ATM deletion with dual recombinase technology preferentially radiosensitizes tumor endothelium

Journal of Clinical Investigation

Volumn 124, Issue 8, 2014, Pages 3325-3338

  Moding, Everett J ^a   Lee, Chang Lung ^a   Castle, Katherine D ^a   Oh, Patrick ^a   Mao, Lan ^a   Zha, Shan ^b   Min, Hooney D ^a   Ma, Yan ^a   Das, Shiva ^a   Kirsch, David G ^a  

^a DUKE UNIVERSITY   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; ATM PROTEIN; ATM PROTEIN, MOUSE; RECOMBINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATM GENE; CELL CYCLE PROGRESSION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE; GENE DELETION; HEART; HEART MUSCLE NECROSIS; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIZATION; SARCOMA; TUMOR CELL; ANIMAL; CELL CYCLE; DEFICIENCY; GENETICS; HEART MUSCLE; HUMAN; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; RADIATION RESPONSE; SARCOMA, EXPERIMENTAL; SOFT TISSUE NEOPLASMS; TRANSGENIC MOUSE; TUMOR MICROENVIRONMENT;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE DELETION; HEART; HUMANS; MICE; MICE, TRANSGENIC; MYOCARDIUM; RADIATION TOLERANCE; RECOMBINASES; SARCOMA, EXPERIMENTAL; SOFT TISSUE NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84905482240     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73932     Document Type: Article

References (62)

1. Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 2005;104(6):1129-1137.
2. Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer. 2011;11(4):239-253.
3. Moding EJ, Kastan MB, Kirsch DG. Strategies for optimizing the response of cancer and normal tissues to radiation. Nat Rev Drug Discov. 2013;12(7):526-542.
4. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer. 2003;3(3):155-168.
5. Kastan MB, Lim DS. The many substrates and functions of ATM. Nat Rev Mol Cell Biol. 2000;1(3):179-186.
6. Paterson MC, Smith PJ. Ataxia telangiectasia: an inherited human disorder involving hypersensitivity to ionizing radiation and related DNA-damaging chemicals. Annu Rev Genet. 1979;13:291-318.
7. Rainey MD, Charlton ME, Stanton RV, Kastan MB. Transient inhibition of ATM kinase is sufficient to enhance cellular sensitivity to ionizing radiation. Cancer Res. 2008;68(18):7466-7474.
8. Hickson I, et al. Identification and characterization of a novel and specific inhibitor of the ataxiatelangiectasia mutated kinase ATM. Cancer Res. 2004;64(24):9152-9159.
9. Biddlestone-Thorpe L, et al. ATM kinase inhibition preferentially sensitizes p53-mutant glioma to ionizing radiation. Clin Cancer Res. 2013;19(12):3189-3200.
10. Kirsch DG, et al. p53 controls radiation-induced gastrointestinal syndrome in mice independent of apoptosis. Science. 2010;327(5965):593-596.
11. Lee CL, et al. p53 functions in endothelial cells to prevent radiation-induced myocardial injury in mice. Sci Signal. 2012;5(234):ra52.
12. Barlow C, et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell. 1996;86(1):159-171.
13. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 1996;10(19):2411-2422.
14. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
15. Garcia-Barros M, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science. 2003;300(5622):1155-1159.
16. Suit HD, Willers H. Comment on "Tumor response to radiotherapy regulated by endothelial cell apoptosis" (I). Science. 2003;302(5652):1894.
17. Brown M, et al. Comment on "Tumor response to radiotherapy regulated by endothelial cell apoptosis" (II). Science. 2003;302(5652):1894.
18. Okuno Y, Nakamura-Ishizu A, Otsu K, Suda T, Kubota Y. Pathological neoangiogenesis depends on oxidative stress regulation by ATM. Nat Med. 2012;18(8):1208-1216.
19. Falk P. Differences in vascular pattern between the spontaneous and the transplanted C3H mouse mammary carcinoma. Eur J Cancer Clin Oncol. 1982;18(2):155-165.
20. Lee CL, et al. Generation of primary tumors with Flp recombinase in FRT-flanked p53 mice. Dis Model Mech. 2012;5(3):397-402.
21. Kirsch DG, et al. A spatially and temporally restricted mouse model of soft tissue sarcoma. Nat Med. 2007;13(8):992-997.
22. Paris F, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293(5528):293-297.
23. White D, et al. The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation. Mol Cancer Res. 2012;10(3):401-414.
24. Zha S, et al. Ataxia telangiectasia-mutated protein and DNA-dependent protein kinase have complementary V (D) J recombination functions. Proc Natl Acad Sci U S A. 2011;108(5):2028-2033.
25. Alva JA, et al. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn. 2006;235(3):759-767.
26. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9):593-605.
27. Srinivas S, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4.
28. Laitinen L. Griffonia simplicifolia lectins bind specifically to endothelial cells and some epithelial cells in mouse tissues. Histochem J. 1987;19(4):225-234.
29. Maddox DE, Shibata S, Goldstein IJ. Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. Proc Natl Acad Sci U S A. 1982;79(1):166-170.
30. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 2008;15(7):1153-1162.
31. Vasquez KO, Casavant C, Peterson JD. Quantitative whole body biodistribution of fluorescentlabeled agents by non-invasive tomographic imaging. PLoS One. 2011;6(6):e20594.
32. Stewart FA, Hoving S, Russell NS. Vascular damage as an underlying mechanism of cardiac and cerebral toxicity in irradiated cancer patients. Radiat Res. 2010;174(6):865-869.
33. Bunz F, et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science. 1998;282(5393):1497-1501.
34. Westphal CH, Rowan S, Schmaltz C, Elson A, Fisher DE, Leder P. atm and p53 cooperate in apoptosis suppression of tumorigenesis, but not in resistance to acute radiation toxicity. Nat Genet. 1997;16(4):397-401.
35. Hobson B, Denekamp J. Endothelial proliferation in tumours and normal tissues: continuous labelling studies. Br J Cancer. 1984;49(4):405-413.
36. Denekamp J, Hobson B. Endothelial-cell proliferation in experimental tumours. Br J Cancer. 1982;46(5):711-720.
37. Parry D, et al. Dinaciclib (SCH 727965), a novel potent cyclin-dependent kinase inhibitor. Mol Cancer Ther. 2010;9(8):2344-2353.
38. Lin BT, Gruenwald S, Morla AO, Lee WH, Wang JY. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J. 1991;10(4):857-864.
39. Akiyama T, Ohuchi T, Sumida S, Matsumoto K, Toyoshima K. Phosphorylation of the retinoblastoma protein by cdk2. Proc Natl Acad Sci U S A. 1992;89(17):7900-7904.
40. Scholzen T, Gerdes J. The Ki-67 protein: from the known the unknown. J Cell Physiol. 2000;182(3):311-322.
41. Ch'ang HJ, et al. ATM regulates target switching to escalating doses of radiation in the intestines. Nat Med. 2005;11(5):484-490.
42. Wang YA, Elson A, Leder P. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc Natl Acad Sci U S A. 1997;94(26):14590-14595.
43. Takao N, et al. Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene. 1999;18(50):7002-7009.
44. Westphal CH, et al. Loss of atm radiosensitizes multiple p53 null tissues. Cancer Res. 1998;58(24):5637-5639.
45. Jiang H, et al. The combined status of ATM and p53 link tumor development with therapeutic response. Genes Dev. 2009;23(16):1895-1909.
46. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med. 2002;8(11):1249-1256.
47. Bentzen S. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer. 2006;6(9):702-713.
48. Fenton BM, Lord EM, Paoni SF. Intravascular HBO (2) saturations, perfusion hypoxia in spontaneous transplanted tumor models. Int J Cancer. 2001;93(5):693-698.
49. Field SB, Needham S, Burney IA, Maxwell RJ, Coggle JE, Griffiths JR. Differences in vascular response between primary and transplanted tumours. Br J Cancer. 1991;63(5):723-726.
50. Sharpless NE, Depinho RA. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov. 2006;5(9):741-754.
51. Olive KP, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 2009;324(5933):1457-1461.
52. Singh M, et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nat Biotechnol. 2010;28(6):585-593.
53. Chen Z, et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature. 2012;483(7391):613-617.
54. Young NP, Crowley D, Jacks T. Uncoupling cancer mutations reveals critical timing of p53 loss in sarcomagenesis. Cancer Res. 2011;71(11):4040- 4047.
55. Lin X, Fuks Z, Kolesnick R. Ceramide mediates radiation-induced death of endothelium. Crit Care Med. 2000;28(4 suppl):N87-N93.
56. Fuks Z, Kolesnick R. Engaging the vascular component of the tumor response. Cancer Cell. 2005;8(2):89-91.
57. Budach W, Taghian A, Freeman J, Gioioso D, Suit HD. Impact of stromal sensitivity on radiation response of tumors. J Natl Cancer Inst. 1993;85(12):988-993.
58. Krause M, et al. EGFR-TK inhibition before radiotherapy reduces tumour volume but does not improve local control: differential response of cancer stem cells and nontumourigenic cells? Radiother Oncol. 2007;83(3):316-325.
59. Zips D, et al. Impact of adjuvant inhibition of vascular endothelial growth factor receptor tyrosine kinases on tumor growth delay and local tumor control after fractionated irradiation in human squamous cell carcinomas in nude mice. Int J Radiat Oncol Biol Phys. 2005;61(3):908-914.
60. Jackson EL, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 2001;15(24):3243- 3248.
61. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet. 2001;29(4):418-425.
62. Valentin-Vega YA, et al. Mitochondrial dysfunction in ataxia-telangiectasia. Blood. 2012;119(6):1490-1500.