DOI: 10.1002/bies.950120906. Multiple mechanisms in the regulation of ethanol‐inducible cytochrome P450IIE1

Multiple mechanisms in the regulation of ethanol‐inducible cytochrome P450IIE1

10.1002/bies.950120906

Crossref journal-article

Wiley

BioEssays (311)

Abstract

AbstractCytochrome P450IIE1 is involved in the metabolic activation of many xenobiotics involved with human toxicity. In particular, cellular concentrations of P450IIE1 are significantly induced by the most widely abused drug in our society today, alcohol. As a result, the synthesis and degradation of this form of P450 has significant health consequences. The regulation of the steady‐state concentration of P450IIE1 is an extremely complex process. The enzyme is regulated by transcriptional activation, mRNA stabilization, increased mRNA translatability and decreased protein degradation. The principal mechanism which controls the induction process depends on the chemical nature of the inducer, the age, and the nutritional and hormonal status of the animal. There also appear to be significant sex differences in the expression of P450IIE1. It is entirely possible that the regulation of the enzyme concentration under any given set of conditions will involve all of the mechanisms to different extents.

Bibliography

Koop, D. R., & Tierney, D. J. (1990). Multiple mechanisms in the regulation of ethanolâinducible cytochrome P450IIE1. BioEssays, 12(9), 429â435. Portico.

Authors 2

Dennis R. Koop (first)
Daniel J. Tierney (additional)

