DOI: 10.1002/bies.950151102. Discerning the function of p53 by examining its molecular interactions

Discerning the function of p53 by examining its molecular interactions

10.1002/bies.950151102

Crossref journal-article

Wiley

BioEssays (311)

Abstract

AbstractOf the many genes mutated on the road to tumor formation, few have received as much attention as p53. The gene has come to occupy center stage for the simple reason that it is more frequently altered in human tumors than any other known gene, undergoing mutation at a significant rate in almost every tumor type in which it has been studied. This association between p53 mutation and tumorigenesis has spurred a flurry of research attempting to delineate the normal function of p53 and, by extension, the role of p53 mutation in tumor formation. At the cellular level, p53 has been shown to suppress growth. Recent efforts to further discern the function of p53 have centered on the underlying molecular basis for this growth suppression. In particular, research has focused on the identification of cellular molecules (specifically DNA and proteins) with which the p53 protein associates. p53 has now been shown to bind DNA in a sequence‐specific manner, and mounting evidence suggests that p53 acts as a transcription factor, perhaps regulating the expression levels of genes involved in the inhibition of cell growth. The logical next step in understanding p53 function involves the resolution of two questions: (1) what are the physiological transcriptional targets of p53, and (2) what cellular proteins regulate or mediate the ability of p53 to modulate transcription? Some initial clues to these puzzles are now emerging, and these form the subject of this review.

Bibliography

Oliner, J. D. (1993). Discerning the function of p53 by examining its molecular interactions. BioEssays, 15(11), 703â707. Portico.

Authors 1

Jonathan D. Oliner (first)

