Interleukin 2 Enhances Natural Killer Cell Activity Through Induction of Gamma Interferon
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1 INFECTION AND IMMUNITY, Sept. 1983, p /83/9992-6$2.O/O Copyright 1983, Amerian Soiety for Mirobiology Vol. 41, No. 3 Interleukin 2 Enhanes Natural Killer Cell Ativity Through Indution of Gamma Interferon DOUGLAS A. WEIGENT,* G. JOHN STANTON, AND HOWARD M. JOHNSON Department of Mirobiology, University of Texas Medial Branh, Galveston, Texas 7755 Reeived 28 February 1983/Aepted 6 June 1983 Highly purified interleukin 2 (IL 2), free of interferon ativity, enhaned natural killer (NK) ell ativity against tumor ells in mouse spleen ell ultures and in human peripheral lymphoyte ultures in a manner similar to that of interferon (IFN). We determined that IL 2 enhaned NK ativity indiretly in a asade manner by the indution of gamma IFN (IFN-y) in the ultures, whih atually mediated the enhaned killing. Aordingly, lymphoyte ultures treated with IL 2 alone produed 1 to 1 U of IFN per ml in 6 to 24 h of ulture. The IFN was typed as IFN-y by speifi antibodies. Speifi antibodies either to natural IFN--y or to a syntheti peptide orresponding to the human IFN-y N-terminal amino aids, when added to ultures treated with IL 2, ompletely bloked IL 2 enhanement of NK ell ativity for both the mouse and human systems. IL 2- indued proliferation was not affeted by the antibodies. Thus, the enhanement of NK ell ativity by IL 2 is ompletely mediated by IL 2-indued IFN--y. The findings learly indiate a asade effet whereby one lymphokine (IL 2) indues the prodution of another. The latter lymphokine (IFN-i) then mediates an important biologial effet (natural killing). Natural killer (NK) ells are a heterogeneous group of effetor ells that are apable of ytotoxiity ag'ainst a variety of target ells without obvious prior sensitization (8). NK ells are partiularly ytotoxi against tumor ell lines and virus-infeted ells (4, 18), and thus they may play an important role in host defense. NK ell ytotoxi ativity has been shown to be dramatially enhaned by treatment with interferon (IFN) ail in the mouse (3, 6) and IFN-a and IFN-P in humans (2) before the addition to target ells. Reently, interleukin 2 (IL 2) or T- ell growth fator that was devoid of antiviral ativity was also shown to be apable of enhaning NK ell ytotoxi ativity in the mouse system (7, 12). The independene of IL 2 enhanement of NK ativity from that of IFN-a/P was demonstrated by showing that the onomitant addition of these two lymphokines to NK ells resulted in the augmentation of NK ativity to levels not obtainable with either lymphokine alone (7, 22). It is possible that a given lymphokine, in addition to having a diret effet on ells, may indue lymphoytes to produe other lymphokines whih may be responsible for biologial effets attributable to the original lymphokine. We have shown, for example, that IL 2 alone an indue mouse lymphoytes to make IFN--y (22). Thus, the possibility exists that the NK-ell-enhaning effets of IL 2 may be partially or totally attributable to IFN-y. The data presented here demonstrate that this is, in fat, the ase and that studies omparing IL 2 and IFN-a/, enhanement of NK ell ativity were atually omparing IL 2-indued IFN--y and IFN-a/I. We show that there is no evidene that IL 2 is apable of enhaning NK ell ativity in either the mouse or human system, exept by its ability to indue IFN-,y. MATERIALS AND METHODS Cell preparations. C57BL/6 female mie, 4 to 8 weeks old (Jakson Laboratories, Bar Harbor, Maine) were sarified, the spleens were aseptially removed, and ell suspensions prepared in Eagle minimum essential medium (EMEM) supplemented with 2% fetal bovine serum,.1% peniillin-streptomyin, 4,ug of garamyin per ml, and.75% sodium biarbonate. Human leukoytes were prepared from peripheral blood by the Fioll-Hypaque gradient separation method (2). Plasti adherent ells from both mouse and human ell preparations were removed by inubating 5 ml of a 1 x 17 ells per ml suspension in plasti tissue ulture dishes for 1 h at 37 C. For IFN--y or IL 2 treatment,.3 ml of a lymphoyte suspension (1 x 16 ells per ml) was added to various dilutions of IFN--y or IL 2 and inubated for various times at 37 C. The ells were washed twie by entrifugation, suspended in EMEM, and added to target ells as desribed below. Control lymphoytes were inubated in EMEM without IFN or IL 2 and otherwise treated the same as the test lymphoytes. IFN--y and IL 2 preparations. Mouse and human IFN-y (15 U per mg of protein) were prepared by 992 Downloaded from on May 3, 218 by guest
