Interferon Production by Human Leukocytes In
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1 APPED MICROBIOLOGY, Nov. 1969, p Copyright 1969 American Society for Microbiology Vol. 18, No. 5 Printed in.s.a. Interferon Production by Human Leukocytes In Vitro: Some Biological Characteristicsl SPENCER H. S. LEE2 Department of Microbiology, Faculty of Medicine, Dalhousie niversity, Halifax, Nova Scotia, Canada Received for publication 28 July 1969 Interferon was optimally produced in human peripheral leukocyte cultures incubated for approximately 19 hr in the presence of Sendai virus at a multiplicity of 1 to 5 EID5/cell. For determining whether deoxyribonucleic acid (DNA) synthesis per se was essential for interferon production, 1-,8-D-arabinofuranosylcytosine (Ara-C), a potent DNA inhibitor was studied for its effect on interferon production in leukocytic and bone marrow cell cultures. These cells showed no impaired capacity to produce interferon when treated with 15 Ag of Ara-C per ml. Interferon yields were also determined in leukocyte cultures treated with actinomycin D (.1 ;Ig/ml) and puromycin (1 ;g/ml) at various times before and after virus inoculation. The data suggested that sequential transcriptive and translational events were required for the de novo synthesis of interferon by the infected leukocytes, in a manner similar to other known virus-induced interferon-producing systems. The synthesis of macromolecules and the effects of antimetabolites in leukocytes and bone marrow cell cultures were followed by measuring the incorporation of thymidine-2-14c, uridine-5-3h, and L-phenylalanine-I-"4C. The effect of.1 ;ig of actinomycin per ml on the capacity of leukemic leukocytes to produce interferon was also studied. Preliminary data showed that, in contrast to nonleukemic leukocytes, interferon production by leukemic leukocytes was only partially inhibited by actinomycin. Recently investigations in this laboratory (8, 9) as well as in others (4, 13) have compared the ability of leukocyte cultures from leukemic and nonleukemic subjects to produce interferon when infected with a virus. A depressed interferon production in acute lymphocytic, acute myelogenous, and to some degree in chronic lymphocytic leukemia has been observed, but a normal or enhanced interferon yield occurs in chronic myelogenous leukemia (9). The significance of these findings is obscure at the moment. As a logical extension of the previous studies, it was desirable to investigate some of the basic mechanisms involved in the production of interferon by virus-induced leukocytes. It is possible that the variations in interferon response observed in the studies of leukemic and nonleukemic leukocytes may arise from a fundamental difference in the interferon production mechanism of these cells. The present communication describes some of the preliminary findings. I Presented at the 69th Annual Meeting of the American Society for Microbiology, Miami Beach, Fla., 4-9 May Present address: Department of Bacteriology, Faculty of Medicine, The niversity of Liverpool, Liverpool 3, England. MATERIALS AND METHODS Preparation of leukocytic and bone marrow cell sus. pensions. The procedure for preparing leukocyte suspensions from normal or leukemic subjects was the same as described previously (8). Heparinied peripheral blood was incubated at 37 C for 3 min or longer with added dextran at a proportion of 1:6 to aid sedimentation of erythrocytes. The leukocyte-rich plasma was removed and centrifuged at 1, rev/min for 1 min. The pellet was washed three times and resuspended in Eagle's diploid medium containing 1% inactivated calf serum. The leukocytes were counted in a hemacytometer. Heparinied bone marrow aspirates in.5- to l-ml amounts were obtained from patients who suffered neither from hematologic nor from malignant diseases. Each sample was immediately treated with eight volumes of.83% ammonium chloride for 1 min at 4 C to remove excess erythrocyte contamination (14). The suspension was then centrifuged and the pellet was processed as for peripheral leukocyte preparation. No attempt was made to separate the cells into different types. A 3-ml suspension of approximately 2.5 X 16 cells/ml was used for experiments in which interferon production was induced by Sendai virus, or in which the synthesis activity of the cells was measured. Viruses. An egg-adapted strain (Sendai) of parainfluena virus type I used to induce interferon forma- 731
