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For the Detection of Microbial Antigens ROBERT H JOURNAL OF CLINICAL MICROBIOLOGY, Mar. 1984, p. 356-360 Vol. 19, No. 3 0095-1137/84/030356-05$02.00/0 Copyright © 1984, American Society for Microbiology Enzyme Immunoassays in Which Biotinillated 1-Lactamase is Used for the Detection of Microbial Antigens ROBERT H. YOLKEN* AND SIOK-BI WEE Eudowood Division of Infectious Diseases, Department ofPediatrics, School of Medicine, The Johns Hopkins Ilospital, Baltimore, Maryland 21205 Received 24 June 1983/Accepted 23 November 1983 The performance characteristics of enzyme immunoassays are determined to a great extent by the enzyme-substrate system utilized for the immunoassay. Beta-lactamases (penicillin amido-beta-lactamhy- drolase EC 3.5.2.6) offer a number of advantages which might make them useful in immunoassay systems. We linked beta-lactamase from Bacillus cereus with biotin and used the biotinillated enzyme to devise immunoassay systems for the detection of a number of microbial antigens. An assay system in which antibodies to the polyribitol phosphate antigen of Haemophilus influenzae type b were used was capable of detecting between 0.4 and 1.6 ng of that antigen. Similarly, an assay in which antibodies to the common antigens of adenoviruses and biotin-linked beta-lactamase were used was capable of detecting between 1 and 10 50% tissue culture infective doses of a strain of enteric-type adenovirus. When applied to the detection of rotavirus, a similar system in which biotinillated beta-lactamase was used was capable of detecting small amounts of antigen in a standard rotavirus preparation. This assay could also detect virus in 36 of 37 stool specimens from children with rotavirus gastroenteritis. The positive specimens could easily be distinguished from negative ones by the naked eye, and a permanent record of the qualitative results could be obtained by the use of a standard office photocopying machine. Beta-lactamases have promise for use in practical enzyme immunoassay systems, especially in situations in which expensive colorimetric instrumen- tation is not available. Enzyme immunoassays (EIAs) are attaining widespread (Biosearch Research Chemicals, San Rafael, Calif.) by the use in the detection of microbial antigens in clinical speci- method of Bayer et al. (3) with a biotin-beta-lactamase ratio mens. EIA systems utilize enzyme substrate reactions to of 2 to 1 (mg/mg). The enzyme was reacted with the biotin measure the binding of antigen to specific antibody (16, 18, ester for 3 h at 25°C, and the unreacted biotin ester was 24). The performance characteristics of EIAs are thus deter- removed by extensive dialysis. The biotinillated enzyme was mined to a great extent by the reaction kinetics of the stored at -20°C until use. enzyme substrate system used (20, 21). Enzymes which are Avidin DH was obtained from Vector Laboratories, Sun- currently in widespread use include alkaline phosphatase nyvale, Calif. Avidin from streptomyces was obtained from (24), horseradish peroxidase (1), and beta-galactosidase (19). Bethesda Research Laboratories, Gaithersburg, Md. Avidin These enzymes are used largely because they can be linked from egg white was obtained from Sigma. Biotinillated to immunoglobulin molecules to yield stable antibody-en- horseradish peroxidase was obtained from Vector Labora- zyme conjugates which retain a substantial portion of the tories. Goat antibody to rotavirus was obtained from Refer- enzymatic and antigen-binding activities of the original re- ence Reagents Branch, National Institute of Allergy and agents (2, 12). Beta-lactamases represent another group of Infectious Diseases, Bethesda, Md. Goat and rabbit antibod- enzymes which can be utilized in EIA systems (5, 7, 9). ies to adenovirus were obtained from MA Bioproducts, These enzymes, which hydrolyze beta-lactams to the corre- Walkersville, Md. Burro antibody to polyribitol phosphate sponding open-ring penicillinoic acids, have the advantage of of Haemophilus influenzae type b (PRP) was obtained from widespread availability and favorable reaction kinetics and John Robbins, Bethesda, Md. Chicken antibody to rota- have the availability of substrates without mutagenic or virus, isolated from the yolks of immunized hens, was carcinogenic potential (4, 13, 17). In addition, beta-lacta- obtained from Marc van Regenmortel, Strasbourg, France. mases can be linked to biotin, thus allowing their use in A 2% stool filtrate from a child with gastroenteritis was recently described avidin-biotin systems (6, 23). This report used as a standard rotavirus antigen. This preparation con- describes the development of solid-phase ETAs in which tains rotavirus antigen detectable at a 1:640 dilution by a biotinillated antibodies, avidin, and biotin-labeled beta-lacta- standard indirect EIA (24). A standard isolate of enteric-type mase are used for the detection of viral and bacterial adenovirus was obtained from the stool of a child with antigens. adenovirus gastroenteritis and cultivated in an adenovirus- transformed cell line (Grahm's 293 cells) as