Human embryonic stem cells fail to activate CHK1 and commit to apoptosis in response to DNA replication stress

Stem Cells

Volumn 30, Issue 7, 2012, Pages 1385-1393

  Desmarais, Joëlle A ^a   Hoffmann, Michele J ^a   Bingham, Gregg ^a   Gagou, Mary E ^a   Meuth, Mark ^a   Andrews, Peter W ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Chromosome aberration; DNA repair; DNA replication; Embryonal carcinoma; Embryonic stem cells; Genetic variation; S phase cell cycle checkpoints

Indexed keywords

ACTIN; ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; DNA TOPOISOMERASE (ATP HYDROLYSING); GAMMA H2AX PREOTEIN; HISTONE H2AX; PROTEIN A; RAD51 PROTEIN; SINGLE STRANDED DNA; THYMIDINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CHROMATIN; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA REPLICATION STRESS; EMBRYONAL CARCINOMA; EMBRYONIC STEM CELL; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; S PHASE CELL CYCLE CHECKPOINT;

APOPTOSIS; CELL CYCLE; CELL LINE; CHROMOSOME ABERRATIONS; DNA REPAIR; DNA REPLICATION; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VARIATION; HUMANS; IMMUNOBLOTTING; PROTEIN KINASES;

EID: 84862858052     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1117     Document Type: Article

References (52)