2 VOL. 41, 1983 previously desribed methods (13, 16). Highly purified mouse IL 2 was produed and purified by gel filtration, hydrophobi hromatography, and eletrofousing as previously desribed and kindly provided by W. R. Benjamin and J. J. Farrar (9). Highly purified human IL 2 was produed and purified as previously desribed and kindly provided by J. J. Oppenheim and T. Kasahara (19). Mouse and human IL 2 prepared in this manner did not ontain any detetable IFN. Antibodies to mouse IFN-y. Rabbit antibodies to partially purified natural mouse and human IFN-y, as well as antibodies to a syntheti peptide orresponding to 2 N-terminal amino aids of human IFN-y based on DNA data, were prepared as previously desribed (11, 14, 17). The antibodies against mouse IFN-y were absorbed against C57BL/6 spleen ells (5 x 16 ells per ml of sera), and antibodies to human IFN--y were absorbed against human peripheral blood lymphoytes (PBL). The neutralization of IFN-y in preparations ontaining IFN--y or IL 2 or both was aomplished by adding serial dilutions of anti--y antibody. The suspensions were mixed in a total volume of 1,ul and inubated at room temperature for 1 h before the supernatants were assayed for antiviral ativity and enhanement of NK ell ativity. Antibodies to both mouse and human IFN-y did not neutralize the ability of IL 2 to stimulate DNA synthesis in an IL 2- dependent T-ell line (CT6), did not inhibit the ativity of purified IL 1 on murine thymoytes, or inhibit olony-stimulating fator ativity when tested in standard laboratory assays. The antibodies were therefore highly speifi for IFN-y. Proliferation assay. Both mouse and human IL 2 were assayed on an IL 2-dependent T-ell line (CT6) in a 48-h inubation (9). The ultures were inubated in tripliate, and 1,uCi of [3H]thymidine ([3H]TdR; speifi ativity, 2 Ci/mmol) was added to eah well for the last 4 h of inubation. At harvest, 1%o trihloroaeti aid was added. The ells were harvested with a multiple automati sample harvester, washed with 5% trihloroaeti aid, and ounted for [3H]TdR inorporation in a liquid sintillation ounter. IFN assay. We assayed mouse IFN by a miroplaque redution method, using approximately 4 PFU of vesiular stomatitis virus per well in mouse L ells as desribed previously (1). Human IFN was assayed on WISH ells by a ytopathi assay using Sindbis virus as desribed elsewhere (1). Eah point represents the mean of three assays, eah performed in tripliate. In our studies, a onentration of 1 U of IFN--y per ml is defined as the onentration required to derease the number of PFU/well, or the ytopathi effet, by 5%o. One unit of our IFN-y inhibits virus repliation about as muh as 1 U of NIH referene fibroblast IFN. Assay of NK ell ativity. Mouse L ells were propagated in 96-well mirotiter plates (Falon Plastis, Oxnard, Calif.) in EMEM with antibiotis and 2% fetal bovine serum and prelabeled with sodium hromate (51Cr) at a onentration of 1.Ci/2 x 1' ells per 4 h at 37 C. After inubation, the target ells were washed three times with EMEM, and human or mouse lymphoytes were added at an effetor-to-target-ell ratio of 1:1. Speifi 51Cr release was determined from tripliate ultures after inubation at 37 C for 18 h. The standard deviation of tripliate assays was less than 5%. The perent speifi 51Cr release was alulated as R = (E - SIM - S) x 1 where E is the ounts per IL2, NK ACTIVITY, AND IFN-y 993 minute in the experimental wells, S is spontaneous release, and M is the maximal release in the presene of 1% saponin. RESULTS IL 2 