DOI: 10.1126/science.1828618. Programmed Cell Death of T Cells Signaled by the T Cell Receptor and the α <sub>3</sub> Domain of Class I MH

Programmed Cell Death of T Cells Signaled by the T Cell Receptor and the α 3 Domain of Class I MH

10.1126/science.1828618

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

As well as being activated or rendered unresponsive, mature T lymphocytes can be deleted, depending on the signals received by the cell. Deletion by programmed cell death (apoptosis) is triggered if a T cell that has received a signal through its T cell receptor complex also receives a signal through the α 3 domain of its class I major histocompatibility complex (MHC) molecule. Such a signal can be delivered by a CD8 molecule, which recognizes the α 3 domain, or by an antibody to this domain. Precursors of both cytotoxic T lymphocytes (CTL's) and T helper cells are sensitive to this signal but become resistant at some point before completing differentiation into functioning CTL's or T helper cells. Because CTL's carry CD8, they can induce cell death in T cells that recognize them. This pathway may be important in both removal of autoreactive T cells and immunoregulation.

Bibliography

Sambhara, S. R., & Miller, R. G. (1991). Programmed Cell Death of T Cells Signaled by the T Cell Receptor and the Î± 3 Domain of Class I MH. Science, 252(5011), 1424â1427.

Authors 2

Suryaprakash R. Sambhara (first)
Richard G. Miller (additional)

