Abstract
Kurloff cells may represent a major component of NK cell activity in the guinea pig. We have pursued to characterize the mechanism of their action. Using murine target cells, we found Kurloff cell cytotoxicity to be selective for the NK-sensitive YAC-1 target cell, with minimal activity against the NK-resistant P815 target cell. In the presence of PHA, but not ConA, cytotoxicity was markedly augmented against both YAC-1 and P815. While effector-target conjugate formation was observed with YAC-1 cells but not P815 cells in control cultures, it was augmented with both target cell types in cultures with PHA. Pretreatment alone with PHA was ineffective, however. NK cell activity of Kurloff cells was dependent on extracellular Ca++ and entry of Ca++ into the effector cells, as demonstrated by abrogation of cytotoxicity when extracellular Ca++ was chelated with EDTA or EGTA, or following treatment with the Ca++ channel blockers-verapamil and diltiazem. Furthermore, inhibition of PKC by H7 resulted in significant reduction of Kurloff cell-mediated NK activity, while pretreatment of effector cells with the PKC activator TPA enhanced NK activity. Kurloff cells could also be stimulated to produce serine esterases by contact with target cells or treatment with phorbol ester and ionophore. Finally, a majority of Kurloff cells, identified by the monoclonal antibody 14D1, reacted with the human NK cell marker CD56. Taken together, these data suggest that Kurloff cells have NK-like characteristics and activity, with target cell selectivity, and that their lytic mechanisms involve influx of extracellular Ca++, PKC activation and serine esterase production.
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Kurloff, M. G. 1889. Blood cells in spenectomized animals after one year of life.Vrach 10:515–538. Cited by Ledingham (3).
Foà, P., andT. Carbone. 1889. Beitrage zur histologie und physiopathologie des milz der saugethiere.Beitr. Path. Anat. 5:227–252. Cited by Ledingham (3).
Ledingham, J. C. G. 1940. Sex hormones and the Foà-Kurloff cell.J. Path. Bac. 50:201–219.
Bimes, C., A. Guilhem, andJ. Izard. 1964. Origine des lymphocytes à corps de Foà-Kurloff.C.R. Ass. Anat. 124:299–303.
Ruth, R. F., C. P. Allen, andH. R. Wolfe. 1964. The effect of thymus on lymphoid tissue.In: The Thymus in immunology. R. A. Good and A. E. Gabrielsen, Eds., Harper and Row, NewYork pp. 183–205.
Ernström, U., andG. Sandberg. 1971. On the origin of Foà-Kurloff cells.Scand. J. Haemat. 8:380–391.
Kittas, C., M. A. Parsons, andL. Henry. 1979. A light and electron microscope study on the origin of Foà-Kurloff cells.Br. J. Exp. Path. 60:276–285.
Marshall, A. H. E., K. V. Swettenham, andB. Vernon-Roberts. 1970. The function of the Kurloff cell and its possible relation to the immunological status of the guinea-pig placenta.J. Anat. 106:414–415.
Marshall, A. H. E., K. V. Swettenham, B. Vernon-Roberts, andP. A. Revell. 1971. Studies on the function of the Kurloff cell.Int. Arch. Allergy 40:137–152.
Eremin, O., R. R. A. Coombs, J. Ashby, andD. Plumb. 1980. Natural cytotoxicity in the guinea-pig: the natural killer (NK) cell activity of the Kurloff cell.Immunol. 41:367–378.
Eremin, O., A. B. Wilson, R. R. A. Coombs, J. Ashby, andD. Plumb. 1980. Antibody-dependent cellular cytotoxicity in the guinea pig: the role of the Kurloff cell.Cell. Immunol. 55:312–327.
Landemore, G., C. Debout, M. Quillec, andJ. Izard. 1984. Isolation of Kurloff cells by Percoll density gradient centrifugation. Protein labelling with 35S-methionine of these cells.Biol. Cell. 50:121–126.
Noga, S. J., S. J. Normann, andR. S. Weiner. 1984. Isolation of guinea pig monocytes and Kurloff cells: characterization of monocyte subsets by morphology, cytochemistry, and adherence.Lab. Invest. 51:244–251.
Debout, C., M. Quillec, andJ. Izard. 1984. Natural killer activity of Kurloff cells: a direct demonstration on purified Kurloff cell suspensions.Cell. Immunol. 87:674–677.
Maghni, K., C.Robidoux, J.Laporte, A.Hallée, P.Borgeat, and P.Sirois. 1991. Purification of natural killer-like Kurloff cells and arachidonic acid metabolisms. Submitted for publication.
