DOI: 10.1002/ijc.2910290108. Generation <i>in vitro</i> of HLA‐restricted EB virus‐specific cytotoxic human T cells by autologous lymphoblastoid cell lines: The roles of previous EB virus infection and foetal calf serum

Generation in vitro of HLA‐restricted EB virus‐specific cytotoxic human T cells by autologous lymphoblastoid cell lines: The roles of previous EB virus infection and foetal calf serum

10.1002/ijc.2910290108

Crossref journal-article

Wiley

International Journal of Cancer (311)

Abstract

AbstractThe cytotoxic response of human lymphocytes to the autologous lymphoblastoid cell line (LCL) was investigated with five Epstein‐Barr virus (EBV)‐seropositive and four seronegative donors and an additional donor who seroconverted during the course of the study. LCL stimulation was carried out usually at a stimulator‐to‐responder cell ratio which varied from 1:200 to 1:20,000. Cytotoxic T cells from 7‐ and 14‐day cultures were assayed on autologous and allogeneic LCL target cells and the K562 line, using the 51Cr release assay. Without exception, the cytotoxic T cells generated in 7‐ and 14‐day LCL‐stimulated cultures from seropositive donors were strongly lytic for the autologous LCL. With some donors, the cytotoxic response increased with increasing autologous LCL stimulation, while with others even the lowest level of stimulation induced a potent response. Overall, the cytotoxic T cells generated in cultures from seropositive donors showed a striking preferential lysis of the autologous LCL and cross‐reactive killing of allogeneic LCL target cells matched for certain HLA‐B antigens. Lysis of the K562 line, an indicator target for natural‐killer‐like activity, was consistently negligible. In comparison to the considerable self‐preferred lysis obtained with T cells from LCL‐stimulated cultures, the level of autologous killing by T cells generated in control unstimulated cultures was relatively low. The cytotoxicity patterns obtained with cytotoxic T cells generated in cultures from seronegative donors were markedly different from those obtained with seropositive donors. The level of autologous killing by T cells harvested from LCL‐stimulated cultures was considerably lower than that obtained with seropositive donors and often did not increase above that seen in control cultures, except at the highest stimulatory dose. Moreover, preferential lysis of the autologous LCL target cells by T cells from LCL‐stimulated cultures was essentially due to the foetal calf serum (FCS)‐induced cytotoxicity and there was no obvious HLA‐antigen‐restricted killing of allogeneic target cells. Lysis of K562 target cells was generally more pronounced at the highest level of stimulation than that observed with seropositive donors. The distinctive cytotoxic T‐cell response patterns observed with the seropositive and seronegative donor cultures were both observed with cultures from an individual donor who was tested before and after infectious mononucleosis. Our cytotoxicity data are interpreted as indicating that with LCL‐stimulated cultures from seropositive donors the cytotoxic T‐cell response to autologous LCL is predominantly directed against EBV‐associated antigens and is HLA‐antigen restricted. In contrast, with seronegative donor cultures, the cytotoxic T‐cell response is primarily due to FCS‐induced cytotoxicity, although a response against other LCL‐associated antigens may be superimposed in cultures stimulated with high levels of autologous LCL.

Bibliography

Misko, I. S., Kane, R. G., & Pope, J. H. (1982). Generation in vitro of HLAârestricted EB virusâspecific cytotoxic human T cells by autologous lymphoblastoid cell lines: The roles of previous EB virus infection and foetal calf serum. International Journal of Cancer, 29(1), 41â48. Portico.

