Chronic p53-independent p21 expression causes genomic instability by deregulating replication licensing

Nature Cell Biology

Volumn 18, Issue 7, 2016, Pages 777-789

  Galanos, Panagiotis ^a   Vougas, Konstantinos ^b   Walter, David ^c   Polyzos, Alexander ^b   Maya Mendoza, Apolinar ^d   Haagensen, Emma J ^e   Kokkalis, Antonis ^b   Roumelioti, Fani Marlen ^b   Gagos, Sarantis ^b   Tzetis, Maria ^a   Canovas, Begona ^f   Igea, Ana ^f   Ahuja, Akshay K ^g   Zellweger, Ralph ^g   Havaki, Sofia ^a   Kanavakis, Emanuel ^a,h   Kletsas, Dimitris ⁱ   Roninson, Igor B ^j   Garbis, Spiros D ^k   Lopes, Massimo ^g   Nebreda, Angel ^f,l   Thanos, Dimitris ^b   Blow, J Julian ^e   Townsend, Paul ^m   SØrensen, Claus Storgaard ^c   Bartek, Jiri ^d,n,o   Gorgoulis, Vassilis G ^a,b,m   more..

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^g UNIVERSITY OF ZURICH   (Switzerland)

^h AGHIA SOPHIA CHILDREN S HOSPITAL   (Greece)

ⁱ INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^j UNIVERSITY OF SOUTH CAROLINA   (United States)

^k UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^l INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^m UNIVERSITY OF MANCHESTER   (United Kingdom)

ⁿ PALACKÝ UNIVERSITY   (Czech Republic)

^o KAROLINSKA INSTITUTE   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; MUTANT PROTEIN; PROTEIN P53; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLINE; TP53 PROTEIN, HUMAN;

ARTICLE; CARCINOGENICITY; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; DNA REPLICATION; DNA REPLICATION LICENSING DEREGULATION; DRUG RESISTANCE; GENOMIC INSTABILITY; GENOMICS; HUMAN; HUMAN CELL; HUMAN TISSUE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENESCENCE; TUMOR CELL; TUMOR PROMOTION; UPREGULATION; CELL CULTURE; GENETICS; METABOLISM; NEOPLASM;

CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84975299921     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3378     Document Type: Article

References (75)

