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Cancer Immunology, Immunotherapy : CII logoLink to Cancer Immunology, Immunotherapy : CII
. 1991 Jan;34(1):1–8. doi: 10.1007/BF01741317

T cell targeting in cancer therapy

Reinder L H Bolhuis 1, Els Sturm 1, Eric Braakman 1
PMCID: PMC11038718  PMID: 1760806

Abstract

Targeting of immune cells by bispecific antibodies has proven a powerful tool for the investigation of cellular cytotoxicity, lymphocyte activation and induction of cytokine production, as well as to represent an innovative form of immunotherapy for the treatment of cancer. The hallmark of this approach is the use of the specificity of monoclonal antibodies to join target and immune cells by virtue of the dual specificity of bispecific antibodies for the two entities. More precisely the bispecific antibody has two different binding sites, which are capable of recognizing tumor associated antigens on the one hand and lymphocyte activation sites on the other. This process of crosslinking results in the activation of the lymphocyte and triggering of its lytic machinery, as well as lymphokine production. A major advantage of this therapeutic modality is, that use is made of the normal cellular immune defence system and therefore is only associated with minor toxicity. The distinct lymphocyte populations, which can be used for adoptive immunotherapy and the various bispecific antibody preparations, as well as the chimeric immunoglobulin/T cell receptor construction are the major topics of this review.

Key words: T lymphocytes, Bispecific antibody, Cancer therapy

References

  • 1.Abraham N, Miceli M, Parnes JR, Veilette A. Enhancement of T-cell responsiveness by the lymphocyte-specific tyrosine protein kinase p56lck . Nature. 1991;350:62. doi: 10.1038/350062a0. [DOI] [PubMed] [Google Scholar]
  • 2.Alarcon I, Cuturi MC, Trinchieri G, Perussia B. Interaction of Fc receptor (CD16) ligands induces transcription of interleukin 2 receptor (CD25) and lymphokine genes and expression of their products in human natural killer cells. J Exp Med. 1988;167:452. doi: 10.1084/jem.167.2.452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Alcover A, Albertini C, Acuto O, Clayton LK, Transy C, Spagnoli GC, Moingeon P, Lopez P, Reinherz EL. Interdependence of CD3-Ti and CD2 activation pathways in human T lymphocytes. EMBO J. 1988;7:1973. doi: 10.1002/j.1460-2075.1988.tb03035.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Anderson P, Blue ML, Morimoto C, Schlossman SF. Crosslinking of T3 (CD3) with T4 (CD4) enhances the proliferation of resting T lymphocytes. J Immunol. 1987;139:678. [PubMed] [Google Scholar]
  • 5.Anderson PM, Caligiuri M, Ritz J, Schlossman SF. CD3-negative natural killer cells express ζ TCR as part of a novel molecular complex. Nature. 1989;341:159. doi: 10.1038/341159a0. [DOI] [PubMed] [Google Scholar]
  • 6.Anderson P, Caligiuri M, O'Brien C, Manley T, Ritz J, Schlossman SF. Fcγ receptor type III (CD16) is included in the ζNK receptor complex expressed by human natural killer cells. Proc Natl Acad Sci USA. 1990;87:2274. doi: 10.1073/pnas.87.6.2274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Becker MLB, Near R, Mudgett-Hunter M, Margolies MN, Kubo RT, Kaye J, Hedrick SM. Expression of a hybrid immunoglobulin-T-cell receptor protein in transgenic mice. Cell. 1989;58:911. doi: 10.1016/0092-8674(89)90943-4. [DOI] [PubMed] [Google Scholar]
  • 8.Berke G. Interaction of cytotoxic T lymphocytes and target cells. Prog Allergy. 1980;27:69. [PubMed] [Google Scholar]