Authors 3

I. S. Misko (first)
R. G. Kane (additional)
J. H. Pope (additional)

References 44 Referenced 10

{'key': 'e_1_2_1_2_1', 'first-page': '204s', 'article-title': 'Human cytotoxic T‐cell responses to trinitrophenyl hapten and influenza virus. Diversity of restriction antigens and specificity of HLA‐linked genetic regulation', 'volume': '152', 'author': 'Biddison W. E.', 'year': '1980', 'journal-title': 'J. exp. Med.'} / J. exp. Med. / Human cytotoxic T‐cell responses to trinitrophenyl hapten and influenza virus. Diversity of restriction antigens and specificity of HLA‐linked genetic regulation by Biddison W. E. (1980)
10.1002/ijc.2910270210
10.1111/j.1365-3083.1979.tb02717.x
10.1016/0090-1229(80)90080-X
10.4049/jimmunol.126.5.1697 / J. Immunol. / In vitro induction of HLA‐restricted cytotoxic T lymphocytes against autologous Epstein‐Barr virus transformed B lymphoblastoid cell lines by Fukukawa T. (1981)
10.4049/jimmunol.121.6.2533 / J. Immunol. / Mouse T‐cell mediated cytolysis specifically triggered by cytophilic xenogeneic serum determinants: a caveat for the interpretation of experiments done under syngeneic conditions by Golstein P. (1978)
10.1084/jem.149.6.1537
{'key': 'e_1_2_1_9_1', 'first-page': '1', 'article-title': 'Antibody‐dependent cellular cytotoxicity (ADCC) against Epstein‐Barr virus‐determined membrane antigens. I. Reactivity in sera from normal persons and from patients with acute infectious mononucleosis', 'volume': '25', 'author': 'Jondal M.', 'year': '1976', 'journal-title': 'Clin. exp. Immunol.'} / Clin. exp. Immunol. / Antibody‐dependent cellular cytotoxicity (ADCC) against Epstein‐Barr virus‐determined membrane antigens. I. Reactivity in sera from normal persons and from patients with acute infectious mononucleosis by Jondal M. (1976)
Klein E. Masucci M. G. Berthold W. andBlazar B. Lymphocyte‐mediated cytotoxicity towards virus‐induced tumor cells: natural and activated killer lymphocytes in man. In:Viruses in naturally occurring cancer. Cold Spring Harbor Conferences on Cell Proliferation Vol. 7 1187–1197(1980).
10.1084/jem.143.5.1042
{'key': 'e_1_2_1_12_1', 'first-page': '1393', 'article-title': 'Spontaneous cell‐mediated cytotoxicity and generation of HLA‐unrelated cytotoxic effector cells during MLC in vitro', 'volume': '11', 'author': 'Leibold W.', 'year': '1979', 'journal-title': 'Transplant. Proc.'} / Transplant. Proc. / Spontaneous cell‐mediated cytotoxicity and generation of HLA‐unrelated cytotoxic effector cells during MLC in vitro by Leibold W. (1979)
10.1016/0008-8749(79)90122-9
10.4049/jimmunol.126.2.729 / J. Immunol. / Further characterization of the human autologous mixed leukocyte reaction (MLR) by MacDermott R. P. (1981)
10.4049/jimmunol.124.5.2458 / J. Immunol. / Disappearance of the NK effect after explantation of lymphocytes and generation of similar nonspecific cytotoxicity correlated to the level of blastogenesis in activated cultures by Masucci M. G. (1980)
10.4049/jimmunol.121.6.2165 / J. Immunol. / Generation of cytotoxic lymphocytes in the autologous mixed lymphocyte culture by Miller R. A. (1978)
10.1016/0008-8749(79)90313-7
10.1002/ijc.2910270415
10.1016/0165-2478(81)90055-9
10.1073/pnas.77.7.4247
10.1099/0022-1317-17-2-233
10.1002/ijc.2910150316
10.1002/ijc.2910220604
10.1038/266546a0
10.1002/ijc.2910270505
10.1002/ijc.2910230505
10.1038/283865a0
10.1038/253461a0
10.4049/jimmunol.123.2.584 / J. Immunol. / Specificity and suppressor function of human T cells responsive to autologous non‐T cells by Sakane T. (1979)
10.1073/pnas.75.7.3464
10.1084/jem.149.3.565
10.4049/jimmunol.124.3.1045 / J. Immunol. / In vitro induction of cytotoxic T lymphocytes specific for Epstein‐Barr virus‐transformed cells: kinetics of autologous restimulation by Sugamura K. (1980)
10.4049/jimmunol.125.4.1625 / J. Immunol. / Generation of autoreactive cytotoxic lymphocytes by spontaneously established autologous lymphoblastoid cell line by Sumiya M. (1980)
10.1111/j.1365-3083.1975.tb02680.x
10.4049/jimmunol.125.4.1426 / J. Immunol. / Memory of Epstein‐Barr virus‐specific cytotoxic T cells in normal seropositive adults as revealed by an in vitro restimulation method by Tanaka Y. (1980)
10.4049/jimmunol.124.3.1111 / J. Immunol. / Cytotoxic T cells generated in the autologous mixed lymphocyte reaction. I. Primary autologous mixed lymphocyte reactions by Tomonari K. (1980)
10.4049/jimmunol.126.5.1742 / J. Immunol. / T lymphocyte‐mediated cytotoxicity against autologous EBV‐genome‐bearing B cells by Tsoukas C. D. (1981)
10.1084/jem.146.6.1809
10.4049/jimmunol.123.3.1322 / J. Immunol. / Stimulators and inhibitors of lymphocyte DNA synthesis in supernatants from human lymphoid cell lines by Vesole D. H. (1979)
10.1016/0008-8749(78)90032-1
10.1016/S0008-8749(78)80023-9
{'key': 'e_1_2_1_42_1', 'first-page': '310', 'article-title': 'Lymphocyte transformation induced by autologous cells. III. Lymphoblast‐induced lymphocyte stimulation does not correlate with EB viral antigen expression or immunity', 'volume': '116', 'author': 'Weksler M. E.', 'year': '1976', 'journal-title': 'J. Immunol.'} / J. Immunol. / Lymphocyte transformation induced by autologous cells. III. Lymphoblast‐induced lymphocyte stimulation does not correlate with EB viral antigen expression or immunity by Weksler M. E. (1976)
10.1084/jem.146.6.1833
{'key': 'e_1_2_1_44_1', 'first-page': '3842', 'article-title': 'Fetal calf serum‐induced blastogenic and cytotoxic response of human lymphocytes', 'volume': '36', 'author': 'Zielske J. V.', 'year': '1976', 'journal-title': 'Cancer Res.'} / Cancer Res. / Fetal calf serum‐induced blastogenic and cytotoxic response of human lymphocytes by Zielske J. V. (1976)
10.1016/S0065-2776(08)60262-X

Dates

Type	When
Created	18 years, 6 months ago (Feb. 19, 2007, 1:45 p.m.)
Deposited	1 year, 9 months ago (Nov. 12, 2023, 6:32 a.m.)
Indexed	1 year, 9 months ago (Nov. 12, 2023, 7:34 p.m.)
Issued	43 years, 7 months ago (Jan. 15, 1982)
Published	43 years, 7 months ago (Jan. 15, 1982)
Published Online	19 years, 1 month ago (July 20, 2006)
Published Print	43 years, 7 months ago (Jan. 15, 1982)

Funders 0

None

BibTeX

@article{Misko_1982, title={Generation in vitro of HLA‐restricted EB virus‐specific cytotoxic human T cells by autologous lymphoblastoid cell lines: The roles of previous EB virus infection and foetal calf serum}, volume={29}, ISSN={1097-0215}, url={http://dx.doi.org/10.1002/ijc.2910290108}, DOI={10.1002/ijc.2910290108}, number={1}, journal={International Journal of Cancer}, publisher={Wiley}, author={Misko, I. S. and Kane, R. G. and Pope, J. H.}, year={1982}, month=jan, pages={41–48} }

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