indution of IFN-y and enhanement of NK ell ativity. Sine the role of indued IFN--y in the IL 2 enhanement of NK ell ativity was the question addressed, it seemed appropriate to first examine the ability of highly purified IL 2 to indue IFN-y and to enhane NK ell ativity in both the mouse and human systems. Mouse IL 2 was evaluated by inubating mouse spleen ells for 18 h with various onentrations of IL 2 (Fig. 1A). Spleen ells treated with IL 2 (1 to 15 U) ontaining no detetable IFN ativity produed detetable levels of IFN after treatment with as little as 1 U of IL 2. Peak titers of IFN ativity were observed after treatment with 6 U of IL 2. All of the IFN ativity indued by IL 2 was demonstrated to be IFN-y by neutralization with speifi antibody (data not shown) (17). The level of IL 2-enhaned NK ell ativity was proportional to the amount of IFN--y produed. The inubation of human IL 2 with human PBL also resulted in the prodution of IFN-y and enhanement of NK ell ativity (Fig. 1B). As with the mouse system, NK ell ativity was proportional to the amount of IFN--y produed. The data from both systems are suggestive of a possible role for IFN--y in the mediation of IL 2 enhanement of NK ell ativity. Kinetis of IFN-'y prodution and enhanement of NK ell ativity by lymphoytes treated with IL 2. Having established that a dose-response relationship existed between the extent of IL 2 enhanement of NK ell ativity and the amount of IFN-y produed by lymphoyte ultures, we next addressed the question of the relationship of the kinetis of IFN--y prodution and enhanement of NK ell ativity. We first determined the kinetis of IL 2-indued IFN-y prodution and enhanement of NK ell ativity in mouse spleen ells inubated with 3 U of IL 2 during a 3-h period (Fig. 2A). Detetable levels of IFN and NK ell ativity were observed as early as 6 h after ulture initiation. The indued NK ell ativity profile peaked at 24 h and was similar to and losely assoiated with inreased IFN-y prodution, suggesting a role for IFN-y in the mediation of the IL 2 effets. The inubation of human IL 2 with human PBL also resulted in the early prodution of IFN, with peak levels at 24 h (Fig. 2B). The type of IFN at all stages of prodution was y as determined by neutralization tests (data not shown). Human NK ell ativity quantitatively paralleled IFN--y prodution, again suggesting a role for IFN-,y in the mediation of IL 2 enhanement of NK ell ativity. Downloaded from on May 3, 218 by guest
3 994 WEIGENT, STANTON, AND JOHNSON INFECT. IMMUN. 6o A ZD.2 4 x 1 8 E N.22 a- 6 C zil IL 2, units/ml IL 2, units/ml FIG. 1. Dose-response urves of mouse (A) and human (B) IL 2 indution of IFN-y and enhanement of NK ell ativity. Various onentrations of IL 2 were added to marophage-depleted spleen ells or human PBL (1 x 17/ml). IFN () and NK ell ativity () were measured 24 h after the initiation of ulture. Inhibition of mouse IL 2 enhanement of NK ell ativity by antibodies to mouse IFN-y. To determine more diretly whether IL 2 indution of IFN--y was responsible for IL 2 enhanement of NK ell ativity, we treated mouse spleen ell ultures with antibodies to IFN-y at the time of IL 2 treatment. The rationale was to neutralize IFN-y as it was produed and to determine how this affeted IL 2 enhanement of NK ell :R, 4 N.22 ativity. Representative data (Fig. 3A) showed a marked inhibition of ytotoxi ativity in suh IL 2-treated ultures. The dose-response profile of the inhibition of ytotoxiity with antibodies to IFN--y orresponded to the neutralization of IFN--y ativity (data not shown). In the same experiment, a ontrol IFN-y preparation was added to ultures ontaining antibodies, and a similar dose-response profile of the inhibition of 2l Il. Downloaded from on May 3, 218 by guest Time, hr Time, hr FIG. 2. Kinetis of IFN prodution and enhanement of NK ell ativity by mouse spleen ells (A) and human PBL (B) treated with IL 2. Mouse or human IL 2 (3 U eah) was added to PBL, IFN-y () prodution and enhanement of NK ell ativity () from IL 2-treated ultures were measured during a 36-h period.
