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In Vitro Culture of Baylisascaris Procyonis and Initial Analysis of Larval Excretory-Secretory Antigens

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In Vitro Culture of Baylisascaris Procyonis and Initial Analysis of Larval Excretory-Secretory Antigens Proc. Helminthol. Soc. Wash. 55(1), 1988, pp. 15-18 In Vitro Culture of Baylisascaris procyonis and Initial Analysis of Larval Excretory-Secretory Antigens W. M. BOYCE, B. A. BRANSTETTER, AND K. R. KAZACOS Department of Veterinary Microbiology, Pathology and Public Health, School of Veterinary Medicine, Purdue University, West Lafayette, Indiana 47907 ABSTRACT: Larvae of Baylisascaris procyonis hatched from embryonated eggs were cultured in vitro for 6 wk. Larvae molted once during culture, and increased in length from x = 0.278 to 0.513 mm. Sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) and immunoblotting of excretory-secretory (ES) ma- terials collected from these cultures demonstrated a heterogeneous group of antigenic proteins ranging from 10 to 70 kd. Immunoblots using these ES antigens allowed for the differential diagnosis of B. procyonis from Toxocara canis infections in rabbits, and they may prove useful in the immunodiagnosis of B. procyonis infections in other species, including humans. KEY WORDS: nematode, in vitro culture, Baylisascaris procyonis, Toxocara canis, excretory-secretory (ES) antigens, SDS-PAGE, immunoblotting, immunodiagnosis. Baylisascaris procyonis, the common ascarid dium (DMEM, GIBCO), containing 100 units/ml pen- of raccoons (Procyon lotor}, has recently emerged icillin and 100 /ug/ml streptomycin, in 24-well poly- as an important cause of larva migrans in ani- styrene tissue culture plates (Corning Glass Works, Corning, New York). Each well contained 2 ml DMEM mals and humans (Kazacos, 1986). Currently, with a larval concentration of 10,000/ml. Larvae were definitive diagnosis of larva migrans due to B. maintained for 6 wk at 37°C in 5% CO2 and compressed procyonis requires microscopic identification of air and the media changed weekly. Larval mortality larvae either within or recovered from host tis- was assessed on a weekly basis by examining 100 larvae stained with 1:10,000 new methylene blue. Dead larvae sues (Buffet al., 1984; Fox etal., 1985). A specific rapidly absorbed the dye along their cuticles while live immunoassay for B. procyonis infections is larvae remained largely unstained and were motile. therefore highly desirable. Excretory-secretory Samples of larvae were also collected at regular inter- (ES) materials released by parasitic nematodes vals and fixed in hot alcohol-formalin-acetic acid (AFA) during in vitro culture represent a potential source for morphometric and developmental analyses. Culture medium collected at weekly intervals was of useful diagnostic antigens. This report de- dialyzed against DPBS and concentrated by diafiltra- scribes an in vitro culture technique for larvae tion using spiral cartridge and stir cell apparatuses with of B. procyonis, and the initial analysis of ES molecular weight exclusion limits of 10,000 (Amicon antigens collected from this system. Corp., Danvers, Massachusetts). Protein concentration determinations, SDS-PAGE, and immunoblotting were Materials and Methods performed according to manufacturer's instructions, utilizing equipment and reagents obtained from Bio- Adult B. procyonis were obtained from the intestines Rad (Richmond, California). SDS-PAGE was per- of naturally infected raccoons, and eggs were collected formed under reducing conditions in a discontinuous and embryonated as described by Kazacos et al. (1981). system utilizing 4% stacking and either 12% or 15% Embryonated eggs were washed 3 times in 0.85% NaCl separating gels. Following completion of the SDS-PAGE and decoated for 30-90 min (without agitation) at 37°C run, gels were either silver stained or the proteins were in a 1:1 mixture of 5.25% sodium hypochlorite and 1% electrophoretically transferred from the gels onto ni- NaOH. Decoating was stopped when the outer layers trocellulose using a Bio-Rad transblot apparatus. SDS- of the egg shells had been removed and the remaining PAGE and silver staining were performed with be- vitelline membranes became distorted by the move- tween 3.5 and 4.5 ng of protein collected from each of ments of the enclosed larvae. Following decoating, eggs the 6 wk of culture. Immunoblotting was performed were washed 4 times in 0.85% NaCl and hatched in with pooled protein samples collected from the 1st 3 Earle's balanced salt solution (EBSS, Grand Island Bi- wk of culture, utilizing 200 /ug of protein per 16x11 ological Co. [GIBCO], Grand Island, New York) as cm gel. described for Ascaris suum by Urban et al. (1981). The Following protein transfer, the portion of the nitro- resulting larval suspension was washed 2 times in EBSS cellulose containing molecular weight standards was and layered over sterile cotton gauze in a glass funnel cut off and stained with 0.1% amido black. Reactive and maintained overnight at 37°C. The following sites were blocked