DOI: 10.1073/pnas.96.7.3745. A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage

10.1073/pnas.96.7.3745

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Checkpoints maintain the order and fidelity of the eukaryotic cell cycle, and defects in checkpoints contribute to genetic instability and cancer. Much of our current understanding of checkpoints comes from genetic studies conducted in yeast. In the fission yeast Schizosaccharomyces pombe (Sp), SpRad3 is an essential component of both the DNA damage and DNA replication checkpoints. The SpChk1 and SpCds1 protein kinases function downstream of SpRad3. SpChk1 is an effector of the DNA damage checkpoint and, in the absence of SpCds1, serves an essential function in the DNA replication checkpoint. SpCds1 functions in the DNA replication checkpoint and in the S phase DNA damage checkpoint. Human homologs of both SpRad3 and SpChk1 but not SpCds1 have been identified. Here we report the identification of a human cDNA encoding a protein (designated HuCds1) that shares sequence, structural, and functional similarity to SpCds1. HuCds1 was modified by phosphorylation and activated in response to ionizing radiation. It was also modified in response to hydroxyurea treatment. Functional ATM protein was required for HuCds1 modification after ionizing radiation but not after hydroxyurea treatment. Like its fission yeast counterpart, human Cds1 phosphorylated Cdc25C to promote the binding of 14-3-3 proteins. These findings suggest that the checkpoint function of HuCds1 is conserved in yeast and mammals.

Bibliography

Brown, A. L., Lee, C.-H., Schwarz, J. K., Mitiku, N., Piwnica-Worms, H., & Chung, J. H. (1999). A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage. Proceedings of the National Academy of Sciences, 96(7), 3745â3750.

Authors 6

Alexandra L. Brown (first)
Chang-Hun Lee (additional)
Julie K. Schwarz (additional)
Nesanet Mitiku (additional)
Helen Piwnica-Worms (additional)
Jay H. Chung (additional)

References 62 Referenced 202

L H Hartwell, T A Weinert Science 246, 629–634 (1989). (10.1126/science.2683079) / Science by Hartwell L H (1989)
T A Weinert, G L Kiser, L H Hartwell Genes Dev 8, 652–665 (1994). (10.1101/gad.8.6.652) / Genes Dev by Weinert T A (1994)
R Kato, H Ogawa Nucleic Acids Res 22, 3104–3112 (1994). (10.1093/nar/22.15.3104) / Nucleic Acids Res by Kato R (1994)
G Jimenez, J Yucel, R Rowley, S Subramani Proc Natl Acad Sci USA 89, 4952–4956 (1992). (10.1073/pnas.89.11.4952) / Proc Natl Acad Sci USA by Jimenez G (1992)
B L Seaton, J Yucel, P Sunnerhagen, S Subramani Gene 119, 83–89 (1992). (10.1016/0378-1119(92)90069-2) / Gene by Seaton B L (1992)
T Enoch, A M Carr, P Nurse Genes Dev 6, 2035–2046 (1992). (10.1101/gad.6.11.2035) / Genes Dev by Enoch T (1992)
N J Bentley, D A Holtzman, G Flaggs, K S Keegan, A DeMaggio, J C Ford, M Hoekstra, A M Carr EMBO J 15, 6641–6651 (1996). (10.1002/j.1460-2075.1996.tb01054.x) / EMBO J by Bentley N J (1996)
A J Lustig, T D Petes Proc Natl Acad Sci USA 83, 1398–1402 (1986). (10.1073/pnas.83.5.1398) / Proc Natl Acad Sci USA by Lustig A J (1986)
D M Morrow, D A Tagle, Y Shiloh, F S Collins, P Hieter Cell 82, 831–840 (1995). (10.1016/0092-8674(95)90480-8) / Cell by Morrow D M (1995)
P W Greenwell, S L Kronmal, S E Porter, J Gassenhuber, B Obermaier, T D Petes Cell 82, 823–829 (1995). (10.1016/0092-8674(95)90479-4) / Cell by Greenwell P W (1995)
Y Sanchez, B A Desany, W J Jones, Q Liu, B Wang, S J Elledge Science 271, 357–360 (1996). (10.1126/science.271.5247.357) / Science by Sanchez Y (1996)
T Naito, A Matsuura, F Ishikawa Nat Genet 20, 203–206 (1998). (10.1038/2517) / Nat Genet by Naito T (1998)