  • 9.Biassoni R, Ferrini S, Prigione I, Moretta A, Long EO. CD3 negative lymphokine activated cytotoxic cells express the CD3εgene. J Immunol. 1988;140:1685. [PubMed] [Google Scholar]
  • 10.Bierer BE, Peterson A, Gorga JC, Herrmann SH, Burakoff SJ. Synergistic T cell activation via the physiological ligands for CD2 and the T cell receptor. J Exp Med. 1988;168:1145. doi: 10.1084/jem.168.3.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Blue ML, Hafler DA, Craig KA, Levine H, Schlossman SF. Phosphorylation of CD4 and CD8 molecules following T cell triggering. J Immunol. 1987;139:3949. [PubMed] [Google Scholar]
  • 12.Bolhuis RLH, Braakman E. Lymphocyte-mediated responses: activation of, and lysis by, cytotoxic lymphocytes. Curr Opinion Immunol. 1988;1:236. doi: 10.1016/0952-7915(88)90007-6. [DOI] [PubMed] [Google Scholar]
  • 13.Bolhuis RLH, Van de Griend RJ. PHA induced proliferation and cytolytic activity in T3+ but not in T3− cloned lymphocytes, requires the involvement of the T3 antigen for signal transmission. Cell Immunol. 1985;93:46. doi: 10.1016/0008-8749(85)90387-9. [DOI] [PubMed] [Google Scholar]
  • 14.Bolhuis RLH, Roozemond RC, van de Griend RJ. Induction and blocking of cytolysis in CD2+, CD3− NK and CD2+, CD3+ cytotoxic T lymphocytes via CD2, 50kD sheep erythrocyte receptor. J Immunol. 1986;136:3939. [PubMed] [Google Scholar]
  • 15.Bolhuis RLH, Gravekamp C, van de Griend RJ. Cell-cell interactions. Clin Immunol Allerg. 1986;6:29. [Google Scholar]
  • 16.Borst J, Van de Griend RJ, Van Oostveen H, Ang S, Melief CJM, Seidman JG, Bolhuis RLH. A T-cell receptor/CD3 complex found on cloned functional lymphocytes. Nature. 1987;325:683. doi: 10.1038/325683a0. [DOI] [PubMed] [Google Scholar]
  • 17.Braakman E, Goedegebuure PS, Vreugdenhil RJ, Segal DM, Shaw S, Bolhuis RLH. ICAM− melanoma cells are relatively resistant to CD3 mediated T-cell lysis. Int J Cancer. 1990;46:475. doi: 10.1002/ijc.2910460325. [DOI] [PubMed] [Google Scholar]
  • 18.Breitmeyer JB, Daley JF, Levine HB, Schlossman SF. The T11 (CD2) molecule is functionally linked to the T3/Ti T cell receptor in the majority of T cells. J Immunol. 1987;139:2899. [PubMed] [Google Scholar]
  • 19.Brenner MB, Towbridge IS, Strominger JL. Crosslinking of human T cell receptor proteins. Association between T cell idiotypic β subunits and the T3 glycoprotein heavy subunit. Cell. 1985;40:183. doi: 10.1016/0092-8674(85)90321-6. [DOI] [PubMed] [Google Scholar]
  • 20.Brenner MB, McLean J, Dialynas DPB, Strominger JL, Smith JA, Owen FL, Seidman JG, Ip S, Rosen F, Krangel MS. Identification of a putative second T-cell receptor. Nature. 1986;322:145. [Google Scholar]
  • 21.Brown MH, Cantrell DA, Brattsand G, Crumpton MJ, Gullberg M. The CD2 antigen associates with the T-cell antigen receptor CD3 antigen complex on the surface of human T lymphocytes. Nature. 1989;339:551. doi: 10.1038/339551a0. [DOI] [PubMed] [Google Scholar]
  • 22.Bubenik J, Jakoubkova J, Krakora P, Baresova M, Helbich P, Vicklicky V, Malaskova V. Cellular immunity to renal carcinomas in man. Int J Cancer. 1971;8:503. doi: 10.1002/ijc.2910080319. [DOI] [PubMed] [Google Scholar]
  • 23.Burnet FM. The concept of immunological surveillance. Prog Exp Tumor Res. 1970;13:1. doi: 10.1159/000386035. [DOI] [PubMed] [Google Scholar]
  • 24.Canevari S, Ménard S, Mezzanzanica D, Miotti S, Pupa SM, Lanzavecchia A, Colnaghi MI. Anti-ovarian carcinoma anti-T3 heteroconjugates or hybrid antibodies induce tumor cell lysis by cytotoxic T cells. Int J Cancer. 1988;42:18. doi: 10.1002/ijc.2910410707. [DOI] [PubMed] [Google Scholar]
