DOI: 10.1126/science.3262923. 2,3,7,8-Tetrachlorodibenzo- <i>p</i> -Dioxin Kills Immature Thymocytes by Ca <sup>2+</sup> -Mediated Endonuclease Activation

2,3,7,8-Tetrachlorodibenzo- p -Dioxin Kills Immature Thymocytes by Ca 2+ -Mediated Endonuclease Activation

10.1126/science.3262923

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Suspensions of thymocytes from young rats were incubated with 2,3,7,8- tetrachlorodibenzo- p -dioxin (TCDD), which resulted in a sustained increase in cytosolic free Ca 2+ concentration followed by DNA fragmentation and loss of cell viability. Both the Ca 2+ increase and DNA fragmentation were prevented in cells treated with the inhibitor of protein synthesis, cycloheximide, and DNA fragmentation and cell killing were not detected when cells were incubated in a "Ca 2+ -free" medium or pretreated with high concentrations of the calcium probe, quin-2 tetraacetoxymethyl ester. These results indicate that TCDD can kill immature thymocytes by initiating a suicide process similar to that previously described for glucocorticoid hormones.

Bibliography

McConkey, D. J., Hartzell, P., Duddy, S. K., HÃ¥kansson, H., & Orrenius, S. (1988). 2,3,7,8-Tetrachlorodibenzo- p -Dioxin Kills Immature Thymocytes by Ca 2+ -Mediated Endonuclease Activation. Science, 242(4876), 256â259.

Authors 5

David J. McConkey (first)
Pia Hartzell (additional)
Steven K. Duddy (additional)
Helen Håkansson (additional)
Sten Orrenius (additional)