References 83 Referenced 21

10.1126/science.1905840
10.1126/science.2649981
10.1126/science.2157286
10.1016/0092-8674(90)90409-8
10.1016/0092-8674(91)90529-8
10.1073/pnas.86.22.8763
10.1016/0092-8674(89)90045-7
10.1126/science.2144057
10.1128/MCB.10.11.5772
10.1073/pnas.79.20.6309
10.1038/356215a0
10.1038/348747a0
10.1126/science.1978757
{'key': 'e_1_2_1_15_2', 'first-page': '6304', 'article-title': 'Participation of p53 protein in the cellular response to DNA damage', 'volume': '53', 'author': 'Kastan M. B.', 'year': '1991', 'journal-title': 'Cancer Res.'} / Cancer Res. / Participation of p53 protein in the cellular response to DNA damage by Kastan M. B. (1991)
10.1073/pnas.89.16.7491
10.1016/0092-8674(92)90593-2
{'key': 'e_1_2_1_18_2', 'first-page': '2212', 'article-title': 'Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents', 'volume': '53', 'author': 'Tishler R. B.', 'year': '1993', 'journal-title': 'Cancer Res.'} / Cancer Res. / Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents by Tishler R. B. (1993)
10.1128/MCB.13.3.1415
10.1073/pnas.89.10.4495
10.1038/362849a0
10.1038/362847a0
10.1073/pnas.87.16.6166
10.1126/science.2047879
10.1038/ng0492-45
10.1128/MCB.12.6.2866
10.1126/science.2144363
10.1126/science.2144364
10.1126/science.256.5058.827
10.1093/nar/20.7.1539
10.1128/MCB.9.10.4196
10.1111/j.1749-6632.1992.tb38657.x
10.1128/MCB.11.2.1009
10.1073/pnas.88.11.4570
10.1101/gad.6.7.1143
10.1073/pnas.88.22.9979
10.1073/pnas.88.17.7605
10.1002/j.1460-2075.1992.tb05375.x
10.1073/pnas.89.24.12028
10.1016/0092-8674(92)90039-F
{'key': 'e_1_2_1_41_2', 'first-page': '1183', 'article-title': 'Wild‐type but not mutant p53 can repress transcription initiation in vitro by interfering with the binding of basal transcription factors to the TATA motif', 'volume': '8', 'author': 'Ragimov N.', 'year': '1993', 'journal-title': 'Oncogene'} / Oncogene / Wild‐type but not mutant p53 can repress transcription initiation in vitro by interfering with the binding of basal transcription factors to the TATA motif by Ragimov N. (1993)
10.1016/S0021-9258(18)53769-8
10.1128/MCB.13.6.3291
10.1038/334037a0
10.1038/334721a0
10.1101/gad.2.6.718
10.1038/363281a0
10.1101/gad.5.11.1946
10.1016/0092-8674(91)90530-C
10.1038/345783a0
10.1073/pnas.88.12.5124
10.1016/0092-8674(91)90188-5
10.1101/gad.5.12b.2441
10.1038/351588a0
10.1016/0092-8674(90)90683-6
10.1016/0092-8674(91)90321-O
{'key': 'e_1_2_1_57_2', 'first-page': '571', 'article-title': 'Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the “hot spot” mutant phenotypes', 'volume': '1', 'author': 'Hinds P. W.', 'year': '1990', 'journal-title': 'Cell Growth Differ.'} / Cell Growth Differ. / Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the “hot spot” mutant phenotypes by Hinds P. W. (1990)
10.1016/0092-8674(92)90644-R
10.1007/BF01535205
10.1002/j.1460-2075.1991.tb07676.x
{'key': 'e_1_2_1_61_2', 'first-page': '495', 'article-title': 'Identification and cloning of a novel amplified DNA sequence in human malignant fibrous histiocytoma derived from a region of chromosome 12 frequently rearranged in soft tissue tumors', 'volume': '2', 'author': 'Meltzer P. S.', 'year': '1991', 'journal-title': 'Cell Growth Differ.'} / Cell Growth Differ. / Identification and cloning of a novel amplified DNA sequence in human malignant fibrous histiocytoma derived from a region of chromosome 12 frequently rearranged in soft tissue tumors by Meltzer P. S. (1991)
10.1073/pnas.83.4.1031
10.1126/science.3563490
10.1016/0165-4608(86)90377-8
10.1038/358080a0
10.1038/362857a0
10.1128/MCB.13.1.301
{'key': 'e_1_2_1_68_2', 'first-page': '2231', 'article-title': 'p53 mutation and MDM2 amplification in human soft tissue sarcomas', 'volume': '53', 'author': 'Leach F. S.', 'year': '1993', 'journal-title': 'Cancer Res.'} / Cancer Res. / p53 mutation and MDM2 amplification in human soft tissue sarcomas by Leach F. S. (1993)
10.1002/j.1460-2075.1993.tb05678.x
10.1073/pnas.82.12.4055
10.1126/science.183.4120.46
10.1073/pnas.87.12.4766
{'key': 'e_1_2_1_73_2', 'first-page': '795', 'article-title': 'p53 interacts with p34cdc2 in mammalian cells: implication for cell cycle control and oncogenesis', 'volume': '5', 'author': 'Sturzbecher H.‐W.', 'year': '1990', 'journal-title': 'Oncogene'} / Oncogene / p53 interacts with p34cdc2 in mammalian cells: implication for cell cycle control and oncogenesis by Sturzbecher H.‐W. (1990)
10.1002/j.1460-2075.1990.tb07524.x
{'key': 'e_1_2_1_75_2', 'first-page': '1519', 'article-title': 'Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression', 'volume': '8', 'author': 'Fiscella M.', 'year': '1993', 'journal-title': 'Oncogene'} / Oncogene / Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression by Fiscella M. (1993)
10.1016/0092-8674(92)90562-Q
10.1038/320182a0
10.1128/MCB.7.8.2863
10.1126/science.1659741
10.1073/pnas.90.11.5100
10.1016/S0065-230X(08)60302-4
10.1016/0092-8674(79)90293-9
10.1038/278261a0
10.1073/pnas.76.5.2420

Dates

Type	When
Created	20 years, 6 months ago (Feb. 25, 2005, 4:15 a.m.)
Deposited	1 year, 10 months ago (Oct. 26, 2023, 3:05 a.m.)
Indexed	1 year, 8 months ago (Dec. 24, 2023, 7:50 p.m.)
Issued	31 years, 10 months ago (Nov. 1, 1993)
Published	31 years, 10 months ago (Nov. 1, 1993)
Published Online	20 years, 6 months ago (Feb. 5, 2005)
Published Print	31 years, 10 months ago (Nov. 1, 1993)

