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Characterization of a High Molecular Weight Antigen of Cryptosporidium

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Characterization of a High Molecular Weight Antigen of Cryptosporidium Characterization of a high molecular weight antigen of Cryptosporidium parvum micronemes possessing epitopes that are cross-reactive with all parasitic life cycle stages B Robert, H Antoine, F Dreze, P Coppe, A Collard To cite this version: B Robert, H Antoine, F Dreze, P Coppe, A Collard. Characterization of a high molecular weight antigen of Cryptosporidium parvum micronemes possessing epitopes that are cross-reactive with all parasitic life cycle stages. Veterinary Research, BioMed Central, 1994, 25 (4), pp.384-398. hal- 00902231 HAL Id: hal-00902231 https://hal.archives-ouvertes.fr/hal-00902231 Submitted on 1 Jan 1994 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Original article Characterization of a high molecular weight antigen of Cryptosporidium parvum micronemes possessing epitopes that are cross-reactive with all parasitic life cycle stages B Robert1 H Antoine F Dreze P Coppe A Collard2 1 Département de Virologie; 2 Département d’immunologie, Centre d’Économie Rurale, 1, rue du Carmel, B-6900 Marloie, Belgium (Received 18 November 1993; accepted 25 February 1994) Summary ― Crossreacting antigens between life cycle stages of Cryptosporidium parvum (Proto- zoa, Apicomplexa) were detected using monoclonal antibodies (mAbs). Shared epitopes were demon- strated by immunoelectron microscopy, at the level of micronemes of the sporozoite and merozoite stages; some dense granules were also labelled but not so intensively. The parasitophorous vacuole membranes of all intracellular stages, the wall-forming bodies of macrogametes and the outer oocyst walls all shared these epitopes. The antigens that bear these epitopes were characterized using the whole oocyst and sporozoite stages as sources of antigenic material. Complex labelling patterns were observed on Western blots. However, all the mAbs used in this study recognized an antigen of more than 500 kDa. The glycoproteinic nature of this antigen was demonstrated by its sensitivity to pronase and periodate treatments. The expression of this high molecular weight immunoreactive antigen in the intracellular stages of C parvum was not investigated and remains to be found. Cryptosporidium parvum / microneme / parasitophorous vacuole / wall-forming bodies / oocyst wall Résumé ― Caractérisation d’un antigène de haut poids moléculaire localisé au niveau des micronèmes des zoites et possédant des épitopes communs avec tous les autres stades de Cryptosporidium parvum. Des antigènes communs à tous les stades du cycle parasitaire de Cryptosporidium parvum (Protozoa, Apicomplexa) ont été mis en évidence à l’aide d’anticorps monoclonaux (mAbs). Par immunoélectromiscroscopie, des épitopes communs ont été démontrés au niveau des micronèmes des stades sporozoites et mérozoites ; le marquage des granules * Correspondence and reprints denses de ces stades a également pu être observé mais d’une manière sporadique. Ces mêmes épitopes ont également été démontrés au niveau de la membrane de la vacuole parasitophore, de tous les stades, des «wall-forming bodies» des macrogamètes et de la paroi externe de l’oocyste. Les antigènes portant ces épitopes ont été caractérisés en utilisant les stades oocystes et sporozoites comme source d’antigène. Sur western blots, des profils anügéniques complexes ont été observés ; cependant, tous les anticorps monoclonaux décrits dans cet article ont en commun la reconnaissance d’un antigène de plus de 500 kDa. Il s’agit d’une glycoprotéine comme en témoigne sa sensibilité à la pronase et au traitement par le périodate. La démonstration de la présence de cette glycoprotéine, au niveau des stades intracellulaires de Cryptosporidium parvum mériterait d’être entreprise lors d’une étude ultérieure. cryptosporidium parvum / micronèmes / vacuole parasitophore / «wall-forming bodies» / paroi de l’oocyste INTRODUCTION the parasitophorous vacuole by invading zoites. Cross-reactive epitopes shared by micronemes and macrogametes were also Invasive stages of Apicomplexan parasites described by Bonnin et al (1993). possess characteristic organelles which are thought to be associated with the penetra- Using monoclonal antibodies, immuno- tion / invasion of the host cell (Scholtyseck electron microscopy and Western blotting, and Mehihorn, 1970). Three types of mem- we have investigated the antigenic struc- brane-bound organelles have been ture of micronemes of zoites, and we have described: (i) rhoptries, which are amphora- tried to show that epitopes associated with shaped, secretory granules (Perkins, 1992), these membrane-bound organelle were also connected by ductules to the tip of the api- expressed at all other life cycle stages