2 732 LEE APPL. MIcRoBIL. b- I.- AL MIL b- EXPT x 5- SENDAI VIRS MLTIPLICITY (LOGI E I D, ) FiG. 1. Effect of virus multiplicity on interferon production in human leukocyte cultures. tion in leukocytic or bone marrow cell cultures was prepared as before (7). A stock of Sindbis virus used in interferon assay was propagated in primary chick embryo fibroblast cultures and titrated in human embryo fibroblasts of skin and muscle (HESM) origin. For purposes of interferon assay, a challenge dose of 5, TCID5Q of the virus was used. Tissue culture. Stock cultures of HESM cells were propagated in Eagle's diploid medium supplemented with 15% fetal calf serum as described previously (9), and were used between passages 1 and 4. Chromosomal analyses of the cells in the early and 4th passages showed them to be of the normal female karyotype. For interferon assay, 2-day-old confluent monolayer cultures of HESM prepared in screw-capped tubes (16 X 125 mm) or Leighton tubes (window sie, 11 X 55 mm) were used. Interferon production and assay. The protocol for interferon production and assay was similar to those reported recently (9). nless otherwise stated, leukocyte or bone marrow cell suspensions were incubated with Sendai virus at an input of 1 to 5 EID&o/cell. After 18 to 2 hr of incubation, the culture fluids were harvested and centrifuged at 3, rev'/min for 15 min. and the supernatant fluids were stored at 4 C for interferon assay. All preparations to be assayed were routinely acidified to ph 2 with 1 N HCl for 24 hr at 4 C, neutralied, and heated at 56 C for 1 hr. Serial threefold dilutions of the preparations were titrated in tube cultures of HESM cells for inhibitory activity against Sindbis virus; three or four tubes per dilution were used. Interferon titer was expressed as a 5% protection titer (INDro) as described previously (7). Radioactivity determination and materials. Thymidine-2-14C (TdR-2-14C; 1 mc/mmole) was obtained from Schwar BioResearch, Inc., Orangeburg, N.Y.; uridine-5-3h (24.6 c/mmole), from New England Nuclear Corp., Boston, Mass.; and L-phenylalanine- 1-14C (1.3 mc/mmole). from Calbiochem, Los Angeles, Calif. TdR-2-14C and L-phenylalanine-1-"4C were used at a concentration of.1 iuc/ml; uridine-5-3h was used at 1 lc/ml. To determine deoxyribonucleic acid (DNA), ribonucleic acid (RNA), and protein synthesis in leukocytic or bone marrow cell cultures, continuous labeling studies were carried out. The respective radioactive precursor was added, unless otherwise stated, at the initiation of the cultures. Samples were taken at the specified times, washed, fractionated and analyed by the method of Levine et al. (1). All trichloroacetic acid-precipitable fractions were collected onto glassfiber filters (Reeve Angel) and washed three times with 5% trichloroacetic acid; in the case of nucleic acid fractions, ether was used as a final wash. The filters were dried and radioactivity was measured in a Nuclear-Chicago scintillation counter. Chemicals. Dextran (6%, w/v, in saline) was obtained from Pharmachem, Bethlehem, Pa.; 1-t-Darabinofuranosylcytosine hydrochloride (Ara-C), from The pjohn Co., Kalamaoo, Mich.; actinomycin D, from Mann Research Laboratories, New York, N.Y.; and puromycin dihydrochloride, from Nutritional Biochemicals Corp., Cleveland, Ohio. RESLTS AND DISCSSION Preliminary experiments determined the conditions for optimal interferon induction by Sendai virus in freshly prepared leukocyte cultures at 37 C. Figure 1 illustrates the effect of multiplicity of virus infection on interferon production measured 18 to 24 hr after infection of normal leukocytes. The optimal yield of interferon was obtained in a -j I- 2- Oo L6 I 1 EXPT 1 -x 2-e HiORS AFTER VIRS INOCLATION FiG. 2. Rate of interferon production in human leukocyte cultures infected with Sendai virus at a multiplicity of infection of 16.
