Functional interplay between the DNA-damage-response kinase ATM and ARF tumour suppressor protein in human cancer

Nature Cell Biology

Volumn 15, Issue 8, 2013, Pages 967-977

  Velimezi, Georgia ^a   Liontos, Michalis ^a   Vougas, Konstantinos ^b   Roumeliotis, Theodoros ^b,c   Bartkova, Jirina ^d   Sideridou, Maria ^a   Dereli Oz, Ayguel ^e   Kocylowski, MacIej ^d   Pateras, Ioannis S ^a   Evangelou, Kostas ^a   Kotsinas, Athanassios ^a   Orsolic, Ines ^f   Bursac, Sladana ^f   Cokaric Brdovcak, Maja ^f   Zoumpourlis, Vassilis ^g   Kletsas, Dimitris ^h   Papafotiou, George ^b   Klinakis, Apostolos ^b   Volarevic, Sinisa ^f   Gu, Wei ⁱ   Bartek, Jiri ^d,j   Halazonetis, Thanos D ^e   Gorgoulis, Vassilis G ^a,b   more..

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f UNIVERSITY OF RIJEKA   (Croatia)

^g INSTITUTE OF BIOLOGY   (Greece)

^h INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

ⁱ New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^j PALACKÝ UNIVERSITY   (Czech Republic)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; ATM PROTEIN; MESSENGER RNA; NUCLEOPHOSMIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN KINASE; PROTEIN NEK2A; PROTEIN ULF; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARF GENE; ARTICLE; ATM GENE; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG NON SMALL CELL CANCER; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

ADP-RIBOSYLATION FACTOR 1; ANIMALS; CARRIER PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; MALE; MICE; NEOPLASMS; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMES; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84881481725     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2795     Document Type: Article

References (76)

