Regulation of FANCD2 by the mTOR pathway contributes to the resistance of cancer cells to DNA double-strand breaks

Cancer Research

Volumn 73, Issue 11, 2013, Pages 3393-3401

  Shen, Changxian ^a   Oswald, Duane ^a   Phelps, Doris ^a   Cam, Hakan ^a   Pelloski, Christopher E ^b   Pang, Qishen ^c   Houghton, Peter J ^a  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZD 8055; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; FANCONI ANEMIA GROUP D2 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MELPHALAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER RADIOTHERAPY; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA CROSS LINKING; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; FANCD2 GENE; FANCONI ANEMIA; FEMALE; GENETIC TRANSCRIPTION; LYMPHOBLAST; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RADIOSENSITIVITY; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; WILD TYPE;

ADOLESCENT; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CHILD; CHILD, PRESCHOOL; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FEMALE; HETEROGRAFTS; HUMANS; MICE; MICE, SCID; PHOSPHORYLATION; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84878551066     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4282     Document Type: Article

References (39)

1. Cerqueira A, Santamaria D, Martinez-Pastor B, Cuadrado M, Fernandez-Capetillo O, Barbacid M. Overall Cdk activity modulates the DNA damage response in mammalian cells. J Cell Biol 2009;187:773-80.
2. Aylon Y, Liefshitz B, Kupiec M. The CDK regulates repair of doublestrand breaks by homologous recombination during the cell cycle. EMBO J 2004;23:4868-75.
3. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004;431:1011-7.
4. Salk JJ, Fox EJ, Loeb LA. Mutational heterogeneity in human cancers: origin and consequences. Annu Rev Pathol 2010;5:51-75.
5. Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006;441:424-30.
6. Heitman J, Movva NR, Hall MN. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 1991;253:905-9.
7. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011;12:21-35.
8. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell 2006;124:471-84.
9. Bjornsti MA, Houghton PJ. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004;4:335-48.
10. Cam H, Easton JB, High A, Houghton PJ. mTORC1 signaling under hypoxic conditions is controlled by ATM-dependent phosphorylation of HIF-1alpha. Mol Cell 2010;40:509-20.
11. Shen C, Lancaster CS, Shi B, Guo H, Thimmaiah P, Bjornsti MA. TOR signaling is a determinant of cell survival in response to DNA damage. Mol Cell Biol 2007;27:7007-17.
12. Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov 2009;8:627-44.
13. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 2009;27:2278-87.
14. Yap TA, Garrett MD, Walton MI, Raynaud F, de Bono JS, Workman P. Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises. Curr Opin Pharmacol 2008;8:393-412.
15. Chresta CM, Davies BR, Hickson I, Harding T, Cosulich S, Critchlow SE, et al. AZD8055 is a potent, selective, and orally bioavailable ATPcompetitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res 2010;70:288-98.
16. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 2009;284: 8023-32.
17. Houghton PJ, Gorlick R, Kolb EA, Lock R, Carol H, Morton CL, et al. Initial testing (stage 1) of the mTOR kinase inhibitor AZD8055 by the pediatric preclinical testing program. Pediatric Blood Cancer 2012;58: 191-9.
18. Houghton PJ, Morton CL, Gorlick R, Lock RB, Carol H, Reynolds CP, et al. Stage 2 combination testing of rapamycin with cytotoxic agents by the Pediatric Preclinical Testing Program. Mol Cancer Ther 2010;9: 101-12.
19. Kennedy RD, Chen CC, Stuckert P, Archila EM, De la Vega MA, Moreau LA, et al. Fanconi anemia pathway-deficient tumor cells are hypersensitive to inhibition of ataxia telangiectasia mutated. J Clin Invest 2007;117:1440-9.
20. Pichierri P, Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J 2004;23:1178-87.
21. Liu R, Liu D, Trink E, Bojdani E, Ning G, Xing M. The Akt-specific inhibitor MK2206 selectively inhibits thyroid cancer cells harboring mutations that can activate the PI3K/Akt pathway. J Clin Endocrinol Metab 2011;96:E577-85.
22. Rui L, Fisher TL, Thomas J, White MF. Regulation of insulin/insulin-like growth factor-1 signaling by proteasome-mediated degradation of insulin receptor substrate-2. J Biol Chem 2001;276:40362-7.
23. Saab R, Bills JL, Miceli AP, Anderson CM, Khoury JD, Fry DW, et al. Pharmacologic inhibition of cyclin-dependent kinase 4/6 activity arrests proliferation in myoblasts and rhabdomyosarcoma-derived cells. Mol Cancer Ther 2006;5:1299-308.
24. Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 2004;3:1427-38.
25. Hoskins EE, Gunawardena RW, Habash KB, Wise-Draper TM, Jansen M, Knudsen ES, et al. Coordinate regulation of Fanconi anemia gene expression occurs through the Rb/E2F pathway. Oncogene 2008;27: 4798-808.
26. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, Scharer OD, et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009;326:1698-701.
27. Joo W, Xu G, Persky NS, Smogorzewska A, Rudge DG, Buzovetsky O, et al. Structure of the FANCI-FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 2011;333:312-6.
28. Bogliolo M, Lyakhovich A, Callen E, Castella M, Cappelli E, Ramirez MJ, et al. Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J 2007;26: 1340-51.
29. Sobeck A, Stone S, Costanzo V, de Graaf B, Reuter T, de Winter J, et al. Fanconi anemia proteins are required to prevent accumulation of replication-associated DNA double-strand breaks. Mol Cellular Biol 2006;26:425-37.
30. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER III, Hurov KE, Luo J, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007;316:1160-6.
31. Bandhakavi S, Kim YM, Ro SH, Xie H, Onsongo G, Jun CB, et al. Quantitative nuclear proteomics identifies mTOR regulation of DNA damage response. Mol Cell Proteomics 2010;9:403-14.
32. Gaur S, Chen L, Yang L, Wu X, Un F, Yen Y. Inhibitors of mTOR overcome drug resistance from topoisomerase II inhibitors in solid tumors. Cancer Lett 2011;311:20-8.
33. Huang S, Yang ZJ, Yu C, Sinicrope FA. Inhibition of mTOR kinase by AZD8055 can antagonize chemotherapy-induced cell death through autophagy induction and down-regulation of p62/sequestosome 1. J Biol Chem 2011;286:40002-12.
34. Chen H, Ma Z, Vanderwaal RP, Feng Z, Gonzalez-Suarez I, Wang S, et al. The mTOR inhibitor rapamycin suppresses DNA double-strand break repair. Radiat Res 2011;175:214-24.
35. Moldovan GL, D'Andrea AD. How the fanconi anemia pathway guards the genome. Annu Rev Genet 2009;43:223-49.
36. Kitao H, Takata M. Fanconi anemia: a disorder defective in the DNA damage response. Int J Hematol 2011;93:417-24.
37. Kee Y, D'Andrea AD. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 2010;24:1680-94.
38. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007;28:739-45.
39. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008;9:616-27.