References 30 Referenced 379

BOWEN, D.L., SELECTIVE SUPPRESSIVE EFFECTS OF GLUCOCORTICOIDS ON THE EARLY EVENTS IN THE HUMAN B-CELL ACTIVATION PROCESS, JOURNAL OF IMMUNOLOGY 133: 1885 (1984). (10.4049/jimmunol.133.4.1885) / JOURNAL OF IMMUNOLOGY (1984)
BURTON, K, STUDY OF THE CONDITIONS AND MECHANISM OF THE DIPHENYLAMINE REACTION FOR THE COLORIMETRIC ESTIMATION OF DEOXYRIBONUCLEIC ACID, BIOCHEMICAL JOURNAL 62: 315 (1956). (10.1042/bj0620315) / BIOCHEMICAL JOURNAL (1956)
CANGA, L, HEART AS A TARGET ORGAN IN 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN TOXICITY - DECREASED BETA-ADRENERGIC RESPONSIVENESS AND EVIDENCE OF INCREASED INTRACELLULAR CALCIUM, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 905 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
CEREDIG, R, PRECURSORS OF T-CELL GROWTH-FACTOR PRODUCING CELLS IN THE THYMUS - ONTOGENY, FREQUENCY, AND QUANTITATIVE RECOVERY IN A SUBPOPULATION OF PHENOTYPICALLY MATURE THYMOCYTES DEFINED BY MONOCLONAL ANTIBODY-GK-1.5, JOURNAL OF EXPERIMENTAL MEDICINE 158: 1654 (1983). (10.1084/jem.158.5.1654) / JOURNAL OF EXPERIMENTAL MEDICINE (1983)
CHANDLER, V.L., DNA-SEQUENCES BOUND SPECIFICALLY BY GLUCOCORTICOID RECEPTOR INVITRO RENDER A HETEROLOGOUS PROMOTER HORMONE RESPONSIVE INVIVO, CELL 33: 489 (1983). (10.1016/0092-8674(83)90430-0) / CELL (1983)
COHEN, J.J., GLUCOCORTICOID ACTIVATION OF A CALCIUM-DEPENDENT ENDONUCLEASE IN THYMOCYTE NUCLEI LEADS TO CELL-DEATH, JOURNAL OF IMMUNOLOGY 132: 38 (1984). (10.4049/jimmunol.132.1.38) / JOURNAL OF IMMUNOLOGY (1984)
DUKE, R.C., DIFFERENCES IN TARGET-CELL DNA FRAGMENTATION INDUCED BY MOUSE CYTOTOXIC LYMPHOCYTES-T AND NATURAL-KILLER-CELLS, JOURNAL OF IMMUNOLOGY 137: 1442 (1986). (10.4049/jimmunol.137.5.1442) / JOURNAL OF IMMUNOLOGY (1986)
Duke, R. C., Proceedings of the National Academy of Sciences of the United States of America 80: 6361 (1983). / Proceedings of the National Academy of Sciences of the United States of America (1983)
GREENLEE, W.F., EVIDENCE FOR DIRECT ACTION OF 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN (TCDD) ON THYMIC EPITHELIUM, TOXICOLOGY AND APPLIED PHARMACOLOGY 79: 112 (1985). (10.1016/0041-008X(85)90373-4) / TOXICOLOGY AND APPLIED PHARMACOLOGY (1985)
KNUTSON, J.C., 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN - FAILURE TO DEMONSTRATE TOXICITY IN 23 CULTURED-CELL TYPES, TOXICOLOGY AND APPLIED PHARMACOLOGY 54: 377 (1980). (10.1016/0041-008X(80)90163-5) / TOXICOLOGY AND APPLIED PHARMACOLOGY (1980)
LUSTER, M.I., SELECTIVE EFFECTS OF 2,3,7,8-TETRACHLORODIBENZO-P-DIOXIN AND CORTICOSTEROID ON INVITRO LYMPHOCYTE MATURATION, JOURNAL OF IMMUNOLOGY 140: 928 (1988). (10.4049/jimmunol.140.3.928) / JOURNAL OF IMMUNOLOGY (1988)
MCCONKEY D.J. unpublished data.
MCCONNELL, E.E., COMPARATIVE TOXICITY OF CHLORINATED DIBENZO-P-DIOXINS IN MICE AND GUINEA-PIGS, TOXICOLOGY AND APPLIED PHARMACOLOGY 44: 335 (1978). (10.1016/0041-008X(78)90195-3) / TOXICOLOGY AND APPLIED PHARMACOLOGY (1978)
