The anti-tumour compound, RH1, causes mitochondria-mediated apoptosis by activating c-Jun N-terminal kinase

British Journal of Pharmacology

Volumn 163, Issue 3, 2011, Pages 567-585

  Park, Moon Taek ^a   Song, Min Jeong ^a   Oh, Eun Taex ^a   Lee, Hyemi ^a   Choi, Bo Hwa ^a   Jeong, Seong Yun ^b   Choi, Eun Kyung ^b   Park, Heon Joo ^a  

^a Inha University School of Medicine   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

Author keywords

AIF; Bax; Endo G; JNK; mitochondria; RH1

Indexed keywords

2,5 DIAZIRIDINYL 3 (HYDROXYMETHYL) 6 METHYL 1,4 BENZOQUINONE; ANTINEOPLASTIC AGENT; APOPTOSIS INDUCING FACTOR; ENDONUCLEASE G; PROTEIN BAX; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; AZIRIDINES; BCL-2-ASSOCIATED X PROTEIN; BENZOQUINONES; CASPASES; CELL LINE, TUMOR; ENDODEOXYRIBONUCLEASES; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NAD(P)H DEHYDROGENASE (QUINONE); PROTEIN TRANSPORT;

EID: 79955894624     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01233.x     Document Type: Article

References (59)

