DOI: 10.1091/mbc.11.8.2605. The Yeast<i>TEL1</i>Gene Partially Substitutes for Human<i>ATM</i>in Suppressing Hyperrecombination, Radiation-Induced Apoptosis and Telomere Shortening in A-T Cells

The YeastTEL1Gene Partially Substitutes for HumanATMin Suppressing Hyperrecombination, Radiation-Induced Apoptosis and Telomere Shortening in A-T Cells

10.1091/mbc.11.8.2605

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Homozygous mutations in the human ATM gene lead to a pleiotropic clinical phenotype of ataxia-telangiectasia (A-T) patients and correlating cellular deficiencies in cells derived from A-T donors. Saccharomyces cerevisiae tel1 mutants lacking Tel1p, which is the closest sequence homologue to the ATM protein, share some of the cellular defects with A-T. Through genetic complementation of A-T cells with the yeast TEL1 gene, we provide evidence that Tel1p can partially compensate for ATM in suppressing hyperrecombination, radiation-induced apoptosis, and telomere shortening. Complementation appears to be independent of p53 activation. The data provided suggest that TEL1 is a functional homologue of human ATM in yeast, and they help to elucidate different cellular and biochemical pathways in human cells regulated by the ATM protein.

Bibliography

Fritz, E., Friedl, A. A., Zwacka, R. M., Eckardt-Schupp, F., & Meyn, M. S. (2000). The YeastTEL1Gene Partially Substitutes for HumanATMin Suppressing Hyperrecombination, Radiation-Induced Apoptosis and Telomere Shortening in A-T Cells. Molecular Biology of the Cell, 11(8), 2605â2616.

Authors 5

Eberhard Fritz (first)
Anna A. Friedl (additional)
Ralf M. Zwacka (additional)
Friederike Eckardt-Schupp (additional)
M. Stephen Meyn (additional)