  • 25.Cantrell D, Davies AA, Londei M, Feldman M, Crumpton MJ. Association of phosphorylation of the T3 antigen with immune activation of T lymphocytes. Nature. 1987;325:540. doi: 10.1038/325540a0. [DOI] [PubMed] [Google Scholar]
  • 26.Cepko CL, Roberts BE, Mulligan RC. Construction and applications of a highly transmissible murine retrovirus shuttle vector. Cell. 1984;37:1053. doi: 10.1016/0092-8674(84)90440-9. [DOI] [PubMed] [Google Scholar]
  • 27.Chothia C, Boswell BW, Lesk AM. The outline structure of the T-cell αβ receptor. EMBO J. 1988;7:3745. doi: 10.1002/j.1460-2075.1988.tb03258.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Davis MM, Bjorkman PJ. T-cell antigen receptor genes and T-cell recognition. Nature. 1988;334:395. doi: 10.1038/334395a0. [DOI] [PubMed] [Google Scholar]
  • 29.Dembic Z, Haas W, Weiss S, McCubrey J, Kiefer H, Von Boehmer H, Steinmetz M. Transfer of specificity by murine α and β T cell receptor genes. Nature. 1986;320:232. doi: 10.1038/320232a0. [DOI] [PubMed] [Google Scholar]
  • 30.Dustin ML, Springer TA. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 1989;341:619. doi: 10.1038/341619a0. [DOI] [PubMed] [Google Scholar]
  • 31.Ehrlich P. Über den jetzigen Stand der Karzinomforschung. Ned Tijdschr Geneesk. 1909;35:273. [Google Scholar]
  • 32.Eshhar Z, Gross G. Chimeric T cell receptor which incorporates the anti-tumor specificity of a monoclonal antibody with the cytolytic activity of T cells: a model system for immunotherapeutical approach. Br J Cancer. 1990;62(Suppl 10):27. [PMC free article] [PubMed] [Google Scholar]
  • 33.Ferrari G, Rossini S, Giavazzi R, Maggioni D, Nobili N, Soldati M, Ungers G, Mavilio F, Gilboa E, Bordignon C. An in vivo model of somatic cell gene therapy for human severe combined immunodeficiency. Science. 1991;251:1363. doi: 10.1126/science.1848369. [DOI] [PubMed] [Google Scholar]
  • 34.Finn OJ, Persons DA, Bendt KM, Pirami L, Ricciardi P. Retroviral transduction of protein kinase C-γ into cytotoxic T lymphocyte clones leads to immortalization with retention of specific function. J Immunol. 1990;146:1099. [PubMed] [Google Scholar]
  • 35.Fisch P, Malkovsky M, Kovats S, Sturm E, Braakman E, Klein BS, Voss SD, Morrissey LW, DeMars R, Welch WJ, Bolhuis RLH, Sondel PM. Recognition by human Vγ9/Vδ2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science. 1990;250:1269. doi: 10.1126/science.1978758. [DOI] [PubMed] [Google Scholar]
  • 36.Fleisher B. Acquisitions of specific cytotoxic activity by human T4+ T lymphocytes in culture. Nature. 1984;308:365. doi: 10.1038/308365a0. [DOI] [PubMed] [Google Scholar]
  • 37.Fleischer B, Sturm E, De Vries JE, Spits H. Triggering of cytotoxic T lymphocytes and NK cells via the Tp103 pathway is dependent on the expression of the T cell receptor/CD3 complex. J Immunol. 1988;141:1103. [PubMed] [Google Scholar]
  • 38.Goedegebuure PS, Segal DM, Braakman E, Vreugdenhil RJ, van Krimpen BA, van de Griend RJ, Bolhuis RLH. Induction of lysis by T cell receptor γδ+/CD3+ T lymphocytes via CD2 requires triggering via the T11.1 epitope only. J Immunol. 1989;142:1797. [PubMed] [Google Scholar]
  • 39.Goedegebuure PS, Braakman E, Segal DM, Vreugdenhil RJ, Bolhuis RLH. Lymphocyte leukocyte function-associated antigen-1 interacting with target cell intercellular adhesion molecule-1 coactivates cytolysis triggered via CD16 on the receptor involved or major histocompatibility antigen-unrestricted lysis. Int Immunol. 1990;2:1213. doi: 10.1093/intimm/2.12.1213. [DOI] [PubMed] [Google Scholar]