1. Sherr, C. J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 6, 663-673 (2006). (Pubitemid 44285999)
2. Kim, W. Y. & Sharpless, N. E. The regulation of INK4/ARF in cancer and aging. Cell 127, 265-275 (2006). (Pubitemid 44572384)
3. Bartek, J., Bartkova, J. & Lukas, J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 26, 7773-7779 (2007). (Pubitemid 350242463)
4. Halazonetis, T. D., Gorgoulis, V. G. & Bartek, J. An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355 (2008). (Pubitemid 351354863)
5. Jackson, S. P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071-1078 (2009).
6. Negrini, S., Gorgoulis, V. G. & Halazonetis, T. D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11, 220-228 (2010).
7. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
8. Kastan, M. B. & Bartek, J. Cell-cycle checkpoints and cancer. Nature 432, 316-323 (2004). (Pubitemid 39551659)
9. Kamijo, T. et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91, 649-659 (1997). (Pubitemid 27513656)
10. Stott, F. J. et al. The alternative product from the human CDKN2A locus, p14ARF, participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 17, 5001-5014 (1998). (Pubitemid 28408466)
11. Kamijo, T. et al. Loss of the ARF tumor suppressor reverses premature replicative arrest but not radiation hypersensitivity arising from disabled atm function. Cancer Res. 59, 2464-2469 (1999). (Pubitemid 29242298)
12. Shiloh, Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168 (2003). (Pubitemid 37328868)
13. Efeyan, A. et al. Limited role of murine ATM in oncogene-induced senescence and p53-dependent tumor suppression. PLoS One 4, e5475 (2009).
14. Hickson, I. et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159 (2004). (Pubitemid 39665530)
15. DiTullio, R. A. Jr et al. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 12, 998-1002 (2002).
16. Tsantoulis, P. K. & Gorgoulis, V. G. Involvement of E2F transcription factor family in cancer. Eur. J. Cancer 41, 2403-2414 (2005). (Pubitemid 41540618)
17. 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).
18. Ramirez, R. D. et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 64, 9027-9034 (2004). (Pubitemid 39665513)
19. Sato, M. et al. Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res. 66, 2116-2128 (2006).
20. Inoue, R., Asker, C., Klangby, U., Pisa, P. & Wiman, K. G. Induction of the human ARF protein by serum starvation. Anticancer Res. 19, 2939-2943 (1999). (Pubitemid 30042574)
21. Chen, D., Shan, J., Zhu, W. G., Qin, J. & Gu, W. Transcription- independent ARF regulation in oncogenic stress-mediated p53 responses. Nature 464, 624-627 (2010).
22. Enomoto, T., Lindstrom, M. S., Jin, A., Ke, H. & Zhang, Y. Essential role of the B23/NPM core domain in regulating ARF binding and B23 stability. J. Biol. Chem. 281, 18463-18472 (2006). (Pubitemid 44035505)
23. Colombo, E. et al. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol. Cell. Biol. 25, 8874-8886 (2005). (Pubitemid 41429079)
24. Kuo, M. L., den Besten, W., Bertwistle, D., Roussel, M. F. & Sherr, C. J. N-terminal polyubiquitination and degradation of the Arf tumor suppressor. Genes Dev. 18, 1862-1874 (2004). (Pubitemid 39025096)
25. Huang, M., Itahana, K., Zhang, Y. & Mitchell, B. S. Depletion of guanine nucleotides leads to the Mdm2-dependent proteasomal degradation of nucleostemin. Cancer Res. 69, 3004-3012 (2009).
26. Lee, C., Smith, B. A., Bandyopadhyay, K. & Gjerset, R. A. DNA damage disrupts the p14ARF-B23 (nucleophosmin) interaction and triggers a transient subnuclear redistribution of p14ARF. Cancer Res. 65, 9834-9842 (2005). (Pubitemid 41541462)
27. Matsuoka, S. et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007). (Pubitemid 46877472)
28. Lin, C. Y. et al. Dephosphorylation of nucleophosmin by PP1 β facilitates pRB binding and consequent E2F1-dependent DNA repair. Mol. Biol. Cell 21, 4409-4417 (2010).
29. Tang, X. et al. A novel ATM-dependent pathway regulates protein phosphatase 1 in response to DNA damage. Mol. Cell. Biol. 28, 2559-2566 (2008). (Pubitemid 351542357)
30. Scheer, U. & Benavente, R. Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12, 14-21 (1990).
31. Trinkle-Mulcahy, L., Sleeman, J. E. & Lamond, A. I. Dynamic targeting of protein phosphatase 1 within the nuclei of living mammalian cells. J. Cell Sci. 114, 4219-4228 (2001). (Pubitemid 33138659)
32. Hayward, D. G. & Fry, A. M. Nek2 kinase in chromosome instability and cancer. Cancer Lett. 237, 155-166 (2006). (Pubitemid 43777084)
33. Noguchi, K., Fukazawa, H., Murakami, Y. & Uehara, Y. Nucleolar Nek11 is a novel target of Nek2A in G1/S-arrested cells. J. Biol. Chem. 279, 32716-32727 (2004). (Pubitemid 39014731)
34. Colombo, E., Alcalay, M. & Pelicci, P. G. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene 30, 2595-2609 (2011).
35. Sugimoto, M., Kuo, M. L., Roussel, M. F. & Sherr, C. J. Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol. Cell 11, 415-424 (2003). (Pubitemid 36293835)
36. Itahana, K. et al. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol. Cell 12, 1151-1164 (2003). (Pubitemid 37487925)
37. Grandori, C. et al. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 7, 311-318 (2005). (Pubitemid 40331133)
38. Lessard, F. et al. The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I. Mol. Cell 38, 539-550 (2010).
39. Huang, M., Ji, Y., Itahana, K., Zhang, Y. & Mitchell, B. Guanine nucleotide depletion inhibits pre-ribosomal RNA synthesis and causes nucleolar disruption. Leuk. Res. 32, 131-141 (2008). (Pubitemid 350103806)
40. Cox, J. & Mann, M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80, 273-299 (2011).
41. Li, Z. et al. Systematic comparison of label-free, metabolic labeling, and isobaric chemical labeling for quantitative proteomics on LTQ Orbitrap Velos. J. Proteome. Res. 11, 1582-1590 (2012).