References 76 Referenced 23

10.1016/0027-5107(80)90101-3 / Mutat. Res. by Aurias A. (1980)
10.1126/science.281.5383.1674 / Science by Banin S. (1998)
10.1038/387516a0 / Nature by Baskaran R. (1997)
10.1080/09553009414550211 / Int. J. Radiat. Biol. by Beamish H. (1994)
10.1073/pnas.93.26.15075 / Proc. Natl. Acad. Sci. USA by Brush G.S. (1996)
10.1006/excr.1997.3907 / Exp. Cell Res. by Bryan T.M. (1998)
10.1002/j.1460-2075.1995.tb00098.x / EMBO J. by Bryan T.M. (1995)
10.1126/science.281.5383.1677 / Science by Canman C.E. (1998)
10.1016/0027-5107(73)90265-0 / Mutat. Res. by Capizzi R.L. (1972)
10.1016/S0952-7915(99)80074-0 / Curr. Opin. Immunol. by Carney J.P. (1999)
10.1002/(SICI)1097-0142(19990615)85:12<2616::AID-CNCR18>3.0.CO;2-J / Cancer by Chen Z. (1999)
10.1002/j.1460-2075.1992.tb05245.x / EMBO J. by Counter C.M. (1992)
10.1128/JVI.68.5.3410-3414.1994 / J. Virol. by Counter C.M. (1994)
10.1080/095530098142365 / Int. J. Radiat. Biol. by Dikomey E. (1998)
{'key': 'B16', 'first-page': '1400', 'volume': '56', 'author': 'Duchaud E.', 'year': '1996', 'journal-title': 'Cancer Res.'} / Cancer Res. by Duchaud E. (1996)
10.1016/S1097-2765(00)80128-8 / Mol. Cell by Emili A. (1998)
10.1080/095530097144076 / Int. J. Radiat. Biol. by Foray N. (1997)
10.1073/pnas.94.9.4538 / Proc. Natl. Acad. Sci. USA by Fritz E. (1997)
10.1038/336577a0 / Nature by Gatti R.A. (1988)
10.1093/hmg/5.4.433 / Hum. Mol. Genet. by Gilad S. (1996)
10.1016/0092-8674(95)90479-4 / Cell by Greenwell P.W. (1995)
10.1016/0378-1119(89)90189-3 / Gene by Groger R.K. (1989)
10.1016/S0959-437X(97)80125-6 / Curr. Opin. Genet. Dev. by Hoekstra M.F. (1997)
10.1093/nar/19.17.4780 / Nucleic Acids Res. by Ijdo J.W. (1991)
10.1073/pnas.89.11.4952 / Proc. Natl. Acad. Sci. USA by Jimenez G. (1992)
10.1016/S0360-3016(96)00500-7 / Int. J. Radiat. Oncol. Biol. Phys. by Jung M. (1997)
10.1016/0092-8674(92)90593-2 / Cell by Kastan M.B. (1992)
10.1101/gad.10.19.2423 / Genes Dev. by Keegan K.S. (1996)
10.1126/science.270.5233.50 / Science by Keith C.T. (1995)
10.1038/sj.onc.1202571 / Oncogene by Kharbanda S. (1998)
10.1128/MCB.14.2.961 / Mol. Cell. Biol. by Klingelhutz A.J. (1994)
10.1006/bbrc.1999.0389 / Biochem. Biophys. Res. Commun. by Kohli M. (1999)
10.1016/0165-4608(91)90164-P / Cancer Genet. Cytogenet. by Kojis T.L. (1991)
{'key': 'B36', 'first-page': '2707', 'volume': '13', 'author': 'Lakin N.D.', 'year': '1996', 'journal-title': 'Oncogene'} / Oncogene by Lakin N.D. (1996)
{'key': 'B37', 'first-page': '177', 'volume': '15', 'author': 'Lavin M.F.', 'year': '1997', 'journal-title': 'Annu. Rev. Genet.'} / Annu. Rev. Genet. by Lavin M.F. (1997)
10.1093/nar/12.17.6685 / Nucleic Acids. Res. by Leer R.J. (1984)
10.1101/gad.10.11.1310 / Genes Dev. by Li B. (1996)
10.1074/jbc.271.8.4497 / J. Biol. Chem. by Luo C.M. (1996)
10.1073/pnas.83.5.1398 / Proc. Natl. Acad. Sci. USA by Lustig A.J. (1986)
10.1093/genetics/152.4.1501 / Genetics by Matsuura A. (1999)
10.1038/ng0796-350 / Nat. Genet. by Metcalfe J.A. (1996)
