Mouse models of DNA double-strand break repair and neurological disease

DNA Repair

Volumn 7, Issue 7, 2008, Pages 1051-1060

  Frappart, Pierre Olivier ^a   McKinnon, Peter J ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

DNA repair; Double strand breaks; Homologous recombination; Nervous system; Neurodegeneration; Non homologous end joining

Indexed keywords

ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN TUMOR; CELL CYCLE; DEGENERATIVE DISEASE; DNA REPAIR; DNA STRAND BREAKAGE; HOMOLOGOUS RECOMBINATION; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; DISEASE MODELS, ANIMAL; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HUMANS; MICE; MODELS, ANIMAL; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES;

EID: 44949178279     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.03.007     Document Type: Article

References (119)

1. Williams R.W., and Herrup K. The control of neuron number. Annu. Rev. Neurosci. 11 (1988) 423-453
2. Katyal S., and McKinnon P.J. DNA repair deficiency and neurodegeneration. Cell Cycle 6 (2007)
3. McKinnon P.J., and Caldecott K.W. DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet. 8 (2007) 37-55
4. Rass U., Ahel I., and West S.C. Defective DNA repair and neurodegenerative disease. Cell 130 (2007) 991-1004
5. Cleaver J.E. Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer 5 (2005) 564-573
6. Rolig R.L., and McKinnon P.J. Linking DNA damage and neurodegeneration. Trends Neurosci. 23 (2000) 417-424
7. Nouspikel T., and Hanawalt P.C. When parsimony backfires: neglecting DNA repair may doom neurons in Alzheimer's disease. Bioessays 25 (2003) 168-173
8. Shackelford D.A. DNA end joining activity is reduced in Alzheimer's disease. Neurobiol. Aging 27 (2006) 596-605
9. Jacobsen M. Developmental Neurobiology (1991), Plenum Press, New York
10. Chan W.Y., Lorke D.E., Tiu S.C., and Yew D.T. Proliferation and apoptosis in the developing human neocortex. Anat. Rec. 267 (2002) 261-276
11. Dehay C., and Kennedy H. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8 (2007) 438-450
12. Goldowitz D., and Hamre K. The cells and molecules that make a cerebellum. Trends Neurosci. 21 (1998) 375-382
13. Huang Z.J., Di Cristo G., and Ango F. Development of GABA innervation in the cerebral and cerebellar cortices. Nat. Rev. Neurosci. 8 (2007) 673-686
14. Wang V.Y., and Zoghbi H.Y. Genetic regulation of cerebellar development. Nat. Rev. Neurosci. 2 (2001) 484-491
15. Masland R.H. Neuronal cell types. Curr. Biol. 14 (2004) R497-R500
16. Masland R.H. Neuronal diversity in the retina. Curr. Opin. Neurobiol. 11 (2001) 431-436
17. Battiste J., Helms A.W., Kim E.J., Savage T.K., Lagace D.C., Mandyam C.D., Eisch A.J., Miyoshi G., and Johnson J.E. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 134 (2007) 285-293
18. Helleday T., Lo J., van Gent D.C., and Engelward B.P. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst.) 6 (2007) 923-935
19. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4 (2003) 435-445
20. Lieber M.R., Ma Y., Pannicke U., and Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4 (2003) 712-720
21. Aimone J.B., Wiles J., and Gage F.H. Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9 (2006) 723-727
22. Bhardwaj R.D., Curtis M.A., Spalding K.L., Buchholz B.A., Fink D., Bjork-Eriksson T., Nordborg C., Gage F.H., Druid H., Eriksson P.S., and Frisen J. Neocortical neurogenesis in humans is restricted to development. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 12564-12568
23. Lie D.C., Colamarino S.A., Song H.J., Desire L., Mira H., Consiglio A., Lein E.S., Jessberger S., Lansford H., Dearie A.R., and Gage F.H. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437 (2005) 1370-1375
24. Tashiro A., Sandler V.M., Toni N., Zhao C., and Gage F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442 (2006) 929-933