References 46 Referenced 155

ALLEN, H, DOMAIN INTERACTIONS OF H-2 CLASS-I ANTIGENS ALTER CYTO-TOXIC T-CELL RECOGNITION SITES, NATURE 309: 279 (1984). (10.1038/309279a0) / NATURE (1984)
ALTEVOGT, P, BIOCHEMICAL-COMPARISON OF HLA-DR MOLECULES DERIVED FROM AUTOLOGOUS HUMAN T-LYMPHOBLASTS AND B-LYMPHOBLASTS, EUROPEAN JOURNAL OF IMMUNOLOGY 10: 908 (1980). (10.1002/eji.1830101204) / EUROPEAN JOURNAL OF IMMUNOLOGY (1980)
AZUMA, E, ROLE OF LYMPHOKINE-ACTIVATED KILLER CELLS AS MEDIATORS OF VETO AND NATURAL SUPPRESSION, JOURNAL OF IMMUNOLOGY 141: 2601 (1988). (10.4049/jimmunol.141.8.2601) / JOURNAL OF IMMUNOLOGY (1988)
BEVAN, M.J., CYTOTOXIC EFFECTS OF ANTIGEN-INDUCED AND MITOGEN-INDUCED T-CELLS ON VARIOUS TARGETS, JOURNAL OF IMMUNOLOGY 114: 559 (1975). (10.4049/jimmunol.114.2_Part_1.559) / JOURNAL OF IMMUNOLOGY (1975)
10.1038/326082a0
CASSELL, D.J., REGULATION OF THE CYTOTOXIC LYMPHOCYTE-T RESPONSE AGAINST QA-1 ALLOANTIGENS, JOURNAL OF IMMUNOLOGY 144: 4075 (1990). (10.4049/jimmunol.144.11.4075) / JOURNAL OF IMMUNOLOGY (1990)
CHARRON, D, JOURNAL OF EXPERIMENTAL MEDICINE 152: 1275 (1980). / JOURNAL OF EXPERIMENTAL MEDICINE (1980)
CLAESSON, M.H., FUNCTIONAL-HETEROGENEITY IN ALLOSPECIFIC CYTO-TOXIC LYMPHOCYTE-T CLONES .1. CTL CLONES EXPRESS STRONG ANTI-SELF SUPPRESSIVE ACTIVITY, JOURNAL OF EXPERIMENTAL MEDICINE 160: 1702 (1984). (10.1084/jem.160.6.1702) / JOURNAL OF EXPERIMENTAL MEDICINE (1984)
CONNOLLY, J.M., RECOGNITION BY CD8 ON CYTOTOXIC LYMPHOCYTES-T IS ABLATED BY SEVERAL SUBSTITUTIONS IN THE CLASS-I ALPHA-3 DOMAIN - CD8 AND THE T-CELL RECEPTOR RECOGNIZE THE SAME CLASS-I MOLECULE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 87: 2137 (1990). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1990)
EVANS, G.A., EXON SHUFFLING - MAPPING POLYMORPHIC DETERMINANTS ON HYBRID MOUSE TRANSPLANTATION ANTIGENS, NATURE 300: 755 (1982). (10.1038/300755a0) / NATURE (1982)
FINK, P.J., VETO CELLS, ANNUAL REVIEW OF IMMUNOLOGY 6: 115 (1988). (10.1146/annurev.iy.06.040188.000555) / ANNUAL REVIEW OF IMMUNOLOGY (1988)
FINK, P.J., STUDIES ON THE MECHANISM OF SUPPRESSION OF PRIMARY CYTO-TOXIC RESPONSES BY CLONED CYTO-TOXIC LYMPHOCYTES-T, JOURNAL OF IMMUNOLOGY 133: 1769 (1984). (10.4049/jimmunol.133.4.1769) / JOURNAL OF IMMUNOLOGY (1984)
FINK, P.J., CLONED CYTOLYTIC T-CELLS CAN SUPPRESS PRIMARY CYTO-TOXIC RESPONSES DIRECTED AGAINST THEM, JOURNAL OF IMMUNOLOGY 133: 1775 (1984). (10.4049/jimmunol.133.4.1775) / JOURNAL OF IMMUNOLOGY (1984)
GRAF, L, EXPRESSION OF IA-ANTIGENS IN A MURINE T-LYMPHOMA VARIANT, MOLECULAR IMMUNOLOGY 22: 1371 (1985). (10.1016/0161-5890(85)90059-8) / MOLECULAR IMMUNOLOGY (1985)
HAMBOR, J.E., CD8 FUNCTIONS AS AN INHIBITORY LIGAND IN MEDIATING THE IMMUNOREGULATORY ACTIVITY OF CD8+ CELLS, JOURNAL OF IMMUNOLOGY 145: 1646 (1990). (10.4049/jimmunol.145.6.1646) / JOURNAL OF IMMUNOLOGY (1990)
10.1084/jem.160.2.452