K Savitsky, S Sfez, D A Tagle, Y Ziv, A Sartiel, F S Collins, Y Shiloh, G Rotman Hum Mol Genet 4, 2025–2032 (1995). (10.1093/hmg/4.11.2025) / Hum Mol Genet by Savitsky K (1995)
K A Cimprich, T B Shin, C T Keith, S L Schreiber Proc Natl Acad Sci USA 93, 2850–2855 (1996). (10.1073/pnas.93.7.2850) / Proc Natl Acad Sci USA by Cimprich K A (1996)
S Banin, L Moyal, S Shieh, Y Taya, C W Anderson, L Chessa, N I Smorodinsky, C Prives, Y Reiss, Y Shiloh, Y Ziv Science 281, 1674–1677 (1998). (10.1126/science.281.5383.1674) / Science by Banin S (1998)
C E Canman, D S Lim, K A Cimprich, Y Taya, K Tamai, K Sakaguchi, E Appella, M B Kastan, J D Siliciano Science 281, 1677–1679 (1998). (10.1126/science.281.5383.1677) / Science by Canman C E (1998)
P A Jeggo, A M Carr, A R Lehmann Trends Genet 14, 312–316 (1998). (10.1016/S0168-9525(98)01511-X) / Trends Genet by Jeggo P A (1998)
W A Cliby, C J Roberts, K A Cimprich, C M Stringer, J R Lamb, S L Schreiber, S H Friend EMBO J 17, 159–169 (1998). (10.1093/emboj/17.1.159) / EMBO J by Cliby W A (1998)
Z Sun, D S Fay, F Marini, M Foiani, D F Stern Genes Dev 10, 395–406 (1996). (10.1101/gad.10.4.395) / Genes Dev by Sun Z (1996)
N Rhind, P Russell Genetics 149, 1729–1737 (1998). (10.1093/genetics/149.4.1729) / Genetics by Rhind N (1998)
M N Boddy, B Furnari, O Mondesert, P Russell Science 280, 909–912 (1998). (10.1126/science.280.5365.909) / Science by Boddy M N (1998)
J M Sidorova, L L Breeden Genes Dev 11, 3032–3045 (1997). (10.1101/gad.11.22.3032) / Genes Dev by Sidorova J M (1997)
Z Zhou, S J Elledge Cell 75, 1119–1127 (1993). (10.1016/0092-8674(93)90321-G) / Cell by Zhou Z (1993)
H D Lindsay, D J Griffiths, R J Edwards, P U Christensen, J M Murray, F Osman, N Walworth, A M Carr Genes Dev 12, 382–395 (1998). (10.1101/gad.12.3.382) / Genes Dev by Lindsay H D (1998)
Y Zeng, K C Forbes, Z Wu, S Moreno, H Piwnica-Worms, T Enoch Nature (London) 395, 507–510 (1998). (10.1038/26766) / Nature (London) by Zeng Y (1998)
T Enoch, P Nurse Cell 60, 665–673 (1990). (10.1016/0092-8674(90)90669-6) / Cell by Enoch T (1990)
P Jin, Y Gu, D O Morgan J Cell Biol 134, 963–970 (1996). (10.1083/jcb.134.4.963) / J Cell Biol by Jin P (1996)
X S Ye, R R Fincher, A Tang, K O’Donnell, S A Osmani EMBO J 15, 3599–3610 (1996). (10.1002/j.1460-2075.1996.tb00729.x) / EMBO J by Ye X S (1996)
C Y Peng, P R Graves, R S Thoma, Z Wu, A S Shaw, H Piwnica-Worms Science 277, 1501–1505 (1997). (10.1126/science.277.5331.1501) / Science by Peng C Y (1997)
A Kumagai, P S Yakowec, W G Dunphy Mol Biol Cell 9, 345–354 (1998). (10.1091/mbc.9.2.345) / Mol Biol Cell by Kumagai A (1998)
H Murakami, H Okayama Nature (London) 374, 817–819 (1995). (10.1038/374817a0) / Nature (London) by Murakami H (1995)
N Walworth, S Davey, D Beach Nature (London) 363, 368–371 (1993). (10.1038/363368a0) / Nature (London) by Walworth N (1993)
F Al-Khodairy, E Fotou, K S Sheldrick, D J F Griffiths, A R Lehmann, A M Carr Mol Biol Cell 5, 147–160 (1994). (10.1091/mbc.5.2.147) / Mol Biol Cell by Al-Khodairy F (1994)
Y Sanchez, C Wong, R S Thoma, R Richman, Z Wu, H Piwnica-Worms, S J Elledge Science 277, 1497–1501 (1997). (10.1126/science.277.5331.1497) / Science by Sanchez Y (1997)
A Kumagai, Z Guo, K H Emami, S X Wang, W G Dunphy J Cell Biol 142, 1559–1569 (1998). (10.1083/jcb.142.6.1559) / J Cell Biol by Kumagai A (1998)
M S Singer, D E Gottschling Science 266, 404–409 (1994). (10.1126/science.7545955) / Science by Singer M S (1994)
S Ogg, B Gabrielli, H Piwnica-Worms J Biol Chem 269, 30461–30469 (1994). (10.1016/S0021-9258(18)43836-7) / J Biol Chem by Ogg S (1994)
C-Y Peng, P R Graves, S Ogg, R S Thoma, M J Byrnes, Z Wu, M Stephenson, H Piwnica-Worms Cell Growth Differ 9, 197–208 (1998). / Cell Growth Differ by Peng C-Y (1998)