  • 40.Gorochov G, Gross G, Waks T, Eshhar Z. Expression of chimeric Ab/TCR genes as functional receptor molecules in human and mouse T cells. In: Lotz MT, Finn OJ, editors. Cellular immunity and the immunopathology of cancer. New York: Wiley-Liss Inc; 1990. p. 45. [Google Scholar]
  • 41.Goverman J, Gomez SM, Segesman KD, Hunkapiller T, Lang WE, Hood L. Chimeric immunoglobulin-T-cell receptor complex formation and activation. Cell. 1990;60:929. doi: 10.1016/0092-8674(90)90341-b. [DOI] [PubMed] [Google Scholar]
  • 42.Gross G, Gorochov G, Waks T, Eshhar Z. Generation of effector T cells expressing chimeric T cell receptor with antibody type specificity. Transplant Proc. 1989;21:127. [PubMed] [Google Scholar]
  • 43.Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci USA. 1989;86:10024. doi: 10.1073/pnas.86.24.10024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Haskins K, Kubo R, White J, Pigeon M, Kappler J, Marrack P. The major histocompatibility complex restricted antigen receptor on T cells. Isolation with a monoclonal antibody. J Exp Med. 1983;161:1513. doi: 10.1084/jem.157.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Hedrick SM, Nielsen EA, Kavaler J, Cohen DI, Davis MM. Sequence relationships between putative T cell receptor polypeptides and immunoglobulins. Nature. 1984;308:153. doi: 10.1038/308153a0. [DOI] [PubMed] [Google Scholar]
  • 46.Hercend T, Schmidt RE. Characteristics and uses of natural killer cells. Immunol Today. 1988;9:291. doi: 10.1016/0167-5699(88)91317-5. [DOI] [PubMed] [Google Scholar]
  • 47.Hersey P, Bolhuis RLH. “Nonspecific” MHC-unrestricted killer cells and their receptors. Immunol Today. 1987;8:233. doi: 10.1016/0167-5699(87)90173-3. [DOI] [PubMed] [Google Scholar]
  • 48.Hombach J, Tsubata T, Leclercq L, Stappert H, Reth M. Molecular components of the B-cell antigen receptor complex of the IgM class. Nature. 1990;343:760. doi: 10.1038/343760a0. [DOI] [PubMed] [Google Scholar]
  • 49.Hünig T, Kiefenthaler G, Meyer zum Buschenfelde KH, Meuer SC. Alternative pathway activation of T cells by binding of CD2 to its cell-surface ligand. Nature. 1987;326:298. doi: 10.1038/326298a0. [DOI] [PubMed] [Google Scholar]
  • 50.Karpovsky B, Titus JA, Stephany DA, Segal DM. Production of target-specific receptor cells using hetero-cross-linked-aggregates containing anti-target cell and anti-Fcγreceptor antibodies. J Exp Med. 1984;160:1686. doi: 10.1084/jem.160.6.1686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Kasid A, Morecki S, Aebersold PM, Cornetta K, Culver K, Freeman S, Director E, Lotze MT, Blaese RM, Anderson WF, Rosenberg SA. Human gene transfer: characterization of human tumor-infiltrating lymphocytes as vehicles for retroviralmediated gene transfer in man. Proc Natl Acad Sci USA. 1990;87:473. doi: 10.1073/pnas.87.1.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Figdor CG, van Kooyk Y, Keizer GD. On the mode of action of LFA-1. Immunol Today. 1990;II:277. doi: 10.1016/0167-5699(90)90112-m. [DOI] [PubMed] [Google Scholar]
  • 53.Brenner MB, McLean J, Scheft H, Ruberdy J, Ang S-L, Seidman SG, Devlin P, Krangel MS. Two forms of the T-cell receptor gamma protein found on peripheral blood cytotoxic T lymphocytes. Nature. 1987;325:689. doi: 10.1038/325689a0. [DOI] [PubMed] [Google Scholar]
  • 54.Krensky AM, Sanchez-Madrid F, Robbins E, Nagy JA, Springer TA, Burakoff SJ. The functional significance, distribution, and structure of LFA-1, LFA-2 and LFA-3; cell surface antigens associated with CTL target interactions. J Immunol. 1983;131:611. [PubMed] [Google Scholar]