4 VOL. IVL2, 41, 1983 NK ACTIVITY, AND IFN-y A 6 F B. x m4 4 ' 2 o a- 1:6 1:2 1:6 1:18 1:54 None Dilution of antibody._ x 4.C 2. ~ 1:6 1:2 1:6 1:181:54 None Dilution of antibody FIG. 3. Inhibition of mouse (A) and human (B) IL 2 enhanement of NK ell ativity by antibodies to mouse and human IFN-y, respetively. Approximately 5 U of IL 2 per ml or 3 U of IFN-y per ml was inubated with equal volumes of various dilutions of antibodies to IFN--y (1:6 dilution; neutralizes 5 U of IFN--y per ml) for 1 h. The mixtures were inubated with PBL for 18 h, after whih the ells were washed and assayed for NK ell ativity. The unenhaned reativity of mouse spleen ells and human PBL was 12 and 7%, respetively. Symbols:, IFN--y plus anti-ifn--y;, IL 2 plus anti-ifn--y. enhaned natural killing and IFN--y ativity was seen. The same antibodies used above had no effet on the ability of IL 2 to stimulate DNA synthesis in an IL 2-dependent T-ell line, whereas the antiviral ativity of IFN-y was inhibited by >97%. We onlude that antibodies to mouse IFN-y probably bloked the enhanement of NK ell ativity by sequestering the IFN-y that was indued by IL 2. Inhibition of human IL 2 enhanement of NK eu ativity by antibodies to human IFN--y. We next investigated whether the IL 2 enhanement of NK ell ativity in the human system ould also be similarly regulated by antibodies to IFNy. Aordingly, various onentrations of rabbit antibodies to human IFN-y were added to PBL ultures that had been treated with IL 2. As with the mouse system, the enhanement of human NK ell ativity by IL 2 and the appearane of IFN-y ativity were bloked in a dose-response manner by the antibodies (Fig. 3B). Again, the antibodies did not blok the diret effet of human IL 2 on the stimulation of DNA synthesis in an IL 2-dependent T-ell line, whereas they inhibited IFN--y ativity by >99% (Table 1). Finally, highly speifi antibodies to human IFN--y were tested to determine whether they ould blok the enhanement of NK ell ativity as did antibodies to natural IFN--y. These antibodies were prepared in rabbits against a syntheti peptide omprising the inferred 2 N- terminal amino aids of human IFN--y based on DNA sequene (11). The results show that these antibodies also neutralized the ability of IL 2 to enhane killing (Table 2). This latter observation with antibodies to a hemially defined TABLE 1. Effet of antibodies in IFN--y on IFN-y indution of antiviral state and IL 2 indution of proliferation in an IL 2-dependent ell line Residual % Neu- Lymphokine Treatmenta ativity traliza- (U/mi) tion Human IFN--y None 3 b NRS 3 Anti-HuIFN-y <3 >99 Human IL 2 None 55 Anti-HuIFN--y Mouse IFN-y None 1 NRS 1 Anti-MoIFN-y <3 >97 Mouse IL 2 None 3 Anti-MoIFN-y a Normal rabbit serum (NRS) and rabbit antibodies to mouse (Mo) or human (Hu) IFN-y were inubated with the appropriate IL 2 (5 U eah) for 1 h at room temperature before being added to mouse spleen ells or human PBL. After this, the effet of the antibodies on the antiviral state and IL 2-indued proliferation was measured as desribed in the text. b, None. Downloaded from on May 3, 218 by guest
5 996 WEIGENT, STANTON, AND JOHNSON TABLE 2. Inhibition of enhaned NK ell ativity indued by human IL 2 with speifi antibodies to a syntheti peptide orresponding to the N-terminal region of IFN--y Cyto- % Neu- Lymphokine Treatmenta toxiity tralizaabove tion ontrol Human IL 2 None 36 b NRS 34 6 Antipeptide (1:1) Antipeptide (1:3) Antipeptide 34 6 (1:1) Human IFN--y None 51 NRS 49 4 Antipeptide (1:1) Antipeptide (1:3) Antipeptide (1:1) a Normal rabbit serum (NRS) and rabbit antibodies to a syntheti peptide of human IFN-y were inubated with IL 2 or IFN-y (5 U eah) for 1 h at room temperature