1. Aoki H, Kang PM, Hampe J, Yoshimura K, Noma T, Matsuzaki M, et al,. (2002). Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J Biol Chem 277: 10244-10250. (Pubitemid 34968139)
2. Ariyama H, Qin B, Baba E, Tanaka R, Mitsugi K, Harada M, et al,. (2006). Gefitinib, a selective EGFR tyrosine kinase inhibitor, induces apoptosis through activation of Bax in human gallbladder adenocarcinoma cells. J Cell Biochem 97: 724-734.
3. Asher G, Lotem J, Cohen B, Sachs L, Shaul Y, (2001). Regulation of p53 stability and p53-dependent apoptosis by NADH quinine oxidoreductase 1. Proc Natl Acad Sci USA 98: 1188-1193. (Pubitemid 32121208)
4. Bacus SS, Gudkov AV, Lowe M, Lyass L, Yung Y, Komarov AP, et al,. (2001). Taxol-induced apoptosis depends on MAP kinase pathways (ERK and p38) and is independent of p53. Oncogene 202: 147-155. (Pubitemid 32150260)
5. Benson AM, Hunkeler MJ, Talalay P, (1980). Increase of NAD(P)H:quinone reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity. Proc Natl Acad Sci USA 77: 5216-5220. (Pubitemid 11195538)
6. Bivik C, Ollinger K, (2008). JNK mediates UVB-induced apoptosis upstream lysosomal membrane permeabilization and Bcl-2 family proteins. Apoptosis 13: 1111-1120.
7. Cao X, Deng X, May WS, (2003). Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax. Blood 102: 2605-2614. (Pubitemid 37193602)
8. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N, et al,. (2003). JNK-dependent Release of Mitochondrial Protein, Smac, during Apoptosis in Multiple Myeloma (MM) Cells. J Biol Chem 278: 17593-17596. (Pubitemid 36799359)
9. Choi YJ, Lim SY, Woo JH, Kim YH, Kwon YK, Suh SI, et al,. (2003). Sodium orthovanadate potentiates EGCG-induced apoptosis that is dependent on the ERK pathway. Biochem Biophys Res Commun 305: 176-185. (Pubitemid 36535425)
10. Cummings J, Ritchie A, Butler J, Ward TH, Langdon S, (2003). Activity profile of the novel aziridinylbenzoquinones MeDZQ and RH1 in human tumor xenografts. Anticancer Res 23: 3979-3983. (Pubitemid 37474352)
11. Dadakhujaev S, Jung EJ, Noh HS, Hah YS, Kim CJ, Kim DR, (2009). Interplay between autophagy and apoptosis in TrkA-induced cell death. Autophagy 5: 103-105.
12. Danson S, Ward TH, Butler J, Ranson M, (2004). DT-diaphorase: a target for new anticancer drugs. Cancer Treat Rev 30: 437-449. (Pubitemid 38968124)
13. Danson S, Ranson M, Denneny O, Cummings J, Ward TH, (2007). Validation of the comet-X assay as a pharmacodynamic assay for measuring DNA cross-linking produced by the novel anticancer agent RH1 during a phase 1 clinical trial. Cancer Chemother Pharmacol 60: 851-861. (Pubitemid 47389391)
14. Daugas E, Nochy D, Ravagnan L, Loeffler M, Susin SA, Zamzami N, et al,. (2000). Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476: 118-123. (Pubitemid 30410801)
15. Dehn DL, Inayat-Hussain SH, Ross D, (2005). RH1 induces cellular damage in an NAD(P)H:quinone oxidoreductase 1-dependent manner: relationship between DNA cross-linking, cell cycle perturbations, and apoptosis. J Pharmacol Exp Ther 313: 771-779. (Pubitemid 40604178)
16. Fan M, Goodwin M, Vu T, Brantley-Finley C, Gaarde WA, Chambers TC, (2000). Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ERK cascade. J Biol Chem 275: 29980-29985.
17. Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, et al,. (2001). Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 153: 999-1010.
18. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A, (2001). Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J Biol Chem 276: 23341-23348.
19. Glading A, Bodnar RJ, Reynolds IJ, Shiraha H, Satish L, Potter DA, et al,. (2004). Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol 24: 2499-2512. (Pubitemid 38326004)
20. Haupt S, Berger M, Goldberg Z, Haupt Y, (2003). Apoptosis-the p53 network. J Cell Sci 116: 4077-4085. (Pubitemid 37337082)
21. Hengartner MO, (2000). The biochemistry of apoptosis. Nature 407: 770-776.
22. Ho CY, Li HY, (2010). DNA damage during mitosis invokes a JNK-mediated stress response that leads to cell death. J Cell Biochem 110: 725-731.
23. Huang DC, Strasser A, (2000). BH3-Only proteins-essential initiators of apoptotic cell death. Cell 103: 839-842.
24. Hussein D, Holt SV, Brookes KE, Klymenko T, Adamski JK, Hogg A, et al,. (2009). Preclinical efficacy of the bioreductive alkylating agent RH1 against paediatric tumours (2009). Br J Cancer 101: 55-63.
25. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, et al,. (2001). Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410: 549-554. (Pubitemid 32267191)
26. Kang YH, Lee SJ, (2008). The role of p38 MAPK and JNK in Arsenic trioxide-induced mitochondrial cell death in human cervical cancer cells. J Cell Physiol 217: 23-33.
27. Katagiri C, Masuda K, Urano T, Yamashita K, Araki Y, Kikuchi K, et al,. (2005). Phosphorylation of Ser-446 determines stability of MKP-7. J Biol Chem 280: 14716-14722. (Pubitemid 40562819)
28. Kharbanda S, Saxena S, Yoshida K, Pandey P, Kaneki M, Wang Q, et al,. (2000). Translocation of SAPK/JNK to Mitochondria and Interaction with Bcl-xL in Response to DNA Damage. J Biol Chem 275: 322-327. (Pubitemid 30038988)
29. Kim JY, Kim CH, Stratford IJ, Patterson AV, Hendry JH, (2004a). The bioreductive agent RH1 and gamma-irradiation both cause G2/M cell cycle phase arrest and polyploidy in a p53-mutated human breast cancer cell line. Int J Radiat Oncol Biol Phys 58: 376-385. (Pubitemid 38142462)
30. Kim JY, Patterson AV, Stratford IJ, Hendry JH, (2004b). The importance of DT-diaphorase and hypoxia in the cytotoxicity of RH1 in human breast and non-small cell lung cancer cell lines. Anticancer Drugs 15: 71-77. (Pubitemid 39140175)