NICOTERA, P, CYSTAMINE INDUCES TOXICITY IN HEPATOCYTES THROUGH THE ELEVATION OF CYTOSOLIC CA-2+ AND THE STIMULATION OF A NONLYSOSOMAL PROTEOLYTIC SYSTEM, JOURNAL OF BIOLOGICAL CHEMISTRY 261: 4628 (1986). / JOURNAL OF BIOLOGICAL CHEMISTRY (1986)
Orrenius, S., Calcium and Cell Function: 186 (1986). / Calcium and Cell Function (1986)
Orrenius S. Oxy-Radicals in Molecular Biology and Pathology (1988).
OSTERGAARD, H.L., CYTOTOXIC LYMPHOCYTE-T MEDIATED LYSIS WITHOUT RELEASE OF SERINE ESTERASE, NATURE 330: 71 (1987). (10.1038/330071a0) / NATURE (1987)
Payvar, F., Proceedings of the National Academy of Sciences of the United States of America 78: 6628 (1981). / Proceedings of the National Academy of Sciences of the United States of America (1981)
POELLINGER, L, MOL MECHANISM STEROI: 755 (1985). / MOL MECHANISM STEROI (1985)
POLAND, A, STEREOSPECIFIC, HIGH AFFINITY BINDING OF 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN BY HEPATIC CYTOSOL - EVIDENCE THAT BINDING SPECIES IS RECEPTOR FOR INDUCTION OF ARYL-HYDROCARBON HYDROXYLASE, JOURNAL OF BIOLOGICAL CHEMISTRY 251: 4936 (1976). (10.1016/S0021-9258(17)33205-2) / JOURNAL OF BIOLOGICAL CHEMISTRY (1976)
POLAND, A, "2,3,7,8-TETRACHLORODIBENZO-P-DIOXIN - SEGREGATION OF TOXICITY WITH THE AH LOCUS, MOLECULAR PHARMACOLOGY 17: 86 (1980). / MOLECULAR PHARMACOLOGY (1980)
ROHOLL, PJM, T-CELL DIFFERENTIATION IN THE RABBIT .2. CON-A AND PHA RESPONSE OF THYMUS, SPLEEN AND LYMPH-NODE CELLS AND OF THYMUS SUBPOPULATIONS - INFLUENCE OF DEXAMETHASONE TREATMENT, THYMUS 5: 167 (1983). / THYMUS (1983)
SCHUETZ, E.G., INDUCTION OF CYTOCHROME-P-450 BY GLUCOCORTICOIDS IN RAT-LIVER .1. EVIDENCE THAT GLUCOCORTICOIDS AND PREGNENOLONE 16-ALPHA-CARBONITRILE REGULATE DEHEPATOCYTES AND IN THE LIVER INVIVO, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 1999 (1984). (10.1016/S0021-9258(17)43507-1) / JOURNAL OF BIOLOGICAL CHEMISTRY (1984)
TRENN, G, EXOCYTOSIS OF CYTOLYTIC GRANULES MAY NOT BE REQUIRED FOR TARGET-CELL LYSIS BY CYTOTOXIC LYMPHOCYTES-T, NATURE 330: 72 (1987). (10.1038/330072a0) / NATURE (1987)
TUCKER, A.N., SUPPRESSION OF B-CELL DIFFERENTIATION BY 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN, MOLECULAR PHARMACOLOGY 29: 372 (1986). / MOLECULAR PHARMACOLOGY (1986)
UCKER, D.S., CYTOTOXIC LYMPHOCYTES-T AND GLUCOCORTICOIDS ACTIVATE AN ENDOGENOUS SUICIDE PROCESS IN TARGET-CELLS, NATURE 327: 62 (1987). (10.1038/327062a0) / NATURE (1987)
VONTSCHARNER, V, CALCIUM FLUXES AND CALCIUM BUFFERING IN HUMAN-NEUTROPHILS, JOURNAL OF BIOLOGICAL CHEMISTRY 261: 10163 (1986). (10.1016/S0021-9258(18)67505-2) / JOURNAL OF BIOLOGICAL CHEMISTRY (1986)
WYLLIE, A.H., INTERNATIONAL REVIEW OF CYTOLOGY 68: 251 (1980). (10.1016/S0074-7696(08)62312-8) / INTERNATIONAL REVIEW OF CYTOLOGY (1980)
WYLLIE, A.H., CHROMATIN CLEAVAGE IN APOPTOSIS - ASSOCIATION WITH CONDENSED CHROMATIN MORPHOLOGY AND DEPENDENCE ON MACROMOLECULAR-SYNTHESIS, JOURNAL OF PATHOLOGY 142: 67 (1984). (10.1002/path.1711420112) / JOURNAL OF PATHOLOGY (1984)
10.1038/284555a0