Henkart, P. A., J. T. Lewis, andJ. R. Ortaldo. 1986. Preparation of target antigens specifically recognized by human natural killer cells.Nat. Immun. Cell Growth Regul. 5:113–126.
Pelé, J. P., C. Robidoux, andP. Sirois. 1989. Guinea pig lung cells. Method of isolation and partial purification, identification, ultrastructure, and cell count.Inflammation 13:103–123.
Boyde, A., R. A. Weiss, andP. Vesely. 1972. Scanning electron microscopy of cells in culture.Exp. Cell. Res. 71:313–324.
Ostergaard, H. L., andW. R. Clark. 1989. Evidence for multiple lytic pathways used by tototoxic T lymphocytes.J. Immunol. 143:2120–2126.
Naspitz, Ch.K., andM. Richter. 1968. The action of phytohemagglutinin in vivo and in vitro, a review.Prog. All. 12:1–85.
Plaut, M., J. E. Bubbers, andC. S. Henney. 1976. Studies on the mechanism of lymphocyte-mediated cytolysis. VII. Two stages in the T cell-mediated lytic cycle with distinct cation requirements.J. Immunol. 116:150–155.
Hiserodt, J. C., L. J. Britvan, andS. R. Targan. 1982. Characterization of the cytolytic reaction mechanism of the human natural killer (NK) lymphocyte: resolution into binding, programming, and killer cell-independent steps.J. Immunol. 129:1782–1787.
Quan, P. C., T. Ishizaka, andB. R. Bloom. 1982. Studies on the mechanism of NK cellysis.J. Immunol. 128:1786–1791.
Gately, M. K., andE. Martz. 1979. Early steps in specific tumor cell lysis by sensitized mouse T lymphocytes. III. Resolution of two distinct roles for Ca++ in the cytolytic process.J. Immunol. 122:482–489.
Ng, J., B. B. Fredholm, andM. Jondal. 1987. Studies on the Ca++ dependence of human NK cell killing.Biochem. Pharmacol. 36:3943–3949.
Roder, J. C., R. Kiessling, P. Biberfeld, andB. Andersson. 1978. Target-effector interaction in the natural killer (NK) cell system. II. The isolation of NK cells and studies on the mechanism of killing.J. Immunol. 121:2509–2517.
Hidaka, H., M. Inagaki, S. Kawamoto, andY. Sasaki. 1984. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase.C. Biochem. 23:5036–5041.
Edwards, B. S., H. A. Nolla, andR. R. Hoffman. 1989. Relationship between target cell recognition and temporal fluctuations in intracellular Ca2+ of human NK cells.J. Immunol. 143:1058–1065.
Masera, R., G. Gatti, M. L. Sartori, R. Carignola, A. Salvadori, E. Magro, andA. Angeli. 1989. Involvement of Ca2+-dependent pathways in the inhibition of human natural killer (NK) cell activity by cortisol.Immunopharmacol. 18:11–22.
Richards, A. L., andJ. Y. Djeu. 1990. Calcium-dependent natural killer and calcium-independent natural cytotoxic activities in an IL-2 dependent killer cell line.J. Immunol. 145:3144–3149.
Carpen, O., I. Virtanen, andE. Saksela. 1981. The cytotoxic activity of human natural killer cells requires an intact secretory apparatus.Cell. Immunol. 58:97–106.
Atkinson, E. A., J. M. Gerrard, G. E. Hildes, andA. H. Greenberg. 1990. Studies of the mechanism of natural killer (NK) degranulation and cytotoxicity.J. Leuk. Biol. 47:39–48.
Takayama, H., G. Trenn, W. Humphrey Jr., J. A. Bluestone, P. A. Henkart, andM. V. Sitkovsky. 1987. Antigen receptor-triggered secretion of a trypsin-type esterase from cytotoxic T lymphocytes.J. Immunol. 138:566–569.
Altman, A., andH. J. Rapp. 1978. Natural cell-mediated cytotoxicity in guinea pigs: properties and specificity of natural killer cells.J. Immunol. 121:2244–2252.
Harrison, C. J., andM. G. Myers. 1988. Peripheral blood mononuclear cell-mediated cytolytic activity during cytomegalovirus (CMV) infection of guinea pigs.J. Med. Virol. 25:441–453.
Wilson, A. B., andR. R. A. Coombs. 1971. Passive sensitization of tissue cells. IV. Guinea-pig antibodies cytophilic for basophils and Kurloff cells.Int. Arch. Allergy 40:19–46.
Wilson, A. B., andR. R. A. Coombs. 1973. Rosette-formation between guinea pig lymphoid cells and rabbit erythrocytes—a possible T-cell marker.Int. Arch. Allergy 44:544–552.
