Norcantharidin induces melanoma cell apoptosis through activation of TR3 dependent pathway

Cancer Biology and Therapy

Volumn 12, Issue 11, 2011, Pages 1005-1014

  Liu, Shujing ^a   Yu, Hong ^a   Kumar, Suresh M ^a   Martin, James S ^a   Bing, Zhanyong ^a   Sheng, Weiqi ^b   Bosenberg, Marcus ^c   Xu, Xiaowei ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Shanghai Tumor Hospital   (China)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Melanoma; Norcantharidin; TR3

Indexed keywords

B RAF KINASE; CANTHARIDIN; CASPASE 3; CISPLATIN; CYTOCHROME C; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NK KAPPA B2; NORCANTHARIDIN; NUCLEAR RECEPTOR NUR77; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BAX; PROTEIN BCL 2; TEMOZOLOMIDE; TR3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL NUCLEUS; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; ENZYME RELEASE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MELANOMA; MELANOMA CELL; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; MELANOMA; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 82755162410     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.12.11.18380     Document Type: Article

References (44)

1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000; 50:7-33; PMID:10735013; http://dx.doi.org/10.3322/canjclin. 50.1.7
2. Wingo PA, Ries LA, Giovino GA, Miller DS, Rosenberg HM, Shopland DR, et al. Annual report to the nation on the status of cancer, 1973-1996, with a special section on lung cancer and tobacco smoking. J Natl Cancer Inst 1999; 91:675-90; PMID:10218505; http://dx.doi.org/10.1093/jnci/91.8.675
3. Rigel DS, Carucci JA. Malignant melanoma: prevention, early detection, and treatment in the 21st century. CA Cancer J Clin 2000; 50:215-36, quiz 37-40; PMID:10986965; http://dx.doi.org/10.3322/canjclin.50.4.215
4. Eggermont AM, Kirkwood JM. Re-evaluating the role of dacarbazine in metastatic melanoma: what have we learned in 30 years? Eur J Cancer 2004; 40:1825-36; PMID:15288283; http://dx.doi.org/10.1016/j.ejca.2004.04.030
5. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010; 363:809-19; PMID:20818844; http://dx.doi.org/10.1056/NEJMoa1002011
6. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
7. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010; 468:968-72; PMID: 21107320; http://dx.doi.org/10. 1038/nature09627
8. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF (V600E) inhibition by RTK or N-RAS upregulation. Nature 2010; 468:973-7; PMID:21107323; http://dx.doi.org/10.1038/nature09626
9. Solit DB, Rosen N. Resistance to BRAF inhibition in melanomas. N Engl J Med 2011; 364:772-4; PMID: 21345109; http://dx.doi.org/10.1056/NEJMcibr1013704
10. Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 2010; 18:683-95; PMID:21156289; http://dx.doi.org/10.1016/j.ccr. 2010.11.023
11. Ivanov VN, Bhoumik A, Ronai Z. Death receptors and melanoma resistance to apoptosis. Oncogene 2003; 22:3152-61; PMID:12789291; http://dx.doi.org/10.1038/ sj.onc.1206456
12. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell 1997; 88:347-54; PMID:9039261; http://dx.doi.org/10.1016/ S0092- 8674(00)81873-5
13. Rudin CM, Thompson CB. Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu RevMed 1997; 48:267-81;PMID:9046961; http://dx.doi.org/10.1146/annurev.med.48.1.267
14. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 1999; 6:1028-42; PMID:10578171; http://dx.doi.org/10.1038/sj.cdd.4400598