42. Falck, J., Mailand, N., Syljuasen, R. G., Bartek, J. & Lukas, J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410, 842-847 (2001). (Pubitemid 32303786)
43. Choi, J. et al. Selective requirement of H2B N-Terminal tail for p14ARF induced chromatin silencing. Nucleic. Acids Res. 39, 9167-9180 (2011).
44. Sarkaria, J. N. et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59, 4375-4382 (1999). (Pubitemid 29418757)
45. Gorgoulis, V. G. et al. Alterations of the p16-pRb pathway and the chromosome locus 9p21-22 in non-small-cell lung carcinomas: relationship with p53 and MDM2 protein expression. Am. J. Pathol. 153, 1749-1765 (1998). (Pubitemid 28550663)
46. Gorgoulis, V. G. et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913 (2005). (Pubitemid 40559004)
47. Zeng, Y., Kotake, Y., Pei, X. H., Smith, M. D. & Xiong, Y. p53 binds to and is required for the repression of Arf tumor suppressor by HDAC and polycomb. Cancer Res. 71, 2781-2792 (2011).
48. Jiang, H. et al. The combined status of ATM and p53 link tumor development with therapeutic response. Genes Dev. 23, 1895-1909 (2009).
49. Gorgoulis, V. G. & Halazonetis, T. D. Oncogene-induced senescence: the bright and dark side of the response. Curr. Opin. Cell Biol. 22, 816-827 (2010).
50. Di Micco, R. et al. DNA damage response activation in mouse embryonic fibroblasts undergoing replicative senescence and following spontaneous immortalization. Cell Cycle 7, 3601-3606 (2008).
51. Churchman, M. L., Roig, I., Jasin, M., Keeney, S. & Sherr, C. J. Expression of ARF tumor suppressor in spermatogonia facilitates meiotic progression in male germ cells. Plos Genetics 7, e1002157 (2011).
52. Takubo, K. et al. Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA-induced cell-cycle arrest. Cell Stem. Cell 2, 170-182 (2008). (Pubitemid 351168710)
53. Li, Y. et al. ATM activity contributes to the tumor-suppressing functions of p14ARF. Oncogene 23, 7355-7365 (2004). (Pubitemid 39382138)
54. Eymin, B. et al. p14ARF activates a Tip60-dependent and p53-independent ATM/ATR/CHK pathway in response to genotoxic stress. Mol. Cell Biol. 26, 4339-4350 (2006). (Pubitemid 43788032)
55. Khan, S. H., Moritsugu, J. & Wahl, G. M. Differential requirement for p19ARF in the p53-dependent arrest induced by DNA damage, microtubule disruption, and ribonucleotide depletion. Proc. Natl Acad. Sci. USA 97, 3266-3271 (2000). (Pubitemid 30183290)
56. Mitsuhashi, S. et al. Tautomycetin is a novel and specific inhibitor of serine/threonine protein phosphatase type 1, PP1. Biochem. Biophys. Res. Commun. 287, 328-331 (2001). (Pubitemid 32917599)
57. Gorgoulis, V. G. et al. p53 activates ICAM-1 (CD54) expression in an NF-kB-independent manner. EMBO J. 22, 1567-1578 (2003). (Pubitemid 36417405)
58. Liontos, M. et al. Deregulated overexpression of hCdt1 and hCdc6 promotes malignant behavior. Cancer Res. 67, 10899-10909 (2007). (Pubitemid 350145919)
59. Sideridou, M. et al. Cdc6 expression represses E-cadherin transcription and activates adjacent replication origins. J Cell Biol. 195, 1123-1140 (2011).
60. Bartkova, J. et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637 (2006). (Pubitemid 44864442)
61. Hershko, T. & Ginsberg, D. Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F1 mediates apoptosis. J. Biol. Chem. 279, 8627-8634 (2004). (Pubitemid 38295917)
62. Cescutti, R., Negrini, S., Kohzaki, M. & Halazonetis, T. D. TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint. EMBO J. 29, 3723-3732 (2010).
63. Andersen, J. S. et al. Directed proteomic analysis of the human nucleolus. Curr. Biol 12, 1-11 (2002).
64. 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). (Pubitemid 39297739)
65. Zacharatos, P. et al. Distinct expression patterns of the transcription factor E2F-1 in relation to tumour growth parameters in common human carcinomas. J. Pathol. 203, 744-753 (2004). (Pubitemid 38961560)
66. Honrado, E. et al. Immunohistochemical expression of DNA repair proteins in familial breast cancer differentiate BRCA2-associated tumors. J. Clin. Oncol. 23, 7503-7511 (2005). (Pubitemid 46291813)
67. Kilpivaara, O. et al. Correlation of CHEK2 protein expression and c.1100delC mutation status with tumor characteristics among unselected breast cancer patients. Int. J. Cancer 113, 575-580 (2005). (Pubitemid 40038733)
68. Geradts, J., Kratzke, R. A., Niehans, G. A. & Lincoln, C. E. Immunohistochemical detection of the cyclin-dependent kinase inhibitor 2/multiple tumor suppressor gene 1 (CDKN2/MTS1) product p16INK4A in archival human solid tumors: correlation with retinoblastoma protein expression. Cancer Res. 55, 6006-6011 (1995).
69. Vestey, S. B. et al. p14ARF expression in invasive breast cancers and ductal carcinoma in situ-relationships to p53 and Hdm2. Breast Cancer Res 6, R571-R585 (2004).
70. Shilov, I. V. et al. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell Proteom. 6, 1638-1655 (2007). (Pubitemid 47506173)
71. Tang, W. H., Shilov, I. V. & Seymour, S. L. Nonlinear fitting method for determining local false discovery rates from decoy database searches. J. Proteome Res. 7, 3661-3667 (2008).
72. R Development Core Team. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. 409 (2012).
73. Subramanian, A. et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005). (Pubitemid 41528093)
74. Mootha, V. K. et al. PGC-1alpha-responsive genes involved in oxidative phos-phorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273 (2003). (Pubitemid 36792858)
75. Warnes, G. R. Includes R source code and/or documentation contributed by (in alphabetical order): Bolker, B. et al. gplots: various R programming tools for plotting data. R package version 2.10.1 (2011).
76. Brooks, D. G., James, R. M, Patek, C. E., Williamson, J. & Arends, M. J. Mutant K-ras enhances apoptosis in embryonic stem cells in combination with DNA damage and is associated with increased levels of p19(ARF). Oncogene 20, 2144-2152 (2001). (Pubitemid 32424008)