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

. 2009 Jan ; 39 (2) : 201-11. [epub] 20080726

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid18708063

Grantová podpora
Wellcome Trust - United Kingdom
072255/Z/03/Z Wellcome Trust - United Kingdom

Odkazy

PubMed 18708063
PubMed Central PMC2625449
DOI 10.1016/j.ijpara.2008.06.010
PII: S0020-7519(08)00264-6
Knihovny.cz E-zdroje

A transcriptional product of a gene encoding cathepsin B-like peptidase in the bird schistosome Trichobilharzia regenti was identified and cloned. The enzyme was named TrCB2 due to its 77% sequence similarity to cathepsin B2 from the important human parasite Schistosoma mansoni. The zymogen was expressed in the methylotropic yeast Pichia pastoris; procathepsin B2 underwent self-processing in yeast media. The peptidolytic activity of the recombinant enzyme was characterised using synthetic fluorogenic peptide substrates at optimal pH 6.0. Functional studies using different specific inhibitors proved the typical cathepsin B-like nature of the enzyme. The S(2) subsite specificity profile of recombinant TrCB2 was obtained. Using monospecific antibodies against the recombinant enzyme, the presence of cathepsin B2 was confirmed in extracts from cercariae (infective stage) and schistosomula (early post-cercarial stage) of T. regenti on Western blots. Also, cross-reactivity was observed between T. regenti and S. mansoni cathepsins B2 in extracts of cercariae, schistosomula or adults. In T. regenti, the antisera localised the enzyme to post-acetabular penetration glands of cercariae implying an important role in the penetration of host skin. The ability of recombinant TrCB2 to degrade skin, serum and nervous tissue proteins was evident. Elastinolytic activity suggests that the enzyme might functionally substitute the histolytic role of the serine class elastase known from S. mansoni and Schistosoma haematobium but not found in Schistosoma japonicum or in bird schistosomes.

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Abdulla M.H., Lim K.C., Sajid M., McKerrow J.H., Caffrey C.R. Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med. 2007;4:e14. PubMed PMC

Baig S., Damian R.T., Peterson D.S. A novel cathepsin B active site motif is shared by helminth bloodfeeders. Exp. Parasitol. 2002;101:83–89. PubMed

Bharadwaj M., Bharadwaj D., Hati R.N. Characterization of a membrane protease from rat submaxillary-gland mitochondria that possess thrombin-like activity. Biochem. J. 1996;313:193–199. PubMed PMC

Bieth J.G. Pancreatic elastase. In: Barrett A.J., Rawlings N.D., Woessner J.F., editors. vol. 2. Elsevier; Amsterdam: 2004. pp. 504–1508. (Handbook of Proteolytic Enzymes).

Bretthauer R.K., Castellino F.J. Glycosylation of Pichia pastoris-derived proteins. Biotechnol. Appl. Biochem. 1999;30:193–200. PubMed

Brown P.L., Mecham L., Tisdale C., 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. 1992;186:549–555. PubMed

Caffrey C.R., Salter J.P., Lucas K.D., Khiem D., Hsieh I., Lim K.C., Ruppel A., McKerrow J.H., Sajid M. SmCB2, a novel tegumental cathepsin B from adult Schistosoma mansoni. Mol. Biochem. Parasitol. 2002;121:49–61. PubMed

Caffrey C.R., McKerrow J.H., Salter J.P., Sajid M. Blood ’n’ guts: an update on schistosome digestive peptidases. Trends Parasitol. 2004;20:241–248. PubMed

Choe Y., Leonetti F., Greenbaum D.C., Lecaille F., Bogyo M., Brömme D., Ellman J.A., Craik C.S. Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem. 2006;281:12824–12832. PubMed

Cleland W.W. Dithiothreitol, a new protective agent for SH groups. Biochemistry. 1964;3:480–482. PubMed

Cocude C., Pierrot C., Cêtre C., Fontaine J., Godin C., Capron A., Khalife J. Identification of a developmentally regulated Schistosoma mansoni serine protease homologous to mouse plasma kallikrein and human factor I. Parasitology. 1999;118:389–396. PubMed

Dalton J.P., Clough K.A., Jones M.K., Brindley P.J. Characterization of the cathepsin-like cysteine proteinases of Schistosoma mansoni. Infect. Immun. 1996;64:1328–1334. PubMed PMC

Dalton J.P., Clough K.A., Jones M.K., Brindley P.J. The cysteine proteinases of Schistosoma mansoni cercariae. Parasitology. 1997;114:105–112. PubMed

Delcroix M., Sajid M., Caffrey C.R., Lim K.C., Dvořák J., Hsieh I., Bahgat M., Dissous C., McKerrow J.H. A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J. Biol Chem. 2006;281:39316–39329. PubMed

Dolečková K., Kašný M., Mikeš L., Mutapi F., Stack C., Mountford A.P., 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. 2007;54:94–98. PubMed

Dvořák J., Delcroix M., Rossi A., Vopálenský V., Pospíšek M., Šedinová M., Mikeš L., Sajid M., Sali A., McKerrow J.H., Horák P., Caffrey C.R. Multiple cathepsin B isoforms in schistosomula of Trichobilharzia regenti: identification, characterisation and putative role in migration and nutrition. Int. J. Parasitol. 2005;35:895–910. PubMed

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., McKerrow J.H. Differential use of protease families for invasion by schistosome cercariae. Biochimie. 2008;90:345–358. PubMed

Greenbaum D., Medzihradszky K.F., Burlingame A., Bogyo M. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 2000;7:569–581. PubMed

Horák P., Kolářová L., Dvořák J. Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite. 1998;5:349–357. PubMed

