Checkpoint kinase 2 (Chk2) inhibits the activity of the Cdc45/MCM2-7/GINS (CMG) replicative helicase complex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 33, 2012, Pages 13163-13170

  Ilves, Ivar ^a,b   Tamberg, Nele ^a,b   Botchan, Michael R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

Eukaryotic DNA replication; S phase checkpoint response

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 5; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; PHOSPHATASE; PROTEIN CDC45; PROTEIN GINS; PROTEIN PSF2; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DROSOPHILA; EMBRYO; IONIZING RADIATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN SUBUNIT; RADIATION EXPOSURE;

ANIMALS; DNA HELICASES; DNA REPLICATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING;

EID: 84865188025     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211525109     Document Type: Article

References (52)

1. Méchali M (2010) Eukaryotic DNA replication origins: Many choices for appropriate answers. Nat Rev Mol Cell Biol 11:728-738.
2. Ilves I, Petojevic T, Pesavento JJ, Botchan MR (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 37:247-258.
3. Kang YH, Galal WC, Farina A, Tappin I, Hurwitz J (2012) Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase epsilon in rolling circle DNA synthesis. Proc Natl Acad Sci USA 109:6042-6047.
4. Moyer SE, Lewis PW, Botchan MR (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci USA 103:10236-10241. (Pubitemid 44051150)
5. Evrin C, et al. (2009) A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc Natl Acad Sci USA 106:20240-20245.
6. Remus D, et al. (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139:719-730.
7. Yardimci H, Loveland AB, Habuchi S, van Oijen AM, Walter JC (2010) Uncoupling of sister replisomes during eukaryotic DNA replication. Mol Cell 40:834-840.
8. Botchan M, Berger J (2010) DNA replication: Making two forks from one prereplication complex. Mol Cell 40:860-861.
9. Costa A, et al. (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18:471-477.
10. Gambus A, et al. (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8:358-366.
11. Pacek M, Tutter AV, Kubota Y, Takisawa H, Walter JC (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21:581-587. (Pubitemid 43228013)
12. Labib K (2010) How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells? Genes Dev 24:1208-1219.
13. Lopez-Mosqueda J, et al. (2010) Damage-induced phosphorylation of Sld3 is important to block late origin firing. Nature 467:479-483.
14. Zegerman P, Diffley JF (2010) Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation. Nature 467:474-478.
15. Berens TJ, Toczyski DP (2012) Keeping it together in times of stress: Checkpoint function at stalled replication forks. Mol Cell 45:585-586.
16. De Piccoli G, et al. (2012) Replisome stability at defective DNA replication forks is independent of S phase checkpoint kinases. Mol Cell 45:696-704.
17. Painter RB, Young BR (1975) X-ray-induced inhibition of DNA synthesis in Chinese hamster ovary, human HeLa, and Mouse L cells. Radiat Res 64:648-656.
18. Painter RB, Young BR (1980) Radiosensitivity in ataxia-telangiectasia: A new explanation. Proc Natl Acad Sci USA 77:7315-7317. (Pubitemid 11189463)
19. Watanabe I (1974) Radiation effects on DNA chain growth in mammalian cells. Radiat Res 58:541-556.
20. Bartkova J, et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864-870. (Pubitemid 40558993)
21. Gorgoulis VG, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434:907-913. (Pubitemid 40559004)
22. Ciccia A, Elledge SJ (2010) The DNA damage response: Making it safe to play with knives. Mol Cell 40:179-204.
23. Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39-85. (Pubitemid 39050363)
24. Stracker TH, Usui T, Petrini JH (2009) Taking the time to make important decisions: The checkpoint effector kinases Chk1 and Chk2 and the DNA damage response. DNA Repair (Amst) 8:1047-1054.
25. Boos D, et al. (2011) Regulation of DNA replication through Sld3-Dpb11 interaction is conserved from yeast to humans. Curr Biol 21:1152-1157.
