Improved apoptotic cell death in drug-resistant non-small-cell lung cancer cells by tumor necrosis factor-related apoptosis-inducing ligand-based treatments

Journal of Pharmacology and Experimental Therapeutics

Volumn 348, Issue 3, 2014, Pages 360-371

  Gatti, L ^a   Cossa, G ^a   Tinelli, S ^a   Carenini, N ^a   Arrighetti, N ^a   Pennati, M ^a   Cominetti, D ^a   De Cesare, M ^a   Zunino, F ^a   Zaffaroni, N ^a   Perego, P ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ARSENIC TRIOXIDE; CISPLATIN; SANGUINARINE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER MODEL; CELL STRAIN A549; CELL STRAIN A549/PT; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR XENOGRAFT; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; BENZOPHENANTHRIDINES; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HUMANS; ISOQUINOLINES; LUNG NEOPLASMS; OXIDES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84896731328     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.210054     Document Type: Article

References (46)

1. Adhami VM, Aziz MH, Reagan-Shaw SR, Nihal M, Mukhtar H, and Ahmad N (2004) Sanguinarine causes cell cycle blockade and apoptosis of human prostate carcinoma cells via modulation of cyclin kinase inhibitor-cyclin-cyclin- dependent kinase machinery. Mol Cancer Ther 3:933-940.
2. Ahsan H, Reagan-Shaw S, Breur J, and Ahmad N (2007) Sanguinarine induces apoptosis of human pancreatic carcinoma AsPC-1 and BxPC-3 cells via modulations in Bcl-2 family proteins. Cancer Lett 249:198-208.
3. Baritaki S, Huerta-Yepez S, Sakai T, Spandidos DA, and Bonavida B (2007) Chemotherapeutic drugs sensitize cancer cells to TRAIL-mediated apoptosis: upregulation of DR5 and inhibition of Yin Yang 1. Mol Cancer Ther 6:1387-1399.
4. Beretta GL, Benedetti V, Cossa G, Assaraf YG, Bram E, Gatti L, Corna E, Carenini N, Colangelo D, and Howell SB, et al. (2010) Increased levels and defective glycosylation of MRPs in ovarian carcinoma cells resistant to oxaliplatin. Biochem Pharmacol 79:1108-1117.
5. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, and Tinelli S, et al. (2009) Highly tumorigenic lung cancer CD1331 cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106:16281-16286.
6. Bhojani MS, Rossú BD, and Rehemtulla A (2003) TRAIL and anti-tumor responses. Cancer Biol Ther 2(4, Suppl 1)S71-S78.
7. Chen GQ, Zhu J, Shi XG, Ni JH, Zhong HJ, Si GY, Jin XL, Tang W, Li XS, and Xong SM, et al. (1996) In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 88:1052-1061.
8. Choi WY, Jin CY, Han MH, Kim GY, Kim ND, Lee WH, Kim SK, and Choi YH (2009) Sanguinarine sensitizes human gastric adenocarcinoma AGS cells to TRAILmediated apoptosis via down-regulation of AKT and activation of caspase-3. Anticancer Res 29:4457-4465.
9. Debiton E, Madelmont JC, Legault J, and Barthomeuf C (2003) Sanguinarineinduced apoptosis is associated with an early and severe cellular glutathione depletion. Cancer Chemother Pharmacol 51:474-482.
10. Fulda S (2013) The dark side of TRAIL signaling. Cell Death Differ 20:845-846.
11. Gatti L, Beretta GL, Cossa G, Zunino F, and Perego P (2009) ABC transporters as potential targets for modulation of drug resistance. Mini Rev Med Chem 9: 1102-1112.
12. Godowski KC (1989) Antimicrobial action of sanguinarine. J Clin Dent 1:96-101.
13. Grandi M, Geroni C, and Giuliani FC (1986) Isolation and characterization of a human colon adenocarcinoma cell line resistant to doxorubicin. Br J Cancer 54: 515-518.
14. Hao C, Song JH, Hsi B, Lewis J, Song DK, Petruk KC, Tyrrell DL, and Kneteman NM (2004) TRAIL inhibits tumor growth but is nontoxic to human hepatocytes in chimeric mice. Cancer Res 64:8502-8506.
15. Hussain AR, Al-Jomah NA, Siraj AK, Manogaran P, Al-Hussein K, Abubaker J, Platanias LC, Al-Kuraya KS, and Uddin S (2007) Sanguinarine-dependent induction of apoptosis in primary effusion lymphoma cells. Cancer Res 67:3888-3897.
