Loss of ATM/Chk2/p53 Pathway Components Accelerates Tumor Development and Contributes to Radiation Resistance in Gliomas

Cancer Cell

Volumn 18, Issue 6, 2010, Pages 619-629

  Squatrito, Massimo ^a   Brennan, Cameron W ^a   Helmy, Karim ^a   Huse, Jason T ^a   Petrini, John H ^a   Holland, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ATM PROTEIN; CHECKPOINT KINASE 2; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; GENETIC CODE; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; IONIZING RADIATION; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIOSENSITIVITY; WILD TYPE;

EID: 78650014447     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2010.10.034     Document Type: Article

References (58)

1. Antoni L., Sodha N., Collins I., Garrett M.D. CHK2 kinase: cancer susceptibility and cancer therapy - two sides of the same coin?. Nat. Rev. Cancer 2007, 7:925-936.
2. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
3. Bartek J., Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003, 3:421-429.
4. Bartek J., Bartkova J., Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 2007, 26:7773-7779.
5. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
6. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.V., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
7. Bartkova J., Horejsi Z., Sehested M., Nesland J.M., Rajpert-De Meyts E., Skakkebaek N.E., Stucki M., Jackson S., Lukas J., Bartek J. DNA damage response mediators MDC1 and 53BP1: constitutive activation and aberrant loss in breast and lung cancer, but not in testicular germ cell tumours. Oncogene 2007, 26:7414-7422.
8. Bartkova J., Hamerlik P., Stockhausen M.T., Ehrmann J., Hlobilkova A., Laursen H., Kalita O., Kolar Z., Poulsen H.S., Broholm H., et al. Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 2010, 29:5095-5102.
9. Bencokova Z., Kaufmann M.R., Pires I.M., Lecane P.S., Giaccia A.J., Hammond E.M. ATM activation and signaling under hypoxic conditions. Mol. Cell. Biol. 2009, 29:526-537.
10. Bleau A.M., Howard B.M., Taylor L.A., Gursel D., Greenfield J.P., Lim Tung H.Y., Holland E.C., Boockvar J.A. New strategy for the analysis of phenotypic marker antigens in brain tumor-derived neurospheres in mice and humans. Neurosurg. Focus 2008, 24:E28.
11. Bleau A.M., Hambardzumyan D., Ozawa T., Fomchenko E.I., Huse J.T., Brennan C.W., Holland E.C. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009, 4:226-235.
12. Brat D.J., Castellano-Sanchez A.A., Hunter S.B., Pecot M., Cohen C., Hammond E.H., Devi S.N., Kaur B., Van Meir E.G. Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res. 2004, 64:920-927.
13. Brennan C., Momota H., Hambardzumyan D., Ozawa T., Tandon A., Pedraza A., Holland E. Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS ONE 2009, 4:e7752.
14. Bristow R.G., Hill R.P. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat. Rev. Cancer 2008, 8:180-192.
15. Charles N., Ozawa T., Squatrito M., Bleau A.M., Brennan C.W., Hambardzumyan D., Holland E.C. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010, 6:141-152.
16. Cybulski C., Gorski B., Huzarski T., Masojc B., Mierzejewski M., Debniak T., Teodorczyk U., Byrski T., Gronwald J., Matyjasik J., et al. CHEK2 is a multiorgan cancer susceptibility gene. Am. J. Hum. Genet. 2004, 75:1131-1135.
17. Dai C., Celestino J.C., Okada Y., Louis D.N., Fuller G.N., Holland E.C. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 2001, 15:1913-1925.
18. Durocher D., Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 2001, 13:225-231.
19. Freiberg R.A., Hammond E.M., Dorie M.J., Welford S.M., Giaccia A.J. DNA damage during reoxygenation elicits a Chk2-dependent checkpoint response. Mol. Cell. Biol. 2006, 26:1598-1609.
20. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
21. Gibson S.L., Bindra R.S., Glazer P.M. Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Res. 2005, 65:10734-10741.
22. Gibson S.L., Bindra R.S., Glazer P.M. CHK2-dependent phosphorylation of BRCA1 in hypoxia. Radiat. Res. 2006, 166:646-651.
23. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio R.A., Kastrinakis N.G., Levy B., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907-913.
24. Hambardzumyan D., Squatrito M., Carbajal E., Holland E.C. Glioma formation, cancer stem cells, and akt signaling. Stem Cell Rev. 2008, 4:203-210.
25. Hammond E.M., Dorie M.J., Giaccia A.J. ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J. Biol. Chem. 2003, 278:12207-12213.
26. Hirao A., Kong Y.Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S.J., Mak T.W. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 2000, 287:1824-1827.