D E Gottschling, O M Aparicio, B L Billington, V A Zakian Cell 63, 751–762 (1990). (10.1016/0092-8674(90)90141-Z) / Cell by Gottschling D E (1990)
K W Runge, V A Zakian Mol Cell Biol 16, 3094–3105 (1996). (10.1128/MCB.16.6.3094) / Mol Cell Biol by Runge K W (1996)
O M Aparicio, B L Billington, D E Gottschling Cell 66, 1279–1287 (1991). (10.1016/0092-8674(91)90049-5) / Cell by Aparicio O M (1991)
G Kyrion, K Liu, C Liu, A J Lustig Genes Dev 7, 1146–1159 (1993). (10.1101/gad.7.7a.1146) / Genes Dev by Kyrion G (1993)
J S Thompson, X Ling, M Grunstein Nature (London) 369, 245–247 (1994). (10.1038/369245a0) / Nature (London) by Thompson J S (1994)
D F Stern, P Zheng, D R Beidler, C Zerillo Mol Cell Biol 11, 987–1001 (1991). / Mol Cell Biol by Stern D F (1991)
I Oishi, S Sugiyama, H Otani, H Yamamura, Y Nishida, Y Minami Mech Dev 71, 49–63 (1998). (10.1016/S0925-4773(97)00200-1) / Mech Dev by Oishi I (1998)
D Weigel, H Jackle Cell 63, 455–456 (1990). (10.1016/0092-8674(90)90439-L) / Cell by Weigel D (1990)
K Hofmann, P Bucher Trends Biochem Sci 20, 347–349 (1995). (10.1016/S0968-0004(00)89072-6) / Trends Biochem Sci by Hofmann K (1995)
Z Sun, J Hsiao, D S Fay, D F Stern Science 281, 272–274 (1998). (10.1126/science.281.5374.272) / Science by Sun Z (1998)
D S Fay, Z Sun, D F Stern Curr Genet 31, 97–105 (1997). (10.1007/s002940050181) / Curr Genet by Fay D S (1997)
S M Feller, R Ren, H Hanafusa, D Baltimore Trends Biochem Sci 19, 453–458 (1994). (10.1016/0968-0004(94)90129-5) / Trends Biochem Sci by Feller S M (1994)
R Baskaran, L D Wood, L L Whitaker, C E Canman, S E Morgan, Y Xu, C Barlow, D Baltimore, A Wynshaw-Boris, M B Kastan, J Y Wang Nature (London) 387, 516–519 (1997). (10.1038/387516a0) / Nature (London) by Baskaran R (1997)
T Shafman, K K Khanna, P Kedar, K Spring, S Kozlov, T Yen, K Hobson, M Gatei, N Zhang, D Watters, et al. Nature (London) 387, 520–523 (1997). (10.1038/387520a0) / Nature (London) by Shafman T (1997)
T G Schmidt, J Koepke, R Frank, A Skerra J Mol Biol 255, 753–766 (1996). (10.1006/jmbi.1996.0061) / J Mol Biol by Schmidt T G (1996)
T Weinert Curr Opin Genet Dev 8, 185–193 (1998). (10.1016/S0959-437X(98)80140-8) / Curr Opin Genet Dev by Weinert T (1998)
D Lydall, Y Nikolsky, D K Bishop, T Weinert Nature (London) 383, 840–843 (1996). (10.1038/383840a0) / Nature (London) by Lydall D (1996)
K S McKim, J K Jang, W E Theurkauf, R S Hawley Nature (London) 362, 364–366 (1993). (10.1038/362364a0) / Nature (London) by McKim K S (1993)
L Weber, B Byers Genetics 131, 55–63 (1992). (10.1093/genetics/131.1.55) / Genetics by Weber L (1992)
K S Keegan, D A Holtzman, A W Plug, E R Christenson, E E Brainerd, G Flaggs, N J Bentley, E M Taylor, M S Meyn, S B Moss, et al. Genes Dev 10, 2423–2437 (1996). (10.1101/gad.10.19.2423) / Genes Dev by Keegan K S (1996)
G Flaggs, A W Plug, K M Dunks, K E Mundt, J C Ford, M R Quiggle, E M Taylor, C H Westphal, T Ashley, M F Hoekstra, A M Carr Curr Biol 7, 977–986 (1997). (10.1016/S0960-9822(06)00417-9) / Curr Biol by Flaggs G (1997)
Y Ziv, A Bar-Shira, I Pecker, P Russell, T J Jorgensen, I Tsarfati, Y Shiloh Oncogene 15, 159–167 (1997). (10.1038/sj.onc.1201319) / Oncogene by Ziv Y (1997)
K O Hartley, D Gell, G C Smith, H Zhang, N Divecha, M A Connelly, A Admon, S P Lees-Miller, C W Anderson, S P Jackson Cell 82, 849–856 (1995). (10.1016/0092-8674(95)90482-4) / Cell by Hartley K O (1995)
T Blunt, N J Finnie, G E Taccioli, G C Smith, J Demengeot, T M Gottlieb, R Mizuta, A J Varghese, F W Alt, P A Jeggo, et al. Cell 80, 813–823 (1995). (10.1016/0092-8674(95)90360-7) / Cell by Blunt T (1995)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 10:42 a.m.)
Deposited	3 years, 2 months ago (June 7, 2022, 12:27 a.m.)
Indexed	3 months, 2 weeks ago (May 13, 2025, 12:07 a.m.)
