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Tases from Ribonucleic Acid Tumor Viruses JOURNAL OF VIROLOGY, Jan. 1972, p. 110-115 Vol. 9, No. I Copyright © 1972 American Society for Microbiology Printed in U.S.A. Immunological Relationships of Reverse Transcrip- tases from Ribonucleic Acid Tumor Viruses WADE P. PARKS, EDWARD M. SCOLNICK, JEFFREY ROSS, GEORGE J. TODARO, AND STUART A. AARONSON Viral Carcinogenesis Branch and Viral Leukemia and Lymphoma Branch, National Cancer Institute, Bethesda, Maryland 20014 Received for publication 12 October 1971 Antiserum to partially purified reverse transcriptase from the Schmidt-Ruppin strain of Rous sarcoma virus has been prepared and characterized. Antibody to the avian polymerase inhibited the reverse transcriptase activity of avian C-type viruses but had no effect on the polymerase activity from C-type viruses of other classes. The known mammalian C-type viral polymerases were significantly inhibited only by the antiserum to murine C-type viral polymerases; reverse transcriptases from four other mammalian viruses were immunologically distinct from both avian and mam- malian C-type viral polymerases. Partially purified murine leukemia viral DNA po- lymerase activity was comparably reduced by specific antibody regardless of the tem- plate used for enzyme detection. Antibody to the deoxyribonucleic acid (DNA) grown in a line of sheep testes cells and kindly pro- polymerase activities of murine C-type viruses vided by K. K. Takemoto and L. B. Stone (NIH, has been previously demonstrated in the sera of Bethesda, Md.). Mason-Pfizer monkey virus (MP- rats with murine leukemia virus (MuLV)-re- MV; reference 9) was grown in either monkey embryo cells or a human lymphoblastoid line (NC-37); some leasing tumors and in the sera of rabbits im- MP-MV preparations were provided by M. Ahmed. munized with partially purified murine viral The primate syncytium-forming ("foamy") virus polymerases (2). These studies suggested that the type 3 was propagated in monkey kidney cells or rat reverse transcriptases of mammalian C-type cells (13). viruses were immunologically related. In the Polymerase purification. DNA polymerase from the present report, we describe the preparation of a Rauscher strain of murine leukemia virus (R-MuLV), rabbit antiserum against a partially purified the Schmidt-Ruppin strain of Rous sarcoma virus avian C-type viral reverse transcriptase and (SR-RSV), and the MP-MV were partially purified by extend our previous studies of the immunological gel filtration and phosphocellulose chromatography as reported earlier, except that the dextran-poly- relationships between viral reverse transcriptases. ethylene glycol step was omitted (14). AND METHODS Preparation of antisera. New Zealand white rabbits MATERIALS (2 to 3 kg) were inoculated with 1 to 2 ml of con- Viruses. The sources of several of the viruses used centrated, partially purified viral polymerase (<5 jug in the present studies have been detailed previously of protein) emulsified with an equal volume of com- (16); they were purified by sucrose density gradient plete Freund's adjuvant. Inoculation was either into sedimentation and were used as 100- to 300-fold con- the hind footpads or at multiple subcutaneous sites. centrates unless otherwise specified. Rous-associated Booster doses were administered subcutaneously at viruses types 1 and 2 (RAV-1 and RAV-2) and the subsequent 2- to 3-week intervals. Control rabbit sera Bryan strain of Rous sarcoma virus (B-RSV) were consisted of either preimmunization bleedings from obtained from the Viral Resources and Logistics the same rabbits or sera from comparable nonim- Segment, National Cancer Institute, National In- munized rabbits. stitutes of Health (NIH), Bethesda, Md. The C-type Chromatographic procedures. High-titered antisera virus of ophidian origin (viper virus) originally de- were fractionated by precipitation with 50% am- scribed by Zeigal and Clark (17) was grown in a viper monium sulfate, and the immunoglobulin G (IgG) spleen cell line and kindly provided by R. Gilden was purified by (DEAE) chroma- (Flow Laboratories, Rockville, Md.). A nontrans- diethylaminoethyl forming "helper" leukemia virus (RaLV) was isolated tography as previously described (2). The immuno- from a stock of the rat-tropic sarcoma virus, MSV-0 globulin fractions were concentrated by ultrafiltration (1). The rat mammary carcinoma cell line R-35, pro- with a P-30 membrane (Amicon, Lexington, Mass.), ducing a C-type virus (4), was kindly supplied by M. and protein concentrations were determined by the Ahmed (Pfizer, Maywood, N.J.). Visna virus was procedure of Lowry et al. (10). 