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In vitro stimulation of penetration gland emptying by Trichobilharzia szidati and T. regenti (Schistosomatidae) cercariae. Quantitative collection and partial characterization of the products

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Abstract

Induction of penetration gland emptying by cercariae of the bird schistosomes Trichobilharzia szidati and T. regenti employing linoleic acid, linolenic acid, praziquantel and calcium ionophore A23187 showed that both postacetabular and circumacetabular cells released their content at chosen stimulant concentrations. The gland secretions consisted of soluble and insoluble parts. The former one adhering to the ground seemed to have different saccharide composition from the glands of Schistosoma mansoni. It bound labelled saccharides, thus exhibiting lectin-like activity. Protein profiles of the latter one were identical after stimulation by all four stimulants in T. szidati. The soluble secretions contained several proteolytic enzymes; 31 kDa and 33 kDa cysteine proteases were identified in E/S products of T. szidati and T. regenti, respectively. The circumacetabular glands contained a significant amount of calcium. Immunohistochemistry revealed that the origin of E/S products after in vitro stimulation is in both penetration glands and tegumental structures. No crossreactivity was observed between the bird schistosomes and a serum raised against S. mansoni elastase.

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References

  • Austin FG, Stirewalt MA, Danzinger RE (1972) Stimulatory effect of rat skin lipid fractions on cercarial penetration behavior. Exp Parasitol 31:217–224

    Article  CAS  PubMed  Google Scholar 

  • Austin FG, Frappaolo P, Gilbert B, Landis W, da Rosa MN, Stirewalt MA (1974) Further studies of Schistosoma mansoni cercarial stimulation by crude egg lecithin and other lipids. Parasitology 69:455–463

    CAS  PubMed  Google Scholar 

  • Bahgat M, Ruppel A (2002) Biochemical comparison of the serine protease (elastase) activities in cercarial secretions from Trichobilharzia ocellata and Schistosoma mansoni. Parasitol Res 88:495–500

    Article  CAS  PubMed  Google Scholar 

  • Bahgat M, Francklow K, Doenhoff MJ, Li YL, Ramzy RMR, Kirsten C, Ruppel A (2001) Infection induces antibodies against the cercarial secretions, but not against the cercarial elastases of Schistosoma mansoni, Schistosoma haematobium, Schistosoma japonicum and Trichobilharzia ocellata. Parasite Immunol 23:557–565

    Article  CAS  PubMed  Google Scholar 

  • Barrett AJ, Kirschke H (1981) Cathepsin B, cathepsin H and cathepsin L. Methods Enzymol 80:535–561

    CAS  PubMed  Google Scholar 

  • Blažová K, Kolářová L, Horák P, Frýzková M (2004) Development of Trichobilharzia regenti in ducks: new routes of transmission and treatment with praziquantel (in Czech). Czech and Slovak Parasitological Days, Ostravice, Czech Republic p 2, 17– 21 May 2004 (Abstract Book)

    Google Scholar 

  • Bruckner DA (1974) Differentiation of pre- and postacetabular glands of schistosome cercariae using apomorphine as a stain. J Parasitol 60:752–756

    CAS  PubMed  Google Scholar 

  • Chavez-Olortegui C, Resende M, Tavares CAP (1992) Purification and characterization of a 47 kDa protease from Schistosoma mansoni cercarial secretion. Parasitology 105:211–218

    CAS  PubMed  Google Scholar 

  • Coles GC, Jansson HB, Zuckerman BM (1988) Lectin studies of surface carbohydrates and induction of gland secretion in the free-living stages of Schistosoma mansoni. J Chem Ecol 14:691–700

    Article  CAS  Google Scholar 

  • Dalton JP, Clough KA, Jones MK, Brindley PJ (1997) The cysteine proteinases of Schistosoma mansoni cercariae. Parasitology 114:105–112

    Article  PubMed  Google Scholar 

  • Day TA, Bennett JL, Pax RA (1992) Praziquantel: the enigmatic antiparasitic. Parasitol Today 8:342–344

    Article  CAS  PubMed  Google Scholar 

  • Dorsey CH, Stirewalt MA (1971) Schistosoma mansoni: fine structure of cercarial acetabular glands. Exp Parasitol 30:199–214

