NSCLC cells demonstrate differential mode of cell death in response to the combined treatment of radiation and a DNAPKcs inhibitor

Oncotarget

Volumn 6, Issue 6, 2015, Pages 3848-3860

  Yu, Lan ^a   Shang, Zeng Fu ^a,b,d   Hsu, Feng Ming ^a,c   Zhang, Zhang ^a   Tumati, Vasu ^a   Lin, Yu Fen ^a   Chen, Benjamin P C ^a   Saha, Debabrata ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d Collaborative Innovation Center of Radiation Medicine of Jiangsu Higher Education Institutions ^*  (China)

Author keywords

Apoptosis; Autophagy; Mitotic Catastrophe; Radiosensitizer; Senescence

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE H3; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NU 7441; POLO LIKE KINASE 1; S6 KINASE; UNCLASSIFIED DRUG; 8-DIBENZOTHIOPHEN-4-YL-2-MORPHOLIN-4-YL-CHROMEN-4-ONE; CHROMONE DERIVATIVE; DNA DEPENDENT PROTEIN KINASE; MORPHOLINE DERIVATIVE; PROTEIN KINASE INHIBITOR; RADIOSENSITIZING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL ACTIVATION; CELL AGING; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPAIR; DRUG EFFICACY; ENZYME PHOSPHORYLATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; IONIZING RADIATION; LUNG CANCER CELL LINE; MITOSIS SPINDLE; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, NON-SMALL-CELL LUNG; CHEMORADIOTHERAPY; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; HUMAN; LUNG NEOPLASMS; NUDE MOUSE; PATHOLOGY; RADIATION RESPONSE; TUMOR CELL LINE;

ANIMALS; AUTOPHAGY; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CHEMORADIOTHERAPY; CHROMONES; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MORPHOLINES; PROTEIN KINASE INHIBITORS; RADIATION-SENSITIZING AGENTS; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924228790     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2975     Document Type: Article

References (51)