Horák P., Dvořák J., Kolářová L., Trefil L. Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology. 1999;119:577–581. PubMed

Horák P., Kolářová L. Bird schistosomes: do they die in mammalian skin? Trends Parasitol. 2001;17:66–69. PubMed

Horák P., Kolářová L., Adema C.M. Biology of the schistosome genus Trichobilharzia. Adv. Parasitol. 2002;52:155–233. PubMed

Hrádková K., Horák P. Neurotropic behaviour of Trichobilharzia regenti in ducks and mice. J. Helminthol. 2002;76:137–141. PubMed

Kašný M., Mikeš L., Dalton J.P., Mountford A.P., Horák P. Comparison of cysteine peptidase activities in Trichobilharzia regenti and Schistosoma mansoni cercariae. Parasitology. 2007;134:1599–1609. PubMed

Khersonsky O., Roodveldt C., Tawfik D.S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 2006;10:498–508. PubMed

Klose A., Zigrino P., Dennhöfer R., Mauch C., Hunzelmann N. Identification and discrimination of extracellularly active cathepsins B and L in high-invasive melanoma cells. Anal. Biochem. 2006;353:57–62. PubMed

Kolářová L., Horák P., Čada F. Histopathology of CNS and nasal infections caused by Trichobilharzia regenti in vertebrates. Parasitol. Res. 2001;87:644–650. PubMed

Kouřilová P., Hogg K.G., Kolářová L., Mountford A.P. Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reactions. J. Immunol. 2004;172:3766–3774. PubMed

Li Y.L., Idris M.A., Corachan M., Han J.J., Kirschfink M., 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. 1996;82:14–18. PubMed

Marikovsky M., Parizade M., Arnon R., Fishelson Z. Complement regulation on the surface of cultured schistosomula and adult worms of Schistosoma mansoni. Eur. J. Immunol. 1990;20:221–227. PubMed

Mason R.W., Johnson D.A., Barrett A.J., Chapman H.A. Elastinolytic activity of human cathepsin-L. Biochem. J. 1986;233:925–927. PubMed PMC

McKerrow J.H., Salter J. Invasion of skin by Schistosoma cercariae. Trends Parasitol. 2002;18:193–195. PubMed

Mikeš L., Man P. Purification and characterization of a saccharide-binding protein from penetration glands of Diplostomum pseudospathaceum – a bifunctional molecule with cysteine protease activity. Parasitology. 2003;127:69–77. PubMed

Mikeš L., Zídková L., Kašný M., Dvořák J., 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. 2005;96:230–241. PubMed

Musil D., Zucic D., Turk D., Engh R.A., Mayr I., Huber R., Popovic T., Turk V., Towatari T., Kutunuma N., Bode W. The refined 2.15 Å X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 1991;10:2321–2330. PubMed PMC

Nielsen H., Engelbrecht J., Brunak S., 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. 1997;8:581–599. PubMed

Novinec M., Grass R.N., Stark W.J., Turk V., Baici A., Lenarcic B. Interaction between human cathepsins K, L, and S and elastins – mechanism of elastinolysis and inhibition by macromolecular inhibitors. J. Biol. Chem. 2007;282:7893–7902. PubMed

Nowak N., Lotter H., Tannich E., 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. 2004;279:38260–38266. PubMed

Pleass J.R., Aboobaker A.A., Schmitt A.O. Piggybacking schistosome invasion: similarities are only skin deep. Trends Parasitol. 2008;24:153–156. PubMed

Reis F.C., Costa T.F., Sulea T., Mezzetti A., Scharfstein J., Brömme D., Ménard R., 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. 2007;274:1224–1234. PubMed

Renslo A.R., McKerrow J.H. Drug discovery and development for neglected parasitic diseases. Nat. Chem. Biol. 2006;2:701–710. PubMed

Rosenthal P.J., Sijwali P.S., Singh A., Shenai B.R. Cysteine proteases of malaria parasites: targets for chemotherapy. Curr. Pharm. Des. 2002;8:1659–1672. PubMed

Rucker R.B., Dubick M.A. Elastin metabolism and chemistry: potential roles in lung development and structure. Environ. Health Persp. 1984;55:179–191. PubMed PMC

Salter J.P., Lim K.C., Hansell E., Hsieh I., McKerrow J.H. Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J. Biol. Chem. 2000;275:38667–38673. PubMed

Salter J.P., Choe Y., Albrecht H., Franklin C., Lim K.C., Craik C.S., McKerrow J.H. Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J. Biol. Chem. 2002;277:24618–24624. PubMed

Shaw E., Mohanty S., Colic A., Stoka V., Turk V. The affinity-labelling of cathepsin S with peptidyl diazomethyl ketones. Comparison with the inhibition of cathepsin L and calpain. FEBS Lett. 1993;334:340–342. PubMed

Skelly P.J., Shoemaker C.B. Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J. Parasitol. 2001;87:1218–1221. PubMed

Spiess E., Brüning A., Gack S., Ulbricht B., Spring H., Trefz G., 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. 1994;42:917–929. PubMed

Towatari T., Nikawa T., Murata M., Yokoo C., Tamai M., Hanada K., Katunuma N. Novel epoxysuccinyl peptides A selective inhibitor of cathepsin B in vivo. FEBS Lett. 1991;280:311–315. PubMed

Turk B., Turk D., Turk V. Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta. 2000;1477:98–111. PubMed

Yoshino T.P., Lodes M.J., Rege A.A., Chappell C.L. Proteinase activity in miracidia, transformation excretory–secretory products, and primary sporocysts of Schistosoma mansoni. J. Parasitol. 1993;79:23–31. PubMed

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