References 51 Referenced 168

10.3109/10409239009090607
10.1016/0163-7258(90)90029-2
{'key': 'e_1_2_1_4_2', 'first-page': '243', 'article-title': 'The molecular biology of cytochrome P450s', 'volume': '40', 'author': 'Gonzalez F. J.', 'year': '1989', 'journal-title': 'Pharmacol. Rev.'} / Pharmacol. Rev. / The molecular biology of cytochrome P450s by Gonzalez F. J. (1989)
10.1016/0168-9525(90)90174-5
10.1016/0163-7258(90)90006-N
10.1016/0163-7258(90)90030-6
10.1016/S0021-9258(18)34356-4 / J. Biol. Chem. / Purification and characterization of a unique isozyme of cytochrome P‐450 from liver microsomes of ethanol‐treated rabbits by Koop D. R. (1982)
10.1111/j.1530-0277.1986.tb05179.x
10.1016/S0021-9258(18)68622-3 / J. Biol. Chem. / Organization and differential expression of two highly similar genes in the rabbit alcohol‐inducible cytochrome P‐450 subfamily by Khani S. C. (1988)
10.1016/S0021-9258(17)38768-9 / J. Biol. Chem. / Identification of ethanol inducible P‐450 isozyme 3a as the acetone and acetol monooxygenase of rabbit microsomes by Koop D. R. (1985)
10.1016/0306-4522(90)90154-V
10.1016/0014-5793(85)80790-0
10.1073/pnas.82.12.4065
10.1016/S0021-9258(18)66620-7 / J. Biol. Chem. / Complementary DNA and protein sequences of ethanol‐inducible rat and human cytochrome P‐450s: Transcriptional and post‐transcriptional regulation of the rat enzyme by Song B.‐J. (1986)
10.1111/j.1365-2362.1989.tb00273.x
10.1021/bi00370a001
10.1093/bja/63.1.103
10.1016/S0021-9258(18)68880-5 / J. Biol. Chem. / The rat P450IIE1 gene: Complete intron and exon sequence, chromosome mapping, and correlation of developmental expression with specific 5′ cytosine demethylation by Umeno M. (1988)
{'key': 'e_1_2_1_20_2', 'first-page': '5948', 'article-title': 'Regulation of N‐nitrosodimethylamine demethylase in rat liver and kidney', 'volume': '47', 'author': 'Hong J.', 'year': '1987', 'journal-title': 'Cancer Res.'} / Cancer Res. / Regulation of N‐nitrosodimethylamine demethylase in rat liver and kidney by Hong J. (1987)
{'key': 'e_1_2_1_21_2', 'first-page': 'A2244', 'article-title': 'Serum acetone and P450IIE1 levels in pregnant rats', 'volume': '4', 'author': 'Casazza J. P.', 'year': '1990', 'journal-title': 'FASEB J.'} / FASEB J. / Serum acetone and P450IIE1 levels in pregnant rats by Casazza J. P. (1990)
10.1210/mend-1-8-542
10.1016/0003-9861(88)90610-8
{'key': 'e_1_2_1_24_2', 'first-page': '140', 'article-title': 'Hepatic cytochrome P450j induction in the spontaneously diabetic BB rat', 'volume': '33', 'author': 'Bellward G. D.', 'year': '1988', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Hepatic cytochrome P450j induction in the spontaneously diabetic BB rat by Bellward G. D. (1988)
{'key': 'e_1_2_1_25_2', 'first-page': '119', 'article-title': 'Effect of testosterone and growth hormone treatment on hepatic microsomal P450 expression in the diabetic rat', 'volume': '37', 'author': 'Thummel K. E.', 'year': '1990', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Effect of testosterone and growth hormone treatment on hepatic microsomal P450 expression in the diabetic rat by Thummel K. E. (1990)