    Article  CAS  PubMed  Google Scholar 

  • Dorsey CH, Stirewalt MA (1977) Schistosoma mansoni: localization of calcium-detecting reagents in electron-lucent areas of specific preacetabular gland granules. Z Parasitenkd 54:165–173

    Article  CAS  PubMed  Google Scholar 

  • Dresden MH, Asch HL (1977) Calcium carbonate content of the preacetabular glands of Schistosoma mansoni cercariae. J Parasitol 63:163–165

    CAS  PubMed  Google Scholar 

  • Dresden MH, Edlin EM (1975) Schistosoma mansoni: calcium content of cercariae and its effects on protease activity in vitro. J Parasitol61:398–402

    CAS  Google Scholar 

  • Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M (2000) Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem Biol 7:569–581

    Article  CAS  PubMed  Google Scholar 

  • Haas W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106:349–364

    Google Scholar 

  • Haas W, Schmitt R (1982) Characterization of chemical stimuli for the penetration of Schistosoma mansoni cercariae. I. Effective substances, hosts specificity. Z Parasitenkd 66:293–307

    Article  CAS  PubMed  Google Scholar 

  • Haas W, van de Roemer A (1998) Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata: penetration processes and stimulating host signals. Parasitol Res 84:787–795

    Article  CAS  PubMed  Google Scholar 

  • Haas W, Diekhoff D, Koch K, Schmalfuss G, Loy C (1997) Schistosoma mansoni cercariae: stimulation of acetabular gland secretion is adapted to the chemical composition of mammalian skin. J Parasitol 83:1079–1085

    CAS  PubMed  Google Scholar 

  • Hara I, Hara S, Fusco AC, Shibuya T (1993) Role of calcium ion in Schistosoma mansoni cercarial tail loss induced by unsaturated fatty acids. Am Soc Parasitol 79:504–509

    CAS  Google Scholar 

  • Horák P (1995) Developmentally regulated expression of surface carbohydrate residues on larval stages of the avian schistosome Trichobilharzia szidati. Folia Parasitol 42:255–265

    PubMed  Google Scholar 

  • Horák P, Grubhoffer L, Mikeš L, Tichá M (1997) Lectins of Trichobilharzia szidati cercariae. Parasite 1:27–35

    Google Scholar 

  • Horák P, Kovář L, Kolářová L, Nebesářová J (1998) Cercaria-schistosomulum surface transformation of Trichobilharzia szidati and its putative immunological impact. Parasitology 116:139–147

    Article  PubMed  Google Scholar 

  • Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233

    Article  PubMed  Google Scholar 

  • Landsperger WJ, Stirewalt MA, Dresden MH (1982) Purification and properties of a proteolytic enzyme from the cercariae of the human trematode parasite Schistosoma mansoni. Biochem J 201:137–144

    CAS  PubMed  Google Scholar 

  • Linder E (1985) Schistosoma mansoni: visualization with fluorescent lectins of secretions and surface carbohydrates of living cercariae. Exp Parasitol 59:307–312

    Article  CAS  PubMed  Google Scholar 

  • Linder E (1986) Fluorochrome-labelled lectins reveal secreted glycoconjugates of schistosome larvae. Parasitol Today 2:219–221

    Article  CAS  PubMed  Google Scholar 

  • MacInnis AJ (1969) Identification of chemicals triggering cercarial penetration responses of Schistosoma mansoni. Nature 224:1221–1222

    CAS  PubMed  Google Scholar 

  • Marikovsky M, Arnon R, Fishelson Z (1988) Proteases secreted by transforming schistosomula of Schistosoma mansoni promote resistance to killing by complement. J Immunol 141:273–278

    CAS  PubMed  Google Scholar 

  • Marikovsky M, Arnon R, Fishelson Z (1990) Schistosoma mansoni: localization of the 28 kDa secreted protease in cercaria. Parasite Immunol 12:389–401

    CAS  PubMed  Google Scholar 

  • Matsumura K, Shimada M, Sato K, Aoki Y (1990) Praziquantel-induced secretion of proteolytic enzyme from Schistosoma mansoni cercariae. J Parasitol 76:436–438

    CAS  PubMed  Google Scholar 

  • Matsumura K, Mitsui Y, Sato K, Sakamoto M, Aoki Y (1991) Schistosoma mansoni: possible involvement of protein kinase C in linoleic acid-induced proteolytic enzyme release from cercariae. Exp Parasitol 72:311–320