Issued	26 years, 4 months ago (March 30, 1999)
Published	26 years, 4 months ago (March 30, 1999)
Published Online	26 years, 4 months ago (March 30, 1999)
Published Print	26 years, 4 months ago (March 30, 1999)

Funders 0

None

BibTeX

@article{Brown_1999, title={A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage}, volume={96}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.96.7.3745}, DOI={10.1073/pnas.96.7.3745}, number={7}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Brown, Alexandra L. and Lee, Chang-Hun and Schwarz, Julie K. and Mitiku, Nesanet and Piwnica-Worms, Helen and Chung, Jay H.}, year={1999}, month=mar, pages={3745–3750} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        5,
        13
      ]
    ],
    "date-time": "2025-05-13T04:07:43Z",
    "timestamp": 1747109263073
  },
  "reference-count": 62,
  "publisher": "Proceedings of the National Academy of Sciences",
  "issue": "7",
  "content-domain": {
    "domain": [
      "www.pnas.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        3,
        30
      ]
    ]
  },
  "abstract": "<jats:p>\n            Checkpoints maintain the order and fidelity of the eukaryotic cell cycle, and defects in checkpoints contribute to genetic instability and cancer. Much of our current understanding of checkpoints comes from genetic studies conducted in yeast. In the fission yeast\n            <jats:italic>Schizosaccharomyces pombe</jats:italic>\n            (Sp), SpRad3 is an essential component of both the DNA damage and DNA replication checkpoints. The SpChk1 and SpCds1 protein kinases function downstream of SpRad3. SpChk1 is an effector of the DNA damage checkpoint and, in the absence of SpCds1, serves an essential function in the DNA replication checkpoint. SpCds1 functions in the DNA replication checkpoint and in the S phase DNA damage checkpoint. Human homologs of both SpRad3 and SpChk1 but not SpCds1 have been identified. Here we report the identification of a human cDNA encoding a protein (designated HuCds1) that shares sequence, structural, and functional similarity to SpCds1. HuCds1 was modified by phosphorylation and activated in response to ionizing radiation. It was also modified in response to hydroxyurea treatment. Functional ATM protein was required for HuCds1 modification after ionizing radiation but not after hydroxyurea treatment. Like its fission yeast counterpart, human Cds1 phosphorylated Cdc25C to promote the binding of 14-3-3 proteins. These findings suggest that the checkpoint function of HuCds1 is conserved in yeast and mammals.\n          </jats:p>",
  "DOI": "10.1073/pnas.96.7.3745",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T14:42:40Z",
    "timestamp": 1027694560000
  },
  "page": "3745-3750",
  "update-policy": "http://dx.doi.org/10.1073/pnas.cm10313",
  "source": "Crossref",
  "is-referenced-by-count": 202,
  "title": "A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage",
  "prefix": "10.1073",
  "volume": "96",
  "author": [
    {
      "given": "Alexandra L.",
      "family": "Brown",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    },
    {
      "given": "Chang-Hun",
      "family": "Lee",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    },
    {
      "given": "Julie K.",
      "family": "Schwarz",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    },
    {
      "given": "Nesanet",
      "family": "Mitiku",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    },
    {
      "given": "Helen",
      "family": "Piwnica-Worms",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    },
    {
      "given": "Jay H.",
      "family": "Chung",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Building 10-7D13, 10 Center Drive, Bethesda, MD, 20892-1654; and Department of Cell Biology and Physiology and Howard Hughes Medical Institute, Washington University School of Medicine, Box 8228, 660 South Euclid Avenue, St. Louis, MO 63110"
        }
      ]
    }
  ],
  "member": "341",
  "published-online": {
    "date-parts": [
      [
        1999,
        3,
        30
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_3_4_1_2",
      "doi-asserted-by": "crossref",
      "first-page": "629",
      "DOI": "10.1126/science.2683079",
      "volume": "246",
      "author": "Hartwell L H",
      "year": "1989",
      "unstructured": "L H Hartwell, T A Weinert Science 246, 629\u2013634 (1989).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "652",
      "DOI": "10.1101/gad.8.6.652",
      "volume": "8",
      "author": "Weinert T A",
      "year": "1994",
      "unstructured": "T A Weinert, G L Kiser, L H Hartwell Genes Dev 8, 652\u2013665 (1994).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "3104",
      "DOI": "10.1093/nar/22.15.3104",
      "volume": "22",
      "author": "Kato R",
      "year": "1994",
      "unstructured": "R Kato, H Ogawa Nucleic Acids Res 22, 3104\u20133112 (1994).",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "e_1_3_4_4_2",
      "doi-asserted-by": "crossref",
      "first-page": "4952",
      "DOI": "10.1073/pnas.89.11.4952",
      "volume": "89",
      "author": "Jimenez G",
      "year": "1992",
      "unstructured": "G Jimenez, J Yucel, R Rowley, S Subramani Proc Natl Acad Sci USA 89, 4952\u20134956 (1992).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "83",