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 13, 2024, 10:28 p.m.)
Indexed	1 month, 3 weeks ago (July 11, 2025, 6:26 a.m.)
Issued	36 years, 10 months ago (Oct. 14, 1988)
Published	36 years, 10 months ago (Oct. 14, 1988)
Published Print	36 years, 10 months ago (Oct. 14, 1988)

Funders 0

None

BibTeX

@article{McConkey_1988, title={2,3,7,8-Tetrachlorodibenzo- p -Dioxin Kills Immature Thymocytes by Ca 2+ -Mediated Endonuclease Activation}, volume={242}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.3262923}, DOI={10.1126/science.3262923}, number={4876}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={McConkey, David J. and Hartzell, Pia and Duddy, Steven K. and Håkansson, Helen and Orrenius, Sten}, year={1988}, month=oct, pages={256–259} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        11
      ]
    ],
    "date-time": "2025-07-11T10:26:36Z",
    "timestamp": 1752229596505
  },
  "reference-count": 30,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "4876",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1988,
        10,
        14
      ]
    ]
  },
  "abstract": "<jats:p>\n            Suspensions of thymocytes from young rats were incubated with 2,3,7,8- tetrachlorodibenzo-\n            <jats:italic>p</jats:italic>\n            -dioxin (TCDD), which resulted in a sustained increase in cytosolic free Ca\n            <jats:sup>2+</jats:sup>\n            concentration followed by DNA fragmentation and loss of cell viability. Both the Ca\n            <jats:sup>2+</jats:sup>\n            increase and DNA fragmentation were prevented in cells treated with the inhibitor of protein synthesis, cycloheximide, and DNA fragmentation and cell killing were not detected when cells were incubated in a \"Ca\n            <jats:sup>2+</jats:sup>\n            -free\" medium or pretreated with high concentrations of the calcium probe, quin-2 tetraacetoxymethyl ester. These results indicate that TCDD can kill immature thymocytes by initiating a suicide process similar to that previously described for glucocorticoid hormones.\n          </jats:p>",
  "DOI": "10.1126/science.3262923",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T21:21:15Z",
    "timestamp": 1160083275000
  },
  "page": "256-259",
  "source": "Crossref",
  "is-referenced-by-count": 379,
  "title": "2,3,7,8-Tetrachlorodibenzo-\n            <i>p</i>\n            -Dioxin Kills Immature Thymocytes by Ca\n            <sup>2+</sup>\n            -Mediated Endonuclease Activation",
  "prefix": "10.1126",
  "volume": "242",
  "author": [
    {
      "given": "David J.",
      "family": "McConkey",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Toxicology, Karolinska Institutet, Stockholm, Sweden."
        }
      ]
    },
    {
      "given": "Pia",
      "family": "Hartzell",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Toxicology, Karolinska Institutet, Stockholm, Sweden."
        }
      ]
    },
    {
      "given": "Steven K.",
      "family": "Duddy",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Toxicology, Karolinska Institutet, Stockholm, Sweden."
        }
      ]
    },
    {
      "given": "Helen",
      "family": "H\u00e5kansson",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Toxicology, Karolinska Institutet, Stockholm, Sweden."
        }
      ]
    },
    {
      "given": "Sten",
      "family": "Orrenius",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Toxicology, Karolinska Institutet, Stockholm, Sweden."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "1885",
      "DOI": "10.4049/jimmunol.133.4.1885",
      "volume": "133",
      "year": "1984",
      "unstructured": "BOWEN, D.L., SELECTIVE SUPPRESSIVE EFFECTS OF GLUCOCORTICOIDS ON THE EARLY EVENTS IN THE HUMAN B-CELL ACTIVATION PROCESS, JOURNAL OF IMMUNOLOGY 133: 1885 (1984).",
      "journal-title": "JOURNAL OF IMMUNOLOGY"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "315",
      "DOI": "10.1042/bj0620315",
      "volume": "62",
      "year": "1956",
      "unstructured": "BURTON, K, STUDY OF THE CONDITIONS AND MECHANISM OF THE DIPHENYLAMINE REACTION FOR THE COLORIMETRIC ESTIMATION OF DEOXYRIBONUCLEIC ACID, BIOCHEMICAL JOURNAL 62: 315 (1956).",
      "journal-title": "BIOCHEMICAL JOURNAL"
    },
    {
      "key": "e_1_2_1_3_1",
      "first-page": "905",
      "volume": "85",
      "year": "1988",
      "unstructured": "CANGA, L, HEART AS A TARGET ORGAN IN 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN TOXICITY - DECREASED BETA-ADRENERGIC RESPONSIVENESS AND EVIDENCE OF INCREASED INTRACELLULAR CALCIUM, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 905 (1988).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "1654",