of cal complex where secreted substances Cryptosporidium parvum. can be discharged (Sinden, 1985); (ii) micronemes, which are smaller, more numerous and may occupy much of the MATERIALS AND METHODS anterior third of the parasite; (iii) dense gran- ules, which are round, densely staining bod- ies (Bannister et al, 1975). Entzeroth et al Parasite and antigen purificafion (1986) have shown that dense granule con- tent was released the into through pellicle Parasites were isolated from faecal samples of the secondary parasitophorous vacuole of naturally infected calves. Oocysts were purified Sarcocystis muris. Dense granules have by ether and sucrose treatments as previously been described in only few species, such described (Robert etal, 1990). The preparation as Plasmodium knowlesi, Sarcocystis muris was sterilized by treatment with commercial and Toxoplasma gondii (Torii et al, 1989b). bleach (1/10 in PBS) for 10 min at 4°C, followed by 2 washes in sterile PBS (NaCl 8 g/l, KCI 0.2 Rhoptries, numerous micronemes and g/l, Na2HP04·2H0 1.15 g/I, KH2pO4 0.2 g/I, pH dense granules have been described in the 7.2). Only very clean preparations (no contami- zoites of the Cryptosporididae family (Vet- nation as seen by phase-contrast microscopy terling etal, 1971; Current and Reese, 1986; examination) were used. Sporozoites were Uni et al, 1987; Ostrovska and obtained by incubating purified oocysts in sterile Paperna, medium 0.5% sodium Bonnin have character- excystation (0.1 % trypsin, 1990). et al (1991 ) taurocholate in PBS, pH 7.6) at 37°C for 30 min ized an antigen family located in the (Wisher and Rose, 1987), and then washed by 2 micronemes. They suggest that the con- centrifugations (4°C; 10 min; 1 500 g) in sterile tents of micronemes might be released in PBS. Immunization of mice, production Labelling after embedding of monoclonal antibodies Ileum segments of OF1 mice experimentally infected in their first week of age, were taken 7 d Monoclonal antibodies were obtained (mAbs) by after oral inoculation of 10 000 oocysts. In the fusion of myeloma cells with Sp2-0-Agl4 first experiment, small ileum segments were fixed of Balb/c mice immunized with C splenocytes in 4% in 0.1 M phosphate We 3 different cellular fusions paraformaldehyde parvum. performed buffer for 4 h at 4°C, and then embedded. Osmi- (Kohler and Milstein, 1975). The first immuniza- cated tissues were prepared for a second labelling tion was realized by intraperitoneal injections of experiment: ileum pieces were fixed in 2.5% glu- at least 10! sonicated et at, oocysts (Ungar taraldehyde in 0.1 M phosphate buffer (pH 7.2) for Immunizations were on 0 1986). performed day 2 h 30 min at 4°C, then washed 3 times with phos- and on and 156. The first was days 14, 31, 149, buffer and with with Freund the phate post-fixed phosphate- given complete adjuvant (CFA), buffered 1 % osmium tetroxide for 1 h at 4°C. After others with incomplete Freund adjuvant (IFA). several rinses in buffer, the tissues were dehy- The fusion was carried out 4 d after the last drated through a grade series of ethanol to 100% booster, and mAb S1 G12 was obtained. For the and then embedded in LR-White resin (London second fusion, called Y (production of Y3A5 and Resin Co) (Bendayan et al, 1987). Thin sections Y14F3 mAbs), the mouse received 5 intraperi- were cut with a diamond knife and collected on toneal immunizations. Intact oocysts (20 x 106) nickel grids (coated, in some cases, with form- were infected, in CFA, 230 d before the fusion; 2 var) and floated for 10 min in PBS/2% BSA, then booster doses, in IFA, were 13 and 29 d given transferred onto culture later. The final boosters consisted of viable hybridomas medium, diluted (v/v) with PBS/BSA for 1 h. After wash- sporozoites (> 4 x 106) and oocysts (12 x 106) in PBS 0.01 % Tween the were suc- injected intraperitoneally, in PBS, 6 and 2 d ing 20, grids floated on rabbit anti-mouse before the fusion. For the third fusion, called AT cessively diluted to 10 in PBS/BSA (production of AT7G10, AT7F7 and AT9H6 immunoglobulin pg/ml and 15 nm gold-protein A conjugate (Amersham) mAbs), 8 x 106 intact oocysts were injected for 30 min and 1 h, The intraperitoneally in CFA 105 d prior to the fusion; respectively. gold conju- gate was diluted 1/50 in PBS/BSA with 1/20 followed 10 d later by an intraperitoneal injec- After 2 washes in PBS-0.01 % Tween 20, tion of 15 x 106 viable purified sporozoites in gelatin. were rinsed with water and stained for 20 PBS. An intrasplenic immunization (Spitz et at, grids min in 4% acetate in water. Control sec- 1984) was performed, 4 d before the fusion, using uranyl tions were in the same manner 11 x 106 sporozoites and oocysts fixed in 4% processed except that mAbs were omitted. Sections were exam- paraformaldehyde at 4°C for 1 h and washed ined with a electron twice with PBS.
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