before being added to human PBL. Eighteen hours later, the ells were washed twie and added to mouse L ell targets where hromium release was determined in an 18-h assay. b, None. syntheti antigen provides ompelling evidene that IFN-y is responsible for the enhaned killing ativity assoiated with IL 2. DISCUSSION Based on the aumulating data, NK ells may play a pivotal role in host defense, partiularly against intraellular infetions and aner (8). It is, therefore, an important observation that IFN an enhane NK ell ativity (3, 6, 2). Reently, IL 2 has also been shown to be apable of enhaning NK ell ativity (7, 12). Three observations appear to be the basis for attributing NK ell-enhaning properties to IL 2 that are distint from IFN enhanement. First, IL 2 free from antiviral ativity was apable of enhaning NK ell ativity (7, 12). Seond, the addition of both IL 2 and IFN-dp to NK ells in the mouse system resulted in the augmentation of NK ell ativity to levels not obtainable with either lymphokine alone (7, 12). Lastly, sublasses of NK ells in the mouse system responded differentially to the enhanement of ativity by IL 2 versus IFN-a/p (15). Two observations on our part suggested the possibility that the NK ell-enhaning effet of INFECT. IMMUN. IL 2 may be due to IFN--y. First, IL 2 indues T ells to make IFN--y without additional obvious stimulation, and thus the produed IFN-y ould atually enhane killing (22). Seond, when IFN-a/l and IFN-y were added together to the appropriate ultures, we have previously noted an augmentation of or potentiation effet on both the antiviral state and the enhanement of NK ell ativity to levels that were not obtainable with either IFN alone (5, 21). We have shown here that, in both the mouse and human systems, the IL 2 enhanement of NK ell ativity is totally due to the ability of highly purified IL 2 to indue IFN--y in lymphoyte ultures. The dose-response and kineti urves for IL 2 enhanement of NK ell ativity and the indution of IFN-y were similar, suggesting that the indued IFN--y was responsible for the NK ell ativity enhanement. More definitively, we were able to ompletely blok IL 2-indued enhanement of NK ell ativity in both the mouse and human systems by adding well-defined speifi antibodies to IFN-y to ultures at the time of IL 2 addition. These antibodies bloked NK ell ativity enhanement and antiviral ativity in a dose-response manner, while having no signifiant effet on the ability of IL 2 to stimulate DNA synthesis in an IL 2- dependent T-ell line. The antibodies were also nonreative with IL 1 and olony-stimulating fator. It is of partiular interest that one of the human antibodies that signifiantly bloked IL 2 enhanement of NK ell ativity was produed by the immunization of rabbits with a syntheti peptide enoded by the 5' end of human IFN-y DNA (11), thus preluding the possibility that ontaminating IL 2 or other lymphokines were in the immunogen. The same antibodies had no effet on IL 2 stimulation of DNA synthesis in an IL 2-dependent T-ell line. The data indiate that highly purified IL 2 enhanes NK ell ativity through its indution of IFN--y. In a general sense, the data presented here point out the interrelationship of lymphokines and funtions: a given lymphokine, in addition to exerting a diret effet on ells, may also indue lymphoytes to produe other lymphokines whih may be responsible for the biologial events of interest. ACKNOWLEDGMENTS We thank Donna Clegg for expert tehnial assistane. Our work was supported by grants CA 2759 and EY 1715 and the MLaughlin Postdotoral Fellowship program. LITERATURE CITED 1. Blalok, J. E., M. P. Langford, J. Georgiades, and G. J. Stanton Nonsensitized lymphoytes produed leukoyte interferon when ultured with foreign ells. Cell. Immunol. 43: Boyum, A Isolation of leukoytes from human Downloaded from on May 3, 218 by guest
