Immunofluorescent Antibody Studies of a Murine Leukemia Virus

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1 JOURNAL OF BACTERIOLOGY, Oct., 1966 Copyright 1966 American Society for Microbiology Vol. 92, No. 4 Printed in U.S.A. Immunofluorescent Antibody Studies of a Murine Leukemia Virus ERIC R. BROWN,' PETER BUINAUSKAS, AND STEVEN. SCHWARTZ Northwestern University Medical School, University ofillinois College of Medicine, and Hektoen Institute for Medical Research of the Cook County Hospital, Chicago, Illinois Received for publication 23 April 1966 ABSTRAcT BROWN, ERIC R. (Northwestern University Medical School, Chicago, Ill.), PETER BUINAUSKAS, AND STEVEN. SCHWARTZ. Immunofluorescent antibody studies of a murine leukemia virus. J. Bacteriol. 92: Correlation was close between in vitro complement fixation, immunodiffusion, and passive cutaneous anaphylaxis tests with the S-63 and GC murine leukemia viruses and immunofluorescence reactions with these viruses. When fluorescein-isothiocyanateconjugated convalescent sera obtained from mice initially infected with S-63 leukemia virus were used, the reactive site was within the cytoplasm of the infected cell. By electron microscopic examination, virus particles were demonstrated in the same areas within the cells that exhibited specific fluorescence with the conjugates. and mesenteric nodes contained the most virus, whereas kidney tissues contained the least amount. Fluorescence was not observed within the nuclei of infected cells. Previous work, describing the origin, histopathology, and biology of the S-63 virus (4, 12), has shown that the S-63 strain of leukemia virus kills newborn ICR mice, but that 8% of young adult mice recover from the virus infection. Antibodies against the virus develop in the recovering mice. Those antibodies can be demonstrated by complement-fixation, immunodiffusion, and passive cutaneous anaphylaxis tests. Amano and Ichikawa (1) reported that leukemia virus proliferation takes place principally at the cellular surface. Osato et al. (16, 17) propagated Friend leukemia virus in mouse embryo tissue cultures and demonstrated by hemadsorption and immunofluorescent methods that virus antigen was located at the cell surface and in the cytoplasm. Yoshida (21) and colleagues, working with the Moloney and Rauscher viruses, showed by indirect immunofluorescence methods that these particles appear in the cytoplasm of the cell and are especially concentrated in megakaryocytes. Their results were confirmed by electron microscopic studies. Because the study of antibodies from convalescent animals eliminates the problem of reactions when mouse tissues are used in heterologous systems, this system seemed superior for deter- Scholar of the Leukemia Society, Inc. 978 mining the localization of the virus in infected tissues with immunofluorescence techniques. Fink and her co-workers (9, 1) and Pasternak (18) demonstrated the applicability of immunofluorescence in the demonstration of murine leukemic antigens in situ, and many workers (4) have demonstrated mouse virus particles by electron microscopy. In the present study, the two methods were combined to localize the site of antibody reaction and to demonstrate the virus antigen. MATERIALS AND METHODS Virus preparation. S-63 virus was purified by methods previously described (11-13). Virus suspensions were mixed with suspensions of Escherichia coli and were passed through a membrane filter (Millipore Filter Corp., Bedford, Mass.) with a pore size of.45, to ensure the continuity of the filter. The filtrates thus obtained were cultured and were found to be sterile for bacterial growth. It was, therefore, assumed that the filters were impervious to the leukemic cells which are larger in size than E. coli cells. Virus suspensions were used to inoculate young adult (4 to 5 week) 25-g ICR mice. The surviving mice served as a source of convalescent antibody. GC virus, a leukemogenic virus carried in this laboratory and displaying antigenic relationships to the S-63 virus, but being 9 to 1% fatal to young adult ICR mice, was also prepared, as previously described (4). These leukemia