31. Klekotka PA, Santoro SA, Wang H, Zutter MM, (2001). Specific residues within the alpha 2 integrin subunit cytoplasmic domain regulate migration and cell cycle progression via distinct MAPK pathways. J Biol Chem 276: 32353-33261.
32. Kroon AM, (1965). Protein synthesis in mitochondria. 3. On the effects of inhibitors on the incorporation of amino acids into protein by intact mitochondria and digitonin fractions. Biochim Biophys Acta 108: 275-284.
33. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, et al,. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489. (Pubitemid 27508237)
34. Lowe SW, Ruley HE, Jacks T, Housman DE, (1993). p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967. (Pubitemid 23289454)
35. Masuda K, Shima H, Katagiri C, Kikuchi K, (2003). Activation of ERK induces phosphorylation of MAPK phosphatase-7, a JNK specific phosphatase, at Ser-446. J Biol Chem 278: 32448-32456. (Pubitemid 37048443)
36. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, et al,. (2003). p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11: 577-590. (Pubitemid 36385115)
37. Nicholson DW, (2000). From bench to clinic with apoptosis-based therapeutic agents. Nature 407: 810-816.
38. Nioi P, Hayes JD, (2004). Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat Res 555: 149-171. (Pubitemid 39359178)
39. Olivier M, Eeles R, Hollstein M, Khan MA, Harris CC, Hainaut P, (2002). The IARC TP53 database: new online mutation analysis and recommendations to users. Hum Mutat 19: 607-614. (Pubitemid 34556481)
40. Park MT, Choi JA, Kim MJ, Um HD, Bae S, Kang CM, et al,. (2003). Suppression of extracellular signal-related kinase and activation of p38 MAPK are two critical events leading to caspase-8- and mitochondria-mediated cell death in phytosphingosine-treated human cancer cells. J Biol Chem 278: 50624-50634. (Pubitemid 37548910)
41. Park MT, Kim MJ, Kang YH, Choi SY, Lee JH, Choi JA, et al,. (2005). Phytosphingosine in combination with ionizing radiation enhances apoptotic cell death in radiation-resistant cancer cells through ROS-dependent and -independent AIF release. Blood 105: 1724-1733.
42. Paumelle R, Tulasne D, Leroy C, Coll J, Vandenbunder B, Fafeur V, (2000). Sequential activation of ERK and repression of JNK by scatter factor/hepatocyte growth factor in madin-darby canine kidney epithelial cells. Mol Biol Cell 11: 3751-3763.
43. Sakahira H, Enari M, Nagata S, (1998). Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391: 96-99. (Pubitemid 28079223)
44. Schroeter H, Boyd CS, Ahmed R, Spencer JP, Duncan RF, Rice-Evans C, et al,. (2003). c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem J 372: 359-369. (Pubitemid 36723881)
45. de Souza-Pinto NC, Mason PA, Hashiguchi K, Weissman L, Tian J, Guay D, et al,. (2009). Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair (Amst) 8: 704-719.
46. Su LT, Chen HC, González-Pagán O, Overton JD, Xie J, Yue L, et al,. (2010). TRPM7 activates m-calpain by stress-dependent stimulation of p38 MAPK and c-Jun N-terminal kinase. J Mol Biol 396: 858-869.
47. Tang PS, Tsang ME, Lodyga M, Bai XH, Miller A, Han B, et al,. (2006). Lipopolysaccharide accelerates caspase-independent but cathepsin B-dependent death of human lung epithelial cells. J Cell Physiol 209: 457-467. (Pubitemid 44484637)
48. Theruvath TP, Snoddy MC, Zhong Z, Lemasters JJ, (2008). Mitochondrial permeability transition in liver ischemia and reperfusion: role of c-Jun N-terminal kinase 2. Transplantation 85: 1500-1504.
49. Toyota H, Yanase N, Yoshimoto T, Moriyama M, Sudo T, Mizuguchi J, (2003). Calpain-induced Bax-cleavage product is a more potent inducer of apoptotic cell death than wild-type Bax. Cancer Lett 189: 221-230. (Pubitemid 35461998)
50. Wada T, Penninger JM, (2004). Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23: 2838-2849. (Pubitemid 38638846)
51. Wang X, Martindale JL, Holbrook NJ, (2000). Requirement for ERK activation in cisplatin-induced apoptosis. J Biol Chem 275: 39435-39443. (Pubitemid 32058968)
52. Ward TH, Danson S, McGown AT, Ranson M, Coe NA, Jayson GC, et al,. (2005). Preclinical evaluation of the pharmacodynamic properties of 2,5-diaziridinyl-3-hydroxymethyl-6-methyl-1,4-benzoquinone. Clin Cancer Res 11: 2695-2701. (Pubitemid 40569471)
53. Werneburg NW, Guicciardi ME, Bronk SF, Kaufmann SH, Gores GJ, (2007). Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J Biol Chem 282: 28960-28970. (Pubitemid 47606073)
54. Winski SL, Hargreaves RH, Butler J, Ross D, (1998). A new screening system for NAD(P)H:quinone oxidoreductase (NQO1)-directed antitumor quinones: identification of a new aziridinylbenzoquinone, RH1, as a NQO1-directed antitumor agent. Clin Cancer Res 4: 3083-3088. (Pubitemid 29001485)
55. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME, (1995). Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331.
56. Xiao D, Singh SV, (2002). Phenethyl isothiocyanate-induced apoptosis in p53-deficient PC-3 human prostate cancer cell line is mediated by extracellular signal-regulated kinases. Cancer Res 62: 3615-3619. (Pubitemid 34728834)
57. Yamaguchi T, Naruishi K, Arai H, Nishimura F, Takashiba S, (2008). IL-6/sIL-6R enhances cathepsin B and L production via caveolin-1-mediated JNK-AP-1 pathway in human gingival fibroblasts. J Cell Physiol 217: 423-432.
58. Yanase N, Ohshima K, Ikegami H, Mizuguchi J, (2000). Cytochrome c release, mitochondrial membrane depolarization, caspase-3 activation, and Bax-alpha cleavage during IFN-alpha-induced apoptosis in Daudi B lymphoma cells. J Interferon Cytokine Res 20: 1121-1129. (Pubitemid 32015252)
59. Yeo JK, Cha SD, Cho CH, Kim SP, Cho JW, Baek WK, et al,. (2002). Se-methylselenocysteine induces apoptosis through caspase activation and Bax cleavage mediated by calpain in SKOV-3 ovarian cancer cells. Cancer Lett 182: 83-92.