25. Fraser M.M., Zhu X., Kwon C.H., Uhlmann E.J., Gutmann D.H., and Baker S.J. Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res. 64 (2004) 7773-7779
26. Koguchi K., Nakatsuji Y., Nakayama K., and Sakoda S. Modulation of astrocyte proliferation by cyclin-dependent kinase inhibitor p27(Kip1). Glia 37 (2002) 93-104
27. Santambrogio L., Belyanskaya S.L., Fischer F.R., Cipriani B., Brosnan C.F., Ricciardi-Castagnoli P., Stern L.J., Strominger J.L., and Riese R. Developmental plasticity of CNS microglia. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 6295-6300
28. Lee Y., and McKinnon P.J. Responding to DNA double strand breaks in the nervous system. Neuroscience 145 (2007) 1365-1374
29. Thacker J., and Zdzienicka M.Z. The mammalian XRCC genes: their roles in DNA repair and genetic stability. DNA Repair (Amst.) 2 (2003) 655-672
30. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., and Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28 (2007) 134-146
31. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., and Jackson S.P. Human CtIP promotes DNA end resection. Nature 450 (2007) 509-514
32. Takeda S., Nakamura K., Taniguchi Y., and Paull T.T. Ctp1/CtIP and the MRN complex collaborate in the initial steps of homologous recombination. Mol. Cell 28 (2007) 351-352
33. Heyer W.D., Li X., Rolfsmeier M., and Zhang X.P. Rad54: the Swiss army knife of homologous recombination?. Nucleic Acids Res. 34 (2006) 4115-4125
34. Thacker J., and Zdzienicka M.Z. The XRCC genes: expanding roles in DNA double-strand break repair. DNA Repair (Amst.) 3 (2004) 1081-1090
35. Wyman C., Ristic D., and Kanaar R. Homologous recombination-mediated double-strand break repair. DNA Repair (Amst.) 3 (2004) 827-833
36. Bassing C.H., and Alt F.W. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst.) 3 (2004) 781-796
37. Lees-Miller S.P., and Meek K. Repair of DNA double strand breaks by non-homologous end joining. Biochimie 85 (2003) 1161-1173
38. Burma S., and Chen D.J. Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst.) 3 (2004) 909-918
39. Ahnesorg P., Smith P., and Jackson S.P. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124 (2006) 301-313
40. Buck D., Malivert L., de Chasseval R., Barraud A., Fondaneche M.C., Sanal O., Plebani A., Stephan J.L., Hufnagel M., le Deist F., Fischer A., Durandy A., de Villartay J.P., and Revy P. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 124 (2006) 287-299
41. Jeggo P., and O'Neill P. The Greek Goddess, Artemis, reveals the secrets of her cleavage. DNA Repair (Amst.) 1 (2002) 771-777
42. Moshous D., Callebaut I., de Chasseval R., Corneo B., Cavazzana-Calvo M., Le Deist F., Tezcan I., Sanal O., Bertrand Y., Philippe N., Fischer A., and de Villartay J.P. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 105 (2001) 177-186
43. Esashi F., Christ N., Gannon J., Liu Y., Hunt T., Jasin M., and West S.C. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434 (2005) 598-604
44. Sharma S. Age-related nonhomologous end joining activity in rat neurons. Brain Res. Bull. 73 (2007) 48-54
45. Friedberg E.C., and Meira L.B. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst.) 5 (2006) 189-209
46. Orii K.E., Lee Y., Kondo N., and McKinnon P.J. Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 10017-10022
47. Couedel C., Mills K.D., Barchi M., Shen L., Olshen A., Johnson R.D., Nussenzweig A., Essers J., Kanaar R., Li G.C., Alt F.W., and Jasin M. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 18 (2004) 1293-1304
48. Mills K.D., Ferguson D.O., Essers J., Eckersdorff M., Kanaar R., and Alt F.W. Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18 (2004) 1283-1292
49. Barnes D.E., Stamp G., Rosewell I., Denzel A., and Lindahl T. Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 8 (1998) 1395-1398
50. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Ferguson D.O., Zhu C., Manis J.P., Horner J., DePinho R.A., and Alt F.W. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5 (2000) 993-1002
51. Gao Y., Sun Y., Frank K.M., Dikkes P., Fujiwara Y., Seidl K.J., Sekiguchi J.M., Rathbun G.A., Swat W., Wang J., Bronson R.T., Malynn B.A., Bryans M., Zhu C., Chaudhuri J., Davidson L., Ferrini R., Stamato T., Orkin S.H., Greenberg M.E., and Alt F.W. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95 (1998) 891-902
52. Lee Y., Barnes D.E., Lindahl T., and McKinnon P.J. Defective neurogenesis resulting from DNA ligase IV deficiency requires Atm. Genes Dev. 14 (2000) 2576-2580
53. Sekiguchi J., Ferguson D.O., Chen H.T., Yang E.M., Earle J., Frank K., Whitlow S., Gu Y., Xu Y., Nussenzweig A., and Alt F.W. Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 3243-3248
54. Gu Y., Sekiguchi J., Gao Y., Dikkes P., Frank K., Ferguson D., Hasty P., Chun J., and Alt F.W. Defective embryonic neurogenesis in Ku-deficient but not DNA-dependent protein kinase catalytic subunit-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 2668-2673
55. Li L., Salido E., Zhou Y., Bhattacharyya S., Yannone S.M., Dunn E., Meneses J., Feeney A.J., and Cowan M.J. Targeted disruption of the Artemis murine counterpart results in SCID and defective V(D)J recombination that is partially corrected with bone marrow transplantation. J. Immunol. 174 (2005) 2420-2428
56. Rooney S., Alt F.W., Sekiguchi J., and Manis J.P. Artemis-independent functions of DNA-dependent protein kinase in Ig heavy chain class switch recombination and development. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 2471-2475
57. Zha S., Alt F.W., Cheng H.L., Brush J.W., and Li Defective G. DNA repair and increased genomic instability in Cernunnos-XLF-deficient murine ES cells. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 4518-4523
58. Karanjawala Z.E., Murphy N., Hinton D.R., Hsieh C.L., and Lieber M.R. Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol. 12 (2002) 397-402
59. Gao Y., Ferguson D.O., Xie W., Manis J.P., Sekiguchi J., Frank K.M., Chaudhuri J., Horner J., DePinho R.A., and Alt F.W. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 404 (2000) 897-900
60. Lee Y., and McKinnon P.J. DNA ligase IV suppresses medulloblastoma formation. Cancer Res. 62 (2002) 6395-6399
61. Yan C.T., Kaushal D., Murphy M., Zhang Y., Datta A., Chen C., Monroe B., Mostoslavsky G., Coakley K., Gao Y., Mills K.D., Fazeli A.P., Tepsuporn S., Hall G., Mulligan R., Fox E., Bronson R., De Girolami U., Lee C., and Alt F.W. XRCC4 suppresses medulloblastomas with recurrent translocations in p53-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 7378-7383
62. O'Driscoll M., Cerosaletti K.M., Girard P.M., Dai Y., Stumm M., Kysela B., Hirsch B., Gennery A., Palmer S.E., Seidel J., Gatti R.A., Varon R., Oettinger M.A., Neitzel H., Jeggo P.A., and Concannon P. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 8 (2001) 1175-1185
63. O'Driscoll M., Gennery A.R., Seidel J., Concannon P., and Jeggo P.A. An overview of three new disorders associated with genetic instability: LIG4 syndrome, RS-SCID and ATR-Seckel syndrome. DNA Repair (Amst.) 3 (2004) 1227-1235
64. Karanjawala Z.E., Hinton D.R., Oh E., Hsieh C.L., and Lieber M.R. Developmental retinal apoptosis in Ku86-/- mice. DNA Repair (Amst.) 2 (2003) 1429-1434
65. Karanjawala Z.E., Adachi N., Irvine R.A., Oh E.K., Shibata D., Schwarz K., Hsieh C.L., and Lieber M.R. The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Repair (Amst.) 1 (2002) 1017-1026
66. Jonkers J., and Berns A. Conditional mouse models of sporadic cancer. Nat. Rev. Cancer 2 (2002) 251-265
67. Deans B., Griffin C.S., Maconochie M., and Thacker J. Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J. 19 (2000) 6675-6685
68. Gowen L.C., Johnson B.L., Latour A.M., Sulik K.K., and Koller B.H. Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat. Genet. 12 (1996) 191-194