27. Hirao A., Cheung A., Duncan G., Girard P.M., Elia A.J., Wakeham A., Okada H., Sarkissian T., Wong J.A., Sakai T., et al. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol. Cell. Biol. 2002, 22:6521-6532.
28. Hirose Y., Berger M.S., Pieper R.O. Abrogation of the Chk1-mediated G(2) checkpoint pathway potentiates temozolomide-induced toxicity in a p53-independent manner in human glioblastoma cells. Cancer Res. 2001, 61:5843-5849.
29. Hirose Y., Katayama M., Mirzoeva O.K., Berger M.S., Pieper R.O. Akt activation suppresses Chk2-mediated, methylating agent-induced G2 arrest and protects from temozolomide-induced mitotic catastrophe and cellular senescence. Cancer Res. 2005, 65:4861-4869.
30. Holland E.C., Varmus H.E. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc. Natl. Acad. Sci. USA 1998, 95:1218-1223.
31. Holland E.C., Hively W.P., DePinho R.A., Varmus H.E. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 1998, 12:3675-3685.
32. Huse J.T., Holland E.C. Genetically engineered mouse models of brain cancer and the promise of preclinical testing. Brain Pathol. 2009, 19:132-143.
33. Ino Y., Wahrer D.C., Bell D.W., Haber D.A., Louis D.N. Mutation analysis of the hCHK2 gene in primary human malignant gliomas. Neurogenetics 2000, 3:45-46.
34. Jack M.T., Woo R.A., Hirao A., Cheung A., Mak T.W., Lee P.W. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 2002, 99:9825-9829.
35. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
36. Kuerbitz S.J., Plunkett B.S., Walsh W.V., Kastan M.B. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. USA 1992, 89:7491-7495.
37. Lavin M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol. 2008, 9:759-769.
38. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006, 9:391-403.
39. Liu G., Parant J.M., Lang G., Chau P., Chavez-Reyes A., El-Naggar A.K., Multani A., Chang S., Lozano G. Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice. Nat. Genet. 2004, 36:63-68.
40. Matsuoka S., Huang M., Elledge S.J. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998, 282:1893-1897.
41. Miyagi K., Mukawa J., Kinjo N., Horikawa K., Mekaru S., Nakasone S., Koga H., Higa Y., Naito M. Astrocytoma linked to familial ataxia-telangiectasia. Acta Neurochir. (Wien) 1995, 135:87-92.
42. Nuciforo P.G., Luise C., Capra M., Pelosi G., d'Adda di Fagagna F. Complex engagement of DNA damage response pathways in human cancer and in lung tumor progression. Carcinogenesis 2007, 28:2082-2088.
43. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
44. Sallinen S.L., Ikonen T., Haapasalo H., Schleutker J. CHEK2 mutations in primary glioblastomas. J. Neurooncol. 2005, 74:93-95.
45. Shih A.H., Dai C., Hu X., Rosenblum M.K., Koutcher J.A., Holland E.C. Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis. Cancer Res. 2004, 64:4783-4789.
46. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 2003, 3:155-168.
47. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 2004, 64:2390-2396.
48. Stracker T.H., Morales M., Couto S.S., Hussein H., Petrini J.H. The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature 2007, 447:218-221.
49. Stracker T.H., Couto S.S., Cordon-Cardo C., Matos T., Petrini J.H. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol. Cell 2008, 31:21-32.
50. Stracker T.H., Usui T., Petrini J.H. Taking the time to make important decisions: The checkpoint effector kinases Chk1 and Chk2 and the DNA damage response. DNA Repair (Amst.) 2009, 8:1047-1054.
51. Takai H., Naka K., Okada Y., Watanabe M., Harada N., Saito S., Anderson C.W., Appella E., Nakanishi M., Suzuki H., et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 2002, 21:5195-5205.
52. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068. The Cancer Genome Atlas Research Network.
53. Theunissen J.W., Petrini J.H. Methods for studying the cellular response to DNA damage: influence of the Mre11 complex on chromosome metabolism. Methods Enzymol. 2006, 409:251-284.
54. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
55. Wang H., Wang S., Shen L., Chen Y., Zhang X., Zhou J., Wang Z., Hu C., Yue W. Chk2 down-regulation by promoter hypermethylation in human bulk gliomas. Life Sci. 2009, 86:185-191.
56. Ward I.M., Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 2001, 276:47759-47762.
57. Ward I.M., Difilippantonio S., Minn K., Mueller M.D., Molina J.R., Yu X., Frisk C.S., Ried T., Nussenzweig A., Chen J. 53BP1 cooperates with p53 and functions as a haploinsufficient tumor suppressor in mice. Mol. Cell. Biol. 2005, 25:10079-10086.
58. Xu Y., Baltimore D. Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 1996, 10:2401-2410.