      "DOI": "10.1016/0378-1119(92)90069-2",
      "volume": "119",
      "author": "Seaton B L",
      "year": "1992",
      "unstructured": "B L Seaton, J Yucel, P Sunnerhagen, S Subramani Gene 119, 83\u201389 (1992).",
      "journal-title": "Gene"
    },
    {
      "key": "e_1_3_4_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "2035",
      "DOI": "10.1101/gad.6.11.2035",
      "volume": "6",
      "author": "Enoch T",
      "year": "1992",
      "unstructured": "T Enoch, A M Carr, P Nurse Genes Dev 6, 2035\u20132046 (1992).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "6641",
      "DOI": "10.1002/j.1460-2075.1996.tb01054.x",
      "volume": "15",
      "author": "Bentley N J",
      "year": "1996",
      "unstructured": "N J Bentley, D A Holtzman, G Flaggs, K S Keegan, A DeMaggio, J C Ford, M Hoekstra, A M Carr EMBO J 15, 6641\u20136651 (1996).",
      "journal-title": "EMBO J"
    },
    {
      "key": "e_1_3_4_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "1398",
      "DOI": "10.1073/pnas.83.5.1398",
      "volume": "83",
      "author": "Lustig A J",
      "year": "1986",
      "unstructured": "A J Lustig, T D Petes Proc Natl Acad Sci USA 83, 1398\u20131402 (1986).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_9_2",
      "doi-asserted-by": "crossref",
      "first-page": "831",
      "DOI": "10.1016/0092-8674(95)90480-8",
      "volume": "82",
      "author": "Morrow D M",
      "year": "1995",
      "unstructured": "D M Morrow, D A Tagle, Y Shiloh, F S Collins, P Hieter Cell 82, 831\u2013840 (1995).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "823",
      "DOI": "10.1016/0092-8674(95)90479-4",
      "volume": "82",
      "author": "Greenwell P W",
      "year": "1995",
      "unstructured": "P W Greenwell, S L Kronmal, S E Porter, J Gassenhuber, B Obermaier, T D Petes Cell 82, 823\u2013829 (1995).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1126/science.271.5247.357",
      "volume": "271",
      "author": "Sanchez Y",
      "year": "1996",
      "unstructured": "Y Sanchez, B A Desany, W J Jones, Q Liu, B Wang, S J Elledge Science 271, 357\u2013360 (1996).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "203",
      "DOI": "10.1038/2517",
      "volume": "20",
      "author": "Naito T",
      "year": "1998",
      "unstructured": "T Naito, A Matsuura, F Ishikawa Nat Genet 20, 203\u2013206 (1998).",
      "journal-title": "Nat Genet"
    },
    {
      "key": "e_1_3_4_13_2",
      "doi-asserted-by": "crossref",
      "first-page": "2025",
      "DOI": "10.1093/hmg/4.11.2025",
      "volume": "4",
      "author": "Savitsky K",
      "year": "1995",
      "unstructured": "K Savitsky, S Sfez, D A Tagle, Y Ziv, A Sartiel, F S Collins, Y Shiloh, G Rotman Hum Mol Genet 4, 2025\u20132032 (1995).",
      "journal-title": "Hum Mol Genet"
    },
    {
      "key": "e_1_3_4_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "2850",
      "DOI": "10.1073/pnas.93.7.2850",
      "volume": "93",
      "author": "Cimprich K A",
      "year": "1996",
      "unstructured": "K A Cimprich, T B Shin, C T Keith, S L Schreiber Proc Natl Acad Sci USA 93, 2850\u20132855 (1996).",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "e_1_3_4_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "1674",
      "DOI": "10.1126/science.281.5383.1674",
      "volume": "281",
      "author": "Banin S",
      "year": "1998",
      "unstructured": "S Banin, L Moyal, S Shieh, Y Taya, C W Anderson, L Chessa, N I Smorodinsky, C Prives, Y Reiss, Y Shiloh, Y Ziv Science 281, 1674\u20131677 (1998).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "1677",
      "DOI": "10.1126/science.281.5383.1677",
      "volume": "281",
      "author": "Canman C E",
      "year": "1998",
      "unstructured": "C E Canman, D S Lim, K A Cimprich, Y Taya, K Tamai, K Sakaguchi, E Appella, M B Kastan, J D Siliciano Science 281, 1677\u20131679 (1998).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_17_2",
      "doi-asserted-by": "crossref",
      "first-page": "312",
      "DOI": "10.1016/S0168-9525(98)01511-X",
      "volume": "14",
      "author": "Jeggo P A",
      "year": "1998",
      "unstructured": "P A Jeggo, A M Carr, A R Lehmann Trends Genet 14, 312\u2013316 (1998).",
      "journal-title": "Trends Genet"
    },
    {
      "key": "e_1_3_4_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "159",
      "DOI": "10.1093/emboj/17.1.159",
      "volume": "17",
      "author": "Cliby W A",
      "year": "1998",
      "unstructured": "W A Cliby, C J Roberts, K A Cimprich, C M Stringer, J R Lamb, S L Schreiber, S H Friend EMBO J 17, 159\u2013169 (1998).",
      "journal-title": "EMBO J"
    },
    {
      "key": "e_1_3_4_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "395",
      "DOI": "10.1101/gad.10.4.395",
      "volume": "10",
      "author": "Sun Z",
      "year": "1996",
      "unstructured": "Z Sun, D S Fay, F Marini, M Foiani, D F Stern Genes Dev 10, 395\u2013406 (1996).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "1729",
      "DOI": "10.1093/genetics/149.4.1729",
      "volume": "149",
      "author": "Rhind N",
      "year": "1998",
      "unstructured": "N Rhind, P Russell Genetics 149, 1729\u20131737 (1998).",