  • 55.Kupfer A, Singer SJ, Janeway CA, Swain SL. Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc Natl Acad Sci USA. 1987;84:5888. doi: 10.1073/pnas.84.16.5888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Kuwana Y, Asakura Y, Utsuomiya N, Nakanishi M, Arata Y, Itoh S, Nagase F, Kurosawa Y. Expression of chimeric receptor composed of immunoglobulin-derived V regions and T-cell receptor-derived C regions. Biochem Biophys Res Commun. 1987;149:960. doi: 10.1016/0006-291x(87)90502-x. [DOI] [PubMed] [Google Scholar]
  • 57.Lafaille JJ, DeCloux A, Bonneville M, Takagaki Y, Tonegawa S. Junctional sequences of T cell receptor γδ genes: implications for γδ T cell lineages and for a novel intermediate of V-(D)-J joining. Cell. 1989;59:859. doi: 10.1016/0092-8674(89)90609-0. [DOI] [PubMed] [Google Scholar]
  • 58.Lanier LL, Dwirla S, Phillips JH. Genomic organization of T cell γ genes in human peripheral blood natural killer cells. J Immunol. 1986;137:3375. [PubMed] [Google Scholar]
  • 59.Lanier LL, Yu G, Phillips JH. Co-association of CD3ζ with a receptor (CD 16) for IgG on human natural killer cells. Nature. 1989;342:803. doi: 10.1038/342803a0. [DOI] [PubMed] [Google Scholar]
  • 60.Lanzavecchia A, Scheidegger D. The use of hybrid hybridomas to target human cytotoxic T lymphocytes. Eur J Immunol. 1987;17:105. doi: 10.1002/eji.1830170118. [DOI] [PubMed] [Google Scholar]
  • 61.Leeuwenberg J, Spits H, Tax W, Capel P. Monoclonal antibodies against T3 induce antigen non specific cellular cytotoxicity. J Immunol. 1985;134:3770. [PubMed] [Google Scholar]
  • 62.Leeuwenberg JFM, Lems SPM, Capel PJA. Anti-T3 induced cytotoxicity: the role of target cell Fc-receptors in the lysis of autologous monocytes and the Fc-independent lysis of T3-positive target cells. Transplant Proc. 1987;19:428. [PubMed] [Google Scholar]
  • 63.Littman DR. The structure of the CD4 and CD8 genes. Annu Rev Immunol. 1987;5:561. doi: 10.1146/annurev.iy.05.040187.003021. [DOI] [PubMed] [Google Scholar]
  • 64.Makgoba MW, Sanders ME, Luce GEG, Dustin ML, Springer TA, Clark EA, Mannoni P, Shaw S. ICAM-1 a ligand for LFA-1 dependent adhesion of B-, T- and myeloid cells. Nature. 1988;331:86. doi: 10.1038/331086a0. [DOI] [PubMed] [Google Scholar]
  • 65.Marlin SD, Springer TA. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1) Cell. 1987;51:813. doi: 10.1016/0092-8674(87)90104-8. [DOI] [PubMed] [Google Scholar]
  • 66.Marrack P, Kappler J. The antigen specific, major histocompatibility complex restricted receptor on T cells. Adv Immunol. 1986;38:1. doi: 10.1016/s0065-2776(08)60005-x. [DOI] [PubMed] [Google Scholar]
  • 67.Martz E. Mechanisms of specific tumor cell lysis by alloimmune T lymphocytes; resolution and characterization of discrete steps in the cellular interaction. Contemp Top Immunobiol. 1977;7:301. doi: 10.1007/978-1-4684-3054-7_9. [DOI] [PubMed] [Google Scholar]
  • 68.Menzer SJ, Smith BR, Barbosa SA, Crimmins MAV, Herrmann SH, Burakoff SJ. CTL adhesion and antigen recognition are discrete steps in the human CTL target cell interaction. J Immunol. 1987;138:1325. [PubMed] [Google Scholar]
  • 69.Meuer SC, Schlossman SF, Reinherz EL. Clonal analysis of human cytotoxic T lymphocytes: T4+ and T8+ T cells recognize products of different major histocompatibility complex regions. Proc Natl Acad Sci USA. 1982;79:4395. doi: 10.1073/pnas.79.14.4395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Meuer SC, Russey RE, Fabbi M, Fox D, Acuto D, Fitzgerald KA, Hodgdon JC, Protentis JP, Schlosmann SF, Reinherz EL. An alternative pathway of T cell activation: a functional role for the 50kD T11 sheep erythrocyte receptor protein. Cell. 1984;36:897. doi: 10.1016/0092-8674(84)90039-4. [DOI] [PubMed] [Google Scholar]