1. Gerard C, Debruyne C. Immunotherapy in the landscape of new targeted treatments for non-small cell lung cancer. Molecular oncology. 2009; 3:409-424.
2. Baas P, Belderbos JS, van den Heuvel M. Chemoradiation therapy in nonsmall cell lung cancer. Current opinion in oncology. 2011; 23:140-149.
3. Christodoulou M, Bayman N, McCloskey P, Rowbottom C, Faivre-Finn C. New radiotherapy approaches in locally advanced non-small cell lung cancer. European journal of cancer. 2014; 50:525-534.
4. Chan DW, Chen BP, Prithivirajsingh S, Kurimasa A, Story MD, Qin J, Chen DJ. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes & development. 2002; 16:2333-2338.
5. Chen BP, Chan DW, Kobayashi J, Burma S, Asaithamby A, Morotomi-Yano K, Botvinick E, Qin J, Chen DJ. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. The Journal of biological chemistry. 2005; 280:14709-14715.
6. Chen BP, Uematsu N, Kobayashi J, Lerenthal Y, Krempler A, Yajima H, Lobrich M, Shiloh Y, Chen DJ. Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. The Journal of biological chemistry. 2007; 282:6582-6587.
7. Shinohara ET, Geng L, Tan J, Chen H, Shir Y, Edwards E, Halbrook J, Kesicki EA, Kashishian A, Hallahan DE. DNA-dependent protein kinase is a molecular target for the development of noncytotoxic radiation-sensitizing drugs. Cancer research. 2005; 65:4987-4992.
8. Deriano L, Guipaud O, Merle-Beral H, Binet JL, Ricoul M, Potocki-Veronese G, Favaudon V, Maciorowski Z, Muller C, Salles B, Sabatier L, Delic J. Human chronic lymphocytic leukemia B cells can escape DNA damage-induced apoptosis through the nonhomologous end-joining DNA repair pathway. Blood. 2005; 105:4776-4783.
9. Hu S, Qu Y, Xu X, Xu Q, Geng J, Xu J. Nuclear survivin and its relationship to DNA damage repair genes in non-small cell lung cancer investigated using tissue array. PloS one. 2013; 8:e74161.
10. Hsu FM, Zhang S, Chen BP. Role of DNA-dependent protein kinase catalytic subunit in cancer development and treatment. Translational cancer research. 2012; 1:22-34.
11. Xing J, Wu X, Vaporciyan AA, Spitz MR, Gu J. Prognostic significance of ataxia-telangiectasia mutated, DNA-dependent protein kinase catalytic subunit, and Ku heterodimeric regulatory complex 86-kD subunit expression in patients with nonsmall cell lung cancer. Cancer. 2008; 112:2756-2764.
12. Leahy JJ, Golding BT, Griffin RJ, Hardcastle IR, Richardson C, Rigoreau L, Smith GC. Identification of a highly potent and selective DNA-dependent protein kinase (DNA-PK) inhibitor (NU7441) by screening of chromenone libraries. Bioorganic & medicinal chemistry letters. 2004; 14:6083-6087.
13. Zhao Y, Thomas HD, Batey MA, Cowell IG, Richardson CJ, Griffin RJ, Calvert AH, Newell DR, Smith GC, Curtin NJ. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer research. 2006; 66:5354-5362.
14. Ciszewski WM, Tavecchio M, Dastych J, Curtin NJ. DNA-PK inhibition by NU7441 sensitizes breast cancer cells to ionizing radiation and doxorubicin. Breast cancer research and treatment. 2014; 143:47-55.
15. Shaheen FS, Znojek P, Fisher A, Webster M, Plummer R, Gaughan L, Smith GC, Leung HY, Curtin NJ, Robson CN. Targeting the DNA double strand break repair machinery in prostate cancer. PloS one. 2011; 6:e20311.
16. Yu L, Tumati V, Tseng SF, Hsu FM, Kim DN, Hong D, Hsieh JT, Jacobs C, Kapur P, Saha D. DAB2IP regulates autophagy in prostate cancer in response to combined treatment of radiation and a DNA-PKcs inhibitor. Neoplasia. 2012; 14:1203-1212.
17. Shang ZF, Huang B, Xu QZ, Zhang SM, Fan R, Liu XD, Wang Y, Zhou PK. Inactivation of DNA-dependent protein kinase leads to spindle disruption and mitotic catastrophe with attenuated checkpoint protein 2 Phosphorylation in response to DNA damage. Cancer research. 2010; 70:3657-3666.
18. Azad A, Jackson S, Cullinane C, Natoli A, Neilsen PM, Callen DF, Maira SM, Hackl W, McArthur GA, Solomon B. Inhibition of DNA-dependent protein kinase induces accelerated senescence in irradiated human cancer cells. Molecular cancer research: MCR. 2011; 9:1696-1707.
19. Daido S, Yamamoto A, Fujiwara K, Sawaya R, Kondo S, Kondo Y. Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer research. 2005; 65:4368-4375.
20. Syljuasen RG, Jensen S, Bartek J, Lukas J. Adaptation to the ionizing radiation-induced G2 checkpoint occurs in human cells and depends on checkpoint kinase 1 and Polo-like kinase 1 kinases. Cancer research. 2006; 66:10253-10257.
21. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer research. 2001; 61:439-444.
22. Gewirtz DA. Autophagy as a mechanism of radiation sensitization in breast tumor cells. Autophagy. 2007; 3:249-250.
23. Gandara D, Narayan S, Lara PN Jr., Goldberg Z, Davies A, Lau DH, Mack P, Gumerlock P, Vijayakumar S. Integration of novel therapeutics into combined modality therapy of locally advanced non-small cell lung cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11:5057s-5062s.