Lis, H., andN. Sharon. 1973. The biochemistry of plant lectins (phytohemagglutinins).Am. Rev. Biochem. 42:541–574.
Wisloff, F., S. S. Froland, andT. E. Michaelsen. 1974. Characterization of subpopulations of human lymphoid cells participating in phytohemagglutinin and concanavalin A-induced cytotoxicity.Int. Arch. Allergy 47:488–497.
De E. De Bracco, M. M., Isturiz, andJ. A. Manni. 1976. Cell-mediated cytotoxicity. Characterization of the effector cells.Immunology 30:325–333.
Nelson, D. L., B. M. Bundy, T. D. West, andW. Strober. 1976. The nature of the effector cells mediating mitogen-induced cellular cytotoxicity (MICC) and antibody-dependent cellular cytotoxicity (ADCC).Cell. Immunol. 23:89–98.
Bonavida, B., A. Robins, andA. Saxon. 1977. Lectin-dependent cellular cytotoxicity in man.Transplantation 23:261–270.
Bolhuis, R. L. H., R. J. van de Griend, andC. P. M. Ronteltap. 1983/84. Clonal expansion of human B73.1-positive natural killer cells or large granular lymphocytes exerting strong antibody-dependent and -independent cytotoxicity and occasionally lectin-dependent cytotoxicity.Nat. Immun. Cell Growth Regul. 3:61–72.
Neighbour, P. A., H. S. Huberman, andY. Kress. 1982. Human large granular lymphocytes and natural killing: ultrastructural studies of strontium-induced degranulation.Eur. J. Immunol. 12:588–595.
Frey, T., H. R. Petty, andH. M. McConnel. 1982. Electron microscopic study of natural killer cell-tumor cell conjugates.Proc. Natl. Acad. Sci. U.S.A. 79:5317–5321.
Kaneda, K., andK. Wake. 1990. Ultrastructural study of in vivo tumor cell lysis by liver-associated natural killer cells.Biochem. Res. 11:137–143.
Chow, S. C., J. Ng, C. Nordstedt, B. B. Fredholm, andM. Jondal. 1988. Phospoinositide breakdown and evidence for protein kinase C involvement during human NK killing.Cell. Immunol. 114:96–103.
Steele, T. A., andZ. Brahmi. 1988. Inhibition of human natural killer cell activity by the protein kinase C inhibitor 1-(5-isoquinolinesulfonyl)-2-methylpiperazine is an early but post-binding event.J. Immunol. 141:3164–3169.
Ortaldo, J. R., H. A. Young, andL. Varesio. 1989. Modulation of CD3− large granular lymphocyte functions by agonist and antagonists of protein kinase C: effects on NK and lymphokine-activated killer activity and production of IFN-γ.J. Immunol. 143:366–371.
Carpen, O., andSaksela, E. 1988. Directed exocytosis in the NK-cell-mediated cytotoxicity. A review.Nat. Immun. Cell Growth Regul. 7:1–12.
Brogan, M., andS. Targan. 1986. Evidence for involvement of serine proteases in the late stages of the natural killer cell lytic reaction.Cell. Immunol. 103:426–433.
Goldfarb, R. H. 1986. Role of neutral urine proteases in tumor cell lysis by natural killer cells (large granular lymphocytes) and activated macrophages.Sem. Thrombos. Hemostas. 12:308–309.
Burkhardt, J. K., S. Hester, andY. Argon. 1989. Two proteins targeted to the same lytic granule compartment undergo very different posttranslational processing.Proc. Natl. Acad. Sci. U.S.A. 86:7128–7132.
Masson, D., P. J. Peters, H. J. Geuze, J. Borst, andJ. Tschopp. 1990. Interaction of chondroitin sulfate with perform and granzymes of cytolytic T-cells is dependent on pH.Biochem. 29:11229–11235.
Yam, L. T., C. Y. Li, andW. H. Crosby. 1971. Cytochemical identification of monocytes and granulocytes.Amer. J. Clin. Path. 55:283–290.
Letaïef, S.-E., G. Landermore, J. Bocquet, andJ. Izard. 1989. Kurloff cell proteoglycans: presence of two main size-populations of intracellular protease-resistant proteochondroitin sulphate. Effect of D-xyloside.Biol. of the Cell. 65:257–263.
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Pouliot, N., Maghni, K., Blanchette, F. et al. Natural killer and lectin-dependent cytotoxic activities of kurloff cells: Target cell selectivity, conjugate formation, and Ca++ dependency. Inflammation 20, 647–671 (1996). https://doi.org/10.1007/BF01488802
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DOI: https://doi.org/10.1007/BF01488802