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Identification of Immunogenic and Antibody-Binding Membrane Proteins of Pathogenic Trichomonas Vaginalis JOHN F

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Identification of Immunogenic and Antibody-Binding Membrane Proteins of Pathogenic Trichomonas Vaginalis JOHN F INFECTION AND IMMUNITY, Apr. 1983, p. 284-291 Vol. 40. No. 1 0019-9567/83/040284-08$02.00/0 Copyright © 1983, American Society for Microbiology Identification of Immunogenic and Antibody-Binding Membrane Proteins of Pathogenic Trichomonas vaginalis JOHN F. ALDERETE Department of Microbiology, The University of Texas Health Science Center at San Antonio, San Antonio, Texas 78284 Received 4 August 1982/Accepted 23 November 1982 Characterization of immunogenic Trichomonas vaginalis membrane proteins was accomplished by using extrinsically and intrinsically labeled organisms and a highly sensitive and specific radioimmunoprecipitation procedure. Intact motile trichomonads were compared with detergent extracts as a source of antigen in radioimmunoprecipitation experiments. Approximately 20 proteins accessible to antibody were identified and ranged in molecular weight from 200,000 to 20,000. Localization on the parasite surface of the highly immunogenic membrane proteins was attempted by using, as the indicator system, formaldehyde-fixed protein A-bearing Staphylococcus aureus pretreated with the various antiserum reagents and incubated with live, motile parasites. Also, indirect immunofluores- cence with fluorescein isothiocyanate-anti-rabbit immunoglobulin was also em- ployed after incubation of organisms with either control serum or antiserum from immunized rabbits or after treatment of trichomonads with the immunoglobulin G fraction from each respective serum. No immunoglobulin G antibody appeared to be directed at the anterior trichomonal flagella or the posterior axostyle, whereas strong fluorescence was detected throughout the rest of the T. vaginalis surface. The biological significance of these data is discussed. Trichomonal vaginitis is a sexually transmit- sexually transmitted disease (10, 13, 18, 20), ted disease responsible for significant morbidity therefore, has necessitated the need for research in both men and women. In symptomatic fe- directed toward identification of possible viru- males, the disease is characterized by pro- lence factors. The characterization of the sur- nounced inflammation of the vagina, foul-smell- face of T. vaginalis has not been accomplished. ing vaginal discharge, severe discomfort, and Furthermore, the use of conventional immuno- tissue cytopathology (10, 13, 18, 20). Although logical methods has failed to identify specific most men appear to be asymptomatic, disease virulence determinants or antigens (10, 11, 21, manifestations are increasingly being docu- 22). Because one of our aims is to assess host mented (19, 20). The causative agent, Trichomo- immunological responses to parasite antigens. nas vaginalis, is the most frequently acquired the nature of antibody responses from immu- protozoan infestation; however, few data are nized or infected experimental animals directed available on key areas of this host-parasite inter- toward immunogenic parasite proteins was re- action which would yield information on possi- cently demonstrated (1). In this report, numer- ble mechanisms of disease pathogenesis. ous highly immunogenic proteins which are ex- Current clinical diagnosis of trichomoniasis is posed on the membranes of intact T. vagintalis tedious, time consuming, highly inadequate, and and reactive with antibody while the membrane based on microscopic detection of the parasite proteins are in their native state are identified. (10, 20). These limitations in diagnosis exacer- The importance of these data is discussed. bate already limited medical care in rural health clinics in our country and the world. Thus, basic research is necessary to address relevant issues MATERIALS AND such as development of sensitive, accurate sero- METHODS logical assays for screening of symptomatic as Growth and radiolabeling of T. vaginalis organisms. well as asymptomatic patients and perhaps mon- T. vaginalis 286 (16) was a generous gift from Miklos Muller, Rockefeller University, New York, N.Y. Par- itoring disease progression. The development of asites were maintained in vitro in an air atmosphere as strategies to identify potential vaccinogen candi- described elsewhere (17) with Diamond Trypticase dates is equally important and necessary. (BBL Microbiology Systems, Cockeysville, Md.)