1. Abbas T, & Dutta A. p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer 9, 400-414 (2009).
2. Roninson I. B. Oncogenic functions of tumour suppressor p21(Waf1/Cip1/Sdi1): association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett. 179, 1-14 (2002).
3. Pateras I. S, Apostolopoulou K, Niforou K, Kotsinas A, & Gorgoulis V. G. p57KIP2: Kiping the cell under control. Mol. Cancer Res. 7, 1902-1919 (2009).
4. Rivlin N, Brosh R, Oren M, & Rotter V. Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis. Genes Cancer 2, 466-474 (2011).
5. Warfel N. A, & El-Deiry W. S. p21WAF1 and tumourigenesis: 20 years after. Curr. Opin. Oncol. 25, 52-58 (2013).
6. Abbas T, Keaton M. A, & Dutta A. Genomic instability in cancer. Cold Spring Harb. Perspect. Biol. 5, a012914 (2013).
7. Blow J. J, & Dutta A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486 (2005).
8. Petrakis T. G, et al. Exploring and exploiting the systemic effects of deregulated replication licensing. Semin. Cancer Biol. 37-38, 3-15 (2016).
9. Blow J. J, & Gillespie P. J. Replication licensing and cancer-A fatal entanglement? Nat. Rev. Cancer 8, 799-806 (2008).
10. Negrini S, Gorgoulis V. G, & Halazonetis T. D. Genomic instability-An evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11, 220-228 (2010).
11. Halazonetis T. D, Gorgoulis V. G, & Bartek J. An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355 (2008).
12. Sideridou M, et al. Cdc6 expression represses E-cadherin transcription and activates adjacent replication origins. J. Cell Biol. 195, 1123-1140 (2011).
13. Karakaidos P, et al. Overexpression of the replication licensing regulators hCdt1 and hCdc6 characterizes a subset of non-small-cell lung carcinomas: synergistic effect with mutant p53 on tumor growth and chromosomal instability-evidence of E2F-1 transcriptional control over hCdt1. Am. J. Pathol. 165, 1351-1365 (2004).
14. Liontos M, et al. Deregulated overexpression of hCdt1 and hCdc6 promotes malignant behavior. Cancer Res. 67, 10899-10909 (2007).
15. Rosai J R. Ackerman?s Surgical Pathology (Elsevier (2011).
16. Velimezi G, et al. Functional interplay between the DNA-damage-response kinase ATM and ARF tumour suppressor protein in human cancer. Nat. Cell Biol. 15, 967-977 (2013).
17. Cooks T, et al. Mutant p53 prolongs NF-B activation and promotes chronic inflammation and inflammation-Associated colorectal cancer. Cancer Cell 23, 634-646 (2013).
18. Agarwal M. L, Agarwal A, Taylor W. R, & Stark G. R. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl Acad. Sci. USA 92, 8493-8497 (1995).
19. Bates S, Ryan K. M, Phillips A. C, & Vousden K. H. Cell cycle arrest and DNA endoreduplication following p21Waf1/Cip1 expression. Oncogene 17, 1691-1703 (1998).
20. Havens C. G, & Walter J. C. Mechanism of CRL4(Cdt2), a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 25, 1568-1582 (2011).
21. Jørgensen S, et al. SET8 is degraded via PCNA-coupled CRL4(CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 192, 43-54 (2011).
22. Gibbs E, et al. The influence of the proliferating cell nuclear antigen-interacting domain of p21(CIP1) on DNA synthesis catalyzed by the human and Saccharomyces cerevisiae polymerase delta holoenzymes. J. Biol. Chem. 272, 2373-2381 (1997).
23. Duursma A, & Agami R. p53-dependent regulation of Cdc6 protein stability controls cellular proliferation. Mol. Cell. Biol. 25, 6937-6947 (2005).
24. Peart M. J, et al. APC/C(Cdc20) targets E2F1 for degradation in prometaphase. Cell Cycle 9, 3956-3964 (2010).
25. Budhavarapu V. N, et al. Regulation of E2F1 by APC/C Cdh1 via K11 linkage-specific ubiquitin chain formation. Cell Cycle 11, 2030-2038 (2012).
26. Vaziri C, et al. A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11, 997-1008 (2003).
27. Gorgoulis V. G et al. p53 activates ICAM-1 CD54) expression in an NF-Bindependent manner. EMBO J. 22, 1567-1578 (2003).
28. Bester A. C, et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446 (2011).
29. Essers J, et al. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25, 9350-9359 (2005).
30. Barlow J. H, et al. Identification of early replicating fragile sites that contribute to genome instability. Cell 152, 620-632 (2013).
31. Beck H, et al. Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J. Cell Biol. 188, 629-638 (2010).
32. Petermann E, & Helleday T. Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 11, 683-687 (2010).
33. Neelsen K. J, et al. Deregulated origin licensing leads to chromosomal breaks by rereplication of a gapped DNA template. Genes Dev. 27, 2537-2542 (2013).
34. Couch F. B, et al. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 27, 1610-1623 (2013).
35. Neelsen K. J, et al. Visualization and interpretation of eukaryotic DNA replication intermediates in vivo by electron microscopy. Methods Mol. Biol. 1094, 177-208 (2014).
36. Zellweger R, et al. Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. J. Cell Biol. 208, 563-579 (2015).
37. Neelsen K. J, & Lopes M. Replication fork reversal in eukaryotes: from dead end to dynamic response. Nat. Rev. Mol. Cell Biol. 16, 207-220 (2015).