{'key': 'B44', 'first-page': '5991', 'volume': '55', 'author': 'Meyn M.S.', 'year': '1995', 'journal-title': 'Cancer Res.'} / Cancer Res. by Meyn M.S. (1995)
10.1126/science.8493577 / Science by Meyn M.S. (1993)
{'key': 'B46', 'first-page': '1206', 'volume': '53', 'author': 'Meyn M.S.', 'year': '1993', 'journal-title': 'Am. J. Hum. Genet.'} / Am. J. Hum. Genet. by Meyn M.S. (1993)
10.1080/09553009414551971 / Int. J. Radiat. Biol. by Meyn M.S. (1994)
10.1034/j.1399-0004.1999.550501.x / Clin Genet. by Meyn M.S. (1999)
{'key': 'B49', 'first-page': '5523', 'volume': '49', 'author': 'Mirzayans R.', 'year': '1989', 'journal-title': 'Cancer Res.'} / Cancer Res. by Mirzayans R. (1989)
10.1128/MCB.17.4.2020 / Mol. Cell. Biol. by Morgan S.E. (1997)
10.1016/0092-8674(95)90480-8 / Cell by Morrow D.M. (1995)
10.1002/j.1460-2075.1994.tb06822.x / EMBO J. by Murnane J.P. (1994)
10.1006/jtbi.1997.0559 / J. Theor. Biol. by Oexle K. (1998)
10.1159/000134069 / Cytogenet. Cell. Genet. by Pandita T.K. (1995)
10.1128/MCB.19.9.6065 / Mol. Cell. Biol. by Ritchie K.B. (1999)
10.1093/hmg/7.10.1555 / Hum. Mol. Genet. by Rotman G. (1998)
10.1128/MCB.16.6.3094 / Mol. Cell. Biol. by Runge K.W. (1996)
10.1126/science.271.5247.357 / Science by Sanchez Y. (1996)
10.1126/science.7792600 / Science. by Savitsky K. (1995)
10.1093/hmg/4.11.2025 / Hum. Mol. Genet. by Savitsky K. (1995)
10.1038/387520a0 / Nature by Shafman T. (1997)
10.1146/annurev.genet.31.1.635 / Annu. Rev. Genet. by Shiloh Y. (1997)
10.1128/jb.178.19.5841-5843.1996 / J. Bacteriol. by Siede W. (1996)
10.2307/3579885 / Radiat. Res. by Sikpi M.O. (1998)
10.1038/sj.onc.1201449 / Oncogene by Smilenov L.B. (1997)
10.1016/S0027-5107(97)00119-X / Mutat. Res. by Sprung C.N. (1997)
10.1128/MCB.17.10.5905 / Mol. Cell. Biol. by Sugimoto K. (1997)
10.1101/gad.10.4.395 / Genes Dev. by Sun Z. (1996)
{'key': 'B69', 'first-page': '4923', 'volume': '58', 'author': 'Takagi M.', 'year': '1998', 'journal-title': 'Cancer Res.'} / Cancer Res. by Takagi M. (1998)
10.1080/09553009414550091 / Int. J. Radiat. Biol. by Taylor A.M. (1994)
{'key': 'B71', 'first-page': '43', 'volume': '4', 'author': 'Uhrhammer N.', 'year': '1999', 'journal-title': 'Int. J. Mol. Med.'} / Int. J. Mol. Med. by Uhrhammer N. (1999)
10.1093/emboj/16.19.6018 / EMBO J. by Vaziri H. (1997)
10.1093/emboj/17.19.5679 / EMBO J. by Vialard J.E. (1998)
10.1038/sj.onc.1201037 / Oncogene by Watters D. (1997)
10.1016/0921-8777(96)00015-8 / Mutat. Res. by Xia S.J. (1996)
10.1074/jbc.273.7.3799 / J. Biol. Chem. by Yuan Z.M. (1998)
10.1073/pnas.94.15.8021 / Proc. Natl. Acad. Sci. USA by Zhang N. (1997)
10.1038/sj.onc.1201319 / Oncogene by Ziv Y. (1997)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 7:57 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:42 p.m.)
Indexed	1 year, 10 months ago (Oct. 7, 2023, 10:13 a.m.)
Issued	25 years ago (Aug. 1, 2000)
Published	25 years ago (Aug. 1, 2000)
Published Print	25 years ago (Aug. 1, 2000)