      "journal-title": "Genetics"
    },
    {
      "key": "e_1_3_4_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "909",
      "DOI": "10.1126/science.280.5365.909",
      "volume": "280",
      "author": "Boddy M N",
      "year": "1998",
      "unstructured": "M N Boddy, B Furnari, O Mondesert, P Russell Science 280, 909\u2013912 (1998).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "3032",
      "DOI": "10.1101/gad.11.22.3032",
      "volume": "11",
      "author": "Sidorova J M",
      "year": "1997",
      "unstructured": "J M Sidorova, L L Breeden Genes Dev 11, 3032\u20133045 (1997).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_23_2",
      "doi-asserted-by": "crossref",
      "first-page": "1119",
      "DOI": "10.1016/0092-8674(93)90321-G",
      "volume": "75",
      "author": "Zhou Z",
      "year": "1993",
      "unstructured": "Z Zhou, S J Elledge Cell 75, 1119\u20131127 (1993).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "382",
      "DOI": "10.1101/gad.12.3.382",
      "volume": "12",
      "author": "Lindsay H D",
      "year": "1998",
      "unstructured": "H D Lindsay, D J Griffiths, R J Edwards, P U Christensen, J M Murray, F Osman, N Walworth, A M Carr Genes Dev 12, 382\u2013395 (1998).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1038/26766",
      "volume": "395",
      "author": "Zeng Y",
      "year": "1998",
      "unstructured": "Y Zeng, K C Forbes, Z Wu, S Moreno, H Piwnica-Worms, T Enoch Nature (London) 395, 507\u2013510 (1998).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "665",
      "DOI": "10.1016/0092-8674(90)90669-6",
      "volume": "60",
      "author": "Enoch T",
      "year": "1990",
      "unstructured": "T Enoch, P Nurse Cell 60, 665\u2013673 (1990).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_27_2",
      "doi-asserted-by": "crossref",
      "first-page": "963",
      "DOI": "10.1083/jcb.134.4.963",
      "volume": "134",
      "author": "Jin P",
      "year": "1996",
      "unstructured": "P Jin, Y Gu, D O Morgan J Cell Biol 134, 963\u2013970 (1996).",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "e_1_3_4_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "3599",
      "DOI": "10.1002/j.1460-2075.1996.tb00729.x",
      "volume": "15",
      "author": "Ye X S",
      "year": "1996",
      "unstructured": "X S Ye, R R Fincher, A Tang, K O\u2019Donnell, S A Osmani EMBO J 15, 3599\u20133610 (1996).",
      "journal-title": "EMBO J"
    },
    {
      "key": "e_1_3_4_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "1501",
      "DOI": "10.1126/science.277.5331.1501",
      "volume": "277",
      "author": "Peng C Y",
      "year": "1997",
      "unstructured": "C Y Peng, P R Graves, R S Thoma, Z Wu, A S Shaw, H Piwnica-Worms Science 277, 1501\u20131505 (1997).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "345",
      "DOI": "10.1091/mbc.9.2.345",
      "volume": "9",
      "author": "Kumagai A",
      "year": "1998",
      "unstructured": "A Kumagai, P S Yakowec, W G Dunphy Mol Biol Cell 9, 345\u2013354 (1998).",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "e_1_3_4_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "817",
      "DOI": "10.1038/374817a0",
      "volume": "374",
      "author": "Murakami H",
      "year": "1995",
      "unstructured": "H Murakami, H Okayama Nature (London) 374, 817\u2013819 (1995).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_32_2",
      "doi-asserted-by": "crossref",
      "first-page": "368",
      "DOI": "10.1038/363368a0",
      "volume": "363",
      "author": "Walworth N",
      "year": "1993",
      "unstructured": "N Walworth, S Davey, D Beach Nature (London) 363, 368\u2013371 (1993).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_33_2",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1091/mbc.5.2.147",
      "volume": "5",
      "author": "Al-Khodairy F",
      "year": "1994",
      "unstructured": "F Al-Khodairy, E Fotou, K S Sheldrick, D J F Griffiths, A R Lehmann, A M Carr Mol Biol Cell 5, 147\u2013160 (1994).",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "e_1_3_4_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "1497",
      "DOI": "10.1126/science.277.5331.1497",
      "volume": "277",
      "author": "Sanchez Y",
      "year": "1997",
      "unstructured": "Y Sanchez, C Wong, R S Thoma, R Richman, Z Wu, H Piwnica-Worms, S J Elledge Science 277, 1497\u20131501 (1997).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_35_2",
      "doi-asserted-by": "crossref",
      "first-page": "1559",
      "DOI": "10.1083/jcb.142.6.1559",
      "volume": "142",
      "author": "Kumagai A",
      "year": "1998",
      "unstructured": "A Kumagai, Z Guo, K H Emami, S X Wang, W G Dunphy J Cell Biol 142, 1559\u20131569 (1998).",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "e_1_3_4_36_2",
      "doi-asserted-by": "crossref",
      "first-page": "404",
      "DOI": "10.1126/science.7545955",
      "volume": "266",
      "author": "Singer M S",
      "year": "1994",
      "unstructured": "M S Singer, D E Gottschling Science 266, 404\u2013409 (1994).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_37_2",
      "doi-asserted-by": "crossref",
      "first-page": "30461",