110 VOL. 9, 1972 REVERSE TRANSCRIPTASES FROM RNA TUMOR VIRUSES III Polymerase assays. Each reaction mixture was RESULTS incubated at 37 C for periods of time (30 to 60 min) when the reaction was still linear and contained in 0.10 Antiserum inhibition of avian and murine poly- or 0.20 ml, as indicated in the appropriate legends: merase. Sera from animals inoculated with 0.04 M tris(hydroxymethyl)aminomethane-hydrochlo- polymerase preparations first demonstrated in- ride (pH 7.8); 0.06 M potassium chloride; 0.002 M hibition of viral enzyme activity 8 to 12 weeks dithiothreitol; 2 X 10- M 3H-thymidine triphosphate after primary immunization. Once an antibody (5,000 counts per min per pmole); and, unless other- response was detected, animals were given ad- wise noted, polyriboadenylic oligodeoxythymidylic ditional inoculations until antiserum titers reached acid (poly rA - oligo dT(l2 l8); Collaborative Research, maximal levels. As shown in Fig. 1A, 19 Mg of Waltham, Mass.; references 12-17). All templates were included at saturating levels: 0.02 absorbancy R-MuLV polymerase antisera reduced R-MuLV unit at 260 nm per 0.1 or 0.2 ml. For reactions con- polymerase activity by more than 50% of the taining poly rA oligo dT or polyriboadenylic-poly- control incorporation, whereas SR-RSV polym- ribouridylic (poly rA. poly rU), the divalent cation erase was unaffected by as much as 162,ug of used was manganese (10-4 M manganese acetate). serum protein. Conversely, antiserum to the SR- In reactions containing "activated" DNA (14) RSV polymerase inhibited partially purified SR- or viral ribonucleic acid (RNA), the divalent RSV enzyme over 90% but had no effect on the cation used was magnesium (6 X 10-3 M magne- R-MuLV polymerase activity (Fig. IB). sium acetate); 5 X 10-4 M unlabeled deoxyaden- Purified DEAE osine triphosphate, deoxycytidine triphosphate, and IgG isolated by chromatog- deoxyguanosine triphosphate were also included. In- raphy from immune sera showed the same pat- corporation in the absence of added templates was terns of inhibition as did whole serum but had a between 0.1 and 0.2 pmoles and was subtracted higher specific activity for enzyme inhibition. where indicated. The sources of isotopes, polymers, Whereas 50 to 100 jig of whole serum protein per and the preparation of enzymes have been pre- reaction was required for 90%/ inhibition of R- viously described (14); enzymes referred to as MuLV polymerase activity (Fig. 2A), less than partially purified represent the Sephadex G-100 or 10,Mg of IgG protein gave comparable inhibition phosphocellulose fractions as indicated in appropriate (Fig. 2B). Although stimulation of viral polym- legends. Murine viral polymerase partially purified by erase was phosphocellulose chromatography does not have activity frequently observed with detectable nuclease activity nor group-specific (gs) whole serum at low concentrations (10 to 50,Mg antigens; both nuclease and gs antigen reactivity are per reaction mixture; reference 2), inhibition of recovered in the column void volume (unpublished viral polymerase by control sera or DEAE- data). MuLV RNA was the gift of M. Hatanaka purified IgG fractions was observed at high pro- (Flow Laboratories, Rockville, Md.). tein levels (>200 mg per reaction mixture). This 100 0 o 80 a_ 0 0 cr_ 660 \ 0 z o 40 0 IL 0 z 20- LUJ 0 CL 0.25 0.5 1.0 2.0 0.25 0.5 1.0 2.0 MICROLITERS SERUM ADDED FIG. 1. Inhibition of partially purified viral polymerase by immune whole sera. The effect of anti-R-MuLV po- lymerase whole sera (76 mg/ml) on 3H-thymidine monophosphate incorporation with phosphocellulose-purified R- MuLV polymerase (3 ,ug, 0) and phosphocellulose-purified SR-RSV (5 ,ug, 0) is shown in Fig. JA. The effect of anti-SR-RSV whole sera (66 mg/ml) on R-MuLV and SR-RSV polymerase activity is shown in Fig. lB. Incorpo- ration in the absence ofserum was 4.2 and 3.8 pmolesfor R-MuLV and SR-RS V, respectively. 112 PARKS ET AL. J. VIROL. A. B. "1- inhibition may be due to contaminating nucleases 160 or proteases in the preparation. Cross-inhibition studies. To characterize further / \ / \ _ the cross-reactivity of antibodies to viral reverse 140 140 s o \transcriptases, the effect of the avian and murine C-type polymerase antisera on the DNA polym- 120 erase activities of other RNA-containing viruses was studied. IgG from antiserum to the SR-RSV >< polymerase inhibited approximately matched 00oo,> enzyme activities from the disrupted virions of and RAV-2 and paritally puri- C> \B-RSV, RAV-1, 80 fied polymerase from avian myeloblastosis virus lto approximately the same degree as noted with La \ cr t lpartially purified SR-RSV polymerase. However, 60 none of these avian viral enzymes was inhibited by IgG from anti-R-MuLV polymerase sera. 40_ . Conversely, antiserum to the SR-RSV polym- erase failed to inhibit significantly the viper C- type viral polymerase or any mammalian C-type 20 viral enzymes. Previous studies have also re- ported inhibition of the hamster C-type viral o IJ. polymerase with similar antisera (2). Under 0 20 40 80 5 10 20 conditions where there was more than 90% in- MICROGRAMS PROTEIN ADDED hibition of the R-MuLV enzyme, the inhibition FIG. 2. Purification of polymerase antibodies by of the rat leukemia and feline leukemia polym- DEAE fractionation.
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