{'key': 'e_1_2_1_26_2', 'first-page': '519', 'article-title': 'Effects of vanadate on expression of hepatic cytochrome P450 in streptozotocin‐diabetic expression rats', 'volume': '18', 'author': 'Donahue B. S.', 'year': '1990', 'journal-title': 'Drug Metab. Dispos.'} / Drug Metab. Dispos. / Effects of vanadate on expression of hepatic cytochrome P450 in streptozotocin‐diabetic expression rats by Donahue B. S. (1990)
10.1210/endo-124-6-2954
{'key': 'e_1_2_1_28_2', 'first-page': '716', 'article-title': 'Suppression of hepatic levels of an ethanol‐inducible P‐450DM/j by growth hormone: Relationship between the increased level of P‐450DM/j and depletion of growth hormone in diabetes', 'volume': '36', 'author': 'Yamazoe Y.', 'year': '1989', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Suppression of hepatic levels of an ethanol‐inducible P‐450DM/j by growth hormone: Relationship between the increased level of P‐450DM/j and depletion of growth hormone in diabetes by Yamazoe Y. (1989)
{'key': 'e_1_2_1_29_2', 'first-page': '2973', 'article-title': 'Molecular basis for the sex‐related difference in renal N‐nitrosodimethylamine demethylase in C3H/HeJ mice', 'volume': '49', 'author': 'Hong J.‐Y.', 'year': '1989', 'journal-title': 'Cancer Res.'} / Cancer Res. / Molecular basis for the sex‐related difference in renal N‐nitrosodimethylamine demethylase in C3H/HeJ mice by Hong J.‐Y. (1989)
10.1042/bj2660675
10.1016/0006-291X(88)90520-7
10.1016/0006-291X(90)90976-T
10.1016/S0021-9258(18)94103-7 / J. Biol. Chem. / Induction of rat hepatic N‐nitrosodimethylamine demethylase by acetone is due to protein stabilization by Song B.‐J. (1989)
10.1016/S0006-291X(88)80010-X
10.1002/hep.1840100407
10.1073/pnas.84.3.638
10.1021/bi00406a019
10.1016/0006-2952(81)90131-3
10.1097/00000542-198503000-00008
10.1016/0006-2952(85)90497-6
{'key': 'e_1_2_1_41_2', 'first-page': 'A1972', 'article-title': 'Induction of rat liver P450IIE1 by ethanol involves increased enzyme synthesis', 'volume': '4', 'author': 'Ito Y.', 'year': '1990', 'journal-title': 'FASEB J.'} / FASEB J. / Induction of rat liver P450IIE1 by ethanol involves increased enzyme synthesis by Ito Y. (1990)
10.1016/0006-291X(88)90539-6
10.1002/jcp.1041340302
{'key': 'e_1_2_1_44_2', 'first-page': '173', 'volume-title': 'Mammalian Cytochromes P‐450, Volume II', 'author': 'Watkins P. B.', 'year': '1987'} / Mammalian Cytochromes P‐450, Volume II by Watkins P. B. (1987)
10.3109/00498258909043168
10.3109/03602538909103565
10.1016/B978-0-12-152828-7.50010-X
10.1146/annurev.cb.03.110187.000245
10.1016/0304-4157(90)90003-U
10.1073/pnas.87.8.3225
10.1016/S0021-9258(18)83673-0 / J. Biol. Chem. / Phosphorylation of native 97‐kDA 3‐hydroxy‐3‐methylglutaryl‐coenzyme A reductase from rat liver. Impact on activity and degradation of the enzyme by Parker R. A. (1989)
10.1016/0003-9861(89)90292-0