      "DOI": "10.1016/S0021-9258(18)43836-7",
      "volume": "269",
      "author": "Ogg S",
      "year": "1994",
      "unstructured": "S Ogg, B Gabrielli, H Piwnica-Worms J Biol Chem 269, 30461\u201330469 (1994).",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "e_1_3_4_38_2",
      "first-page": "197",
      "volume": "9",
      "author": "Peng C-Y",
      "year": "1998",
      "unstructured": "C-Y Peng, P R Graves, S Ogg, R S Thoma, M J Byrnes, Z Wu, M Stephenson, H Piwnica-Worms Cell Growth Differ 9, 197\u2013208 (1998).",
      "journal-title": "Cell Growth Differ"
    },
    {
      "key": "e_1_3_4_39_2",
      "doi-asserted-by": "crossref",
      "first-page": "751",
      "DOI": "10.1016/0092-8674(90)90141-Z",
      "volume": "63",
      "author": "Gottschling D E",
      "year": "1990",
      "unstructured": "D E Gottschling, O M Aparicio, B L Billington, V A Zakian Cell 63, 751\u2013762 (1990).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_40_2",
      "doi-asserted-by": "crossref",
      "first-page": "3094",
      "DOI": "10.1128/MCB.16.6.3094",
      "volume": "16",
      "author": "Runge K W",
      "year": "1996",
      "unstructured": "K W Runge, V A Zakian Mol Cell Biol 16, 3094\u20133105 (1996).",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "e_1_3_4_41_2",
      "doi-asserted-by": "crossref",
      "first-page": "1279",
      "DOI": "10.1016/0092-8674(91)90049-5",
      "volume": "66",
      "author": "Aparicio O M",
      "year": "1991",
      "unstructured": "O M Aparicio, B L Billington, D E Gottschling Cell 66, 1279\u20131287 (1991).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_42_2",
      "doi-asserted-by": "crossref",
      "first-page": "1146",
      "DOI": "10.1101/gad.7.7a.1146",
      "volume": "7",
      "author": "Kyrion G",
      "year": "1993",
      "unstructured": "G Kyrion, K Liu, C Liu, A J Lustig Genes Dev 7, 1146\u20131159 (1993).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_43_2",
      "doi-asserted-by": "crossref",
      "first-page": "245",
      "DOI": "10.1038/369245a0",
      "volume": "369",
      "author": "Thompson J S",
      "year": "1994",
      "unstructured": "J S Thompson, X Ling, M Grunstein Nature (London) 369, 245\u2013247 (1994).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_44_2",
      "first-page": "987",
      "volume": "11",
      "author": "Stern D F",
      "year": "1991",
      "unstructured": "D F Stern, P Zheng, D R Beidler, C Zerillo Mol Cell Biol 11, 987\u20131001 (1991).",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "e_1_3_4_45_2",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1016/S0925-4773(97)00200-1",
      "volume": "71",
      "author": "Oishi I",
      "year": "1998",
      "unstructured": "I Oishi, S Sugiyama, H Otani, H Yamamura, Y Nishida, Y Minami Mech Dev 71, 49\u201363 (1998).",
      "journal-title": "Mech Dev"
    },
    {
      "key": "e_1_3_4_46_2",
      "doi-asserted-by": "crossref",
      "first-page": "455",
      "DOI": "10.1016/0092-8674(90)90439-L",
      "volume": "63",
      "author": "Weigel D",
      "year": "1990",
      "unstructured": "D Weigel, H Jackle Cell 63, 455\u2013456 (1990).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_47_2",
      "doi-asserted-by": "crossref",
      "first-page": "347",
      "DOI": "10.1016/S0968-0004(00)89072-6",
      "volume": "20",
      "author": "Hofmann K",
      "year": "1995",
      "unstructured": "K Hofmann, P Bucher Trends Biochem Sci 20, 347\u2013349 (1995).",
      "journal-title": "Trends Biochem Sci"
    },
    {
      "key": "e_1_3_4_48_2",
      "doi-asserted-by": "crossref",
      "first-page": "272",
      "DOI": "10.1126/science.281.5374.272",
      "volume": "281",
      "author": "Sun Z",
      "year": "1998",
      "unstructured": "Z Sun, J Hsiao, D S Fay, D F Stern Science 281, 272\u2013274 (1998).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_4_49_2",
      "doi-asserted-by": "crossref",
      "first-page": "97",
      "DOI": "10.1007/s002940050181",
      "volume": "31",
      "author": "Fay D S",
      "year": "1997",
      "unstructured": "D S Fay, Z Sun, D F Stern Curr Genet 31, 97\u2013105 (1997).",
      "journal-title": "Curr Genet"
    },
    {
      "key": "e_1_3_4_50_2",
      "doi-asserted-by": "crossref",
      "first-page": "453",
      "DOI": "10.1016/0968-0004(94)90129-5",
      "volume": "19",
      "author": "Feller S M",
      "year": "1994",
      "unstructured": "S M Feller, R Ren, H Hanafusa, D Baltimore Trends Biochem Sci 19, 453\u2013458 (1994).",
      "journal-title": "Trends Biochem Sci"
    },
    {
      "key": "e_1_3_4_51_2",
      "doi-asserted-by": "crossref",
      "first-page": "516",
      "DOI": "10.1038/387516a0",
      "volume": "387",
      "author": "Baskaran R",
      "year": "1997",
      "unstructured": "R Baskaran, L D Wood, L L Whitaker, C E Canman, S E Morgan, Y Xu, C Barlow, D Baltimore, A Wynshaw-Boris, M B Kastan, J Y Wang Nature (London) 387, 516\u2013519 (1997).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_52_2",
      "doi-asserted-by": "crossref",
      "first-page": "520",
      "DOI": "10.1038/387520a0",
      "volume": "387",
      "author": "Shafman T",
      "year": "1997",