26. Costanzo V, et al. (2003) An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol Cell 11:203-213. (Pubitemid 36126601)
27. Heffernan TP, et al. (2007) Cdc7-Dbf4 and the human S checkpoint response to UVC. J Biol Chem 282:9458-9468. (Pubitemid 47104564)
28. Lin DI, Aggarwal P, Diehl JA (2008) Phosphorylation of MCM3 on Ser-112 regulates its incorporation into the MCM2-7 complex. Proc Natl Acad Sci USA 105:8079-8084. (Pubitemid 351904711)
29. Sheu YJ, Stillman B (2010) The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 463:113-117.
30. Li J, et al. (2011) Phosphorylation of MCM3 protein by cyclin E/cyclin-dependent kinase 2 (Cdk2) regulates its function in cell cycle. J Biol Chem 286:39776-39785.
31. Cortez D, Glick G, Elledge SJ (2004) Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci USA 101:10078-10083. (Pubitemid 38891197)
32. Yoo HY, Shevchenko A, Shevchenko A, Dunphy WG (2004) Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J Biol Chem 279:53353-53364. (Pubitemid 40051841)
33. Ishimi Y, Komamura-Kohno Y, Kwon HJ, Yamada K, Nakanishi M (2003) Identification of MCM4 as a target of the DNA replication block checkpoint system. J Biol Chem 278:24644-24650. (Pubitemid 37548619)
34. Matsuoka S, et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160-1166. (Pubitemid 46877472)
35. Shi Y, et al. (2007) Identification of carboxyl-terminal MCM3 phosphorylation sites using polyreactive phosphospecific antibodies. J Biol Chem 282:9236-9243. (Pubitemid 47093468)
36. Huang N, et al. (2011) Baculovirus infection induces a DNA damage response that is required for efficient viral replication. J Virol 85:12547-12556.
37. Schultz KL, Friesen PD (2009) Baculovirus DNA replication-specific expression factors trigger apoptosis and shutoff of host protein synthesis during infection. J Virol 83:11123-11132.
38. Holt LJ, et al. (2009) Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325:1682-1686.
39. Chang YP, Wang G, Bermudez V, Hurwitz J, Chen XS (2007) Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc Natl Acad Sci USA 104:12685-12690. (Pubitemid 47255215)
40. Choi JM, Lim HS, Kim JJ, Song OK, Cho Y (2007) Crystal structure of the human GINS complex. Genes Dev 21:1316-1321.
41. Kamada K, Kubota Y, Arata T, Shindo Y, Hanaoka F (2007) Structure of the human GINS complex and its assembly and functional interface in replication initiation. Nat Struct Mol Biol 14:388-396. (Pubitemid 46685881)
42. Brewster AS, Chen XS (2010) Insights into the MCM functional mechanism: Lessons learned from the archaeal MCM complex. Crit Rev Biochem Mol Biol 45:243-256.
43. Costa A, Onesti S (2009) Structural biology of MCM helicases. Crit Rev Biochem Mol Biol 44:326-342.
44. Brodsky MH, et al. (2004) Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol Cell Biol 24:1219-1231. (Pubitemid 38112184)
45. Peters M, et al. (2002) Chk2 regulates irradiation-induced, p53-mediated apoptosis in Drosophila. Proc Natl Acad Sci USA 99:11305-11310. (Pubitemid 34920921)
46. Wichmann A, Jaklevic B, Su TT (2006) Ionizing radiation induces caspase-dependent but Chk2- and p53-independent cell death in Drosophila melanogaster. Proc Natl Acad Sci USA 103:9952-9957. (Pubitemid 43993604)
47. Serber Z, Ferrell JE, Jr. (2007) Tuning bulk electrostatics to regulate protein function. Cell 128:441-444. (Pubitemid 46198900)
48. Lydeard JR, et al. (2010) Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev 24:1133-1144.
49. Hashimoto Y, Puddu F, Costanzo V (2012) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat Struct Mol Biol 19:17-24.
50. Antoni L, Sodha N, Collins I, Garrett MD (2007) CHK2 kinase: Cancer susceptibility and cancer therapy - Two sides of the same coin? Nat Rev Cancer 7:925-936. (Pubitemid 350165855)
51. Kwak EL, et al. (2006) Mammary tumorigenesis following transgenic expression of a dominant negative CHK2 mutant. Cancer Res 66:1923-1928.
52. Bahassi EM, et al. (2009) Mice with the CHEK2*1100delC SNP are predisposed to cancer with a strong gender bias. Proc Natl Acad Sci USA 106:17111-17116.