An Essential Function for the ATR-Activation-Domain (AAD) of TopBP1 in Mouse Development and Cellular Senescence

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Zhou, Zhong Wei ^a   Liu, Cong ^b   Li, Tang Liang ^a   Bruhn, Christopher ^a   Krueger, Anja ^a   Min, WooKee ^a   Wang, Zhao Qi ^a,c   Carr, Antony M ^b  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; MESSENGER RNA; PROTEIN TOPBP1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL AGING; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DIMERIZATION; EMBRYO; EMBRYO DEVELOPMENT; GENE FUNCTION; GENE INACTIVATION; GENE SILENCING; GENE TARGETING; HETEROZYGOSITY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATOR GENE; SIGNAL TRANSDUCTION; TOPBP1 GENE; ULTRAVIOLET RADIATION; WILD TYPE;

ALLELES; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CARRIER PROTEINS; CELL AGING; CELL PROLIFERATION; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCK-IN TECHNIQUES; MICE; PHOSPHORYLATION; POINT MUTATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84884614941     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003702     Document Type: Article

References (59)

1. Aguilera A, Gomez-Gonzalez B, (2008) Genome instability: a mechanistic view of its causes and consequences. Nature reviews Genetics 9: 204-217.
2. Ciccia A, Elledge SJ, (2010) The DNA damage response: making it safe to play with knives. Molecular cell 40: 179-204.
3. Jackson SP, Bartek J, (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
4. Branzei D, Foiani M, (2010) Maintaining genome stability at the replication fork. Nature reviews Molecular cell biology 11: 208-219.
5. Biton S, Dar I, Mittelman L, Pereg Y, Barzilai A, et al. (2006) Nuclear ataxia-telangiectasia mutated (ATM) mediates the cellular response to DNA double strand breaks in human neuron-like cells. The Journal of biological chemistry 281: 17482-17491.
6. Cimprich KA, Cortez D, (2008) ATR: an essential regulator of genome integrity. Nature reviews Molecular cell biology 9: 616-627.
7. Mavrou A, Tsangaris GT, Roma E, Kolialexi A, (2008) The ATM gene and ataxia telangiectasia. Anticancer research 28: 401-405.
8. You Z, Shi LZ, Zhu Q, Wu P, Zhang YW, et al. (2009) CtIP links DNA double-strand break sensing to resection. Molecular cell 36: 954-969.
9. Ball HL, Myers JS, Cortez D, (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Molecular biology of the cell 16: 2372-2381.
10. Cortez D, Guntuku S, Qin J, Elledge SJ, (2001) ATR and ATRIP: partners in checkpoint signaling. Science 294: 1713-1716.
11. Mordes DA, Nam EA, Cortez D, (2008) Dpb11 activates the Mec1-Ddc2 complex. Proceedings of the National Academy of Sciences of the United States of America 105: 18730-18734.
12. Edwards RJ, Bentley NJ, Carr AM, (1999) A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nature cell biology 1: 393-398.
13. Liu S, Shiotani B, Lahiri M, Marechal A, Tse A, et al. (2011) ATR autophosphorylation as a molecular switch for checkpoint activation. Molecular cell 43: 192-202.
14. Nam EA, Zhao R, Glick GG, Bansbach CE, Friedman DB, et al. (2011) Thr-1989 phosphorylation is a marker of active ataxia telangiectasia-mutated and Rad3-related (ATR) kinase. The Journal of biological chemistry 286: 28707-28714.
15. Zou L, Liu D, Elledge SJ, (2003) Replication protein A-mediated recruitment and activation of Rad17 complexes. Proceedings of the National Academy of Sciences of the United States of America 100: 13827-13832.
16. Lee J, Kumagai A, Dunphy WG, (2007) The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. The Journal of biological chemistry 282: 28036-28044.
17. Cotta-Ramusino C, McDonald ER 3rd, Hurov K, Sowa ME, Harper JW, et al. (2011) A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332: 1313-1317.
18. Wang H, Elledge SJ, (2002) Genetic and physical interactions between DPB11 and DDC1 in the yeast DNA damage response pathway. Genetics 160: 1295-1304.
19. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM, (2007) The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes & development 21: 1472-1477.
20. Furuya K, Poitelea M, Guo L, Caspari T, Carr AM, (2004) Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes & development 18: 1154-1164.
21. Garcia V, Furuya K, Carr AM, (2005) Identification and functional analysis of TopBP1 and its homologs. DNA repair 4: 1227-1239.
22. Bork P, Hofmann K, Bucher P, Neuwald AF, Altschul SF, et al. (1997) A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 11: 68-76.
23. Yu X, Chini CC, He M, Mer G, Chen J, (2003) The BRCT domain is a phospho-protein binding domain. Science 302: 639-642.
24. Zegerman P, Diffley JF, (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445: 281-285.
25. Boos D, Sanchez-Pulido L, Rappas M, Pearl LH, Oliver AW, et al. (2011) Regulation of DNA replication through Sld3-Dpb11 interaction is conserved from yeast to humans. Current biology: CB 21: 1152-1157.
26. Balestrini A, Cosentino C, Errico A, Garner E, Costanzo V, (2010) GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nature cell biology 12: 484-491.
27. Kumagai A, Shevchenko A, Dunphy WG, (2010) Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 140: 349-359.
28. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, et al. (2005) Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Current biology: CB 15: 1364-1375.
29. Mochida S, Esashi F, Aono N, Tamai K, O'Connell MJ, et al. (2004) Regulation of checkpoint kinases through dynamic interaction with Crb2. The EMBO journal 23: 418-428.
30. Qu M, Yang B, Tao L, Yates JR 3rd, Russell P, et al. (2012) Phosphorylation-dependent interactions between Crb2 and Chk1 are essential for DNA damage checkpoint. PLoS genetics 8: e1002817.
31. Kumagai A, Lee J, Yoo HY, Dunphy WG, (2006) TopBP1 activates the ATR-ATRIP complex. Cell 124: 943-955.
32. Lin SJ, Wardlaw CP, Morishita T, Miyabe I, Chahwan C, et al. (2012) The Rad4(TopBP1) ATR-activation domain functions in G1/S phase in a chromatin-dependent manner. PLoS genetics 8: e1002801.
33. Navadgi-Patil VM, Burgers PM, (2008) Yeast DNA replication protein Dpb11 activates the Mec1/ATR checkpoint kinase. The Journal of biological chemistry 283: 35853-35859.
34. Mordes DA, Glick GG, Zhao R, Cortez D, (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes & development 22: 1478-1489.
35. Limbo O, Porter-Goff ME, Rhind N, Russell P, (2011) Mre11 nuclease activity and Ctp1 regulate Chk1 activation by Rad3ATR and Tel1ATM checkpoint kinases at double-strand breaks. Molecular and cellular biology 31: 573-583.
36. Usui T, Ogawa H, Petrini JH, (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Molecular cell 7: 1255-1266.
37. Jeon Y, Lee KY, Ko MJ, Lee YS, Kang S, et al. (2007) Human TopBP1 participates in cyclin E/CDK2 activation and preinitiation complex assembly during G1/S transition. The Journal of biological chemistry 282: 14882-14890.
38. Kim JE, McAvoy SA, Smith DI, Chen J, (2005) Human TopBP1 ensures genome integrity during normal S phase. Molecular and cellular biology 25: 10907-10915.
39. Liu K, Luo Y, Lin FT, Lin WC, (2004) TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes & development 18: 673-686.
40. Liu K, Bellam N, Lin HY, Wang B, Stockard CR, et al. (2009) Regulation of p53 by TopBP1: a potential mechanism for p53 inactivation in cancer. Molecular and cellular biology 29: 2673-2693.
41. Yamane K, Wu X, Chen J, (2002) A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Molecular and cellular biology 22: 555-566.
42. Lee Y, Katyal S, Downing SM, Zhao J, Russell HR, et al. (2012) Neurogenesis requires TopBP1 to prevent catastrophic replicative DNA damage in early progenitors. Nature neuroscience 15: 819-826.
43. Toledo LI, Murga M, Zur R, Soria R, Rodriguez A, et al. (2011) A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nature structural & molecular biology 18: 721-727.
44. Gruber R, Zhou Z, Sukchev M, Joerss T, Frappart PO, et al. (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nature cell biology 13: 1325-1334.
45. Liu K, Lin FT, Ruppert JM, Lin WC, (2003) Regulation of E2F1 by BRCT domain-containing protein TopBP1. Molecular and cellular biology 23: 3287-3304.
46. Liu K, Paik JC, Wang B, Lin FT, Lin WC, (2006) Regulation of TopBP1 oligomerization by Akt/PKB for cell survival. The EMBO journal 25: 4795-4807.
47. Xu X, Tsvetkov LM, Stern DF, (2002) Chk2 activation and phosphorylation-dependent oligomerization. Molecular and cellular biology 22: 4419-4432.
48. Navadgi-Patil VM, Burgers PM, (2009) The unstructured C-terminal tail of the 9-1-1 clamp subunit Ddc1 activates Mec1/ATR via two distinct mechanisms. Molecular cell 36: 743-753.
49. Kumar S, Burgers PM, (2013) Lagging strand maturation factor Dna2 is a component of the replication checkpoint initiation machinery. Genes & development 27: 313-321.
50. Zou L, (2013) Four pillars of the S-phase checkpoint. Genes & development 27: 227-233.
51. Jeon Y, Ko E, Lee KY, Ko MJ, Park SY, et al. (2011) TopBP1 deficiency causes an early embryonic lethality and induces cellular senescence in primary cells. The Journal of biological chemistry 286: 5414-5422.
52. Brown EJ, Baltimore D, (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes & development 14: 397-402.
53. de Klein A, Muijtjens M, van Os R, Verhoeven Y, Smit B, et al. (2000) Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Current biology: CB 10: 479-482.
54. Brown EJ, Baltimore D, (2003) Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes & development 17: 615-628.
55. Woolf PJ, Linderman JJ, (2003) Self organization of membrane proteins via dimerization. Biophysical chemistry 104: 217-227.
56. Yoo HY, Kumagai A, Shevchenko A, Dunphy WG, (2007) Ataxia-telangiectasia mutated (ATM)-dependent activation of ATR occurs through phosphorylation of TopBP1 by ATM. The Journal of biological chemistry 282: 17501-17506.
57. Lindsey-Boltz LA, Sancar A, (2011) Tethering DNA damage checkpoint mediator proteins topoisomerase IIbeta-binding protein 1 (TopBP1) and Claspin to DNA activates ataxia-telangiectasia mutated and RAD3-related (ATR) phosphorylation of checkpoint kinase 1 (Chk1). The Journal of biological chemistry 286: 19229-19236.
58. Zhou Z, Sun X, Zou Z, Sun L, Zhang T, et al. (2010) PRMT5 regulates Golgi apparatus structure through methylation of the golgin GM130. Cell research 20: 1023-1033.
59. Wang ZQ, Auer B, Stingl L, Berghammer H, Haidacher D, et al. (1995) Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes & development 9: 509-520.