    Article  CAS  PubMed  Google Scholar 

  • McKerrow JH, Pino-Heiss S, Linquist R, Werb Z (1985) Purification and characterization of an elastinolytic proteinase secreted by cercariae of Schistosoma mansoni. J Biol Chem 260:3703–3707

    CAS  PubMed  Google Scholar 

  • Mikeš L, Horák P (2001) A protein with lectin activity in penetration glands of Diplostomum pseudospathaceum cercariae. Int J Parasitol 31:245–252

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Modha J, Redman CA, Thornhill JA, Kusel JR (1998) Schistosomes: unanswered questions on the basic biology of the host-parasite relationship. Parasitol Today 14:396–401

    Article  Google Scholar 

  • Müller V, Kimmig P, Frank W (1993) The effect of praziquantel on Trichobilharzia (Digenea, Schistosomatidae), a causative agent of swimmer’s dermatitis in man (in German). Appl Parasitol 34:187–201

    PubMed  Google Scholar 

  • Mussini I, Magreth A, Salviati G (1972) On the criteria for oxalate in sarcoplasmatic reticulum fragments. J Ultrastruct Res 38:459–465

    Article  CAS  PubMed  Google Scholar 

  • Pierrot C, Godin C, Liu JL, Capron A, Khalife J (1996) Schistosoma mansoni elastase: an immune target regulated during the parasite life-cycle. Parasitology 113:519–526

    CAS  PubMed  Google Scholar 

  • Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DTJ, Horák P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95:79–89

    Article  PubMed  Google Scholar 

  • Salter JP, Lim KC, Hansell E, Hsieh I, McKerrow JH (2000) Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J Biol Chem 275:38667–38673

    Article  CAS  PubMed  Google Scholar 

  • Salter JP, Choe Y, Albrecht H, Franklin C, Lim KC, Craik CS, McKerrow JH (2002) Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J Biol Chem 277:24618–24624

    Article  CAS  PubMed  Google Scholar 

  • Shiff CJ, Cmelik SHW, Ley HE, Kriel RL (1972) The influence of human skin lipids on the cercarial penetration responses of Schistosoma haematobium and Schistosoma mansoni. J Parasitol 58:476–480

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Stirewalt MA (1974) Schistosoma mansoni: cercaria to schistosomulum. Adv Parasitol 12:115–182

    CAS  PubMed  Google Scholar 

  • Stirewalt MA, Kruidenier FJ (1961) Activity of the acetabular secretory apparatus of cercariae of Schistosoma mansoni under experimental conditions. Exp Parasitol 11:191–211

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Prof. M. Doenhoff, University of Wales, Bangor, UK and Dr. A. Mountford, University of York, UK, for provision of S. mansoni cercariae, E/S products and antielastase antibodies. Our grateful thanks belong also to Dr. C. Caffrey and Dr. D. Greenbaum, Sandler Center for Basic Research in Parasitic Diseases, UCSF, USA, for the supply of DCG-04 cysteine protease probe, and Prof. M. Tichá, Department of Biochemistry, Charles University Prague, for biotinylated glycosaminoglycans. The project was supported by the grants of the Grant Agency of the Czech Republic no. 524/04/P082 and 524/03/1263, Grant Agency of the Charles University no. 263/2004/B/Bio, the Wellcome Trust Collaborative Research Initiative Grant no. 072255 and the grant of the Ministry of Education of the Czech Republic no. 0021620828. The experiments presented in this paper comply with current laws of the Czech Republic.

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  1. Department of Parasitology, Charles University, Viničná 7, 12844, Prague 2, Czech Republic

    Libor Mikeš, Lenka Zìdková, Martin Kašný, Jan Dvořák & Petr Horák

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  1. Libor Mikeš
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  2. Lenka Zìdková
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  5. Petr Horák
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Correspondence to Libor Mikeš.

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The project was supported by the following grants: Grant Agency of the Czech Republic no. 524/04/P082 and 524/03/1263, Grant Agency of the Charles University no. 263/2004/B/Bio, the Wellcome Trust Collaborative Research Initiative Grant no. 072255 and the grant of the Ministry of Education of the Czech Republic no. 0021620828.

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Mikeš, L., Zìdková, L., Kašný, M. et al. 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, 230–241 (2005). https://doi.org/10.1007/s00436-005-1347-1

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