2 VOL. 92, 1966 IMMUNOFLUORESCENT ANTIBODY IN LEUKEMIA VIRUS 979 virus ifitrates were serologically tested against antisera to known virus antigens. It was found that there was no cross-reaction with antisera prepared from viruses usually found in human, bovine, or murine species. The diagnosis of lymphoid (thymic) leukemia was confirmed by histological examination of the involved tissues. Antisera. Individual pools of sera were collected from the following sources: normal ICR mice of comparable age and sex to the infected mice; convalescent S-63-infected mice between the 5th and 8th week after inoculation, when the symptoms of the disease had subsided and antibody titer was expected to be at its height; GC virus-infected mice which failed to develop leukemia by the 1th to 12th week; rabbits rendered immunologically tolerant to normal mouse tissues and subsequently challenged with either S-63 or GC virus; and normal rabbits (4, 11). Serum from rabbits rendered immunologically tolerant to normal mouse tissue showed no differences from the normal rabbit sera used in the controls, when initially tested. A minimum of 5 mice was used for each pool of serum. Fluorescence studies. Both the direct and indirect fluorescent-antibody techniques were employed in this study. Direct test. -y Globulin was fractionated from each of the pooled test sera by Cohn's (7) cold-ethyl alcohol method, was further purified by passage through a diethylaminoethyl cellulose column (14), and was absorbed against normal tissue antigens before conjugation (5, 11). Fluorecein isothiocyanate (FITC) dye was conjugated to the purified ry globulins by the method of Riggs and his colleagues (2). The conjugated -y globulins were absorbed with silk fibroin by the method of Rappaport (personal communication). A modified Lissamine-Rhodamine RB-2 counterstain technique, as described by Brown and Bittner (2), was used to eliminate further nonspecific fluorescence. Indirect test. Commercially conjugated (FITC) sheep antirabbit and rabbit antiguinea pig sera were obtained for use in these studies (Pentex Corp., Kankakee, Ill.), and the indirect complement-fixation test described by Cherry and his associates (6) was used. Guinea pig complement used in these studies was obtained from Scientific Products, Evanston, Ill. The complement-staining test can be used in any system where an antigen-antibody reaction binds complement. It consists of a test slide and four control slides of antigen. The steps of the procedure follow. The test serum is applied to the test slide and first control slide. Normal serum is applied to the second control slide. Serum is not added to the third control. A commercially prepared (Pentex Corp.) serum known to contain complement-fixing antibody is added to the fourth control slide. Fresh guinea pig serum (complement) diluted 1 :1 with buffered saline solution is added to the test and control slides. Conjugated anti-guinea pig, rabbit y globulin (Pentex Corp.) is added. All slides are incubated at 37 C in a humid chamber for 3 min. The slides are rinsed and soaked in buffered saline solution for 1 min, are drained, and are partly dried. The preparations are then mounted in buffered glycerol and are examined. A Reichert Zetopan microscope with HBO 2 Arc light was used for slide examinations. Slide preparations. Impression smears (6) were prepared from normal, GC virus-infected and S-63 virus-infected mouse spleen, liver, mesenteric node, kidney, and brain tissues. Samples of each tissue were set aside and were fixed in osmic acid for use in the electron microscopic studies, as well as for use as antigens for in vitro immunological tests. In addition, whole cell suspensions were prepared in Hanks balanced salt solution (HBSS), as previously described (4), and a thin suspension was spread on the surface of a precleaned microscope slide for fluorescence studies. For convenience, both the impression smears and cell suspension slides were fixed in cold acetone overnight at 5 C and then were treated with the conjugated antibody system by either the direct or the indirect method. (There was no appreciable difference in the staining intensity between the preparations fixed by the above method and those exposed