previously MATERIALS AND METHODS described (15, 22). The preparation utilized as a standard Beta-lactamase from Bacillus cereus (type I) was obtained antigen contained approximately 1,000 50% tissue culture from Sigma Chemical Co., St. Louis, Mo. The enzyme was infective doses per ml of viable virus as determined by this biotinillated by reaction with N-hydroxysuccinimide ester cultivation system. PRP was obtained from Porter Ander- son, Rochester, N.Y. Rectal swab specimens were obtained from 83 children with acute gastroenteritis. The swabs were placed into 2 ml * Correspondirig author. of phosphate-buffered saline (PBS) and stored at -20°C until 356 VOL. 19, 1984 DETECTION OF MICROBIAL ANTIGENS 357 testing. A total of 37 specimens had rotavirus detectable by a beta-lactamase assays, the results were expressed in terms standard direct EIA (24), using peroxidase-labeled rabbit of percent activity by the following formula: percent activity antirotavirus, whereas the remaining 46 specimens were = (OD spec/OD max) x 100, where OD spec is the optical negative for rotavirus by this assay. density of the specimen measured at 450 nm and OD max is Performance of immunoassays. The optimal dilutions of the maximum optical density measurable in the reaction reagents for each assay were determined by checkerboard system, generally 1.2 optical density units. The assays for titration as previously described (24). Preliminary studies enteric adenovirus and PRP were performed in a manner directed at determining the optimal substrate conditions analogous to that described above, with the exception that were performed by reacting biotinillated beta-lactamase with the reagents for these antigens were substituted for the microtiter wells coated with egg white avidin. Immunoas- rotavirus antigens. In the case of the assays for PRP, burro says for the detection of the microbial antigens were per- anti-PRP was used to coat the solid phase, and biotinillated formed in a manner analogous to that of previously de- burro anti-PRP immunoglobulin G was used as the liquid- scribed enzyme immunoassays in which biotinillated phase antibody. In the case of the assays for adenovirus, antibodies, avidin, and biotinillated enzymes were used (23). goat antiadenovirus was used as the solid-phase antibody, The assay for rotavirus is described as follows. The wells of and biotinillated rabbit antiadenovirus was used as the microtiter plates were coated with goat antirotavirus serum liquid-phase antibody. For both assays, percent activity was or control nonimmune goat serum diluted 1:10,000 in 0.06 M calculated as described above. carbonate buffer (pH 9.6). After incubation overnight at 4°C, the microtiter plates were washed five times with PBS RESULTS containing 0.05% Tween 20 (PBST), and a sample of a Preliminary studies were directed at determining the opti- standard antigen, clinical specimen, or negative control was mal parameters of the assay in which biotinillated beta- added to duplicate or quadruplicate wells. After incubation lactamase was used. These studies were performed by for 1 h at 37°C, the plates were washed, and biotin-labeled binding avidin to the microtiter plates in place of a specific chicken antirotavirus diluted 1:200 in PBST containing 0.5% antimicrobial antibody. After incubation overnight at 4°C, gelatin was added. After incubation for 1 h at 37°C, the plates the plates were washed and processed with optimally diluted were washed, and avidin DH diluted 1:500 in PBS was biotinillated beta-lactamase as described above. Initial stud- added. After incubation for 30 min at 37°C, the plates were ies revealed that a starch-iodine solution containing twice as again washed, and biotinillated beta-lactamase diluted much 12 and KI as had been previously described (13) 1:1,000 in PBST was added. After another incubation for 30 allowed a greater range of linear response and easier visual min at 37°C, the plates were washed, and starch-iodine readings in microtiter plates. Utilizing this starch-iodine substrate, modified from previously described solutions (13), solution (described above) and penicillin G at a concentra- was added. The modified substrate consisted of (milligrams per milliliter) starch, 2; penicillin G, 0.03; I2, 0.06; and KI, 1.6. The amount of decoloration of the starch-iodine sub- 140 strate due to the conversion of penicillin to penicillinoic acid was measured at a wavelength of 570 nm in a microplate 1.26 colorimeter (Dynatech MR-580). In addition, the reactions were scored with the naked eye and were recorded by 1.12 placing the microtiter plate on a standard office photocopier .98 (Xerox). To allow for the comparison of different enzyme substrate systems, the results of the assays with standard r)- .84 antigens were expressed in terms of percent activity by the a 70 following formula: percent activity = 1 - [(OD spec/OD 0 blank) x 100], where OD spec is the optical density of the .56 specimen measured at 570 nm and OD blank is the mean optical density of corresponding wells to which no antigen 42 was added.
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