15. Liang B, Song X, Liu G, Li R, Xie J, Xiao L, et al. Involvement of TR3/Nur77 translocation to the endoplasmic reticulum in ER stress-induced apoptosis. Exp Cell Res 2007; 313:2833-44; PMID:17543302; http://dx.doi.org/10. 1016/j.yexcr.2007.04.032
16. Moll UM, Marchenko N, Zhang XK. p53 and Nur77/ TR3 - transcription factors that directly target mitochondria for cell death induction. Oncogene 2006; 25:4725-43; PMID:16892086; http://dx.doi.org/10.1038/sj.onc.1209601
17. Chen HZ, Zhao BX, Zhao WX, Li L, Zhang B, Wu Q. Akt phosphorylates the TR3 orphan receptor and blocks its targeting to the mitochondria. Carcinogenesis 2008; 29:2078-88; PMID:18713840; http://dx.doi. org/10.1093/carcin/bgn197
18. Zhan YY, Wu Q. [Translocation of orphan receptor TR3 from nuclei to mitochondria induced by staurosporine]. Ai Zheng 2004; 23:1593-8; PMID:15601544
19. Yu H, Kumar SM, Fang D, Acs G, Xu X. Nuclear orphan receptor TR3/Nur77 mediates melanoma cell apoptosis. Cancer Biol Ther 2007; 6:405-12; PMID: 17297306; http://dx.doi.org/10.4161/cbt.6.3.3755
20. Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999; 13:1899-911; PMID:10444588; http://dx.doi.org/10.1101/gad.13.15.1899
21. Er E, Oliver L, Cartron PF, Juin P, Manon S, Vallette FM. Mitochondria as the target of the pro-apoptotic protein Bax. Biochim Biophys Acta 2006; 1757:1301-11; PMID:16836974; http://dx.doi.org/10.1016/j.bbabio.2006.05.032
22. Liao HF, Chen YJ, Chou CH, Wang FW, Kuo CD. Norcantharidin induces cell cycle arrest and inhibits progression of human leukemic Jurkat T cells through mitogen-activated protein kinase-mediated regulation of interleukin-2 production. Toxicol In Vitro 2011; 25:206-12; PMID:21075198; http://dx.doi.org/10.1016/j.tiv.2010.11.001
23. Moed L, Shwayder TA, Chang MW. Cantharidin revisited: a blistering defense of an ancient medicine. Arch Dermatol 2001; 137:1357-60; PMID:11594862
24. Oaks WW, Ditunno JF, Magnani T, Levy HA, Mills LC. Cantharidin poisoning. Arch Intern Med 1960; 105:574-82; PMID:14428136
25. Huang Y, Liu Q, Liu K, Yagasaki K, Zhang G. Suppression of growth of highly-metastatic human breast cancer cells by norcantharidin and its mechanisms of action. Cytotechnology 2009; 59:201-8; PMID:19603282; http://dx.doi.org/10. 1007/s10616-009-9210-3
26. Kok SH, Hong CY, Kuo MY, Lee CH, Lee JJ, Lou IU, et al. Comparisons of norcantharidin cytotoxic effects on oral cancer cells and normal buccal keratinocytes. Oral Oncol 2003; 39:19-26; PMID:12457717; http://dx.doi.org/10. 1016/S1368-8375(01)00129-4
27. Sun ZX, Ma QW, Zhao TD, Wei YL, Wang GS, Li JS. Apoptosis induced by norcantharidin in human tumor cells. World J Gastroenterol 2000; 6:263-5; PMID: 11819571
28. An WW, Wang MW, Tashiro S, Onodera S, Ikejima T. Norcantharidin induces human melanoma A375-S2 cell apoptosis through mitochondrial and caspase pathways. J Korean Med Sci 2004; 19:560-6; PMID:15308848; http://dx.doi.org/10. 3346/jkms.2004.19.4.560
29. Kok SH, Cheng SJ, Hong CY, Lee JJ, Lin SK, Kuo YS, et al. Norcantharidin-induced apoptosis in oral cancer cells is associated with an increase of proapoptotic to antiapoptotic protein ratio. Cancer Lett 2005; 217:43- 52; PMID:15596295; http://dx.doi.org/10.1016/j.canlet. 2004.07.045
30. Chen YN, Cheng CC, Chen JC, Tsauer W, Hsu SL. Norcantharidin-induced apoptosis is via the extracellular signal-regulated kinase and c-Jun-NH2-terminal kinase signaling pathways in human hepatoma HepG2 cells. Br J Pharmacol 2003; 140:461-70; PMID: 12970086; http://dx.doi.org/10.1038/sj.bjp. 0705461