      "DOI": "10.1084/jem.158.5.1654",
      "volume": "158",
      "year": "1983",
      "unstructured": "CEREDIG, R, PRECURSORS OF T-CELL GROWTH-FACTOR PRODUCING CELLS IN THE THYMUS - ONTOGENY, FREQUENCY, AND QUANTITATIVE RECOVERY IN A SUBPOPULATION OF PHENOTYPICALLY MATURE THYMOCYTES DEFINED BY MONOCLONAL ANTIBODY-GK-1.5, JOURNAL OF EXPERIMENTAL MEDICINE 158: 1654 (1983).",
      "journal-title": "JOURNAL OF EXPERIMENTAL MEDICINE"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1016/0092-8674(83)90430-0",
      "volume": "33",
      "year": "1983",
      "unstructured": "CHANDLER, V.L., DNA-SEQUENCES BOUND SPECIFICALLY BY GLUCOCORTICOID RECEPTOR INVITRO RENDER A HETEROLOGOUS PROMOTER HORMONE RESPONSIVE INVIVO, CELL 33: 489 (1983).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "38",
      "DOI": "10.4049/jimmunol.132.1.38",
      "volume": "132",
      "year": "1984",
      "unstructured": "COHEN, J.J., GLUCOCORTICOID ACTIVATION OF A CALCIUM-DEPENDENT ENDONUCLEASE IN THYMOCYTE NUCLEI LEADS TO CELL-DEATH, JOURNAL OF IMMUNOLOGY 132: 38 (1984).",
      "journal-title": "JOURNAL OF IMMUNOLOGY"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "1442",
      "DOI": "10.4049/jimmunol.137.5.1442",
      "volume": "137",
      "year": "1986",
      "unstructured": "DUKE, R.C., DIFFERENCES IN TARGET-CELL DNA FRAGMENTATION INDUCED BY MOUSE CYTOTOXIC LYMPHOCYTES-T AND NATURAL-KILLER-CELLS, JOURNAL OF IMMUNOLOGY 137: 1442 (1986).",
      "journal-title": "JOURNAL OF IMMUNOLOGY"
    },
    {
      "key": "e_1_2_1_8_1",
      "first-page": "6361",
      "volume": "80",
      "year": "1983",
      "unstructured": "Duke, R. C., Proceedings of the National Academy of Sciences of the United States of America 80: 6361 (1983).",
      "journal-title": "Proceedings of the National Academy of Sciences of the United States of America"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "112",
      "DOI": "10.1016/0041-008X(85)90373-4",
      "volume": "79",
      "year": "1985",
      "unstructured": "GREENLEE, W.F., EVIDENCE FOR DIRECT ACTION OF 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN (TCDD) ON THYMIC EPITHELIUM, TOXICOLOGY AND APPLIED PHARMACOLOGY 79: 112 (1985).",
      "journal-title": "TOXICOLOGY AND APPLIED PHARMACOLOGY"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "377",
      "DOI": "10.1016/0041-008X(80)90163-5",
      "volume": "54",
      "year": "1980",
      "unstructured": "KNUTSON, J.C., 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN - FAILURE TO DEMONSTRATE TOXICITY IN 23 CULTURED-CELL TYPES, TOXICOLOGY AND APPLIED PHARMACOLOGY 54: 377 (1980).",
      "journal-title": "TOXICOLOGY AND APPLIED PHARMACOLOGY"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "928",
      "DOI": "10.4049/jimmunol.140.3.928",
      "volume": "140",
      "year": "1988",
      "unstructured": "LUSTER, M.I., SELECTIVE EFFECTS OF 2,3,7,8-TETRACHLORODIBENZO-P-DIOXIN AND CORTICOSTEROID ON INVITRO LYMPHOCYTE MATURATION, JOURNAL OF IMMUNOLOGY 140: 928 (1988).",
      "journal-title": "JOURNAL OF IMMUNOLOGY"
    },
    {
      "key": "e_1_2_1_12_1",
      "unstructured": "MCCONKEY D.J. unpublished data."
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "335",
      "DOI": "10.1016/0041-008X(78)90195-3",
      "volume": "44",
      "year": "1978",
      "unstructured": "MCCONNELL, E.E., COMPARATIVE TOXICITY OF CHLORINATED DIBENZO-P-DIOXINS IN MICE AND GUINEA-PIGS, TOXICOLOGY AND APPLIED PHARMACOLOGY 44: 335 (1978).",
      "journal-title": "TOXICOLOGY AND APPLIED PHARMACOLOGY"
    },
    {
      "key": "e_1_2_1_14_1",
      "first-page": "4628",
      "volume": "261",
      "year": "1986",
      "unstructured": "NICOTERA, P, CYSTAMINE INDUCES TOXICITY IN HEPATOCYTES THROUGH THE ELEVATION OF CYTOSOLIC CA-2+ AND THE STIMULATION OF A NONLYSOSOMAL PROTEOLYTIC SYSTEM, JOURNAL OF BIOLOGICAL CHEMISTRY 261: 4628 (1986).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_15_1",
      "first-page": "186",
      "year": "1986",
      "unstructured": "Orrenius, S., Calcium and Cell Function: 186 (1986).",
      "journal-title": "Calcium and Cell Function"
    },
    {
      "key": "e_1_2_1_16_1",
      "unstructured": "Orrenius S. Oxy-Radicals in Molecular Biology and Pathology (1988)."
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1038/330071a0",
      "volume": "330",
      "year": "1987",
      "unstructured": "OSTERGAARD, H.L., CYTOTOXIC LYMPHOCYTE-T MEDIATED LYSIS WITHOUT RELEASE OF SERINE ESTERASE, NATURE 330: 71 (1987).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_18_1",
      "first-page": "6628",
      "volume": "78",
      "year": "1981",
      "unstructured": "Payvar, F., Proceedings of the National Academy of Sciences of the United States of America 78: 6628 (1981).",
