Deficient DNA damage response and cell cycle checkpoints lead to accumulation of point mutations in human embryonic stem cells

Stem Cells

Volumn 30, Issue 9, 2012, Pages 1901-1910

  Hyka Nouspikel, Nevila ^a   Desmarais, Joëlle ^a   Gokhale, Paul J ^a   Jones, Mark ^a   Meuth, Mark ^a   Andrews, Peter W ^a   Nouspikel, Thierry ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Cancer; Cell cycle checkpoints; DNA damage; Human embryonic stem cells; Nucleotide excision repair; Point mutations

Indexed keywords

ATM PROTEIN; CASPASE 3; CYCLIN DEPENDENT KINASE INHIBITOR 1; NUCLEOTIDE; PROTEIN TYROSINE PHOSPHATASE; STAGE SPECIFIC EMBRYO ANTIGEN 3;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; EMBRYO; EMBRYONIC STEM CELL; EXCISION REPAIR; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MOUSE; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PLURIPOTENT STEM CELL; POINT MUTATION; S PHASE CELL CYCLE CHECKPOINT; ULTRAVIOLET RADIATION;

APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL GROWTH PROCESSES; CELLS, CULTURED; DNA DAMAGE; DNA REPAIR; EMBRYONIC STEM CELLS; HUMANS; POINT MUTATION;

EID: 84865311417     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1177     Document Type: Article

References (70)

1. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-956.
2. Mitsui K, Tokuzawa Y, Itoh H et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003;113:631-642.
3. Shevinsky LH, Knowles BB, Damjanov I et al. Monoclonal antibody to murine embryos defines a stage-specific embryonic antigen expressed on mouse embryos and human teratocarcinoma cells. Cell 1982;30:697-705.
4. 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.
5. 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.
6. Stewart MH, Bendall SC, Levadoux-Martin M et al. Clonal tracking of hESCs reveals differential contribution to functional assays. Nat Methods 2010;7:917-922.
7. Enver T, Pera M, Peterson C et al. Stem cell states, fates, and the rules of attraction. Cell Stem Cell 2009;4:387-397.
8. Ambartsumyan G, Clark AT. Aneuploidy and early human embryo development. Hum Mol Genet 2008;17:R10-15.
9. Wilton L. Preimplantation genetic diagnosis for aneuploidy screening in early human embryos: A review. Prenat Diagn 2002;22:512-518.
10. 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.
11. 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.
12. 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.
13. Solter D. From teratocarcinomas to embryonic stem cells and beyond: A history of embryonic stem cell research. Nat Rev Genet 2006;7:319-327.
14. Blum B, Benvenisty N. The tumorigenicity of diploid and aneuploid human pluripotent stem cells. Cell Cycle 2009;8:3822-3830.
15. Andrews PW. From teratocarcinomas to embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 2002;357:405-417.
16. Rodriguez-Jimenez FJ, Moreno-Manzano V, Lucas-Dominguez R et al. Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 2008;26:2052-2062.
17. 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.
18. Momcilovic O, Choi S, Varum S et al. Ionizing radiation induces ataxia telangiectasia mutated-dependent checkpoint signaling and G(2) but not G(1) cell cycle arrest in pluripotent human embryonic stem cells. Stem Cells 2009;27:1822-1835.
19. Gillet LC, Scharer OD. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 2006;106:253-276.
20. Wood RD. DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 1999;81:39-44.
21. Nouspikel T. DNA repair in differentiated cells: Some new answers to old questions. Neuroscience 2007;145:1213-1221.
22. Nouspikel T. DNA repair in mammalian cells: Nucleotide excision repair: Variations on versatility. Cell Mol Life Sci 2009;66:994-1009.
23. Nouspikel T, Hanawalt PC. DNA repair in terminally differentiated cells. DNA Repair 2002;1:59-75.
24. Nouspikel T, Hanawalt PC. Terminally differentiated human neurons repair transcribed genes but display attenuated global DNA repair and modulation of repair gene expression. Mol Cell Biol 2000;20:1562-1570.
25. Hsu PS, Hanawalt PC, Nouspikel T. Nucleotide excision repair pheno-type of human acute myeloid leukemia cell lines at various stages of differentiation. Mutat Res 2007;614:3-15.
26. Nouspikel TP, Hyka-Nouspikel N, Hanawalt PC. Transcription domain-associated repair in human cells. Mol Cell Biol 2006;26:8722-8730.
27. Hyka-Nouspikel N, Lemonidis K, Lu WT et al. Circulating human B lymphocytes are deficient in nucleotide excision repair and accumulate mutations upon proliferation. Blood 2011;117:6277-6286.
28. Hyka-Nouspikel N, Nouspikel T. Nucleotide excision repair and B lymphoma: Somatic hypermutation is not the only culprit. Cell Cycle 2011;10:2276-2280.
29. Nouspikel T, Hanawalt PC. Impaired nucleotide excision repair upon macrophage differentiation is corrected by E1 ubiquitin-activating enzyme. Proc Natl Acad Sci USA 2006;103:16188-16193.
30. Nouspikel T. Multiple roles of ubiquitination in the control of nucleotide excision repair. Mech Ageing Dev 2011;132:355-365.
31. Kusumoto R, Masutani C, Sugasawa K et al. Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat Res 2001;485:219-227.
32. Kim JK, Patel D, Choi BS. Contrasting structural impacts induced by cis-syn cyclobutane dimer and (6-4) adduct in DNA duplex decamers: Implication in mutagenesis and repair activity. Photochem Photobiol 1995;62:44-50.
33. Stary A, Kannouche P, Lehmann AR et al. Role of DNA polymerase eta in the UV mutation spectrum in human cells. J Biol Chem 2003;278:18767-18775.
34. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K et al. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004;73:39-85.
35. McCulloch SD, Kunkel TA. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 2008;18:148-161.
36. Spivak G, Hanawalt P. Determination of damage and repair in specific DNA sequences. Methods - A Companion To Methods In Enzymology. Edited by Freidberg EC. Academic Press, London. Vol 7,1995:147-161.
37. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
38. Aflatoonian B, Ruban L, Shamsuddin S et al. Generation of Sheffield (Shef) human embryonic stem cell lines using a microdrop culture system. In Vitro Cell Dev Biol Anim 2010;46:236-241.
39. Ford J, Hanawalt PC. Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts. J Biol Chem 1997;272:28073-28080.
40. 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.
41. Lee J, Go Y, Kang I et al. Oct-4 controls cell-cycle progression of embryonic stem cells. Biochem J 2010;426:171-181.
42. Scrima A, Konickova R, Czyzewski BK et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 2008;135:1213-1223.
43. Lehmann AR, Niimi A, Ogi T et al. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst) 2007;6:891-899.
44. Roos WP, Christmann M, Fraser ST et al. Mouse embryonic stem cells are hypersensitive to apoptosis triggered by the DNA damage O(6)-methylguanine due to high E2F1 regulated mismatch repair. Cell Death Differ 2007;14:1422-1432.
45. Kaufmann WK. The human intra-S checkpoint response to UVC-induced DNA damage. Carcinogenesis 2010;31:751-765.
46. Mazroui R, Di Marco S, Kaufman RJ et al. Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol Biol Cell 2007;18:2603-2618.
47. Iakova P, Wang GL, Timchenko L et al. Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO J 2004;23:406-417.
48. Malashicheva AB, Kislyakova TV, Aksenov ND et al. F9 embryonal carcinoma cells fail to stop at G1/S boundary of the cell cycle after gamma-irradiation due to p21WAF1/CIP1 degradation. Oncogene 2000;19:3858-3865.
49. Abbas T, Dutta A. p21 in cancer: Intricate networks and multiple activities. Nat Rev Cancer 2009;9:400-414.
50. Fluckiger AC, Marcy G, Marchand M et al. Cell cycle features of primate embryonic stem cells. Stem Cells 2006;24:547-556.
51. Nakanishi M, Adami GR, Robetorye RS et al. Exit from G0 and entry into the cell cycle of cells expressing p21Sdi1 antisense RNA. Proc Natl Acad Sci USA 1995;92:4352-4356.
52. Bissonnette N, Hunting DJ. p21-Induced cycle arrest in G1 protects cells from apoptosis induced by UV-irradiation or RNA polymerase II blockage. Oncogene 1998;16:3461-3469.
53. Deng C, Zhang P, Harper JW et al. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995;82:675-684.
54. Brugarolas J, Chandrasekaran C, Gordon JI et al. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995;377:552-557.
55. de Waard H, Sonneveld E, de Wit J et al. Cell-type-specific consequences of nucleotide excision repair deficiencies: Embryonic stem cells versus fibroblasts. DNA Repair (Amst) 2008;7:1659-1669.
56. Banuelos CA, Banath JP, MacPhail SH et al. Mouse but not human embryonic stem cells are deficient in rejoining of ionizing radiation-induced DNA double-strand breaks. DNA Repair (Amst) 2008;7:1471-1483.
57. Adams BR, Golding SE, Rao RR et al. Dynamic dependence on ATR and ATM for double-strand break repair in human embryonic stem cells and neural descendants. PLoS One 2010;5:e10001.
58. Maynard S, Swistowska AM, Lee JW et al. Human embryonic stem cells have enhanced repair of multiple forms of DNA damage. Stem Cells 2008;26:2266-2274.
59. Momcilovic O, Knobloch L, Fornsaglio J et al. DNA damage responses in human induced pluripotent stem cells and embryonic stem cells. PLoS One 2010;5:e13410.
60. Smith ML, Ford JM, Hollander MC et al. p53-Mediated DNA repair responses to UV radiation: Studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol Cell Biol 2000;20:3705-3714.
61. Soria G, Podhajcer O, Prives C et al. P21Cip1/WAF1 downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene 2006;25:2829-2838.
62. Avkin S, Sevilya Z, Toube L et al. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol Cell 2006;22:407-413.
63. McDonald ER, 3rd, Wu GS, Waldman T et al. Repair defect in p21 WAF1/CIP1 -/- human cancer cells. Cancer Res 1996;56:2250-2255.
64. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993;362:709-715.
65. Pasqualucci L, Migliazza A, Fracchiolla N et al. BCL-6 mutations in normal germinal center B cells: Evidence of somatic hypermutation acting outside Ig loci. Proc Natl Acad Sci USA 1998;95:11816-11821.
66. Capello D, Vitolo U, Pasqualucci L et al. Distribution and pattern of BCL-6 mutations throughout the spectrum of B-cell neoplasia. Blood 2000;95:651-659.
67. Garcia-Fernandez M, Kissel H, Brown S et al. Sept4/ARTS is required for stem cell apoptosis and tumor suppression. Genes Dev 2010;24:2282-2293.
68. Li F, Tiede B, Massague J et al. Beyond tumorigenesis: Cancer stem cells in metastasis. Cell Res 2007;17:3-14.
69. Jordan CT. Cancer stem cells: Controversial or just misunderstood? Cell Stem Cell 2009;4:203-205.
70. Gerson SL, Reese J, Kenyon J. DNA repair in stem cell maintenance and conversion to cancer stem cells. Ernst Schering Found Symp Proc 2006:231-244.