Dates

Type	When
Created	20 years, 5 months ago (Feb. 25, 2005, 6:23 a.m.)
Deposited	1 year, 10 months ago (Oct. 23, 2023, 1:09 a.m.)
Indexed	3 months ago (May 20, 2025, 7:26 p.m.)
Issued	34 years, 11 months ago (Sept. 1, 1990)
Published	34 years, 11 months ago (Sept. 1, 1990)
Published Online	20 years, 6 months ago (Feb. 5, 2005)
Published Print	34 years, 11 months ago (Sept. 1, 1990)

Funders 0

None

BibTeX

@article{Koop_1990, title={Multiple mechanisms in the regulation of ethanol‐inducible cytochrome P450IIE1}, volume={12}, ISSN={1521-1878}, url={http://dx.doi.org/10.1002/bies.950120906}, DOI={10.1002/bies.950120906}, number={9}, journal={BioEssays}, publisher={Wiley}, author={Koop, Dennis R. and Tierney, Daniel J.}, year={1990}, month=sep, pages={429–435} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        5,
        20
      ]
    ],
    "date-time": "2025-05-20T23:26:59Z",
    "timestamp": 1747783619131
  },
  "reference-count": 51,
  "publisher": "Wiley",
  "issue": "9",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2005,
            2,
            5
          ]
        ],
        "date-time": "2005-02-05T00:00:00Z",
        "timestamp": 1107561600000
      },
      "content-version": "vor",
      "delay-in-days": 5271,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1990,
        9
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Cytochrome P450IIE1 is involved in the metabolic activation of many xenobiotics involved with human toxicity. In particular, cellular concentrations of P450IIE1 are significantly induced by the most widely abused drug in our society today, alcohol. As a result, the synthesis and degradation of this form of P450 has significant health consequences. The regulation of the steady\u2010state concentration of P450IIE1 is an extremely complex process. The enzyme is regulated by transcriptional activation, mRNA stabilization, increased mRNA translatability and decreased protein degradation. The principal mechanism which controls the induction process depends on the chemical nature of the inducer, the age, and the nutritional and hormonal status of the animal. There also appear to be significant sex differences in the expression of P450IIE1. It is entirely possible that the regulation of the enzyme concentration under any given set of conditions will involve all of the mechanisms to different extents.</jats:p>",
  "DOI": "10.1002/bies.950120906",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        2,
        25
      ]
    ],
    "date-time": "2005-02-25T11:23:30Z",
    "timestamp": 1109330610000
  },
  "page": "429-435",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 168,
  "title": "Multiple mechanisms in the regulation of ethanol\u2010inducible cytochrome P450IIE1",
  "prefix": "10.1002",
  "volume": "12",
  "author": [
    {
      "given": "Dennis R.",
      "family": "Koop",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Daniel J.",
      "family": "Tierney",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2005,
        2,
        5
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/10409239009090607"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0163-7258(90)90029-2"
    },
    {
      "key": "e_1_2_1_4_2",
      "first-page": "243",
      "article-title": "The molecular biology of cytochrome P450s",
      "volume": "40",
      "author": "Gonzalez F. J.",
      "year": "1989",
      "journal-title": "Pharmacol. Rev."
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(90)90174-5"
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0163-7258(90)90006-N"
    },
    {
      "key": "e_1_2_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0163-7258(90)90030-6"
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "8472",
      "DOI": "10.1016/S0021-9258(18)34356-4",
      "article-title": "Purification and characterization of a unique isozyme of cytochrome P\u2010450 from liver microsomes of ethanol\u2010treated rabbits",
      "volume": "257",
      "author": "Koop D. R.",
      "year": "1982",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1530-0277.1986.tb05179.x"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "7170",
      "DOI": "10.1016/S0021-9258(18)68622-3",
      "article-title": "Organization and differential expression of two highly similar genes in the rabbit alcohol\u2010inducible cytochrome P\u2010450 subfamily",
      "volume": "263",
      "author": "Khani S. C.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "13607",
      "DOI": "10.1016/S0021-9258(17)38768-9",
      "article-title": "Identification of ethanol inducible P\u2010450 isozyme 3a as the acetone and acetol monooxygenase of rabbit microsomes",
      "volume": "260",
      "author": "Koop D. R.",
      "year": "1985",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(90)90154-V"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(85)80790-0"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.82.12.4065"
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "16 689",
      "DOI": "10.1016/S0021-9258(18)66620-7",
      "article-title": "Complementary DNA and protein sequences of ethanol\u2010inducible rat and human cytochrome P\u2010450s: Transcriptional and post\u2010transcriptional regulation of the rat enzyme",
      "volume": "261",
      "author": "Song B.\u2010J.",
      "year": "1986",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2362.1989.tb00273.x"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00370a001"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bja/63.1.103"
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "4956",
      "DOI": "10.1016/S0021-9258(18)68880-5",
      "article-title": "The rat P450IIE1 gene: Complete intron and exon sequence, chromosome mapping, and correlation of developmental expression with specific 5\u2032 cytosine demethylation",
      "volume": "263",
      "author": "Umeno M.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_20_2",
      "first-page": "5948",
      "article-title": "Regulation of N\u2010nitrosodimethylamine demethylase in rat liver and kidney",