Funders 0

None

BibTeX

@article{Fritz_2000, title={The YeastTEL1Gene Partially Substitutes for HumanATMin Suppressing Hyperrecombination, Radiation-Induced Apoptosis and Telomere Shortening in A-T Cells}, volume={11}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.11.8.2605}, DOI={10.1091/mbc.11.8.2605}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Fritz, Eberhard and Friedl, Anna A. and Zwacka, Ralf M. and Eckardt-Schupp, Friederike and Meyn, M. Stephen}, editor={Wolffe, Alan P.}, year={2000}, month=aug, pages={2605–2616} }

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      "DOI": "10.1016/0027-5107(80)90101-3",
      "volume": "69",
      "author": "Aurias A.",
      "year": "1980",
      "journal-title": "Mutat. Res."
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      "doi-asserted-by": "crossref",
      "first-page": "1674",
      "DOI": "10.1126/science.281.5383.1674",
      "volume": "281",
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      "year": "1998",
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    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "516",
      "DOI": "10.1038/387516a0",
      "volume": "387",
      "author": "Baskaran R.",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "175",
      "DOI": "10.1080/09553009414550211",
      "volume": "65",
      "author": "Beamish H.",
      "year": "1994",
      "journal-title": "Int. J. Radiat. Biol."
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "15075",
      "DOI": "10.1073/pnas.93.26.15075",
      "volume": "93",
      "author": "Brush G.S.",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "370",
      "DOI": "10.1006/excr.1997.3907",
      "volume": "239",
      "author": "Bryan T.M.",
      "year": "1998",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "4240",
      "DOI": "10.1002/j.1460-2075.1995.tb00098.x",
      "volume": "14",
      "author": "Bryan T.M.",
      "year": "1995",
      "journal-title": "EMBO J."
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "1677",
      "DOI": "10.1126/science.281.5383.1677",
      "volume": "281",
      "author": "Canman C.E.",
      "year": "1998",
      "journal-title": "Science"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1016/0027-5107(73)90265-0",
      "volume": "17",
      "author": "Capizzi R.L.",
      "year": "1972",
      "journal-title": "Mutat. Res."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "443",
      "DOI": "10.1016/S0952-7915(99)80074-0",
      "volume": "11",
      "author": "Carney J.P.",
      "year": "1999",
      "journal-title": "Curr. Opin. Immunol."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "2616",
      "DOI": "10.1002/(SICI)1097-0142(19990615)85:12<2616::AID-CNCR18>3.0.CO;2-J",
      "volume": "85",
      "author": "Chen Z.",
      "year": "1999",
      "journal-title": "Cancer"
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "1921",
      "DOI": "10.1002/j.1460-2075.1992.tb05245.x",
      "volume": "11",
      "author": "Counter C.M.",
      "year": "1992",
      "journal-title": "EMBO J."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "3410",
      "DOI": "10.1128/JVI.68.5.3410-3414.1994",
      "volume": "68",
      "author": "Counter C.M.",
      "year": "1994",
      "journal-title": "J. Virol."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "269",
      "DOI": "10.1080/095530098142365",
      "volume": "73",
      "author": "Dikomey E.",
      "year": "1998",
      "journal-title": "Int. J. Radiat. Biol."
    },
    {
      "key": "B16",
      "first-page": "1400",
      "volume": "56",
      "author": "Duchaud E.",
      "year": "1996",
      "journal-title": "Cancer Res."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1016/S1097-2765(00)80128-8",
      "volume": "2",
      "author": "Emili A.",
      "year": "1998",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "449",
      "DOI": "10.1080/095530097144076",
      "volume": "71",
      "author": "Foray N.",
      "year": "1997",
      "journal-title": "Int. J. Radiat. Biol."
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "4538",
      "DOI": "10.1073/pnas.94.9.4538",
      "volume": "94",
      "author": "Fritz E.",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "577",
      "DOI": "10.1038/336577a0",
      "volume": "336",
      "author": "Gatti R.A.",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1093/hmg/5.4.433",
      "volume": "5",
      "author": "Gilad S.",
      "year": "1996",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "823",
      "DOI": "10.1016/0092-8674(95)90479-4",
      "volume": "82",
      "author": "Greenwell P.W.",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "285",
      "DOI": "10.1016/0378-1119(89)90189-3",
      "volume": "81",
      "author": "Groger R.K.",
      "year": "1989",
      "journal-title": "Gene"
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "170",
      "DOI": "10.1016/S0959-437X(97)80125-6",
      "volume": "7",
      "author": "Hoekstra M.F.",
      "year": "1997",
      "journal-title": "Curr. Opin. Genet. Dev."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "4780",
      "DOI": "10.1093/nar/19.17.4780",