31. Chen X, Kis A, Zettl A, Bertozzi CR. A cell nanoinjector based on carbon nanotubes. Proc Natl Acad Sci USA 2007; 104:8218-22; PMID:17485677; http://dx.doi.org/10.1073/pnas.0700567104
32. Li H, Kolluri SK, Gu J, Dawson MI, Cao X, Hobbs PD, et al. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 2000; 289:1159-64; PMID:10947977; http://dx.doi.org/10. 1126/science.289.5482.1159
33. Wilson AJ, Arango D, Mariadason JM, Heerdt BG, Augenlicht LH. TR3/Nur77 in colon cancer cell apoptosis. Cancer Res 2003; 63:5401-7; PMID:14500374
34. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE, Jr., et al. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009; 41:544-52; PMID:19282848; http://dx.doi.org/10.1038/ng.356
35. Fathi AR, Krautheim A, Lucke S, Becker K, Juergen Steinfelder H. Nonradioactive technique to measure protein phosphatase 2A-like activity and its inhibition by drugs in cell extracts. Anal Biochem 2002; 310:208- 14; PMID:12423640; http://dx.doi.org/10.1016/S0003-2697(02)00377-9
36. McCluskey A, Ackland SP, Bowyer MC, Baldwin ML, Garner J, Walkom CC, et al. Cantharidin analogues: synthesis and evaluation of growth inhibition in a panel of selected tumour cell lines. Bioorg Chem 2003; 31: 68-79; PMID:12697169; http://dx.doi.org/10.1016/S0045-2068(02)00524-2
37. Rauh R, Kahl S, Boechzelt H, Bauer R, Kaina B, Efferth T. Molecular biology of cantharidin in cancer cells. Chin Med 2007; 2:8; PMID:17610718; http://dx.doi.org/10.1186/1749-8546-2-8
38. Peng F, Wei YQ, Tian L, Yang L, Zhao X, Lu Y, et al. Induction of apoptosis by norcantharidin in human colorectal carcinoma cell lines: involvement of the CD95 receptor/ligand. J Cancer Res Clin Oncol 2002; 128:223-30; PMID:11935314; http://dx.doi.org/10.1007/s00432-002-0326-5
39. Efferth T, Rauh R, Kahl S, Tomicic M, Bochzelt H, Tome ME, et al. Molecular modes of action of cantharidin in tumor cells. Biochem Pharmacol 2005; 69:811-8; PMID:15710358; http://dx.doi.org/10.1016/j.bcp.2004.12.003
40. Kumar SM, Yu H, Edwards R, Chen L, Kazianis S, Brafford P, et al. Mutant V600E BRAF increases hypoxia inducible factor-1alpha expression in melanoma. Cancer Res 2007; 67:3177-84; PMID:17409425; http://dx.doi.org/10.1158/0008-5472. CAN-06-3312
41. Chen YJ, Shieh CJ, Tsai TH, Kuo CD, Ho LT, Liu TY, et al. Inhibitory effect of norcantharidin, a derivative compound from blister beetles, on tumor invasion and metastasis in CT26 colorectal adenocarcinoma cells. Anticancer Drugs 2005; 16:293-9; PMID:15711181; http://dx.doi.org/10.1097/00001813- 200503000-00008
42. McConville P, Hambardzumyan D, Moody JB, Leopold WR, Kreger AR, Woolliscroft MJ, et al. Magnetic resonance imaging determination of tumor grade and early response to temozolomide in a genetically engineered mouse model of glioma. Clin Cancer Res 2007; 13:2897-904; PMID:17504989; http://dx.doi.org/10. 1158/1078-0432.CCR-06-3058
43. Dankort D, Filenova E, Collado M, Serrano M, Jones K, McMahon M. A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors. Genes Dev 2007; 21:379-84; PMID:17299132; http://dx.doi.org/10.1101/gad.1516407
44. Bosenberg M, Muthusamy V, Curley DP, Wang Z, Hobbs C, Nelson B, et al. Characterization of melanocyte-specific inducible Cre recombinase transgenic mice. Genesis 2006; 44:262-7; PMID:16676322; http://dx.doi.org/10.1002/dvg.20205