6 VOL. 41, 1983 blood. Methyl ellulose, dextran, and fioll as erythroyte-aggregating agents. Sand. J. Clin. Lab. Invest. Suppl. 21: Djeu, F. Y., J. A. Heinbaugh, H. T. Holden, and R. B. Herberman Augmentation of mouse NK ell ativity by IFN and IFN induers. J. Immunol. 122: Djeu, J. Y., N. Stoks, K. Zoon, G. J. Stanton, T. Timonen, and R. B. Herberman Positive self-regulation of ytotoxiity in human natural killer ells by prodution of interferon upon exposure to influenza and herpes viruses. J. Exp. Med. 156: Fleishmann, W. R., Jr., J. A. Georgiades, L. C. Osborne, and H. M. Johnson Potentiation of interferon ativity by mixed preparations of fibroblast and immune interferon. Infet. Immun. 26: Gidlund, M., A. Orn, H. Wigzell, A. Senik, and I. Gresser Enhaned NK ell ativity in mie injeted with interferon and interferon induers. Nature (London) 223: Henney, C. S., K. Kuribayashi, D. E. Kern, and S. Gillis Interleukin 2 augments natural killer ell ativity. Nature (London) 291: Herberman, R. B. (ed.) Natural ell-mediated immunity against tumors. Aademi Press, In., New York. 9. Hilfiker, M. L., R. N. Moore, and J. J. Farrar Biologi properties of hromatographially separated murine thymoma derived interleukin 2 and olony-stimulating fator. J. Immunol. 127: Johnson, H. M Cellular regulation of immune interferon prodution. Antiviral Res. 1: Johnson, H. M., M. P. Langford, B. Lakhhaura, T. Chan, and G. J. Stanton Neutralization of native human gamma interferon (HuIFNy) by antibodies to a syntheti peptide enoded by the 5' end of HuIFNy DNA. J. Immunol. 129: Kuribayashi, K., S. Gillis, D. E. Kern, and C. S. Henney Murine NK ell ultures: effets of interleukin 2 and IFN on ell growth and ytotoxi reativity. J. Immunol. 126: L2, NK ACTIVITY, AND IFN-y Langford, M. P., J. A. Georgiades, G. J. Stanton, F. Dianzani, and H. M. Johnson Large sale prodution and physiohemial harateristis of human immune interferon. Infet. Immun. 26: Langford, M. P., D. A. Weigent, J. A. Georgiades, H. M. Johnson, and G. J. Stanton Antibody to staphylooal enterotoxin A-indued human immune interferon. J. Immunol. 126: Minato, N., L. Reid, and B. R. Bloom On the homogeneity of murine natural killer ells. J. Exp. Med. 154: Osborne, L. C., J. A. Georgiades, and H. M. Johnson Large sale prodution and partial purifiation of mouse immune interferon. Infet. Immun. 23: Osborne, L. C., J. A. Georgiades, and H. M. Johnson Classifiation of interferons with antibody to immune interferon. Cell. Immunol. 53: Roder, J. C., and T. Haliotis Do NK ells play a role in anti-tumor surveillane. Immunol. Today 1: Stadler, B. M., E. H. Berenstein, R. P. Siraganin, and J. J. Oppenheim Monolonal antibody against human interleukin 2 (IL 2). 1. Purifiation of IL2 for the prodution of monolonal antibodies. J. Immunol. 128: Trinhieri, G., D. Santoli, R. R. Dee, and B. B. Knowles Antiviral ativity indued by ulturing lymphoytes with tumor derived or virus-transformed ells. Identifiation of the antiviral ativity as interferon and haraterization of the human effetor lymphoyte subpopulation. J. Exp. Med. 147: Weigent, D. A., M. P. Langford, W. R. Fleishmann, Jr., and G. J. Stanton Potentiation of lymphoyte natural killing by mixtures of alpha or beta interferon with reombinant gamma interferon. Infet. Immun. 4: Yamamoto, J. K., W. L. Farrar, and H. M. Johnson Interleukin 2 regulation of mitogen indution of immune interferon (IFN-y) in spleen ells and thymoytes. Cell. Immunol. 66: Downloaded from on May 3, 218 by guest
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