      "volume": "19",
      "author": "Ijdo J.W.",
      "year": "1991",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "4952",
      "DOI": "10.1073/pnas.89.11.4952",
      "volume": "89",
      "author": "Jimenez G.",
      "year": "1992",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "417",
      "DOI": "10.1016/S0360-3016(96)00500-7",
      "volume": "37",
      "author": "Jung M.",
      "year": "1997",
      "journal-title": "Int. J. Radiat. Oncol. Biol. Phys."
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "587",
      "DOI": "10.1016/0092-8674(92)90593-2",
      "volume": "71",
      "author": "Kastan M.B.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "2423",
      "DOI": "10.1101/gad.10.19.2423",
      "volume": "10",
      "author": "Keegan K.S.",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "50",
      "DOI": "10.1126/science.270.5233.50",
      "volume": "270",
      "author": "Keith C.T.",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "3309",
      "DOI": "10.1038/sj.onc.1202571",
      "volume": "17",
      "author": "Kharbanda S.",
      "year": "1998",
      "journal-title": "Oncogene"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "961",
      "DOI": "10.1128/MCB.14.2.961",
      "volume": "14",
      "author": "Klingelhutz A.J.",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "168",
      "DOI": "10.1006/bbrc.1999.0389",
      "volume": "257",
      "author": "Kohli M.",
      "year": "1999",
      "journal-title": "Biochem. Biophys. Res. Commun."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "143",
      "DOI": "10.1016/0165-4608(91)90164-P",
      "volume": "56",
      "author": "Kojis T.L.",
      "year": "1991",
      "journal-title": "Cancer Genet. Cytogenet."
    },
    {
      "key": "B36",
      "first-page": "2707",
      "volume": "13",
      "author": "Lakin N.D.",
      "year": "1996",
      "journal-title": "Oncogene"
    },
    {
      "key": "B37",
      "first-page": "177",
      "volume": "15",
      "author": "Lavin M.F.",
      "year": "1997",
      "journal-title": "Annu. Rev. Genet."
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "6685",
      "DOI": "10.1093/nar/12.17.6685",
      "volume": "12",
      "author": "Leer R.J.",
      "year": "1984",
      "journal-title": "Nucleic Acids. Res."
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "1310",
      "DOI": "10.1101/gad.10.11.1310",
      "volume": "10",
      "author": "Li B.",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "4497",
      "DOI": "10.1074/jbc.271.8.4497",
      "volume": "271",
      "author": "Luo C.M.",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "1398",
      "DOI": "10.1073/pnas.83.5.1398",
      "volume": "83",
      "author": "Lustig A.J.",
      "year": "1986",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B42",
      "doi-asserted-by": "crossref",
      "first-page": "1501",
      "DOI": "10.1093/genetics/152.4.1501",
      "volume": "152",
      "author": "Matsuura A.",
      "year": "1999",
      "journal-title": "Genetics"
    },
    {
      "key": "B43",
      "doi-asserted-by": "crossref",
      "first-page": "350",
      "DOI": "10.1038/ng0796-350",
      "volume": "13",
      "author": "Metcalfe J.A.",
      "year": "1996",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "B44",
      "first-page": "5991",
      "volume": "55",
      "author": "Meyn M.S.",
      "year": "1995",
      "journal-title": "Cancer Res."
    },
    {
      "key": "B45",
      "doi-asserted-by": "crossref",
      "first-page": "1327",
      "DOI": "10.1126/science.8493577",
      "volume": "260",
      "author": "Meyn M.S.",
      "year": "1993",
      "journal-title": "Science"
    },
    {
      "key": "B46",
      "first-page": "1206",
      "volume": "53",
      "author": "Meyn M.S.",
      "year": "1993",
      "journal-title": "Am. J. Hum. Genet."
    },
    {
      "key": "B47",
      "doi-asserted-by": "crossref",
      "first-page": "S141",
      "DOI": "10.1080/09553009414551971",
      "volume": "66",
      "author": "Meyn M.S.",
      "year": "1994",
      "journal-title": "Int. J. Radiat. Biol."
    },
    {
      "key": "B48",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1034/j.1399-0004.1999.550501.x",
      "volume": "55",
      "author": "Meyn M.S.",
      "year": "1999",
      "journal-title": "Clin Genet."
    },
    {
      "key": "B49",
      "first-page": "5523",
      "volume": "49",
      "author": "Mirzayans R.",
      "year": "1989",
      "journal-title": "Cancer Res."
    },
    {
      "key": "B50",
      "doi-asserted-by": "crossref",
      "first-page": "2020",
      "DOI": "10.1128/MCB.17.4.2020",
      "volume": "17",
      "author": "Morgan S.E.",
      "year": "1997",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "B51",
      "doi-asserted-by": "crossref",
      "first-page": "831",
      "DOI": "10.1016/0092-8674(95)90480-8",
      "volume": "82",
      "author": "Morrow D.M.",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "B52",
      "doi-asserted-by": "crossref",
      "first-page": "4953",
      "DOI": "10.1002/j.1460-2075.1994.tb06822.x",
      "volume": "13",