Funders 0

None

BibTeX

@article{Oliner_1993, title={Discerning the function of p53 by examining its molecular interactions}, volume={15}, ISSN={1521-1878}, url={http://dx.doi.org/10.1002/bies.950151102}, DOI={10.1002/bies.950151102}, number={11}, journal={BioEssays}, publisher={Wiley}, author={Oliner, Jonathan D.}, year={1993}, month=nov, pages={703–707} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2023,
        12,
        25
      ]
    ],
    "date-time": "2023-12-25T00:50:52Z",
    "timestamp": 1703465452440
  },
  "reference-count": 83,
  "publisher": "Wiley",
  "issue": "11",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2005,
            2,
            5
          ]
        ],
        "date-time": "2005-02-05T00:00:00Z",
        "timestamp": 1107561600000
      },
      "content-version": "vor",
      "delay-in-days": 4114,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        11
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Of the many genes mutated on the road to tumor formation, few have received as much attention as p53. The gene has come to occupy center stage for the simple reason that it is more frequently altered in human tumors than any other known gene, undergoing mutation at a significant rate in almost every tumor type in which it has been studied. This association between p53 mutation and tumorigenesis has spurred a flurry of research attempting to delineate the normal function of p53 and, by extension, the role of p53 mutation in tumor formation. At the cellular level, p53 has been shown to suppress growth. Recent efforts to further discern the function of p53 have centered on the underlying molecular basis for this growth suppression. In particular, research has focused on the identification of cellular molecules (specifically DNA and proteins) with which the p53 protein associates. p53 has now been shown to bind DNA in a sequence\u2010specific manner, and mounting evidence suggests that p53 acts as a transcription factor, perhaps regulating the expression levels of genes involved in the inhibition of cell growth. The logical next step in understanding p53 function involves the resolution of two questions: (1) what are the physiological transcriptional targets of p53, and (2) what cellular proteins regulate or mediate the ability of p53 to modulate transcription? Some initial clues to these puzzles are now emerging, and these form the subject of this review.</jats:p>",
  "DOI": "10.1002/bies.950151102",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        2,
        25
      ]
    ],
    "date-time": "2005-02-25T09:15:55Z",
    "timestamp": 1109322955000
  },
  "page": "703-707",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 21,
  "title": "Discerning the function of p53 by examining its molecular interactions",
  "prefix": "10.1002",
  "volume": "15",
  "author": [
    {
      "given": "Jonathan D.",
      "family": "Oliner",
      "sequence": "first",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2005,
        2,
        5
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1905840"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2649981"
    },
    {
      "key": "e_1_2_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2157286"
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90409-8"
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90529-8"
    },
    {
      "key": "e_1_2_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.22.8763"
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90045-7"
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2144057"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.10.11.5772"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.79.20.6309"
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/356215a0"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/348747a0"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1978757"
    },
    {
      "key": "e_1_2_1_15_2",
      "first-page": "6304",
      "article-title": "Participation of p53 protein in the cellular response to DNA damage",
      "volume": "53",
      "author": "Kastan M. B.",
      "year": "1991",
      "journal-title": "Cancer Res."
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.16.7491"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90593-2"
    },
    {
      "key": "e_1_2_1_18_2",
      "first-page": "2212",
      "article-title": "Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents",
      "volume": "53",
      "author": "Tishler R. B.",
      "year": "1993",
      "journal-title": "Cancer Res."
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.13.3.1415"
    },
    {
      "key": "e_1_2_1_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.10.4495"
    },
    {
      "key": "e_1_2_1_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/362849a0"
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/362847a0"
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.87.16.6166"
    },
    {
      "key": "e_1_2_1_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2047879"
    },
    {
      "key": "e_1_2_1_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng0492-45"
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.12.6.2866"
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2144363"
    },
    {
      "key": "e_1_2_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2144364"
    },
    {
      "key": "e_1_2_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.256.5058.827"
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/20.7.1539"
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.9.10.4196"
    },
    {
      "key": "e_1_2_1_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1749-6632.1992.tb38657.x"
    },
    {
      "key": "e_1_2_1_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.11.2.1009"
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.11.4570"
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.6.7.1143"
    },
    {
      "key": "e_1_2_1_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.22.9979"
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.17.7605"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1992.tb05375.x"
    },
    {
      "key": "e_1_2_1_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.24.12028"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90039-F"
    },
    {
      "key": "e_1_2_1_41_2",
      "first-page": "1183",
      "article-title": "Wild\u2010type but not mutant p53 can repress transcription initiation in vitro by interfering with the binding of basal transcription factors to the TATA motif",