- The emergence of trichomoniasis as a major yeast extract-maltose medium (pH 6.2) supplemented 284 VOL. 40, 1983 IMMUNOGENIC T. VAGINALIS MEMBRANE PROTEINS 285 with 10% heat-inactivated horse serum (Kansas City auireus (12) was added to bind the antibody-antigen Biologicals, Inc., Lenexa, Kans.). Only trichomonads complexes. After extensive washing of the protein A- at the late-log stage (24 h) of growth (17) were utilized bearing S. aureus radiolabeled antigen(s) were re- for experiments, and they represented a density of 2.5 leased by suspending pelleted protein A-bearing S. x 10' to 5.0 x 106 actively motile parasites per ml. aureus organisms in 100 p.1 of electrophoresis dissolv- Intrinsic radiolabeling with [35S]methionine (specific ing buffer (3, 17) and boiling for three min. The protein activity, 1,500 Ci/mmol; Amersham Corp., Arlington A-bearing S. aureus cells were then pelleted, and the Heights, Ill.) has been previously described (1, 3, 17). supernatant was electrophoresed as described below Pellets containing 1.4 x 107 to 3.5 x 107 trichomonads for fluorographic detection of immunogenic trichomo- were frozen at -70°C until use or employed immedi- nal proteins. ately for the radioimmunoprecipitation (RIP) assay The analysis of exposed membrane proteins on with whole cells as the antigen as described below. intact, motile T. vaginalis accessible to antibody by Electrophoretic protein patterns offrozen trichomonal RIP was performed immediately after intrinsic or pellets were identical to those of freshly harvested, extrinsic radiolabeling of parasites proteins. This pro- radiolabeled organisms. cedure has been recently and successfully employed Specific radioiodination of membrane proteins was for a bacterial model system (7, 8) and has been accomplished by standard chloramine-T labeling tech- defined as a whole cell (WC) RIP. Approximately 1.25 niques (5). One hundred milliliters containing 2.5 x 108 x 108 trichomonads were pelleted after intrinsic label- motile organisms was washed at least three times in ing with [35S]methionine (1, 17) or chloramine-T-medi- phosphate-buffered saline (PBS) to remove serum pro- ated radioiodination and suspended with 100 p.1 of teins contaminating trichomonal surfaces (17). Tricho- appropriate heat-inactivated control serum or heat- monads were suspended to 1 ml in PBS followed by inactivated antiserum reagent. The suspension was the sequential addition of 3 mCi of Na125I (Amersham) incubated for 120 min at 37°C with occasional gentle and 100 ,ul of 0.4% chloramine-T (Sigma Chemical stirring followed by washing of the trichomonads no Co., St. Louis, Mo.). After a 5-min incubation at room less than twice in PBS. T. vaginalis organisms were temperature with constant gentle stirring, 100 ,ul of then suspended in 200 p.1 of NET (150 mM NaCl, 5 mM 0.4% NaHSO3 was added to terminate the reaction. EDTA, 50 mM Tris-hydrochloride, pH 7.2) buffer and Trichomonads remained motile under these experi- solubilized by the addition of 25 p.l of 10% Z3-12 mental conditions and were washed at least three detergent (4, 6). The preparation was gently homoge- times further with phosphate-buffered Nal (same as nized, and an additional 200 p.l of NET buffer was PBS, except Nal was substituted for NaCl) before added. The extract was then centrifuged at 35,000 rpm aliquoting for freezing at -70°C or immediate use in (Beckman SW50.1 rotor) to remove insoluble debris. the RIP with intact, motile organisms. Regardless of the type of radiolabeling employed for Serum reagents. Prebled control serum and antise- parasites in this WC RIP, greater than 80% of the rum against T. vaginalis strain 286 were generated in radioactivity was recovered in the supernatant after New Zealand white rabbits injected subcutaneously centrifugation. Finally, 100 p.l of 10% (vol/vol) protein and intramuscularly with a mixture of 0.5 ml of tricho- A-bearing S. aureus cells prepared as previously de- monal suspension containing 2.5 x 107 organisms and scribed (2, 3, 12, 17) was added to the clarified, 0.5 ml of Freund complete adjuvant (GIBCO Labora- solubilized extract, and the mixture was again incubat- tories, Grand Island, N.Y.). Booster injections were ed at 370C with occasional shaking. The protein A- performed 2 weeks later with equal amounts of orga- bearing S. aureus cells were then pelleted and washed, nisms in Freund incomplete adjuvant. Parasites were and the adsorbed radiolabeled antigen was processed extensively washed three times in PBS to remove with dissolving buffer as described above. contaminating medium macromolecules adsorbed onto Sodium dodecyl sulfate-polyacrylamide gel electro- parasite surfaces (17). Rabbits were bled 14 days after phoresis. The procedures outlining preparation of total booster immunization, and the sera were stored at T. vaginalis proteins for sodium dodecyl sulfate-poly- -70°C until use. Adsorbed antiserum was generated acrylamide gel electrophoresis and fluorography were by suspension of 1.7 x 107 trichomonads washed three as outlined elsewhere (1, 2, 17). Stacking and separat- times in PBS in 0.5 ml of antiserum, and the incubation ing gels consisted of 3 and 7.5% acrylamide (Bio-Rad was continued for 30 min at 37°C. The serum was Laboratories, Richmond, Calif.), and electrophoresis
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