      "author": "Murnane J.P.",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "B53",
      "doi-asserted-by": "crossref",
      "first-page": "369",
      "DOI": "10.1006/jtbi.1997.0559",
      "volume": "190",
      "author": "Oexle K.",
      "year": "1998",
      "journal-title": "J. Theor. Biol."
    },
    {
      "key": "B54",
      "doi-asserted-by": "crossref",
      "first-page": "86",
      "DOI": "10.1159/000134069",
      "volume": "71",
      "author": "Pandita T.K.",
      "year": "1995",
      "journal-title": "Cytogenet. Cell. Genet."
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    {
      "key": "B55",
      "doi-asserted-by": "crossref",
      "first-page": "6065",
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      "author": "Ritchie K.B.",
      "year": "1999",
      "journal-title": "Mol. Cell. Biol."
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    {
      "key": "B56",
      "doi-asserted-by": "crossref",
      "first-page": "1555",
      "DOI": "10.1093/hmg/7.10.1555",
      "volume": "7",
      "author": "Rotman G.",
      "year": "1998",
      "journal-title": "Hum. Mol. Genet."
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    {
      "key": "B57",
      "doi-asserted-by": "crossref",
      "first-page": "3094",
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      "author": "Runge K.W.",
      "year": "1996",
      "journal-title": "Mol. Cell. Biol."
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      "key": "B58",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1126/science.271.5247.357",
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      "author": "Sanchez Y.",
      "year": "1996",
      "journal-title": "Science"
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    {
      "key": "B59",
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      "first-page": "1749",
      "DOI": "10.1126/science.7792600",
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      "author": "Savitsky K.",
      "year": "1995",
      "journal-title": "Science."
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    {
      "key": "B60",
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      "first-page": "2025",
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      "author": "Savitsky K.",
      "year": "1995",
      "journal-title": "Hum. Mol. Genet."
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      "first-page": "520",
      "DOI": "10.1038/387520a0",
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      "author": "Shafman T.",
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    {
      "key": "B62",
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      "author": "Shiloh Y.",
      "year": "1997",
      "journal-title": "Annu. Rev. Genet."
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    {
      "key": "B63",
      "doi-asserted-by": "crossref",
      "first-page": "5841",
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      "volume": "178",
      "author": "Siede W.",
      "year": "1996",
      "journal-title": "J. Bacteriol."
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    {
      "key": "B64",
      "doi-asserted-by": "crossref",
      "first-page": "627",
      "DOI": "10.2307/3579885",
      "volume": "150",
      "author": "Sikpi M.O.",
      "year": "1998",
      "journal-title": "Radiat. Res."
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    {
      "key": "B65",
      "doi-asserted-by": "crossref",
      "first-page": "2659",
      "DOI": "10.1038/sj.onc.1201449",
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      "author": "Smilenov L.B.",
      "year": "1997",
      "journal-title": "Oncogene"
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    {
      "key": "B66",
      "doi-asserted-by": "crossref",
      "first-page": "177",
      "DOI": "10.1016/S0027-5107(97)00119-X",
      "volume": "379",
      "author": "Sprung C.N.",
      "year": "1997",
      "journal-title": "Mutat. Res."
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      "key": "B67",
      "doi-asserted-by": "crossref",
      "first-page": "5905",
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      "author": "Sugimoto K.",
      "year": "1997",
      "journal-title": "Mol. Cell. Biol."
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      "first-page": "395",
      "DOI": "10.1101/gad.10.4.395",
      "volume": "10",
      "author": "Sun Z.",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B69",
      "first-page": "4923",
      "volume": "58",
      "author": "Takagi M.",
      "year": "1998",
      "journal-title": "Cancer Res."
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      "key": "B70",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1080/09553009414550091",
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      "author": "Taylor A.M.",
      "year": "1994",
      "journal-title": "Int. J. Radiat. Biol."
    },
    {
      "key": "B71",
      "first-page": "43",
      "volume": "4",
      "author": "Uhrhammer N.",
      "year": "1999",
      "journal-title": "Int. J. Mol. Med."
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