The zinc ionophore PCI-5002 radiosensitizes non-small cell lung cancer cells by enhancing autophagic cell death

Journal of Thoracic Oncology

Volumn 6, Issue 9, 2011, Pages 1542-1552

  Kim, Kwang Woon ^a   Speirs, Christina K ^a   Jung, Dae Kwang ^a   Lu, Bo ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Autophagy; Lung cancer; Radiation; Zinc

Indexed keywords

ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; CARBOPLATIN; CASPASE 3; CASPASE 3 INHIBITOR; ETOPOSIDE; EVEROLIMUS; GOSSYPOL; IONOPHORE; KI 67 ANTIGEN; M 867; MAPATUMUMAB; OBLIMERSEN; PCI 5002; RADIOSENSITIZING AGENT; UNCLASSIFIED DRUG; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER RADIOTHERAPY; CELL DEATH; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; TUMOR GROWTH; XENOGRAFT;

EID: 80052273362     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1097/JTO.0b013e3182208fac     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Andriani F, Perego P, Carenini N, et al. Increased sensitivity to cisplatin in non-small cell lung cancer cell lines after FHIT gene transfer. Neoplasia 2006;8:9-17.
3. Fesik SW. Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev 2005;5:876-885. (Pubitemid 41746032)
4. Katz D, Ito E, Liu FF. On the path to seeking novel radiosensitizers. Int J Radiat Oncol Biol Phys 2009;73:988-996.
5. Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol (R Coll Radiol) 2007;19:397-417. (Pubitemid 46995615)
6. Ferreira CG, Span SW, Peters GJ, et al. Chemotherapy triggers apoptosis in a caspase-8-dependent and mitochondria-controlled manner in the non-small cell lung cancer cell line NCI-H460. Cancer Res 2000;60: 7133-7141. (Pubitemid 32059195)
7. Rudin CM, Salgia R, Wang X, et al. Randomized phase II Study of carboplatin and etoposide with or without the bcl-2 antisense oligonucleotide oblimersen for extensive-stage small-cell lung cancer: CALGB 30103. J Clin Oncol 2008;26:870-876. (Pubitemid 351398078)
8. Greco FA, Bonomi P, Crawford J, et al. Phase 2 study of mapatumumab, a fully human agonistic monoclonal antibody which targets and activates the TRAIL receptor-1, in patients with advanced non-small cell lung cancer. Lung Cancer 2008;61:82-90.
9. Yu L, Lenardo MJ, Baehrecke EH. Autophagy and caspases: A new cell death program. Cell Cycle 2004;3:1124-1126. (Pubitemid 40268628)
10. Yu L, Strandberg L, Lenardo MJ. The selectivity of autophagy and its role in cell death and survival. Autophagy 2008;4:567-573.
11. Jaboin JJ, Shinohara ET, Moretti L, et al. The role of mTOR inhibition in augmenting radiation induced autophagy. Technol Cancer Res Treatment 2007;6:443-447. (Pubitemid 47613293)
12. Kim KW, Mutter RW, Cao C, et al. Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J Biol Chem 2006;281:36883-36890. (Pubitemid 46042156)
13. Maiuri MC, Le Toumelin G, Criollo A, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007;26:2527-2539. (Pubitemid 46788315)
14. Moreira JN, Santos A, Simoes S. Bcl-2-targeted antisense therapy (oblimersen sodium): Towards clinical reality. Rev Recent Clin Trials 2006;1:217-235.
15. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999;402:672-676. (Pubitemid 129516338)
16. Martinet W, Agostinis P, Vanhoecke B, et al. Autophagy in disease: A double-edged sword with therapeutic potential. Clin Sci 2009;116:697-712.
17. Lenardo MJ, McPhee CK, Yu L. Autophagic cell death. Methods Enzymol 2009;453:17-31.
18. Liu J, Lin A. Role of JNK activation in apoptosis: A double-edged sword. Cell Res 2005;15:36-42. (Pubitemid 41653963)
19. Lum JJ, Bauer DE, Kong M, et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005;120:237-248. (Pubitemid 40174766)
20. Yu L, Alva A, Su H, et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 2004;304:1500-1502. (Pubitemid 38720930)
21. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell 2005;122:927-939. (Pubitemid 41345209)
22. Kisen GO, Tessitore L, Costelli P, et al. Reduced autophagic activity in primary rat hepatocellular carcinoma and ascites hepatoma cells. Carcinogenesis 1993;14:2501-2505. (Pubitemid 24016585)
23. Schwarze PE, Seglen PO. Reduced autophagic activity, improved protein balance and enhanced in vitro survival of hepatocytes isolated from carcinogen-treated rats. Exp Cell Res 1985;157:15-28. (Pubitemid 16205864)
24. Karantza-Wadsworth V, Patel S, Kravchuk O, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 2007;21:1621-1635. (Pubitemid 47026367)