1. Rossant J. Stem cells from the mammalian blastocyst. Stem Cells 2001;19:477-482. (Pubitemid 33095842)
2. Andrews PW. From teratocarcinomas to embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 2002;357:405-417. (Pubitemid 34489857)
3. Lawson KA, Hage WJ. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 1994;182:68-84; discussion 84-91.
4. Snow MH, Bennett D. Gastrulation in the mouse: Assessment of cell populations in the epiblast of tw18/tw18 embryos. J Embryol Exp Morphol 1978;47:39-52. (Pubitemid 9037414)
5. Hammond EM, Giaccia AJ. The role of ATM and ATR in the cellular response to hypoxia and re-oxygenation. DNA Repair 2004;3:1117-1122. (Pubitemid 38997955)
6. Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 1993;99: 673-679. (Pubitemid 24052018)
7. Walker SK, Hartwich KM, Robinson JS. Long-term effects on off-spring of exposure of oocytes and embryos to chemical and physical agents. Hum Reprod Update 2000;6:564-577.
8. Baker DE, Harrison NJ, Maltby E et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007;25:207-215. (Pubitemid 46227120)
9. Draper JS, Smith K, Gokhale P et al. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 2004;22:53-54. (Pubitemid 38057956)
10. Narva E, Autio R, Rahkonen N et al. High-resolution DNA analysis of human embryonic stem cell lines reveals culture-induced copy number changes and loss of heterozygosity. Nat Biotechnol 2010;28:371-377.
11. Amps K, Andrews PW, Anyfantis G et al. Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat Biotechnol 2011;29:1132-1144.
12. Andrews PW. The selfish stem cell. Nat Biotechnol 2006;24:325-326. (Pubitemid 43372153)
13. Enver T, Soneji S, Joshi C et al. Cellular differentiation hierarchies in normal and culture-adapted human embryonic stem cells. Hum Mol Genet 2005;14:3129-3140. (Pubitemid 41631288)
14. Momcilovic O, Knobloch L, Varum S et al. DNA damage responses in human induced pluripotent stem cells and embryonic stem cells. PLoS One 2010;5:e13410.
15. Barta T, Vinarsky V, Holubcova Z et al. Human embryonic stem cells are capable of executing G1/S checkpoint activation. Stem Cells 2010; 28:1143-1152.
16. Mantel C, Guo Y, Lee MR et al. Checkpoint-apoptosis uncoupling in human and mouse embryonic stem cells: A source of karyotpic instability. Blood 2007;109:4518-4527. (Pubitemid 46743423)
17. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147. (Pubitemid 28516247)
18. Andrews PW, Bronson DL, Benham F et al. A comparative study of eight cell lines derived from human testicular teratocarcinoma. Int J Cancer 1980;26:269-280. (Pubitemid 10049395)
19. Andrews PW, Damjanov I, Simon D et al. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest 1984;50:147-162. (Pubitemid 14199076)
20. Andrews PW, Goodfellow PN, Shevinsky LH et al. Cell-surface antigens of a clonal human embryonal carcinoma cell line: Morphological and antigenic differentiation in culture. Int J Cancer 1982;29:523-531. (Pubitemid 12114626)
21. Bronson DL, Andrews PW, Vessella RL et al. In vitro differentiation of human embryonal carcinoma cells. In: LM Silver, GR Martin and S Strickland, eds. Teratocarcinoma Stem Cells. New York: Cold Spring Harbor Conferences on Cell Proliferation, 1983;10:597-605.
22. Fogh J, Trempe G. New Human Tumor Cell Lines. New York: Plenum Press, 1975.
23. Teshima S, Shimosato Y, Hirohashi S et al. Four new human germ cell tumor cell lines. Lab Invest 1988;59:328-336.
24. Draper JS, Pigott C, Thomson JA et al. Surface antigens of human embryonic stem cells: Changes upon differentiation in culture. J Anat 2002;200(Pt 3):249-258. (Pubitemid 34467317)
25. Gagou ME, Zuazua-Villar P, Meuth M. Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 2010;21:739-752.
26. Rodriguez R, Gagou ME, Meuth M. Apoptosis induced by replication inhibitors in Chk1-depleted cells is dependent upon the helicase cofactor Cdc45. Cell Death Differ 2008;15:889-898. (Pubitemid 351524431)
27. Bolderson E, Scorah J, Helleday T et al. ATM is required for the cellular response to thymidine induced replication fork stress. Hum Mol Genet 2004;13:2937-2945. (Pubitemid 39585226)
28. Mendez J, Stillman B. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: Assembly of prereplication complexes in late mitosis. Mol Cell Biol 2000;20:8602-8612.
29. Syljuasen RG, Sorensen CS, Hansen LT et al. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 2005;25: 3553-3562. (Pubitemid 40559562)
30. Legerski RJ. Repair of DNA interstrand cross-links during S phase of the mammalian cell cycle. Environ Mol Mutagen 2010;51:540-551.
31. Rodriguez R, Meuth M. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell 2006;17:402-412. (Pubitemid 43049492)
32. Myers K, Gagou ME, Zuazua-Villar P et al. ATR and Chk1 suppress a caspase-3-dependent apoptotic response following DNA replication stress. PLoS Genet 2009;5:e1000324.
33. Ciccia A, Elledge SJ. The DNA damage response: Making it safe to play with knives. Mol Cell 2010;40:179-204.
34. Matsuura M, Wakasugi K, Yamashita T et al. Cleavage-mediated activation of CHK1 during apoptosis. J Biol Chem 2008;283: 25485-25491.
35. Meuth M. Chk1 suppressed cell death. Cell Div 2010;5:21.
36. Rogakou EP, Nieves-Neira W, Boon C et al. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000;275:9390-9395. (Pubitemid 30185164)
37. Byun TS, Pacek M, Yee MC et al. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 2005;19:1040-1052. (Pubitemid 40632450)
38. Cimprich KA, Cortez D. ATR: An essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008;9:616-627. (Pubitemid 352032926)
39. Sirbu BM, Couch FB, Feirgerle JT et al. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 2011;25: 1320-1327.
40. Delacroix S, Wagner JM, Kobayashi M et al. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev 2007;21:1472-1477. (Pubitemid 46955719)
41. Petermann E, Helleday T. Pathways of mammalian replication fork restart. Nat Rev Mol Cell Biol 2010;11:683-687.
42. Lundin C, Erixon K, Arnaudeau C et al. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol Cell Biol 2002;22:5869-5878. (Pubitemid 34815835)
43. Sorensen CS, Hansen LT, Dziegielewski J et al. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 2005;7:195-201. (Pubitemid 40268135)
44. Oosterhuis JW, Andrews PW, Knowles BB et al. Effects of cis-platinum on embryonal carcinoma cell lines in vitro. Int J Cancer 1984;34: 133-139. (Pubitemid 14095128)
45. Liu Q, Guntuku S, Cui XS et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 2000;14:1448-1459. (Pubitemid 30421838)
46. Takai H, Tominaga K, Motoyama N et al. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev 2000;14:439-447.
47. Petermann E, Maya-Mendoza A, Zachos G et al. Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol Cell Biol 2006;26:3319-3326.
48. Petermann E, Woodcock M, Helleday T. Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci USA 2010;107:16090-16095.
49. Pines A, Kelstrup CD, Vrouwe MG et al. Global phosphoproteome profiling reveals unanticipated networks responsive to cisplatin treatment of embryonic stem cells. Mol Cell Biol 2011;31:4964-4977.
50. Hanna J, Cheng AW, Saha K et al. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci USA 2010;107:9222-9227.
51. Olariu V, Harrison NJ, Coca D et al. Modeling the evolution of culture-adapted human embryonic stem cells. Stem Cell Res 2009;4: 50-56.
52. Byrne AT, Southgate J, Brison DR, Leese HJ. Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J Reprod Fertil 1999;117:97-105.