with 3% gelatin and the membranes morning, larvae were collected aseptically in 10 ml incubated for 3 hr in a 1:100 dilution of antisera. Anti- aliquots and washed 6 times in warm, sterile Dulbec- sera were obtained from New Zealand White (NZW) co's phosphate buffered saline (DPBS, GIBCO). Larvae rabbits orally inoculated with 10,000 embryonated eggs were dispensed into Dulbecco's modified Eagle's me- of B. procyonis or T. canis. Serum was collected from 15 Copyright © 2011, The Helminthological Society of Washington 16 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY 66 92 66 45 45 31 31 21 14 21 123 4 56 Figure 1. Silver-stained SDS-PAGE gel (15%) of B. procyonis ES proteins collected at weekly intervals (1-6). Molecular weight standards (in kilodaltons) are 14 in far left lane. these rabbits at 14 and 56 days postinfection, respec- A B C D E tively, as well as from uninfected control rabbits. Se- rum was also collected from 2 pet rabbits naturally Figure 2. I mmunohlots of B. procyonis ES antigens infected with B. procyonis following accidental expo- transferred from 12% SDS-PAGE gels. Lane A = Nor- sure to B. procyonis eggs from a raccoon previously mal rabbit sera. Lane B = Toxocara canis antisera, housed in the same cage. The size of the infective dose rabbit, 56 days PI. Lane C = Baylisascaris procyonis and the duration of infection could not be positively antisera, rabbit, 14 days PI. Lanes D and E = Sera determined for these rabbits. However, based on pre- from 2 rabbits naturally infected with Baylisascaris pro- vious observations they had probably ingested large cyonis. Approximate molecular weights (in kilodaltons) numbers of eggs within the previous 3-6 wk (Kazacos, are shown on the right. 1986). Following incubation in rabbit antisera, nitro- cellulose membranes were incubated for 1 hr in a 1:3,000 dilution of goat anti-rabbit IgG (H and L chains) conjugated with horseradish-peroxidase. Color devel- eggs, or recovered following hatching and Baer- opment was visualized after the addition of 4-chloro- mannization, were loosely enclosed in the cuticle 1-naphthol. of the previous stage. Within 24 hr 8% of the larvae had shed this cuticle, and by 72 hr > 90% Results and Discussion of larvae had completed this molt. Larvae con- Initially, decoating of embryonated eggs of B. tinued to grow throughout the culture period, but procyonis required periods of time varying from no further molts were detected. Ascaris suum lar- 30 to 90 min. However, subsequent trials re- vae have also been shown to grow and develop vealed that decoating could routinely be accom- when cultured in DMEM (Urban and Tromba, plished in 30 min when 10 ml of eggs were gently 1982), whereas T. canis larvae did not molt in agitated with 2 changes of 5.25% sodium hy- DMEM when maintained for periods up to 18 pochlorite (without 1 % NaOH) on a shaker plat- mo (de Savigny, 1975). form. Larvae either expressed from embryonated In the present study it is unclear whether the Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 55, NUMBER 1, JANUARY 1988 17 cuticle shed during the first few days of culture in T. canis ES components from different culture represents the 1 st or 2nd molt. Sprent et al. (1973) batches (Speiser and Gottstein, 1984; Badley et stated that the 2nd molt took place 1-2 wk after al., 1987). infection of mice with eggs of either B. devosi or Equal amounts of ES proteins were pooled from B. tasmaniensis, and Douvres et al. (1969) stated the 1 st 3 wk of culture for use in immunoblotting, that the 2nd molt of A. suum occurred in the since larval mortality was > 10% after 3 wk. The liver within 1 wk. In contrast, Maung (1978) major ES proteins identified by silver staining of reported that the 1st 2 molts of A. suum occur polyacrylamide gels were recognized by immu- within the egg, and that 3rd-stage larvae may noblot analysis with sera from rabbits infected hatch from the egg still enclosed within the 2nd- with B. procyonis (Fig. 2). Serum from the T. stage cuticle. Further work is needed to deter- canis infected rabbit cross-reacted with several mine which larval stage of B. procyonis, as well B. procyonis ES antigens, with the notable ex- as other ascarids, hatches from the embryonated ceptions of those having apparent molecular egg. weights of 18, 39 (doublet), and 43 kd. These After hatching and Baermannization, B. pro- results have been substantiated by immunoblot cyonis larvae measured an average of 0.278 mm analysis using sera from several other T. cams- in length (N = 25). The larvae continued to grow infected rabbits, and immunoblotting using ES averaging 0.333 mm at 1 wk, 0.409 mm at 2 wk, antigens has consistently allowed us to differ- 0.451 mm at 3 wk, and 0.513 mm at 6 wk (TV = entiate B. procyonis infections from T. canis in- 25 at each wk). Larval mortality progressively fections in rabbits. increased from 5% (wk 1), to 9% (wk 3), and Toxocara canis larval ES antigens are of prov- finally to near 50% by 6 wk when the cultures en value in the serodiagnosis of toxocaral visceral were terminated.
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