3 VOL. 18, 1969 INTERFERON PRODCTION BY LEIJKOCYTES 733 L I- 14C into the DNA of HESM cells was inhibited by 97 to 99% within 2 hr after the addition of Ara-C at a concentration of 15,pg/ml. Thus, a dosage of 15,jg of Ara-C per ml and a 2-hr preincubation period with the drug was established as the base line for the subsequent experiments. Figure 3 shows the result of a typical TdR-2-14C incorpora S 1- o w - I-. M. I- CONTROL ~~~ BONE MARROW-- LELKOCYTE -o CONTROL * Ara-C a ""Aa Ara-C_ 2 4 HORS AFTER ADDITION OF Ara- C FiG. 3. Effect of 1-fl-D-arabinofuranosylcytosine (Ara-C) on DNA synthesis in human bone marrow and leukocytic cells. TABLE 1. cultures infected with a multiplicity of 1 to 5 EID5o. The kinetics of interferon production in cultures infected with a virus multiplicity of 16 is represented in Fig. 2. Interferon was detected in the supernatant fluid as early as 2 hr after virus inoculation, and a maximum was reached at about the 19th hr. No growth of infectious virus or viral hemagglutinin was detected in these cultures. Earlier experiments by Strander and Cantell (14) yielded comparable results. With the conditions for optimal interferon production in leukocytes determined as being a multiplicity of 1 to 5 ED5o and an incubation time of about 19 hr, experiments were performed to determine whether cellular DNA, RNA, and protein synthesis were essential for interferon production in leukocyte or bone marrow cell cultures. Short intervals of treatment with Ara-C inhibit DNA synthesis and mitosis without affecting RNA or protein synthesis in mouse fibroblasts (12) and chick embryo cells (11). Hence, Ara-C was employed to determine the role of DNA synthesis in interferon production in leukocytic and bone marrow cell cultures. Inhibition of DNA synthesis by Ara-C was first dose-related in 2-dayold monolayer cultures of HESM cells grown in 6-mm petri dishes. DNA synthesis was measured as incorporation of TdR-2-'4C into acid-precipitable materials after 9 min of incubation. The results indicated that the incorporation of TdR-2- Interferon yields in human leukocytic and bone marrow cell cultures with and without 1-,j-D-arabinofuranosylcytosine (Ara-C, 15,g/ml) treatment Interferon yields (INDso/ml) Expt no. Leukocytic Bone marrow Control Ara-C Control Ara-C Mean
4 734 LEE APPL. MICROBIOL. Su5 4 C14 PHENYLALANINE-x H3 RIDINE - 24 / ~~~~~~~X %O X 3Z 3 o~~~~~g Z X x -2 F-X / X )b 1- -~~~~~~~1 M t oactinomyc INo L. - -= =~X HORS AFTER ADDITION OF ANTIMETABOLITE FIG. 4. Effect of actinomycin D and puromycin on RNA and protein synthesis, respectively, in human leukocyte cultures. ~~~~~~ tion experiment in leukocytic and bone marrow cells. The extent of inhibition of DNA synthesis in Ara-C-treated cells, particularly in the marrow cells, was ensured in all experiments by the marked suppression (85 to 95%) of TdR-2-'4C incorporation in the treated cells as compared with the untreated controls. Leukocytic cells, in contrast to the marrow cells, demonstrated very little or no DNA synthesis in culture, as reported by Bond and his co-workers (1). When leukocytic and bone marrow cell cultures were preincubated for 2 hr with 15,.g of Ara-C per ml and then induced to form interferon by the addition of 1 to 5 EID5 of Sendai virus, they produced interferon yields comparable to those in control cells (Table 1). Hrushovet, Wilt, and Lee (6) recently reported that less than 1% of human amnion cells, used as membrane biopsies or as trypsinied cell suspensions, or grown as monolayers on glass, incorporated tritiated thymidine during a 1- and 24-hr incubation period. These amnion cells, as demonstrated by Chany, Fournier, and Falcoff (3), provided a good source of human interferon. To determine whether inhibition of cellular RNA and protein synthesis in leukocyte cultures would affect the ability of the cells to produce interferon, preliminary experiments were performed to measure the incorporation of uridine- 5-3H and L-phenylalanine-1-'4C into RNA and protein, respectively, in control cultures within 1 1 hr after the addition of actinomycin D (. I tg/ ml) and puromycin (1,tg/ml). It is evident (Fig. 4) that control cultures showed increased incorporation of the labeled precursors with time, whereas there was a marked (8 to 9%) inhibition of incorporation of the labeled precursors in cultures treated with actinomycin D and puromycin. ~~~~~~~~~~ IN DC au 2- ACTINOMYCIN-x PROMYCIN-a / HORS ANTIMETABOLITE ADDED FIG. 5. Comparative effect of actinomycin D (.1 1-,pg/ml) and puromycin (1 jug/ml) on 16-hr yield of interferon from Sendai-infected human leukocyte cultures. TABLE 2. Effect of actinomycin D (.1 gg/ml) on the interferon-producing capacity ofleukocytes derived from leukemic patients Type of leukemia Case no. Interferon yields (INDSo/ml) Actinomycin No actinomycin Chronic 317 <4 28 myelogenous Chronic 341 <4 4 lymphocytic 343 < <4 16
