-L. Biochem. J. 233 (1986) 925-927
32. McKerrow J.H., and Salter J. Invasion of skin by Schistosoma cercariae. Trends Parasitol. 18 (2002) 193-195
33. Mikeš L., and Man P. Purification and characterization of a saccharide-binding protein from penetration glands of Diplostomum pseudospathaceum - a bifunctional molecule with cysteine protease activity. Parasitology 127 (2003) 69-77
34. Mikeš L., Zídková L., Kašný M., Dvořák J., and Horák P. In vitro stimulation of penetration gland emptying by Trichobilharzia szidati and T. regenti (Schistosomatidae) cercariae. Quantitative collection and partial characterization of the products. Parasitol. Res. 96 (2005) 230-241
35. Musil D., Zucic D., Turk D., Engh R.A., Mayr I., Huber R., Popovic T., Turk V., Towatari T., Kutunuma N., and Bode W. The refined 2.15 Å X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10 (1991) 2321-2330
36. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural. Syst. 8 (1997) 581-599
37. Novinec M., Grass R.N., Stark W.J., Turk V., Baici A., and Lenarcic B. Interaction between human cathepsins K, L, and S and elastins - mechanism of elastinolysis and inhibition by macromolecular inhibitors. J. Biol. Chem. 282 (2007) 7893-7902
38. Nowak N., Lotter H., Tannich E., and Bruchhaus I. Resistance of Entamoeba histolytica to the cysteine proteinase inhibitor E64 is associated with secretion of pro-enzymes and reduced pathogenicity. J. Biol. Chem. 279 (2004) 38260-38266
39. Pleass J.R., Aboobaker A.A., and Schmitt A.O. Piggybacking schistosome invasion: similarities are only skin deep. Trends Parasitol. 24 (2008) 153-156
40. Reis F.C., Costa T.F., Sulea T., Mezzetti A., Scharfstein J., Brömme D., Ménard R., and Lima A.P. The propeptide of cruzipain - a potent selective inhibitor of the trypanosomal enzymes cruzipain and brucipain, and of the human enzyme cathepsin F. FEBS J. 274 (2007) 1224-1234
41. Renslo A.R., and McKerrow J.H. Drug discovery and development for neglected parasitic diseases. Nat. Chem. Biol. 2 (2006) 701-710
42. Rosenthal P.J., Sijwali P.S., Singh A., and Shenai B.R. Cysteine proteases of malaria parasites: targets for chemotherapy. Curr. Pharm. Des. 8 (2002) 1659-1672
43. Rucker R.B., and Dubick M.A. Elastin metabolism and chemistry: potential roles in lung development and structure. Environ. Health Persp. 55 (1984) 179-191
44. Salter J.P., Lim K.C., Hansell E., Hsieh I., and McKerrow J.H. Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J. Biol. Chem. 275 (2000) 38667-38673
45. Salter J.P., Choe Y., Albrecht H., Franklin C., Lim K.C., Craik C.S., and McKerrow J.H. Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J. Biol. Chem. 277 (2002) 24618-24624
46. Shaw E., Mohanty S., Colic A., Stoka V., and Turk V. The affinity-labelling of cathepsin S with peptidyl diazomethyl ketones. Comparison with the inhibition of cathepsin L and calpain. FEBS Lett. 334 (1993) 340-342
47. Skelly P.J., and Shoemaker C.B. Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J. Parasitol. 87 (2001) 1218-1221
48. Spiess E., Brüning A., Gack S., Ulbricht B., Spring H., Trefz G., and Ebert W. Cathepsin B activity in human lung tumor cell lines: ultrastructural localization, pH sensitivity, and inhibitor status at the cellular level. J. Histochem. Cytochem. 42 (1994) 917-929
49. Towatari T., Nikawa T., Murata M., Yokoo C., Tamai M., Hanada K., and Katunuma N. Novel epoxysuccinyl peptides A selective inhibitor of cathepsin B in vivo. FEBS Lett. 280 (1991) 311-315
50. Turk B., Turk D., and Turk V. Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta 1477 (2000) 98-111
51. Yoshino T.P., Lodes M.J., Rege A.A., and Chappell C.L. Proteinase activity in miracidia, transformation excretory-secretory products, and primary sporocysts of Schistosoma mansoni. J. Parasitol. 79 (1993) 23-31