38. Hanada K, et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14, 1096-1104 (2007).
39. Neelsen K. J, Zanini I. M, Herrador R, & Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 200, 699-708 (2013).
40. Murfuni I, et al. The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation. Oncogene 32, 610-620 (2013).
41. Wu Y, Kantake N, Sugiyama T, & Kowalczykowski S. C. Rad51 protein controls Rad52-mediated DNA annealing. J. Biol. Chem. 283, 14883-14892 (2008).
42. Ottaviani D, LeCain M, & Sheer D. The role of microhomology in genomic structural variation. Trends Genet. 30, 85-94 (2014).
43. Iraqui I, et al. Recovery of arrested replication forks by homologous recombination is error-prone. PLoS Genet. 8, e1002976 (2012).
44. Benson E. K, et al. p53-dependent gene repression through p21 is mediated by recruitment of E2F4 repression complexes. Oncogene 33 3959-3969 (2014).
45. Bartkova J, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637 (2006).
46. Liontos M, et al. Modulation of the E2F1-driven cancer cell fate by the DNA damage response machinery and potential novel E2F1 targets in osteosarcomas. Am. J. Pathol. 175, 376-391 (2009).
47. Gonzalez S, et al. Oncogenic activity of Cdc6 through repression of the INK4/ARF locus. Nature 440, 702-706 (2006).
48. BeausÉjour C. M, et al. Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J. 22, 4212-4222 (2003).
49. Woo R. A, & Poon R. Y. Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle 2, 316-324 (2003).
50. Pines J, & Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-17 (1991).
51. Yu J., et al. A network of p73, p53 and Egr1 is required for efficient apoptosis in tumor cells. Cell Death Differ. 14, 436-446 (2007).
52. Terradas M, Martín M, Tusell L, & Genescà A. DNA lesions sequestered in micronuclei induce a local defective-damage response. DNA Repair (Amst) 8, 1225-1234 (2009).
53. Holland A. J, & Cleveland D. W. Chromoanagenesis and cancer: mechanisms and consequences of localized, complex chromosomal rearrangements. Nat. Med. 18, 1630-1638 (2012).
54. Perkins N. D, et al. Regulation of NF-B by cyclin-dependent kinases associated with the p300 coactivator. Science 275, 523-527 (1997).
55. Viale A, et al. Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature 457, 51-56 (2009).
56. Shay J. W, & Roninson I. B. Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 23, 2919-2933 (2004).
57. Nishitani H, et al. Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25, 1126-1136 (2006).
58. Niculescu A. B, et al. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol. 18, 629-643 (1998).
59. Porter A. C. Preventing DNA over-replication: a Cdk perspective. Cell Div. 3, 3 (2008).
60. Hastings P. J, Ira G, & Lupski J. R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5 e1000327 (2009).
61. Zhang C. Z, Leibowitz M. L, & Pellman D. Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangements. Genes Dev. 27, 2513-2530 (2013).
62. Stephens P. J, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40 (2011).
63. Sikder H. A, Devlin M. K, Dunlap S, Ryu B, & Alani R. M. Id proteins in cell growth and tumorigenesis. Cancer Cell 3, 525-530 (2003).
64. Burrell R. A, McGranahan N, Bartek J, & Swanton C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338-345 (2013).
65. Cha H. H, et al. Glucocorticoids stimulate p21 gene expression by targeting multiple transcriptional elements within a steroid responsive region of the p21waf1/cip1 promoter in rat hepatoma cells. J. Biol. Chem. 273, 1998-2007 (1998).
66. Georgakopoulou E. A, et al. Specific lipofuscin staining as a novel biomarker to detect replicative and stress-induced senescence. A method applicable in cryo-preserved and archival tissues. Aging 5, 37-50 (2013).
67. Evangelou K, et al. The DNA damage checkpoint precedes activation of ARF in response to escalating oncogenic stress during tumorigenesis. Cell Death Differ. 20, 1485-1497 (2013).
68. DelehouzÉ C, et al. CDK/CK1 inhibitors roscovitine and CR8 downregulate amplified MYCN in neuroblastoma cells. Oncogene 33, 5675-5687 (2014).
69. Papachristou E. K, et al. The shotgun proteomic study of the human ThinPrep cervical smear using iTRAQ mass-tagging and 2D LC-FT-Orbitrap-MS: the detection of the human papillomavirus at the protein level. J. Proteome Res. 12, 2078-2089 (2013).
70. Ramirez-Gonzalez R. H, et al. StatsDB: platform-Agnostic storage and understanding of next generation sequencing run metrics. F1000Res. 2, 248 (2013).
71. Langmead B, & Salzberg S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
72. Li H, et al. 1000 genome project data processing subgroup. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
73. Chen K, et al. BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat. Methods 6, 677-681 (2009).
74. de Winter J. C. F. Using the Student?s t-test with extremely small sample sizes. Pract. Assess. Res. Eval. 18, 10 (2013).
75. Venkatraman E. S, & Olshen A. B. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23 657-663 (2007).