      "volume": "47",
      "author": "Hong J.",
      "year": "1987",
      "journal-title": "Cancer Res."
    },
    {
      "key": "e_1_2_1_21_2",
      "first-page": "A2244",
      "article-title": "Serum acetone and P450IIE1 levels in pregnant rats",
      "volume": "4",
      "author": "Casazza J. P.",
      "year": "1990",
      "journal-title": "FASEB J."
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1210/mend-1-8-542"
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-9861(88)90610-8"
    },
    {
      "key": "e_1_2_1_24_2",
      "first-page": "140",
      "article-title": "Hepatic cytochrome P450j induction in the spontaneously diabetic BB rat",
      "volume": "33",
      "author": "Bellward G. D.",
      "year": "1988",
      "journal-title": "Mol. Pharmacol."
    },
    {
      "key": "e_1_2_1_25_2",
      "first-page": "119",
      "article-title": "Effect of testosterone and growth hormone treatment on hepatic microsomal P450 expression in the diabetic rat",
      "volume": "37",
      "author": "Thummel K. E.",
      "year": "1990",
      "journal-title": "Mol. Pharmacol."
    },
    {
      "key": "e_1_2_1_26_2",
      "first-page": "519",
      "article-title": "Effects of vanadate on expression of hepatic cytochrome P450 in streptozotocin\u2010diabetic expression rats",
      "volume": "18",
      "author": "Donahue B. S.",
      "year": "1990",
      "journal-title": "Drug Metab. Dispos."
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1210/endo-124-6-2954"
    },
    {
      "key": "e_1_2_1_28_2",
      "first-page": "716",
      "article-title": "Suppression of hepatic levels of an ethanol\u2010inducible P\u2010450DM/j by growth hormone: Relationship between the increased level of P\u2010450DM/j and depletion of growth hormone in diabetes",
      "volume": "36",
      "author": "Yamazoe Y.",
      "year": "1989",
      "journal-title": "Mol. Pharmacol."
    },
    {
      "key": "e_1_2_1_29_2",
      "first-page": "2973",
      "article-title": "Molecular basis for the sex\u2010related difference in renal N\u2010nitrosodimethylamine demethylase in C3H/HeJ mice",
      "volume": "49",
      "author": "Hong J.\u2010Y.",
      "year": "1989",
      "journal-title": "Cancer Res."
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj2660675"
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(88)90520-7"
    },
    {
      "key": "e_1_2_1_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(90)90976-T"
    },
    {
      "key": "e_1_2_1_33_2",
      "doi-asserted-by": "crossref",
      "first-page": "3568",
      "DOI": "10.1016/S0021-9258(18)94103-7",
      "article-title": "Induction of rat hepatic N\u2010nitrosodimethylamine demethylase by acetone is due to protein stabilization",
      "volume": "264",
      "author": "Song B.\u2010J.",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-291X(88)80010-X"
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/hep.1840100407"
    },
    {
      "key": "e_1_2_1_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.84.3.638"
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00406a019"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-2952(81)90131-3"
    },
    {
      "key": "e_1_2_1_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00000542-198503000-00008"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-2952(85)90497-6"
    },
    {
      "key": "e_1_2_1_41_2",
      "first-page": "A1972",
      "article-title": "Induction of rat liver P450IIE1 by ethanol involves increased enzyme synthesis",
      "volume": "4",
      "author": "Ito Y.",
      "year": "1990",
      "journal-title": "FASEB J."
    },
    {
      "key": "e_1_2_1_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(88)90539-6"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1041340302"
    },
    {
      "key": "e_1_2_1_44_2",
      "first-page": "173",
      "volume-title": "Mammalian Cytochromes P\u2010450, Volume II",
      "author": "Watkins P. B.",
      "year": "1987"
    },
    {
      "key": "e_1_2_1_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/00498258909043168"
    },
    {
      "key": "e_1_2_1_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/03602538909103565"
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/B978-0-12-152828-7.50010-X"
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.cb.03.110187.000245"
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-4157(90)90003-U"
    },
    {
      "key": "e_1_2_1_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.87.8.3225"
    },
    {
      "key": "e_1_2_1_51_2",
      "doi-asserted-by": "crossref",
      "first-page": "4877",
      "DOI": "10.1016/S0021-9258(18)83673-0",
      "article-title": "Phosphorylation of native 97\u2010kDA 3\u2010hydroxy\u20103\u2010methylglutaryl\u2010coenzyme A reductase from rat liver. Impact on activity and degradation of the enzyme",
      "volume": "264",
      "author": "Parker R. A.",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-9861(89)90292-0"
    }
  ],
  "container-title": "BioEssays",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fbies.950120906",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/bies.950120906",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        23
      ]
    ],
    "date-time": "2023-10-23T05:09:03Z",
    "timestamp": 1698037743000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/bies.950120906"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1990,
        9
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "9",
    "published-print": {
      "date-parts": [
        [
          1990,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/bies.950120906"
  ],
  "URL": "http://dx.doi.org/10.1002/bies.950120906",
  "relation": {},
  "ISSN": [
    "0265-9247",
    "1521-1878"
  ],
  "subject": [],
  "container-title-short": "BioEssays",
  "published": {
    "date-parts": [
      [
        1990,
        9
      ]
    ]
  },
  "assertion": [
    {
      "value": "2005-02-05",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}