24. Davis AJ, Chen BP, Chen DJ. DNA-PK: a dynamic enzyme in a versatile DSB repair pathway. DNA repair. 2014; 17:21-29.
25. Kurimasa A, Kumano S, Boubnov NV, Story MD, Tung CS, Peterson SR, Chen DJ. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Molecular and cellular biology. 1999; 19:3877-3884.
26. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene. 2004; 23:2825-2837.
27. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell death and differentiation. 2012; 19:107-120.
28. Vitale I, Galluzzi L, Castedo M, Kroemer G. Mitotic catastrophe: a mechanism for avoiding genomic instability. Nature reviews Molecular cell biology. 2011; 12:385-392.
29. Mikhailov A, Cole RW, Rieder CL. DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Current biology: CB. 2002; 12:1797-1806.
30. Bartek J, Falck J, Lukas J. CHK kinase-a busy messenger. Nature reviews Molecular cell biology. 2001; 2:877-886.
31. Shang Z, Yu L, Lin YF, Matsunaga S, Shen CY, Chen BP. DNA-PKcs activates the Chk2-Brca1 pathway during mitosis to ensure chromosomal stability. Oncogenesis. 2014; 3:e85.
32. Petronczki M, Lenart P, Peters JM. Polo on the Rise-from Mitotic Entry to Cytokinesis with Plk1. Developmental cell. 2008; 14:646-659.
33. Shang ZF, Yu L, Li B, Tu WZ, Wang Y, Liu XD, Guan H, Huang B, Rang WQ, Zhou PK. 4E-BP1 participates in maintaining spindle integrity and genomic stability via interacting with PLK1. Cell cycle. 2012; 11:3463-3471.
34. Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I. Polo-like kinases (Plks) and cancer. Oncogene. 2005; 24:287-291.
35. van Vugt MA, Bras A, Medema RH. Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells. Molecular cell. 2004; 15:799-811.
36. van Vugt MA, Gardino AK, Linding R, Ostheimer GJ, Reinhardt HC, Ong SE, Tan CS, Miao H, Keezer SM, Li J, Pawson T, Lewis TA, Carr SA, Smerdon SJ, Brummelkamp TR, Yaffe MB. A mitotic phosphorylation feedback network connects Cdk1, Plk1, 53BP1, and Chk2 to inactivate the G(2)/M DNA damage checkpoint. PLoS biology. 2010; 8:e1000287.
37. Luce A, Courtin A, Levalois C, Altmeyer-Morel S, Romeo PH, Chevillard S, Lebeau J. Death receptor pathways mediate targeted and non-targeted effects of ionizing radiations in breast cancer cells. Carcinogenesis. 2009; 30:432-439.
38. Castedo M, Perfettini JL, Roumier T, Valent A, Raslova H, Yakushijin K, Horne D, Feunteun J, Lenoir G, Medema R, Vainchenker W, Kroemer G. Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene. 2004; 23:4362-4370.
39. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008; 132:27-42.
40. Zois CE, Koukourakis MI. Radiation-induced autophagy in normal and cancer cells: towards novel cytoprotection and radio-sensitization policies? Autophagy. 2009; 5:442-450.
41. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:5308-5316.
42. Klionsky DJ, Meijer AJ, Codogno P. Autophagy and p70S6 kinase. Autophagy. 2005; 1:59-60discussion 60-5.
43. Radimerski T, Montagne J, Hemmings-Mieszczak M, Thomas G. Lethality of Drosophila lacking TSC tumor suppressor function rescued by reducing dS6K signaling. Genes & development. 2002; 16:2627-2632.
44. Balendran A, Currie R, Armstrong CG, Avruch J, Alessi DR. Evidence that 3-phosphoinositide-dependent protein kinase-1 mediates phosphorylation of p70 S6 kinase in vivo at Thr-412 as well as Thr-252. The Journal of biological chemistry. 1999; 274:37400-37406.
45. Lehman N, Ledford B, Di Fulvio M, Frondorf K, McPhail LC, Gomez-Cambronero J. Phospholipase D2-derived phosphatidic acid binds to and activates ribosomal p70 S6 kinase independently of mTOR. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2007; 21:1075-1087.
46. Bozulic L, Surucu B, Hynx D, Hemmings BA. PKBalpha/Akt1 acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Molecular cell. 2008; 30:203-213.
47. d'Adda di Fagagna F. Living on a break: cellular senescence as a DNA-damage response. Nature reviews Cancer. 2008; 8:512-522.
48. Ben-Porath I, Weinberg RA. The signals and pathways activating cellular senescence. The international journal of biochemistry & cell biology. 2005; 37:961-976.
49. Luo Y, Zou P, Zou J, Wang J, Zhou D, Liu L. Autophagy regulates ROS-induced cellular senescence via p21 in a p38 MAPKalpha dependent manner. Experimental gerontology. 2011; 46:860-867.
50. Goehe RW, Di X, Sharma K, Bristol ML, Henderson SC, Valerie K, Rodier F, Davalos AR, Gewirtz DA. The autophagy-senescence connection in chemotherapy: must tumor cells (self) eat before they sleep? The Journal of pharmacology and experimental therapeutics. 2012; 343:763-778.
51. Raghavan P, Tumati V, Yu L, Chan N, Tomimatsu N, Burma S, Bristow RG, Saha D. AZD5438, an inhibitor of Cdk1, 2, and 9, enhances the radiosensitivity of non-small cell lung carcinoma cells. International journal of radiation oncology, biology, physics. 2012; 84:e507-514.