Mitochondria-derived reactive oxygen species drive GANT61-induced mesothelioma cell apoptosis

Oncotarget

Volumn 6, Issue 3, 2015, Pages 1519-1530

  Lim, Chuan Bian ^a   Prêle, Cecilia M ^a   Baltic, Svetlana ^a   Arthur, Peter G ^b   Creaney, Jenette ^a   Neil Watkins, D ^c   Thompson, Philip J ^a   Mutsaers, Steven E ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Apoptosis; GANT61; Hedgehog; Mesothelioma; Reactive oxygen species

Indexed keywords

ANTINEOPLASTIC AGENT; GANT 61; MITOCHONDRIAL DNA; PROTEIN PATCHED 1; REACTIVE OXYGEN METABOLITE; SONIC HEDGEHOG PROTEIN; SUPEROXIDE; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG; GLI1 PROTEIN, HUMAN; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; TRANSCRIPTION FACTOR;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG RESISTANCE; DRUG TARGETING; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC50; MESOTHELIOMA; MESOTHELIOMA CELL LINE; MITOCHONDRION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; CELL CYCLE CHECKPOINT; CELL CYCLE G1 PHASE; DRUG EFFECTS; GENETICS; HCT116 CELL LINE; HT 29 CELL LINE; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; G1 PHASE; HCT116 CELLS; HT29 CELLS; HUMANS; LUNG NEOPLASMS; MESOTHELIOMA; MITOCHONDRIA; OXIDATIVE STRESS; PYRIDINES; PYRIMIDINES; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84922735590     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2729     Document Type: Article

References (41)