HEUER, J, FUNCTIONAL-STUDIES ON THE ROLE OF I-A MOLECULES EXPRESSED BY THE ANTIGEN-SPECIFIC T-SUPPRESSOR CELL CLONE HF1, JOURNAL OF IMMUNOLOGY 134: 4031 (1985). (10.4049/jimmunol.134.6.4031) / JOURNAL OF IMMUNOLOGY (1985)
KANAGAWA, O, INHIBITION OF MHC CLASS-II-RESTRICTED T-CELL RESPONSE BY LYT-2 ALLOANTIGEN, JOURNAL OF EXPERIMENTAL MEDICINE 170: 901 (1989). (10.1084/jem.170.3.901) / JOURNAL OF EXPERIMENTAL MEDICINE (1989)
KAPLAN, D.R., AN IMMUNOREGULATORY FUNCTION FOR THE CD8 MOLECULE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 8512 (1989). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1989)
KIZIROGLU, F, INVIVO FUNCTIONAL CLONAL DELETION OF RECIPIENT CD4+ T-HELPER PRECURSOR CELLS THAT CAN RECOGNIZE CLASS-II MHC ON INJECTED DONOR LYMPHOID-CELLS, JOURNAL OF IMMUNOLOGY 146: 1104 (1991). (10.4049/jimmunol.146.4.1104) / JOURNAL OF IMMUNOLOGY (1991)
KO, H.S., IA DETERMINANTS ON STIMULATED HUMAN LYMPHOCYTES-T - OCCURRENCE ON MITOGEN-ACTIVATED AND ANTIGEN-ACTIVATED T-CELLS, JOURNAL OF EXPERIMENTAL MEDICINE 150: 246 (1979). (10.1084/jem.150.2.246) / JOURNAL OF EXPERIMENTAL MEDICINE (1979)
KOCH, N, STRUCTURAL COMPARISON OF I-A ANTIGENS PRODUCED BY A CLONED MURINE T-SUPPRESSOR CELL-LINE WITH B-CELL DERIVED I-A, IMMUNOGENETICS 17: 497 (1983). (10.1007/BF00696873) / IMMUNOGENETICS (1983)
LAFFERTY, K.J., ANNU REV IMMUNOL 1: 119 (1983). (10.1146/annurev.iy.01.040183.001003) / ANNU REV IMMUNOL (1983)
10.1073/pnas.84.5.1374
LIE, W.R., PEPTIDE LIGAND-INDUCED CONFORMATION AND SURFACE EXPRESSION OF THE LD CLASS-I MHC MOLECULE, NATURE 344: 439 (1990). (10.1038/344439a0) / NATURE (1990)
MILLER, R.G., QUANTITATIVE-ANALYSIS OF CR-51 RELEASE CYTOTOXICITY ASSAY FOR CYTOTOXIC LYMPHOCYTES, CELLULAR IMMUNOLOGY 14: 284 (1974). (10.1016/0008-8749(74)90212-3) / CELLULAR IMMUNOLOGY (1974)
MILLER, R.G., THE VETO PHENOMENON AND T-CELL REGULATION, IMMUNOLOGY TODAY 7: 112 (1986). (10.1016/0167-5699(86)90151-9) / IMMUNOLOGY TODAY (1986)
MILLER, R.G., CELL-POPULATION IN NU-NU SPLEEN CAN PREVENT GENERATION OF CYTOTOXIC LYMPHOCYTES BY NORMAL SPLEEN-CELLS AGAINST SELF ANTIGENS OF THE NU-NU SPLEEN, JOURNAL OF IMMUNOLOGY 122: 1502 (1979). (10.4049/jimmunol.122.4.1502) / JOURNAL OF IMMUNOLOGY (1979)
MILLER, R.G., AN IMMUNOLOGICAL SUPPRESSOR-CELL INACTIVATING CYTO-TOXIC LYMPHOCYE-T PRECURSOR CELLS RECOGNIZING IT, NATURE 287: 544 (1980). (10.1038/287544a0) / NATURE (1980)
Miller, R. G., Strategies of Immune Regulation: 507 (1980). / Strategies of Immune Regulation (1980)
MUELLER, D.L., CLONAL EXPANSION VERSUS FUNCTIONAL CLONAL INACTIVATION - A COSTIMULATORY SIGNALING PATHWAY DETERMINES THE OUTCOME OF T-CELL ANTIGEN RECEPTOR OCCUPANCY, ANNUAL REVIEW OF IMMUNOLOGY 7: 445 (1989). (10.1146/annurev.iy.07.040189.002305) / ANNUAL REVIEW OF IMMUNOLOGY (1989)