      "journal-title": "Proceedings of the National Academy of Sciences of the United States of America"
    },
    {
      "key": "e_1_2_1_19_1",
      "first-page": "755",
      "year": "1985",
      "unstructured": "POELLINGER, L, MOL MECHANISM STEROI: 755 (1985).",
      "journal-title": "MOL MECHANISM STEROI"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "4936",
      "DOI": "10.1016/S0021-9258(17)33205-2",
      "volume": "251",
      "year": "1976",
      "unstructured": "POLAND, A, STEREOSPECIFIC, HIGH AFFINITY BINDING OF 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN BY HEPATIC CYTOSOL - EVIDENCE THAT BINDING SPECIES IS RECEPTOR FOR INDUCTION OF ARYL-HYDROCARBON HYDROXYLASE, JOURNAL OF BIOLOGICAL CHEMISTRY 251: 4936 (1976).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_21_1",
      "first-page": "86",
      "volume": "17",
      "year": "1980",
      "unstructured": "POLAND, A, \"2,3,7,8-TETRACHLORODIBENZO-P-DIOXIN - SEGREGATION OF TOXICITY WITH THE AH LOCUS, MOLECULAR PHARMACOLOGY 17: 86 (1980).",
      "journal-title": "MOLECULAR PHARMACOLOGY"
    },
    {
      "key": "e_1_2_1_22_1",
      "first-page": "167",
      "volume": "5",
      "year": "1983",
      "unstructured": "ROHOLL, PJM, T-CELL DIFFERENTIATION IN THE RABBIT .2. CON-A AND PHA RESPONSE OF THYMUS, SPLEEN AND LYMPH-NODE CELLS AND OF THYMUS SUBPOPULATIONS - INFLUENCE OF DEXAMETHASONE TREATMENT, THYMUS 5: 167 (1983).",
      "journal-title": "THYMUS"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "1999",
      "DOI": "10.1016/S0021-9258(17)43507-1",
      "volume": "259",
      "year": "1984",
      "unstructured": "SCHUETZ, E.G., INDUCTION OF CYTOCHROME-P-450 BY GLUCOCORTICOIDS IN RAT-LIVER .1. EVIDENCE THAT GLUCOCORTICOIDS AND PREGNENOLONE 16-ALPHA-CARBONITRILE REGULATE DEHEPATOCYTES AND IN THE LIVER INVIVO, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 1999 (1984).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "72",
      "DOI": "10.1038/330072a0",
      "volume": "330",
      "year": "1987",
      "unstructured": "TRENN, G, EXOCYTOSIS OF CYTOLYTIC GRANULES MAY NOT BE REQUIRED FOR TARGET-CELL LYSIS BY CYTOTOXIC LYMPHOCYTES-T, NATURE 330: 72 (1987).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_25_1",
      "first-page": "372",
      "volume": "29",
      "year": "1986",
      "unstructured": "TUCKER, A.N., SUPPRESSION OF B-CELL DIFFERENTIATION BY 2,3,7,8-TETRACHLORODIBENZO-PARA-DIOXIN, MOLECULAR PHARMACOLOGY 29: 372 (1986).",
      "journal-title": "MOLECULAR PHARMACOLOGY"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "62",
      "DOI": "10.1038/327062a0",
      "volume": "327",
      "year": "1987",
      "unstructured": "UCKER, D.S., CYTOTOXIC LYMPHOCYTES-T AND GLUCOCORTICOIDS ACTIVATE AN ENDOGENOUS SUICIDE PROCESS IN TARGET-CELLS, NATURE 327: 62 (1987).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "10163",
      "DOI": "10.1016/S0021-9258(18)67505-2",
      "volume": "261",
      "year": "1986",
      "unstructured": "VONTSCHARNER, V, CALCIUM FLUXES AND CALCIUM BUFFERING IN HUMAN-NEUTROPHILS, JOURNAL OF BIOLOGICAL CHEMISTRY 261: 10163 (1986).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "251",
      "DOI": "10.1016/S0074-7696(08)62312-8",
      "volume": "68",
      "year": "1980",
      "unstructured": "WYLLIE, A.H., INTERNATIONAL REVIEW OF CYTOLOGY 68: 251 (1980).",
      "journal-title": "INTERNATIONAL REVIEW OF CYTOLOGY"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "67",
      "DOI": "10.1002/path.1711420112",
      "volume": "142",
      "year": "1984",
      "unstructured": "WYLLIE, A.H., CHROMATIN CLEAVAGE IN APOPTOSIS - ASSOCIATION WITH CONDENSED CHROMATIN MORPHOLOGY AND DEPENDENCE ON MACROMOLECULAR-SYNTHESIS, JOURNAL OF PATHOLOGY 142: 67 (1984).",
      "journal-title": "JOURNAL OF PATHOLOGY"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/284555a0"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.3262923",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        14
      ]
    ],
    "date-time": "2024-01-14T03:28:05Z",
    "timestamp": 1705202885000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.3262923"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1988,
        10,
        14
      ]
    ]
  },
  "references-count": 30,
  "journal-issue": {
    "issue": "4876",
    "published-print": {
      "date-parts": [
        [
          1988,
          10,
          14
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.3262923"
  ],
  "URL": "http://dx.doi.org/10.1126/science.3262923",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1988,
        10,
        14
      ]
    ]
  }
}