69. Xu X., Qiao W., Linke S.P., Cao L., Li W.M., Furth P.A., Harris C.C., and Deng C.X. Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat. Genet. 28 (2001) 266-271
70. Ludwig T., Chapman D.L., Papaioannou V.E., and Efstratiadis A. Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev. 11 (1997) 1226-1241
71. Sharan S.K., and Bradley A. Murine Brca2: sequence, map position, and expression pattern. Genomics 40 (1997) 234-241
72. Suzuki A., de la Pompa J.L., Hakem R., Elia A., Yoshida R., Mo R., Nishina H., Chuang T., Wakeham A., Itie A., Koo W., Billia P., Ho A., Fukumoto M., Hui C.C., and Mak T.W. Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev. 11 (1997) 1242-1252
73. Frappart P.O., Lee Y., Lamont J., and McKinnon P.J. BRCA2 is required for neurogenesis and suppression of medulloblastoma. EMBO J. 26 (2007) 2732-2742
74. D'Andrea A.D., and Grompe M. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 3 (2003) 23-34
75. Offit K., Levran O., Mullaney B., Mah K., Nafa K., Batish S.D., Diotti R., Schneider H., Deffenbaugh A., Scholl T., Proud V.K., Robson M., Norton L., Ellis N., Hanenberg H., and Auerbach A.D. Shared genetic susceptibility to breast cancer, brain tumors, and Fanconi anemia. J. Natl. Cancer Inst. 95 (2003) 1548-1551
76. Celeste A., Fernandez-Capetillo O., Kruhlak M.J., Pilch D.R., Staudt D.W., Lee A., Bonner R.F., Bonner W.M., and Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5 (2003) 675-679
77. Sedelnikova O.A., Pilch D.R., Redon C., and Bonner W.M. Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2 (2003) 233-235
78. Ward I., and Chen J. Early events in the DNA damage response. Curr. Top. Dev. Biol. 63 (2004) 1-35
79. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
80. Kastan M.B., and Bartek J. Cell-cycle checkpoints and cancer. Nature 432 (2004) 316-323
81. Lavin M.F., and Kozlov S. ATM activation and DNA damage response. Cell Cycle 6 (2007)
82. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31 (2006) 402-410
83. Berkovich E., Monnat Jr. R.J., and Kastan M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9 (2007) 683-690
84. Yang Y.G., Saidi A., Frappart P.O., Min W., Barrucand C., Dumon-Jones V., Michelon J., Herceg Z., and Wang Z.Q. Conditional deletion of Nbs1 in murine cells reveals its role in branching repair pathways of DNA double-strand breaks. EMBO J. 25 (2006) 5527-5538
85. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15 (2001) 2177-2196
86. Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 11 (2001) 71-77
87. Adams K.E., Medhurst A.L., Dart D.A., and Lakin N.D. Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 25 (2006) 3894-3904
88. Cuadrado M., Martinez-Pastor B., Murga M., Toledo L.I., Gutierrez-Martinez P., Lopez E., and Fernandez-Capetillo O. ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J. Exp. Med. 203 (2006) 297-303
89. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., and Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 37-45
90. Myers J.S., and Cortez D. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J. Biol. Chem. 281 (2006) 9346-9350
91. Shechter D., Costanzo V., and Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6 (2004) 648-655
92. Trenz K., Smith E., Smith S., and Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25 (2006) 1764-1774
93. Bi X., Srikanta D., Fanti L., Pimpinelli S., Badugu R., Kellum R., and Rong Y.S. Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 15167-15172
94. Ho G.P., Margossian S., Taniguchi T., and D'Andrea A.D. Phosphorylation of FANCD2 on two novel sites is required for mitomycin C resistance. Mol. Cell Biol. 26 (2006) 7005-7015
95. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald III E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., and Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316 (2007) 1160-1166