  • 71.Milstein C, Cuello AC. Hybrid hybridomas and their use in immunohistochemistry. Nature. 1983;305:537. doi: 10.1038/305537a0. [DOI] [PubMed] [Google Scholar]
  • 72.Moingeon P, Chang HC, Wallner BP, Stebbins C, Frey AZ, Reinherz EL. CD 2 mediated adhesion facilitates T-lymphocyte antigen recognition function. Nature. 1989;339:312. doi: 10.1038/339312a0. [DOI] [PubMed] [Google Scholar]
  • 73.Nitta T, Sato K, Yagita H, Okumura K, Ishii S. Preliminary trial of specific targeting therapy against malignant glioma. Lancet. 1990;335:368. doi: 10.1016/0140-6736(90)90205-j. [DOI] [PubMed] [Google Scholar]
  • 74.Oettgen HC, Kappler J, Tax WJM, Terhorst C. Characterization of the two heavy chains of the T3 complex on the surface of human T lymphocytes. J Biol Chem. 1984;259:12 039. [PubMed] [Google Scholar]
  • 75.Ortaldo JR, Herberman RB. Heterogeneity of natural killer cells. Annu Rev Immunol. 1984;2:359. doi: 10.1146/annurev.iy.02.040184.002043. [DOI] [PubMed] [Google Scholar]
  • 76.Pantaleo G, Olive D, Poggi A, Pozzan T, Moretta L, Moretta A. Antibody-induced modulation of the CD3/T-cell receptor complex causes T-cell refractoriness by inhibiting the early metabolic steps involved in T-cell activation. J Exp Med. 1987;166:619. doi: 10.1084/jem.166.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Parnes JR. Molecular biology and function of CD4 and CD8. Adv Immunol. 1989;44:265. doi: 10.1016/s0065-2776(08)60644-6. [DOI] [PubMed] [Google Scholar]
  • 78.Perez P, Hoffman RW, Shaw S, Bluestone JA, Segal DM. Specific targeting of cytotoxic T-cells by anti-T3 linked to anti-target cell antibody. Nature. 1985;316:354. doi: 10.1038/316354a0. [DOI] [PubMed] [Google Scholar]
  • 79.Perussia B, Trinchieri G, Jackson A, Warner NL, Faust J, Rumpold H, Kraft D, Lanier LL. The Fc receptor for IgG on human natural killer cells: phenotype, functional, and comparative studies with monoclonal antibodies. J Immunol. 1984;133:180. [PubMed] [Google Scholar]
  • 80.Phillips JH, Le AM, Lanier LL. Natural killer cells activated in a human mixed lymphocyte response culture identified by expression of Leu-11 and class II histocompatibility antigens. J Exp Med. 1984;159:993. doi: 10.1084/jem.159.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Ritz J, Schmidt RE, Michon J, Hercend T, Schlossman SF. Characterization of functional surface structures on human natural killer cells. Adv Immunol. 1988;42:181. doi: 10.1016/s0065-2776(08)60845-7. [DOI] [PubMed] [Google Scholar]
  • 82.Rosenberg SA, Aebersold PM, Cornetta K, Kasid A, Morgan RA, Moen R, Karson EM, Lotze MT, Yang JC, Topalian SL, Merino MJ, Culver K, Miller AD, Blaese RM, Anderson WF. Gene transfer into humans: immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N Engl J Med. 1990;323:570. doi: 10.1056/NEJM199008303230904. [DOI] [PubMed] [Google Scholar]
  • 83.Rosenstein Y, Ratnofsky S, Burakoff SJ, Herrmann SH. Direct evidence for binding of CD8 to HLA class I antigens. J Exp Med. 1989;169:149. doi: 10.1084/jem.169.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Saito T, Weis TA, Miller J, Norcross MA, Germain N. Specific antigen-Ia activation of transfected human T cells expressing murine TCRαβ human T3 complexes. Nature. 1987;325:125. doi: 10.1038/325125a0. [DOI] [PubMed] [Google Scholar]