25. Mathew R, White E. Why sick cells produce tumors: The protective role of autophagy. Autophagy 2007;3:502-505. (Pubitemid 47293740)
26. Jin S, White E. Role of autophagy in cancer: Management of metabolic stress. Autophagy 2007;3:28-31. (Pubitemid 46100707)
27. Degenhardt K, Mathew R, Beaudoin B, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006;10:51-64.
28. Cao C, Subhawong T, Albert JM, et al. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 2006;66:10040-10047. (Pubitemid 44672057)
29. Kim KW, Moretti L, Lu B. M867, a novel selective inhibitor of caspase-3 enhances cell death and extends tumor growth delay in irradiated lung cancer models. Plos One 2008;3:e2275.
30. Gewirtz DA, Hilliker ML, Wilson EN. Promotion of autophagy as a mechanism for radiation sensitization of breast tumor cells. Radiother Oncol 2009;92:323-328.
31. Zhuang W, Qin Z, Liang Z. The role of autophagy in sensitizing malignant glioma cells to radiation therapy. Acta Biochim Biophys Sin 2009;41:341-351.
32. Rudolf E, Rudolf K, Radocha J, et al. The role of intracellular zinc in modulation of life and death of Hep-2 cells. Biometals 2003;16:295-309. (Pubitemid 36138799)
33. Plum LM, Rink L, Haase H. The essential toxin: Impact of zinc on human health. Int J Environ Res Public Health 2010;7:1342-1365.
34. Chai F, Truong-Tran AQ, Ho LH, et al. Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: A review. Immunol Cell Biol 1999;77:272-278. (Pubitemid 29251581)
35. Hyun HJ, Sohn J, Ahn YH, et al. Depletion of intracellular zinc induces macromolecule synthesis- and caspase-dependent apoptosis of cultured retinal cells. Brain Res 2000;869:39-48. (Pubitemid 30345773)
36. Moldoveanu T, Liu Q, Tocilj A, et al. The X-ray structure of a BAK homodimer reveals an inhibitory zinc binding site. Mol Cell 2006;24: 677-688. (Pubitemid 44839210)
37. Rudolf E, Rudolf K, Cervinka M. Zinc induced apoptosis in HEP-2 cancer cells: The role of oxidative stress and mitochondria. Biofactors 2005;23:107-120. (Pubitemid 41330501)
38. Lee SJ, Cho KS, Koh JY. Oxidative injury triggers autophagy in astrocytes: The role of endogenous zinc. Glia 2009;57:1351-1361.
39. Hwang JJ, Kim HN, Kim J, et al. Zinc(II) ion mediates tamoxifeninduced autophagy and cell death in MCF-7 breast cancer cell line. Biometals 2010;23:997-1013.
40. Magda D, Lecane P, Wang Z, et al. Synthesis and anticancer properties of water-soluble zinc ionophores. Cancer Res 2008;68:5318-5325.
41. Koopman G, Reutelingsperger CP, Kuijten GA, et al. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994;84:1415-1420. (Pubitemid 24273007)
42. Kim KW, Moretti L, Mitchell LR, et al. Combined Bcl-2/mammalian target of rapamycin inhibition leads to enhanced radiosensitization via induction of apoptosis and autophagy in non-small cell lung tumor xenograft model. Clin Cancer Res 2009;15:6096-6105.
43. Lindsten T, Ross AJ, King A, et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 2000;6:1389-1399. (Pubitemid 32045931)
44. Schleicher SM, Moretti L, Varki V, et al. Progress in the unraveling of the endoplasmic reticulum stress/autophagy pathway and cancer: Implications for future therapeutic approaches. Drug Resist Updat 2010;13: 79-86.
45. Zois CE, Koukourakis MI. Radiation-induced autophagy in normal and cancer cells: Towards novel cytoprotection and radio-sensitization policies? Autophagy 2009;5:442-450.
46. Daido S, Yamamoto A, Fujiwara K, et al. Inhibition of the DNAdependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 2005;65:4368-4375. (Pubitemid 40775676)
47. Ito H, Daido S, Kanzawa T, et al. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol 2005;26:1401-1410.
48. Yao KC, Komata T, Kondo Y, et al. Molecular response of human glioblastoma multiforme cells to ionizing radiation: Cell cycle arrest, modulation of the expression of cyclin-dependent kinase inhibitors, and autophagy. J Neurosurg 2003;98:378-384. (Pubitemid 36151035)
49. Lin LC, Que J, Lin KL, et al. Effects of zinc supplementation on clinical outcomes in patients receiving radiotherapy for head and neck cancers: A double-blinded randomized study. Int J Radiat Oncol Biol Phys 2008;70:368-373.
50. Lin LC, Que J, Lin LK, et al. Zinc supplementation to improve mucositis and dermatitis in patients after radiotherapy for head-and-neck cancers: A double-blind, randomized study. Int J Radiat Oncol Biol Phys 2006; 65:745-750. (Pubitemid 43810226)