      "volume": "8",
      "author": "Ragimov N.",
      "year": "1993",
      "journal-title": "Oncogene"
    },
    {
      "key": "e_1_2_1_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)53769-8"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.13.6.3291"
    },
    {
      "key": "e_1_2_1_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/334037a0"
    },
    {
      "key": "e_1_2_1_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/334721a0"
    },
    {
      "key": "e_1_2_1_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.2.6.718"
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/363281a0"
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.11.1946"
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90530-C"
    },
    {
      "key": "e_1_2_1_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/345783a0"
    },
    {
      "key": "e_1_2_1_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.12.5124"
    },
    {
      "key": "e_1_2_1_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90188-5"
    },
    {
      "key": "e_1_2_1_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.12b.2441"
    },
    {
      "key": "e_1_2_1_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/351588a0"
    },
    {
      "key": "e_1_2_1_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90683-6"
    },
    {
      "key": "e_1_2_1_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90321-O"
    },
    {
      "key": "e_1_2_1_57_2",
      "first-page": "571",
      "article-title": "Mutant p53 DNA clones from human colon carcinomas cooperate with ras in transforming primary rat cells: a comparison of the \u201chot spot\u201d mutant phenotypes",
      "volume": "1",
      "author": "Hinds P. W.",
      "year": "1990",
      "journal-title": "Cell Growth Differ."
    },
    {
      "key": "e_1_2_1_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90644-R"
    },
    {
      "key": "e_1_2_1_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01535205"
    },
    {
      "key": "e_1_2_1_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1991.tb07676.x"
    },
    {
      "key": "e_1_2_1_61_2",
      "first-page": "495",
      "article-title": "Identification and cloning of a novel amplified DNA sequence in human malignant fibrous histiocytoma derived from a region of chromosome 12 frequently rearranged in soft tissue tumors",
      "volume": "2",
      "author": "Meltzer P. S.",
      "year": "1991",
      "journal-title": "Cell Growth Differ."
    },
    {
      "key": "e_1_2_1_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.83.4.1031"
    },
    {
      "key": "e_1_2_1_63_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3563490"
    },
    {
      "key": "e_1_2_1_64_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-4608(86)90377-8"
    },
    {
      "key": "e_1_2_1_65_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/358080a0"
    },
    {
      "key": "e_1_2_1_66_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/362857a0"
    },
    {
      "key": "e_1_2_1_67_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.13.1.301"
    },
    {
      "key": "e_1_2_1_68_2",
      "first-page": "2231",
      "article-title": "p53 mutation and MDM2 amplification in human soft tissue sarcomas",
      "volume": "53",
      "author": "Leach F. S.",
      "year": "1993",
      "journal-title": "Cancer Res."
    },
    {
      "key": "e_1_2_1_69_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1993.tb05678.x"
    },
    {
      "key": "e_1_2_1_70_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.82.12.4055"
    },
    {
      "key": "e_1_2_1_71_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.183.4120.46"
    },
    {
      "key": "e_1_2_1_72_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.87.12.4766"
    },
    {
      "key": "e_1_2_1_73_2",
      "first-page": "795",
      "article-title": "p53 interacts with p34cdc2 in mammalian cells: implication for cell cycle control and oncogenesis",
      "volume": "5",
      "author": "Sturzbecher H.\u2010W.",
      "year": "1990",
      "journal-title": "Oncogene"
    },
    {
      "key": "e_1_2_1_74_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1990.tb07524.x"
    },
    {
      "key": "e_1_2_1_75_2",
      "first-page": "1519",
      "article-title": "Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression",
      "volume": "8",
      "author": "Fiscella M.",
      "year": "1993",
      "journal-title": "Oncogene"
    },
    {
      "key": "e_1_2_1_76_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90562-Q"
    },
    {
      "key": "e_1_2_1_77_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/320182a0"
    },
    {
      "key": "e_1_2_1_78_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.7.8.2863"
    },
    {
      "key": "e_1_2_1_79_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1659741"
    },
    {
      "key": "e_1_2_1_80_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.90.11.5100"
    },
    {
      "key": "e_1_2_1_81_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0065-230X(08)60302-4"
    },
    {
      "key": "e_1_2_1_82_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(79)90293-9"
    },
    {
      "key": "e_1_2_1_83_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/278261a0"
    },
    {
      "key": "e_1_2_1_84_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.76.5.2420"
    }
  ],
  "container-title": "BioEssays",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fbies.950151102",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/bies.950151102",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        26
      ]
    ],
    "date-time": "2023-10-26T07:05:09Z",
    "timestamp": 1698303909000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/bies.950151102"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        11
      ]
    ]
  },
  "references-count": 83,
  "journal-issue": {
    "issue": "11",
    "published-print": {
      "date-parts": [
        [
          1993,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/bies.950151102"
  ],
  "URL": "http://dx.doi.org/10.1002/bies.950151102",
  "relation": {},
  "ISSN": [
    "0265-9247",
    "1521-1878"
  ],
  "subject": [],
  "container-title-short": "BioEssays",
  "published": {
    "date-parts": [
      [
        1993,
        11
      ]
    ]
  },
  "assertion": [
    {
      "value": "2005-02-05",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}