  • 85.Saizawa K, Rojo J, Janeway JA., Jr Evidence for a physical association of CD4 and the CD3:α:β T-cell receptor. Nature. 1987;328:260. doi: 10.1038/328260a0. [DOI] [PubMed] [Google Scholar]
  • 86.Segal DM, Snider DP. Targeting and activation of cytotoxic lymphocytes. Chem Immunol. 1989;47:179. [PubMed] [Google Scholar]
  • 87.Selvaraj PM, Plunkett L, Dustin M, Sanders ME, Shaw S, Springer TA. The T lymphocyte glycoprotein CD2 binds the cell surface ligand LFA-3. Nature. 1987;326:400. doi: 10.1038/326400a0. [DOI] [PubMed] [Google Scholar]
  • 88.Shaw S, Luce GEG, Quinones R, Gress RE, Springer TA, Sanders ME. Two antigen-independent adhesion pathways used by human cytotoxic T-cell clones. Nature. 1986;323:262. doi: 10.1038/323262a0. [DOI] [PubMed] [Google Scholar]
  • 89.Siciliano RF, Pratt JC, Schmidt RE, Ritz J, Reinherz EL. Activation of cytolytic T lymphocytes and natural killer cell function through the T11 sheep erythrocyte binding protein. Nature. 1985;317:428. doi: 10.1038/317428a0. [DOI] [PubMed] [Google Scholar]
  • 90.Sim GK, Yague J, Nelson J, Marrack P, Palmer E, Augustin A, Kappler J. Primary structure of human T cell receptor α chain. Nature. 1984;312:771. doi: 10.1038/312771a0. [DOI] [PubMed] [Google Scholar]
  • 91.Siu G, Clark SP, Yoshikai Y, Malissen M, Yanagi Y, Strauss E, Mak TW, Hood L. The human T cell antigen receptor is encoded by variable, diversity, and joining gene segments that rearrange to generate a complete V gene. Cell. 1984;37:393. doi: 10.1016/0092-8674(84)90369-6. [DOI] [PubMed] [Google Scholar]
  • 92.Sleckman BP, Peterson A, Jones WK, Foran JA, Greenstein JL, Seed B, Burakoff SJ. Expression and function of CD4 in a murine T cell hybridoma. Nature. 1987;328:626. doi: 10.1038/328351a0. [DOI] [PubMed] [Google Scholar]
  • 93.Spits H, Yssel H, Voordouw A, de Vries JE. The role of T8 in the cytotoxic T lymphocyte lines specific for class II and class I major histocompability complex antigens. J Immunol. 1985;134:2294. [PubMed] [Google Scholar]
  • 94.Spits H, Schooten W, Keizer H, van Seventer G, van de Rijn M, Terhorst C, de Vries JE. Alloantigen recognition is preceeded by nonspecific adhesion of cytotoxic T cells and target cells. Science. 1986;232:403. doi: 10.1126/science.3485822. [DOI] [PubMed] [Google Scholar]
  • 95.Spits H, Yssel H, de Vries JE. Analysis of specificity of human TCRγδ+ T cells. Res Immunol. 1990;141:636. doi: 10.1016/0923-2494(90)90073-8. [DOI] [PubMed] [Google Scholar]
  • 96.Springer TA, Dustin ML, Hishimoto TK, Marlin SD. The lymphocyte function associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Annu Rev Immunol. 1987;5:223. doi: 10.1146/annurev.iy.05.040187.001255. [DOI] [PubMed] [Google Scholar]
  • 97.Staertz UD, Kanagawa O, Bevan MJ. Hybrid antibodies can target sites for attack by T-cells. Nature. 1985;314:628. doi: 10.1038/314628a0. [DOI] [PubMed] [Google Scholar]
  • 98.Staunton DE, Dustin ML, Springer TA. Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1. Nature. 1989;339:61. doi: 10.1038/339061a0. [DOI] [PubMed] [Google Scholar]
  • 99.Sturm E, Braakman E, Bontrop RE, Chuchana P, Van de Griend RJ, Koning F, Lefranc MP, Bolhuis RLH. Coordinated Vγ and Vδ genesegment rearrangements in human T-cell receptor γδ lymphocytes. Eur J Immunol. 1989;19:1261. doi: 10.1002/eji.1830190717. [DOI] [PubMed] [Google Scholar]
  • 100.Sturm E, Braakman E, Fisch P, Vreugdenhil RJ, Sondel P, Bolhuis RLH. Human Vγ9-Vδ2 T cell receptor — γδ lymphocytes show specificity to Daudi Burkitt's lymphoma cells. J Immunol. 1990;145:3202. [PubMed] [Google Scholar]