1. Robinson B, Lake R. Advances in malignant mesothelioma. N Engl J Med. 2005; 353:1591-1603.
2. Ceresoli GL, Gridelli C, Santoro A. Multidisciplinary treatment of malignant pleural mesothelioma. Oncologist. 2007; 12:850-863.
3. Ingham P McMahon A. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 2001; 15:3059-3087.
4. van den Brink GR. Hedgehog signaling in development and homeostasis of the gastrointestinal tract. Physiological reviews. 2007; 87:1343-1375.
5. Stone D, Hynes M, Armanini M, Swanson T, Gu Q, Johnson R, Scott M, Pennica D, Goddard A, Phillips H, Noll M, Hooper J, de Sauvage F, Rosenthal A. The tumoursuppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature. 1996; 384:129-134.
6. Taipale J, Cooper MK, Maiti T, Beachy PA. Patched acts catalytically to suppress the activity of Smoothened. Nature. 2002; 418:892-897.
7. Katoh Y, Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med. 2009; 9:873-886.
8. Axelson M, Liu K, Jiang X, He K, Wang J, Zhao H, Kufrin D, Palmby T, Dong Z, Russell AM, Miksinski S, Keegan P. Pazdur R. U.S. Food and Drug Administration approval: vismodegib for recurrent, locally advanced, or metastatic basal cell carcinoma. Clin Cancer Res. 2013; 19:2289-2293.
9. Lauth M, Bergstrom A, Shimokawa T, Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci U S A. 2007; 104:8455-8460.
10. Mazumdar T, Devecchio J, Agyeman A, Shi T, Houghton JA. Blocking Hedgehog survival signaling at the level of the GLI genes induces DNA damage and extensive cell death in human colon carcinoma cells. Cancer Res. 2011; 71:5904-5914.
11. Kawabata N, Ijiri K, Ishidou Y, Yamamoto T, Nagao H, Nagano S, Maeda S, Komiya S, Setoguchi T. Pharmacological inhibition of the Hedgehog pathway prevents human rhabdomyosarcoma cell growth. International journal of oncology. 2011; 39:899-906.
12. Desch P, Asslaber D, Kern D, Schnidar H, Mangelberger D, Alinger B, Stoecher M, Hofbauer SW, Neureiter D, Tinhofer I, Aberger F, Hartmann TN, Greil R. Inhibition of GLI, but not Smoothened, induces apoptosis in chronic lymphocytic leukemia cells. Oncogene. 2010; 29:4885-4895.
13. You M, Varona-Santos J, Singh S, Robbins DJ, Savaraj N, Nguyen DM. Targeting of the Hedgehog signal transduction pathway suppresses survival of malignant pleural mesothelioma cells in vitro. The Journal of thoracic and cardiovascular surgery. 2013; 147:508-516.
14. Wickstrom M, Dyberg C, Shimokawa T, Milosevic J, Baryawno N, Fuskevag OM, Larsson R, Kogner P, Zaphiropoulos PG, Johnsen JI. Targeting the hedgehog signal transduction pathway at the level of GLI inhibits neuroblastoma cell growth in vitro and in vivo. International journal of cancer Journal international du cancer. 2013; 132:1516-1524.
15. Mazumdar T, DeVecchio J, Shi T, Jones J, Agyeman A, Houghton JA. Hedgehog signaling drives cellular survival in human colon carcinoma cells. Cancer Res. 2011; 71:1092-1102.
16. Wang Y, Han C, Lu L, Magliato S, Wu T. Hedgehog signaling pathway regulates autophagy in human hepatocellular carcinoma cells. Hepatology. 2013; 58:995-1010.
17. Fang J, Seki T, Maeda H. Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Advanced drug delivery reviews. 2009; 61:290-302.
18. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Molecular cell. 2012; 48:158-167.
19. Wondrak GT. Redox-directed cancer therapeutics: molecular mechanisms and opportunities. Antioxidants & redox signaling. 2009; 11:3013-3069.
20. Bigelow RL, Chari NS, Unden AB, Spurgers KB, Lee S, Roop DR, Toftgard R, McDonnell TJ. Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J Biol Chem. 2004; 279:1197-1205.
21. Li H, Lui N, Cheng T, Tseng HH, Yue D, Giroux-Leprieur E, Do HT, Sheng Q, Jin JQ, Luh TW, Jablons DM, He B. Gli as a novel therapeutic target in malignant pleural mesothelioma. PLoS One. 2013; 8:e57346.
22. Bosco-Clement G, Zhang F, Chen Z, Zhou HM, Li H, Mikami I, Hirata T, Yagui-Beltran A, Lui N, Do HT, Cheng T, Tseng HH, Choi H, Fang LT, Kim IJ, Yue D, et al. Targeting Gli transcription activation by small molecule suppresses tumor growth. Oncogene. 2014; 33:2087-2097.
23. Tostar U, Toftgard R, Zaphiropoulos PG, Shimokawa T. Reduction of human embryonal rhabdomyosarcoma tumor growth by inhibition of the hedgehog signaling pathway. Genes & cancer. 2010; 1:941-951.
24. Pan D, Li Y, Li Z, Wang Y, Wang P, Liang Y. Gli inhibitor GANT61 causes apoptosis in myeloid leukemia cells and acts in synergy with rapamycin. Leukemia research. 2012; 36:742-748.
25. Nagao H, Ijiri K, Hirotsu M, Ishidou Y, Yamamoto T, Nagano S, Takizawa T, Nakashima K, Komiya S, Setoguchi T. Role of GLI2 in the growth of human osteosarcoma. The Journal of pathology. 2011; 224:169-179.
26. Agyeman A, Jha BK, Mazumdar T, Houghton JA. Mode and specificity of binding of the small molecule GANT61 to GLI determines inhibition of GLI-DNA binding. Oncotarget. 2014; 5:4492-4503.
27. Agyeman A, Mazumdar T, Houghton JA. Regulation of DNA damage following termination of Hedgehog (HH) survival signaling at the level of the GLI genes in human colon cancer. Oncotarget. 2012; 3:854-868.
28. Thomas ZI, Gibson W, Sexton JZ, Aird KM, Ingram SM, Aldrich A, Lyerly HK, Devi GR, Williams KP. Targeting GLI1 expression in human inflammatory breast cancer cells enhances apoptosis and attenuates migration. Br J Cancer. 2011; 104:1575-1586.
29. Wang K, Pan L, Che X, Cui D, Li C. Gli1 inhibition induces cell-cycle arrest and enhanced apoptosis in brain glioma cell lines. Journal of neuro-oncology. 2010; 98:319-327.
30. Chen XL, Cao LQ, She MR, Wang Q, Huang XH, Fu XH. Gli-1 siRNA induced apoptosis in Huh7 cells. World journal of gastroenterology: WJG. 2008; 14:582-589.
31. Lambert C, Apel K, Biesalski HK, Frank J. 2-methoxyestradiol induces caspase-independent, mitochondria-centered apoptosis in DS-sarcoma cells. International journal of cancer Journal international du cancer. 2004; 108:493-501.
32. Ruefli AA, Ausserlechner MJ, Bernhard D, Sutton VR, Tainton KM, Kofler R, Smyth MJ, Johnstone RW. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci U S A. 2001; 98:10833-10838.
33. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annual review of pharmacology and toxicology. 2007; 47:143-183.
34. Jiang F, Zhang Y, Dusting GJ. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacological reviews. 2011; 63:218-242.
35. Chandel NS, Schumacker PT. Cells depleted of mitochondrial DNA (rho0) yield insight into physiological mechanisms. FEBS letters. 1999; 454:173-176.
36. King MP, Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 1989; 246:500-503.
37. Manning LS, Whitaker D, Murch AR, Garlepp MJ, Davis MR, Musk AW, Robinson BW. Establishment and characterization of five human malignant mesothelioma cell lines derived from pleural effusions. International journal of cancer Journal international du cancer. 1991; 47:285-290.
38. Lim CB, Prele CM, Cheah HM, Cheng YY, Klebe S, Reid G, Watkins DN, Baltic S, Thompson PJ, Mutsaers SE. Mutational analysis of hedgehog signaling pathway genes in human malignant mesothelioma. PLoS One. 2013; 8:e66685.
39. Oliver MH, Harrison NK, Bishop JE, Cole PJ, Laurent GJ. A rapid and convenient assay for counting cells cultured in microwell plates: application for assessment of growth factors. Journal of cell science. 1989; 92:513-518.
40. Wu K, Jiang SW, Couch FJ. p53 mediates repression of the BRCA2 promoter and down-regulation of BRCA2 mRNA and protein levels in response to DNA damage. J Biol Chem. 2003; 278:15652-15660.
41. Moro L, Arbini AA, Yao JL, di Sant'Agnese PA, Marra E, Greco M. Mitochondrial DNA depletion in prostate epithelial cells promotes anoikis resistance and invasion through activation of PI3K/Akt2. Cell death and differentiation. 2009; 16:571-583.