96. McKinnon P.J. ATM and ataxia telangiectasia. EMBO Rep. 5 (2004) 772-776
97. O'Driscoll M., and Jeggo P.A. The role of double-strand break repair-insights from human genetics. Nat. Rev. Genet. 7 (2006) 45-54
98. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., Shiloh Y., Crawley J.N., Ried T., Tagle D., and Wynshaw-Boris A. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86 (1996) 159-171
99. Brown E.J., and Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14 (2000) 397-402
100. Elson A., Wang Y., Daugherty C.J., Morton C.C., Zhou F., Campos-Torres J., and Leder P. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 13084-13089
101. Herzog K.H., Chong M.J., Kapsetaki M., Morgan J.I., and McKinnon P.J. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280 (1998) 1089-1091
102. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., and Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10 (1996) 2411-2422
103. Lee Y., Chong M.J., and McKinnon P.J. Ataxia telangiectasia mutated-dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status. J. Neurosci. 21 (2001) 6687-6693
104. Frappart P.O., and McKinnon P.J. BRCA2 function and the central nervous system. Cell Cycle 6 (2007)
105. Carson C.T., Schwartz R.A., Stracker T.H., Lilley C.E., Lee D.V., and Weitzman M.D. The Mre11 complex is required for ATM activation and the G(2)/M checkpoint. EMBO J. 22 (2003) 6610-6620
106. Difilippantonio S., Celeste A., Fernandez-Capetillo O., Chen H.T., Reina San Martin B., Van Laethem F., Yang Y.P., Petukhova G.V., Eckhaus M., Feigenbaum L., Manova K., Kruhlak M., Camerini-Otero R.D., Sharan S., Nussenzweig M., and Nussenzweig A. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7 (2005) 675-685
107. Uziel T., Lerenthal Y., Moyal L., Andegeko Y., Mittelman L., and Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22 (2003) 5612-5621
108. Stracker T.H., Theunissen J.W., Morales M., and Petrini J.H. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst.) 3 (2004) 845-854
109. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates III J.R., Hays L., Morgan W.F., and Petrini J.H. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93 (1998) 477-486
110. Stewart G.S., Maser R.S., Stankovic T., Bressan D.A., Kaplan M.I., Jaspers N.G., Raams A., Byrd P.J., Petrini J.H., and Taylor A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99 (1999) 577-587
111. Taylor A.M., Groom A., and Byrd P.J. Ataxia-telangiectasia-like disorder (ATLD)-its clinical presentation and molecular basis. DNA Repair (Amst.) 3 (2004) 1219-1225
112. Luo G., Yao M.S., Bender C.F., Mills M., Bladl A.R., Bradley A., and Petrini J.H. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7376-7381
113. Xiao Y., and Weaver D.T. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 25 (1997) 2985-2991
114. Zhu J., Petersen S., Tessarollo L., and Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11 (2001) 105-109
115. Kang J., Bronson R.T., and Xu Y. Targeted disruption of NBS1 reveals its roles in mouse development and DNA repair. EMBO J. 21 (2002) 1447-1455
116. Williams B.R., Mirzoeva O.K., Morgan W.F., Lin J., Dunnick W., and Petrini J.H. A murine model of Nijmegen breakage syndrome. Curr. Biol. 12 (2002) 648-653
117. Theunissen J.W., Kaplan M.I., Hunt P.A., Williams B.R., Ferguson D.O., Alt F.W., and Petrini J.H. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol. Cell 12 (2003) 1511-1523
118. Bender C.F., Sikes M.L., Sullivan R., Huye L.E., Le Beau M.M., Roth D.B., Mirzoeva O.K., Oltz E.M., and Petrini J.H. Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev. 16 (2002) 2237-2251
119. Frappart P.O., Tong W.M., Demuth I., Radovanovic I., Herceg Z., Aguzzi A., Digweed M., and Wang Z.Q. An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat. Med. 11 (2005) 538-544