MURAOKA, S, CELLS IN BONE-MARROW AND IN T-CELL COLONIES GROWN FROM BONE-MARROW CAN SUPPRESS GENERATION OF CYTO-TOXIC LYMPHOCYTES-T DIRECTED AGAINST THEIR SELF ANTIGENS, JOURNAL OF EXPERIMENTAL MEDICINE 152: 54 (1980). (10.1084/jem.152.1.54) / JOURNAL OF EXPERIMENTAL MEDICINE (1980)
NAKAMURA, H, INTERLEUKIN-2 ENHANCEMENT OF VETO SUPPRESSOR-CELL FUNCTION IN T-CELL-DEPLETED BONE-MARROW INVITRO AND INVIVO, TRANSPLANTATION 49: 931 (1990). (10.1097/00007890-199005000-00020) / TRANSPLANTATION (1990)
NEWELL, M.K., DEATH OF MATURE T-CELLS BY SEPARATE LIGATION OF CD4 AND THE T-CELL RECEPTOR FOR ANTIGEN, NATURE 347: 286 (1990). (10.1038/347286a0) / NATURE (1990)
OZATO, K, MONOCLONAL-ANTIBODIES TO MOUSE MHC ANTIGENS .3. HYBRIDOMA ANTIBODIES REACTING TO ANTIGENS OF THE H-2B-HAPLOTYPE REVEAL GENETIC-CONTROL OF ISOTYPE EXPRESSION, JOURNAL OF IMMUNOLOGY 126: 317 (1981). (10.4049/jimmunol.126.1.317) / JOURNAL OF IMMUNOLOGY (1981)
OZATO, K, MONOCLONAL-ANTIBODIES TO MOUSE MAJOR HISTOCOMPATIBILITY COMPLEX ANTIGENS .4. A SERIES OF HYBRIDOMA CLONES PRODUCING ANTI-H-2D ANTIBODIES AND AN EXAMINATION OF EXPRESSION OF H-2D ANTIGENS ON THE SURFACE OF THESE CELLS, TRANSPLANTATION 34: 113 (1982). (10.1097/00007890-198209000-00001) / TRANSPLANTATION (1982)
RAMMENSEE, H.G., INTERNATIONAL REVIEWS OF IMMUNOLOGY 4: 175 (1989). (10.3109/08830188909044780) / INTERNATIONAL REVIEWS OF IMMUNOLOGY (1989)
RESKEKUNZ, A.B., CLONED MURINE IA+ BK-BI-2.6.C6 T-CELLS FUNCTION AS ACCESSORY CELLS PRESENTING PROTEIN ANTIGENS TO LONG-TERM-CULTURED ANTIGEN-SPECIFIC T-CELL LINES, JOURNAL OF IMMUNOLOGY 136: 2033 (1986). (10.4049/jimmunol.136.6.2033) / JOURNAL OF IMMUNOLOGY (1986)
SALTER, R.D., A BINDING-SITE FOR THE T-CELL CO-RECEPTOR CD8 ON THE ALPHA-3 DOMAIN OF HLA-A2, NATURE 345: 41 (1990). (10.1038/345041a0) / NATURE (1990)
SAMBHARA S.R. unpublished data.
Sambrook J. Molecular Cloning: A Laboratory Manual 2 E3 (1989).
Shapiro H. M. Practical Flow Cytometry 2: 168 (1988).
SMITH, C.A., ANTIBODIES TO CD3/T-CELL RECEPTOR COMPLEX INDUCE DEATH BY APOPTOSIS IN IMMATURE T-CELLS IN THYMIC CULTURES, NATURE 337: 181 (1989). (10.1038/337181a0) / NATURE (1989)
SWAIN, S.L., T-CELL SUBSETS AND THE RECOGNITION OF MHC CLASS, IMMUNOLOGICAL REVIEWS 74: 129 (1983). (10.1111/j.1600-065X.1983.tb01087.x) / IMMUNOLOGICAL REVIEWS (1983)
TAKAHASHI, T, CLONING OF SELF-MAJOR HISTOCOMPATIBILITY COMPLEX ANTIGEN-SPECIFIC SUPPRESSOR CELLS FROM ADULT BONE-MARROW, JOURNAL OF EXPERIMENTAL MEDICINE 172: 901 (1990). (10.1084/jem.172.3.901) / JOURNAL OF EXPERIMENTAL MEDICINE (1990)
WALLACE, V.A., EUR J IMMUNOL 20: 2471 (1991). / EUR J IMMUNOL (1991)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 6:10 p.m.)
Deposited	1 year, 7 months ago (Jan. 11, 2024, 3:15 p.m.)
Indexed	2 months ago (June 27, 2025, 9:45 a.m.)
Issued	34 years, 2 months ago (June 7, 1991)
Published	34 years, 2 months ago (June 7, 1991)
Published Print	34 years, 2 months ago (June 7, 1991)