      "unstructured": "T Shafman, K K Khanna, P Kedar, K Spring, S Kozlov, T Yen, K Hobson, M Gatei, N Zhang, D Watters, et al. Nature (London) 387, 520\u2013523 (1997).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_53_2",
      "doi-asserted-by": "crossref",
      "first-page": "753",
      "DOI": "10.1006/jmbi.1996.0061",
      "volume": "255",
      "author": "Schmidt T G",
      "year": "1996",
      "unstructured": "T G Schmidt, J Koepke, R Frank, A Skerra J Mol Biol 255, 753\u2013766 (1996).",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "e_1_3_4_54_2",
      "doi-asserted-by": "crossref",
      "first-page": "185",
      "DOI": "10.1016/S0959-437X(98)80140-8",
      "volume": "8",
      "author": "Weinert T",
      "year": "1998",
      "unstructured": "T Weinert Curr Opin Genet Dev 8, 185\u2013193 (1998).",
      "journal-title": "Curr Opin Genet Dev"
    },
    {
      "key": "e_1_3_4_55_2",
      "doi-asserted-by": "crossref",
      "first-page": "840",
      "DOI": "10.1038/383840a0",
      "volume": "383",
      "author": "Lydall D",
      "year": "1996",
      "unstructured": "D Lydall, Y Nikolsky, D K Bishop, T Weinert Nature (London) 383, 840\u2013843 (1996).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_56_2",
      "doi-asserted-by": "crossref",
      "first-page": "364",
      "DOI": "10.1038/362364a0",
      "volume": "362",
      "author": "McKim K S",
      "year": "1993",
      "unstructured": "K S McKim, J K Jang, W E Theurkauf, R S Hawley Nature (London) 362, 364\u2013366 (1993).",
      "journal-title": "Nature (London)"
    },
    {
      "key": "e_1_3_4_57_2",
      "doi-asserted-by": "crossref",
      "first-page": "55",
      "DOI": "10.1093/genetics/131.1.55",
      "volume": "131",
      "author": "Weber L",
      "year": "1992",
      "unstructured": "L Weber, B Byers Genetics 131, 55\u201363 (1992).",
      "journal-title": "Genetics"
    },
    {
      "key": "e_1_3_4_58_2",
      "doi-asserted-by": "crossref",
      "first-page": "2423",
      "DOI": "10.1101/gad.10.19.2423",
      "volume": "10",
      "author": "Keegan K S",
      "year": "1996",
      "unstructured": "K S Keegan, D A Holtzman, A W Plug, E R Christenson, E E Brainerd, G Flaggs, N J Bentley, E M Taylor, M S Meyn, S B Moss, et al. Genes Dev 10, 2423\u20132437 (1996).",
      "journal-title": "Genes Dev"
    },
    {
      "key": "e_1_3_4_59_2",
      "doi-asserted-by": "crossref",
      "first-page": "977",
      "DOI": "10.1016/S0960-9822(06)00417-9",
      "volume": "7",
      "author": "Flaggs G",
      "year": "1997",
      "unstructured": "G Flaggs, A W Plug, K M Dunks, K E Mundt, J C Ford, M R Quiggle, E M Taylor, C H Westphal, T Ashley, M F Hoekstra, A M Carr Curr Biol 7, 977\u2013986 (1997).",
      "journal-title": "Curr Biol"
    },
    {
      "key": "e_1_3_4_60_2",
      "doi-asserted-by": "crossref",
      "first-page": "159",
      "DOI": "10.1038/sj.onc.1201319",
      "volume": "15",
      "author": "Ziv Y",
      "year": "1997",
      "unstructured": "Y Ziv, A Bar-Shira, I Pecker, P Russell, T J Jorgensen, I Tsarfati, Y Shiloh Oncogene 15, 159\u2013167 (1997).",
      "journal-title": "Oncogene"
    },
    {
      "key": "e_1_3_4_61_2",
      "doi-asserted-by": "crossref",
      "first-page": "849",
      "DOI": "10.1016/0092-8674(95)90482-4",
      "volume": "82",
      "author": "Hartley K O",
      "year": "1995",
      "unstructured": "K O Hartley, D Gell, G C Smith, H Zhang, N Divecha, M A Connelly, A Admon, S P Lees-Miller, C W Anderson, S P Jackson Cell 82, 849\u2013856 (1995).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_4_62_2",
      "doi-asserted-by": "crossref",
      "first-page": "813",
      "DOI": "10.1016/0092-8674(95)90360-7",
      "volume": "80",
      "author": "Blunt T",
      "year": "1995",
      "unstructured": "T Blunt, N J Finnie, G E Taccioli, G C Smith, J Demengeot, T M Gottlieb, R Mizuta, A J Varghese, F W Alt, P A Jeggo, et al. Cell 80, 813\u2013823 (1995).",
      "journal-title": "Cell"
    }
  ],
  "container-title": "Proceedings of the National Academy of Sciences",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://pnas.org/doi/pdf/10.1073/pnas.96.7.3745",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        6,
        7
      ]
    ],
    "date-time": "2022-06-07T04:27:00Z",
    "timestamp": 1654576020000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://pnas.org/doi/full/10.1073/pnas.96.7.3745"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        3,
        30
      ]
    ]
  },
  "references-count": 62,
  "journal-issue": {
    "issue": "7",
    "published-print": {
      "date-parts": [
        [
          1999,
          3,
          30
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1073/pnas.96.7.3745"
  ],
  "URL": "http://dx.doi.org/10.1073/pnas.96.7.3745",
  "relation": {},
  "ISSN": [
    "0027-8424",
    "1091-6490"
  ],
  "subject": [],
  "container-title-short": "Proc. Natl. Acad. Sci. U.S.A.",
  "published": {
    "date-parts": [
      [
        1999,
        3,
        30
      ]
    ]
  },
  "assertion": [
    {
      "value": "1998-11-21",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-02-05",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-03-30",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}