to cold acetone for the periods of 1 min to 1 hr.) In vitro immunological testing. Both the control and test sera were studied by complement-fixation, immunodiffusion and passive cutaneous anaphylaxis tests (4) against antigens prepared from both normal and virus infected homogenates of spleen, liver, kidney, and lymph nodes, as previously described. The various sera were studied before fractionation and after -y globulin isolation to determine their specificity before conjugation with the fluorescent dye. Purity of the -y globulin fractions was tested by electrophoretic methods. The complement-fixation tests (13) with pooled sera gave the following titers: (i) pooled GC sera reacted against both the GC and S-63 viral antigens 1:128; (ii) the pooled S-63 convalescent sera reacted against the GC virus antigen 1:128 and against the S-63 virus antigen 1:256; and (iii) the immune tolerant anti-s-63 virus rabbit serum reacted against both the GC and S-63 viral antigens at a titer greater than 1:2,48. Electron microscopy. For electron microscopy, the tissue fixed in osmic acid was embedded in Epon and was stained with uranyl acetate and lead hydroxide. The sections were examined with an RCA EMU-3 electron microscope. The method used was that of Dolowy (8). RESULTS Table 1 summarizes the in vitro immunological tests carried out for each of the various sera. None of the control sera cross-reacted with the leukemic or normal tissue antigens. The convalescent S-63 infected mouse sera were strongly positive in each test and failed to cross-react with the normal tissue antigens. GC-infected mouse sera were positive in the complementfixation test and negative in immunodiffusion and passive cutaneous anaphylaxis tests to the leukemic antigens, and reacted negatively to the normal control material. The immunologically tolerant anti-s-63 virus rabbit sera reacted posi-

3 98 BROWN, BUINAUSKAS, AND SCHWARTZ J. BAC-TERIOL. TABLE 1. Testing of antiseraa Normal Convalescent GC convales- tmmunologically mouse S-63 mouse cent mouse challenged rabbit sera Substance Antigenb sera sera sera rabbit sera CF ID PCAc CF ID PCA CF ID PCA CF ID PCA CF ID PCA Whole sera Normal ICR mouse GC virus _ _ S-63 virus _ - -y Globulin Normal ICR _ + fraction mouse GC virus _ _ S-63 virus _ a Each test was run in duplicate; 'y globulin tended to exhibit anticomplementary properties unless the ph was adjusted to 7.2 to 7.4. b Normal tissue and viral antigens were similarly prepared from mouse spleen, liver, kidney, and lymph node material. c CF, complement-fixation test; ID, immunodiffusion test; PCA, passive cutaneous anaphylaxis test. tively against the leukemic antigens and negatively or weakly positively against normal mouse tissue antigens. The y globulin fractions of the sera gave essentially similar reactions. Paper chromatography and immunoelectrophoretic studies indicated the y globulin to be 96 to 1% free from other protein fractions. After conjugation of both the whole sera and y globulin from each pool, the conjugates were absorbed against mouse-liver powder and silk fibroin to eliminate nonspecific fluorescence and to eliminate dye not bound to protein. As shown in previous work (2, 3), the use of a Lissamine- Rhodamine counterstain further eliminated nonspecific fluorescence in stained preparations. Table 2 shows the results of staining various tissues with each of the conjugates. The degree of fluorescence was based on a to 4 + system, as previously described (2, 3). The indirect complement test generally gave stronger reactions than the direct method. Certain tissues appeared more antigenic than others. An arbitrary classification of fluorescence, in descending order, would be: mesenteric node, spleen, liver, brain, and kidney. The specific fluorescence with either the direct or indirect complement method was in the cytoplasmic area and in the intercellular spaces. The best method for studying the fluorescence reaction was with the cell-suspension technique, as it prevented overlapping of cells and, thus, permitted an easier evaluation of the procedure. Nuclear fluorescence was not seen, and the strongest fluorescence, in all cases, was along the cell membrane. For