Funders 0

None

BibTeX

@article{Sambhara_1991, title={Programmed Cell Death of T Cells Signaled by the T Cell Receptor and the α 3 Domain of Class I MH}, volume={252}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1828618}, DOI={10.1126/science.1828618}, number={5011}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Sambhara, Suryaprakash R. and Miller, Richard G.}, year={1991}, month=jun, pages={1424–1427} }

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      "unstructured": "KANAGAWA, O, INHIBITION OF MHC CLASS-II-RESTRICTED T-CELL RESPONSE BY LYT-2 ALLOANTIGEN, JOURNAL OF EXPERIMENTAL MEDICINE 170: 901 (1989).",
      "journal-title": "JOURNAL OF EXPERIMENTAL MEDICINE"
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      "year": "1989",
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      "DOI": "10.4049/jimmunol.146.4.1104",
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      "year": "1991",
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      "doi-asserted-by": "crossref",
      "first-page": "246",
      "DOI": "10.1084/jem.150.2.246",
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      "year": "1979",
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      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1007/BF00696873",
      "volume": "17",
      "year": "1983",
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    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "119",
      "DOI": "10.1146/annurev.iy.01.040183.001003",
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      "year": "1983",
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      "journal-title": "ANNU REV IMMUNOL"
    },
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      "doi-asserted-by": "crossref",
      "first-page": "439",
      "DOI": "10.1038/344439a0",
      "volume": "344",
      "year": "1990",
      "unstructured": "LIE, W.R., PEPTIDE LIGAND-INDUCED CONFORMATION AND SURFACE EXPRESSION OF THE LD CLASS-I MHC MOLECULE, NATURE 344: 439 (1990).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "284",
      "DOI": "10.1016/0008-8749(74)90212-3",
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      "year": "1974",
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      "journal-title": "CELLULAR IMMUNOLOGY"
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    {
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      "first-page": "112",
      "DOI": "10.1016/0167-5699(86)90151-9",
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      "journal-title": "IMMUNOLOGY TODAY"
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      "key": "e_1_2_1_28_1",
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      "DOI": "10.4049/jimmunol.122.4.1502",
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      "doi-asserted-by": "crossref",
      "first-page": "544",
      "DOI": "10.1038/287544a0",
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      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_30_1",
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      "year": "1980",
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      "journal-title": "Strategies of Immune Regulation"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1146/annurev.iy.07.040189.002305",
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      "year": "1989",
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      "first-page": "54",
      "DOI": "10.1084/jem.152.1.54",
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      "first-page": "931",
      "DOI": "10.1097/00007890-199005000-00020",
      "volume": "49",
      "year": "1990",
      "unstructured": "NAKAMURA, H, INTERLEUKIN-2 ENHANCEMENT OF VETO SUPPRESSOR-CELL FUNCTION IN T-CELL-DEPLETED BONE-MARROW INVITRO AND INVIVO, TRANSPLANTATION 49: 931 (1990).",
      "journal-title": "TRANSPLANTATION"
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      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "286",
      "DOI": "10.1038/347286a0",
      "volume": "347",
      "year": "1990",
      "unstructured": "NEWELL, M.K., DEATH OF MATURE T-CELLS BY SEPARATE LIGATION OF CD4 AND THE T-CELL RECEPTOR FOR ANTIGEN, NATURE 347: 286 (1990).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.4049/jimmunol.126.1.317",
      "volume": "126",
      "year": "1981",
      "unstructured": "OZATO, K, MONOCLONAL-ANTIBODIES TO MOUSE MHC ANTIGENS .3. HYBRIDOMA ANTIBODIES REACTING TO ANTIGENS OF THE H-2B-HAPLOTYPE REVEAL GENETIC-CONTROL OF ISOTYPE EXPRESSION, JOURNAL OF IMMUNOLOGY 126: 317 (1981).",
      "journal-title": "JOURNAL OF IMMUNOLOGY"
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1097/00007890-198209000-00001",
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      "year": "1982",
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      "doi-asserted-by": "crossref",
      "first-page": "175",
      "DOI": "10.3109/08830188909044780",
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      "year": "1989",
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      "journal-title": "INTERNATIONAL REVIEWS OF IMMUNOLOGY"
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      "key": "e_1_2_1_38_1",
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      "first-page": "2033",
      "DOI": "10.4049/jimmunol.136.6.2033",
      "volume": "136",
      "year": "1986",
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      "journal-title": "JOURNAL OF IMMUNOLOGY"
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    {
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      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1038/345041a0",
      "volume": "345",
      "year": "1990",
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      "journal-title": "NATURE"
    },
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      "unstructured": "SAMBHARA S.R. unpublished data."
    },
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      "key": "e_1_2_1_41_1",
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    },
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      "unstructured": "Shapiro H. M. Practical Flow Cytometry 2: 168 (1988)."
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      "doi-asserted-by": "crossref",
      "first-page": "181",
      "DOI": "10.1038/337181a0",
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