  • 101.Swain SL. T cell subsets and the recognition of MHC class. Immunol Rev. 1983;74:129. doi: 10.1111/j.1600-065x.1983.tb01087.x. [DOI] [PubMed] [Google Scholar]
  • 102.Titus JA, Garrido MA, Hecht TT, Winkler DF, Wunderlich JR, Segal DM. Human T-cells targeted with anti-T3 cross-linked to antitumor antibody prevent tumor growth in nude mice. Immunology. 1987;138:4018. [PubMed] [Google Scholar]
  • 103.Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187. doi: 10.1016/S0065-2776(08)60664-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Trinchieri G, Matsumoto-Kobayashi M, Clark SC, Sheera J, London L, Perussia B. Response of resting human peripheral blood natural killer cells to interleukin-2. J Exp Med. 1984;160:1147. doi: 10.1084/jem.160.4.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Van de Griend RJ, Bolhuis RLH, Stoter G, Roozemond R. Regulation of cytolytic activity in CD3− and CD3+ killer cell clones by monoclonal antibodies (anti-CD16, anti-CD2, anti-CD3) depends on the subclass specificity of target cell IgG-FcR. J Immunol. 1987;138:3137. [PubMed] [Google Scholar]
  • 106.Van de Griend RJ, Tax WJM, Van Krimpen BA, Vreugdenhil RJ, Ronteltap CPM, Bolhuis RLH. Lysis of tumor cells by CD3+ 4−8−16+ T cell receptor αβ clones, regulated via CD3 and CD16 activation sites, recombinant interleukin 2 and interferon β. J Immunol. 1987;138:1627. [PubMed] [Google Scholar]
  • 107.Van Dijk J, Tsuruo T, Segal DM, Bolhuis RLH, Colognola R, Van de Griend RJ, Fleuren GJ, Warnaar SO. Bispecific antibodies reactive with the multidrug-resistance-related glycoprotein and CD3 induce lysis of multidrug-resistant tumor cells. Int J Cancer. 1989;44:738. doi: 10.1002/ijc.2910440431. [DOI] [PubMed] [Google Scholar]
  • 108.Van Dijk J, Warnaar SO, Van Eendenburg JDH, Thienpont M, Braakman E, Boot JHA, Fleuren GJ, Bolhuis RLH. Induction of tumor-cell lysis by bi-specific monoclonal antibodies recognizing renal cell carcinoma and CD3 antigen. Int J Cancer. 1989;43:344. doi: 10.1002/ijc.2910430230. [DOI] [PubMed] [Google Scholar]
  • 109.Van Wauwe J, Goosens J, DeCock W, Kung P, Goldstein G. Suppression of human T cell mitogenesis and E-rosette formation by the monoclonal antibody OKT11A. Immunology. 1981;41:865. [PMC free article] [PubMed] [Google Scholar]
  • 110.Vose BM, White W. Tumour-reactive lymphocytes stimulated in mixed lymphocyte and tumour culture. Cancer Immunol Immunother. 1983;15:227. doi: 10.1007/BF00199170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Werfel T, Uciechowski P, Tetteroo PAT, Kurrle R, Deicher H, Schmidt RE. Activation of cloned human natural killer cells via FcγRIII. J Immunol. 1989;142:1102. [PubMed] [Google Scholar]
  • 112.Wright SC, Bonavida B. Studies on the mechanism of natural killer (NK) cell-mediated cytotoxicity (CMC) release of cytotoxic factors specific for NK-sensitive target cells (NKCF) during coculture of NK effector cells with NK target cells. J Immunol. 1982;129:433. [PubMed] [Google Scholar]
  • 113.Yanagi Y, Yoshikai Y, Leggett K, Clark SP, Aleksander I, Mak TW. A human T cell specific cDNA clone encodes a protein having extensive homology to immunoglobulin domains. Nature. 1984;308:145. doi: 10.1038/308145a0. [DOI] [PubMed] [Google Scholar]
  • 114.Young DEJ, Liu CC. Multiple mechanisms of lymphocytemediated killing. Immunol Today. 1988;9:140. doi: 10.1016/0167-5699(88)91201-7. [DOI] [PubMed] [Google Scholar]

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