5 VOL. 18, 1969 INTERFERON PRODCTION BY LEKOCYTES At the concentrations indicated, actinomycin D and puromycin were added to the leukocyte cultures prior to, simultaneously with, or at varying periods after interferon induction by Sendai virus infection. For comparative purposes, the medium used to make up the antimetabolite dilutions was correspondingly added to the control-infected cultures. The experiment was terminated after 19 hr of incubation. Yields of interferon were calculated by using the titers of the matched control cultures, not exposed to either of the antimetabolites, as 1%. The average results of a series of three experiments are summaried in Fig. 5. Little or no interferon was produced by leukocytes exposed to the antimetabolites 1 hr before, or simultaneously with, virus infection. At 2 hr after virus infection, however, the capacity of the cells to produce interferon was almost unaffected by actinomycin D but remained completely impeded by puromycin. These observations indicate that sequential transcriptive and translational events, rather than DNA synthesis per se, are required for the de novo synthesis of interferon by the infected leukocytes. Thus, the leukocytes behave similarly to other known virus-induced interferon-producing systems (2, 5). A preliminary attempt was also made to study the effect of actinomycin D (.1,ug/ml) on interferon production by leukemic leukocytes. The results to date are comparable to those of Hadhay et al. (4). The data in Table 2 show that leukemic leukocytes treated with actinomycin D, 1 hr before they were infected with Sendai virus, produced varying levels of interferon, whereas control cultures of leukemic leukocytes (particularly chronic myelogenous leukocytes), left untreated, consistently showed high levels of interferon production. The functional significance of these data is yet to be explored. Whether these results are due to increased nuclear RNA synthesis in leukemic cells (15) or to different genetic 735 control mechanisms on interferon production between leukemic and nonleukemic cells awaits further investigation. Attempts have also been made to demonstrate preformed interferon in the leukocytes derived from leukemic and nonleukemic subjects, by use of Escherichia coil endotoxins. The data obtained thus far are negative. ACKNOWLEDGMENTS This investigation was supported by grant MA 1461 from the Medical Research Council of Canada. No The able assistance of G. Shaw is gratefully acknowledged. LITERATRE CITED 1. Bond, V. P., T. M. Fliedner, E. P. Cronkite, J. R. Rubini, G. Brecher, and P. K. Schork Proliferative potentials of bone marrow and blood cells studied by in vitro uptake of Ha-thymidine. Acta Haematol. 21: Burke, D. C Mechanisms of interferon production, p In N. B. Finter (ed.), Interferons. North Holland Publishing Co., Amsterdam. 3. Chany, C., F. Fournier, and E. Falcoff A simple system for the mas production of human interferon: the human amniotic memboane, p In G. E. W. Wolstenholme and M. O'Connor (ed.), Interferon (Ciba Foundation Symposium). J. & A. Churchill Ltd., London. 4. Hadhay, G., L. Gergely, F. D. Toth, and G. Segedi Comparative study on the interferon production by the leukocytes of healthy and leukemic subjects. Acta MicrobioL Acad. Sci. Hung. 14: Ho, M., and M. K. Breinig Metabolic determinants of interferon formation. Virology 25: Hrushovet, S. B., J. C. Wilt, and E. S. C. lee The uptake of tritiated thymidine by human amnion cells: a correlation with cell structure. Can. J. Microbiol. 14: Lee, S. H. S., and R. L. Oere Production of interferon by human mononuclear leukocytes. Proc. Soc. Exp. Biol. Med. 118: Lee, S. H. S., R. L Oere, and C. E. van Rooyen Interferon production by human leukocytes In viro. Reduced levels in lymphatic leukemia. Proc. Soc. Exp. Biol. Med. 122: Lee, S. H. S., C. E. van Rooyen, and R. L. Oer Additional studies of interferon production by human leukemic leukocytes In vitro. Cancer Res. 29: Levine, B. M., Y. Becker, C. W. Boone, and H. Eagle Contact inhibition, macromolecular synthesis, and polyribosomes in cultured human diploid fibroblasts. Proc. Nat. Acad. Sci..S.A. 53: Nakata, Y., and J. P. Bader Transformation by murine sarcoma virus: fixation (deoxyribonucleic acid synthesis) and development. J. ViroL 2: Silagi, S Metabolism of 1-a-D-arabinofuranosylcytosine in L cells. Cancer Res. 25: Soloviev, V. D Some results and prospects in the study of endogenous and exogenous interferon, p In G. Rita (ed.), The interferons (an international symposium). Academic Press Inc., New York. 14. Strander, H. and K. Cantell Production of interferon by human leukocytes In vitro. Ann. Med. Exp. Biol. Fenn. 44: Tryfiates, G. P., and J. Laslo Nuclear RNA synthesis in human leukemic cells. Nature 213:
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