the immunofluorescence studies, spleens, mesenteric nodes, brains, livers, and kidneys were obtained from 37 mice with GC virus, 41 S-63 virus-infected mice, and 29 normal mice. Each of the specimens was examined in triplicate. Under similar conditions of staining, each of the virus-infected specimens gave positive results, with the fluorescence being in and around the reticuloendothelial cells, whereas none of the normal tissues showed fluorescence. The degree of fluorescence varied in intensity from animal to animal and from tissue to tissue (Table 2). Electron microscopy revealed virus particles similar to those described by Moloney and others (15, 19). These particles were found budding from the cell membrane and in the intercellular spaces. DISCUSSION When used as a battery, the immunodiffusion, complement-fixation, and passive cutaneous anaphylaxis tests, as previously reported (4, 11, 12), allow differentiation between leukemia virusinfected and normal tissues. The result of the immunofluorescence test has proved to be more specific than the tests previously described (12). It was especially important to determine whether complement was bound by the antigen-antibody reaction, as this reaction is the basis for the indirect fluorescence complement test. As shown in Table 1, complement is bound by this system. The disadvantage of the in vitro tests is that they do not allow visualization of the antigen nor a localization within the cell of the antigenic components. Fluorescence microscopy eliminates these objections. Once the pitfalls of the nonspecific fluorescence are overcome by careful adsorption, and once a predetermination of the specificity of the sera has been obtained, the immunofluorescence test gives highly specific results, as shown in Table 2. Normal tissues failed to fluoresce with either

4 VOL. 92, 1966 IMMUNOFLUORESCENT ANTIBODY IN LEUKEMIA VIRUS 981 TABLE 2. Results of immunofluorescence staining of various mouse tissues Directs Test method Type of sera Tissue FITC-conjugated convalescent S-63 mouse sera FITC-conjugated GCinfected mouse sera FITC-conjugated immunologically tolerant S-63 virus rabbit sera Sera reacted against Normal GC-infected S-63-infected mouse mouse mouse Indirect compleplement fluorescentb Convalescent S-63 mouse sera + complement + FITC anti-guinea pig sera GC-infected mouse sera + complement + FITC anti-guinea pig sera Immunologically tolerant rabbit sera + complement + FITC anti-guinea pig complement a Under the direct method, control conjugates of FITC normal mouse sera and FITC-conjugated rabbit sera failed to fluoresce against any of the above tissues. 6 Under the indirect complement fluorescent method, control systems of normal rabbit or normal mouse sera plus complement plus FITC anti-guinea pig complement failed to react against any of the above tissues. 1± 41 the direct or indirect tests, whereas virus-infected tissues showed varying degrees of fluorescence. Fluorescence was in the cytoplasmic areas, especially around the cytoplasmic membrane in the washed-cell preparations. In the "impression smears," specific fluorescence was not only around the cytoplasmic areas but also within the interstitial spaces. These results do not completely agree with those obtained by Fink and Malmgren (9, 1) with the Rauscher agent; they reported that fluorescence was strong in the nuclei as well as within the cytoplasm. However, our results agree fairly well with these investigators in regard to the degree of fluorescence (presumably degree of viral antigen) in various infected tissues. Fink and Malmgren observed most virus in spleen, then liver, lymph node, and only rarely in kidney, buffy coat, or brain, although they stated that the brain tissue of one mouse, which was highly infectious, showed an overall fluorescence not associated with any particular cell. In our studies, spleen and mesenteric nodes were about equally fluorescent, with brains and liver being less so, and kidney being the poorest. When the observations by fluorescence microscopy were compared

5 982 BROWN. BUINAUSKAS, AND SCHWARTZ J. BACrERIOL. with electron micrographs prepared from the same tissues, correlation between fluorescence and the presence of virus particles was close. More virus was in lymph node and spleen preparations examined with the electron microscope than in the other tissues, and the location of the virus particles was in the same area, i.e., interstitial spaces and cytoplasmic membranes where fluorescence was prominent. Virus particles were not observed within the nuclei of any of the tissues examined by electron microscopy. On the basis of this work, the fluorescence produced by the conjugated specific antisera appears to be due to a reaction with the viral antigen. ACKNOWLEDGMENTS We thank William Dolowy for carrying out the electron microscopic phase of this report and Paul Szantos for performing histological examinations. This investigation was supported by the John A. Hartford Foundation, Inc., and by Public Health service grant CA-3321 from the National Cancer Institute. LITERATURE CITED 1. AMANO, S., AND Y. ICHIKAWA Leukemic cells and etiological virus in long-term culture: Their interrelationships with a consideration of the distribution of viral antigen. Proc. Intern. Congr. Electron Microscopy 2:MM2 2. BROWN, E. R., AND J. J. BITTNER Fluorescent antibody reactions against the mouse mammary tumor agent. Proc. Soc. Exptl. Biol. Med. 16: BROWN, E. R., AND J. J. BITrNER Adaptation of fluorescent microscopy to the determination of genetic variations in mouse mammary tumor agent. Proc. Soc. Exptl. Biol. Med. 16: BROWN, E. R., AND S.. SCHWARTZ Antigenic behavior of S-63 mouse leukemia virus. Blood 27: BYRAN, W. R., MOLONEY, J. B., T. E.O'CONNOR, M. A. FINK, AND A. J. DALTON Viral etiology of leukemia. Ann. Internal Med. 62: CHERRY, W. B., M. GOLDMAN, T. R. CARSKI, AND M. D. MOoDY Fluorescent antibody techniques in the diagnosis of communicable diseases. U.S. Public Health Serv. Publ COHN, E. J., F. R. N. GuRD, D. M. SURGENOR, B. A. BARNES, R. K. BROWN, G. DEROUAUX, J M. GILLESPIE, F. W. HAHNT, W. F. LEVY, C. H. LIu, D. MITrmEMAN, R. F. MOUTON, K. SCHMID, AND E. UROMA A system for the separation of the components of human blood. Quantitative procedures for the separation of the protein components of human plasma. J. Am. Chem. Soc. 72: DoLowy, W. C Morphology of the development of type B virus particles in a transplantable mammary tumor of ICR/Ha mice. J. Natl. Cancer Inst. 34: FINK, M. A., AND R. A. MALMGREN Fluorescent antibody studies of the viral antigen in a murine leukemia (Rauscher). J. Natl. Cancer Inst. 31: FINK, M. A., R. A. MALMGREN, F. J. RAUSCHER, H. D. ORR, AND M. KARON Application of immunofluorescence to the study of human leukemia. J. Natl. Cancer Inst. 33: GREENSPAN, I., E. R. BROWN, S.. SCHWARTZ Immunologically specific antigens in leukemic tissues. Blood 21: GREENSPAN, I., E. R. BROWN, AND S.. SCHwARTZ Antibody response of mice to a leukemogenic virus. Nature 22: KABAT, E. A., AND M. M. MAYER Experimental immunochemistry, 2nd ed., p Charles C Thomas, Publisher, Springfield, Ill. 14. LEVY, H. B., AND H. A. SOBER A simple chromatographic method for preparation of gamma globulin. Proc. Soc. Exptl. Biol. Med. 13: MOLONEY, J. B The recovery of infectious nucleic acid from a virus induced lymphoid neoplasm. Acta Unio Intern. Contra Cancrum 19: OsATO, T., E. A. MIRAND, AND J. T. GRACE, JR Propagation and immunofluorescent investigations of Friend virus in tissue culture. Nature 21 : OsATo, T., E. A. MIRAND, AND J. T. GRACE, JR Hemadsorption and immunofluorescence of friend virus in cell culture. Proc. Soc. Exptl. Biol. Med. 119: PAsTERNAK, G Serologic studies on cells of graffi virus-induced myeloid leukemia in mice. J. Natl. Cancer Inst. 34: PORTER, G. H., A. J. DALTON, J. B. MOLONEY, AND E. A. MITCHELL, Association of electron-dense particles with human acute leukemia. J. Natl. Cancer Inst. 33: RIGGS, J. L., R. J. SEIWALD, J. H. BURCKHALTER, C. M. DOWNS, AND T. G. MErCALF Isothiocyanate compounds as fluorescent labeling agents for immune serum. Am. J. Pathol. 34: YOSHIDA, K., K. L. SMITH, AND D. PINKEL Studies of murine leukemia viruses. I. Detection of Moloney and Rauscher leukemia viruses by indirect immunofluorescence. Proc. Soc. Exptl. Biol. Med. 121:72-81.

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