16. Ichikawa K, Liu W, Zhao L, Wang Z, Liu D, Ohtsuka T, Zhang H, Mountz JD, Koopman WJ, and Kimberly RP, et al. (2001) Tumoricidal activity of a novel antihuman DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 7: 954-960.
17. Jang BC, Park JG, Song DK, Baek WK, Yoo SK, Jung KH, Park GY, Lee TY, and Suh SI (2009) Sanguinarine induces apoptosis in A549 human lung cancer cells primarily via cellular glutathione depletion. Toxicol In Vitro 23:281-287.
18. Jemal A, Bray F, Center MM, Ferlay J, Ward E, and Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69-90.
19. Jin HO, Yoon SI, Seo SK, Lee HC, Woo SH, Yoo DH, Lee SJ, Choe TB, An S, and Kwon TJ, et al. (2006) Synergistic induction of apoptosis by sulindac and arsenic trioxide in human lung cancer A549 cells via reactive oxygen speciesdependent down-regulation of survivin. Biochem Pharmacol 72:1228-1236.
20. Johnstone RW, Frew AJ, and Smyth MJ (2008) The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 8:782-798.
21. Kim S, Lee TJ, Leem J, Choi KS, Park JW, and Kwon TK (2008) Sanguinarineinduced apoptosis: generation of ROS, down-regulation of Bcl-2, c-FLIP, and synergy with TRAIL. J Cell Biochem 104:895-907.
22. Lee JS, Jung WK, Jeong MH, Yoon TR, and Kim HK (2012) Sanguinarine induces apoptosis of HT-29 human colon cancer cells via the regulation of Bax/Bcl-2 ratio and caspase-9-dependent pathway. Int J Toxicol 31:70-77.
23. Lenfeld J, Kroutil M, Marsálek E, Slavík J, Preininger V, and Simánek V (1981) Antiinflammatory activity of quaternary benzophenanthridine alkaloids from Chelidonium majus. Planta Med 43:161-165.
24. Mahady GB and Beecher CW (1994) Quercetin-induced benzophenanthridine alkaloid production in suspension cell cultures of Sanguinaria canadensis. Planta Med 60:553-557.
25. Miller WH, Jr, Schipper HM, Lee JS, Singer J, and Waxman S (2002) Mechanisms of action of arsenic trioxide. Cancer Res 62:3893-3903.
26. Niu C, Yan H, Yu T, Sun HP, Liu JX, Li XS, Wu W, Zhang FQ, Chen Y, and Zhou L, et al. (1999) Studies on treatment of acute promyelocytic leukemia with arsenic trioxide: remission induction, follow-up, and molecular monitoring in 11 newly diagnosed and 47 relapsed acute promyelocytic leukemia patients. Blood 94: 3315-3324.
27. Ong PS, Chan SY, and Ho PC (2012) Microarray analysis revealed dysregulation of multiple genes associated with chemoresistance to As(2)O(3) and increased tumor aggressiveness in a newly established arsenic-resistant ovarian cancer cell line, OVCAR-3/AsR. Eur J Pharm Sci 45:367-378.
28. Park H, Bergeron E, Senta H, Guillemette K, Beauvais S, Blouin R, Sirois J, and Faucheux N (2010) Sanguinarine induces apoptosis of human osteosarcoma cells through the extrinsic and intrinsic pathways. Biochem Biophys Res Commun 399:446-451.
29. Pastorino U (2010) Lung cancer screening. Br J Cancer 102:1681-1686.
30. Perego P, Caserini C, Gatti L, Carenini N, Romanelli S, Supino R, Colangelo D, Viano I, Leone R, and Spinelli S, et al. (1999) A novel trinuclear platinum complex overcomes cisplatin resistance in an osteosarcoma cell system. Mol Pharmacol 55: 528-534.
31. Perego P, Ciusani E, Gatti L, Carenini N, Corna E, and Zunino F (2006) Sensitization to gimatecan-induced apoptosis by tumor necrosis factor-related apoptosis inducing ligand in prostate carcinoma cells. Biochem Pharmacol 71:791-798.
32. Perego P, De Cesare M, De Isabella P, Carenini N, Beggiolin G, Pezzoni G, Palumbo M, Tartaglia L, Pratesi G, and Pisano C, et al. (2001) A novel 7-modified camptothecin analog overcomes breast cancer resistance protein-associated resistance in a mitoxantrone-selected colon carcinoma cell line. Cancer Res 61:6034-6037.
33. Perego P, Romanelli S, Carenini N, Magnani I, Leone R, Bonetti A, Paolicchi A, and Zunino F (1998) Ovarian cancer cisplatin-resistant cell lines: multiple changes including collateral sensitivity to Taxol. Ann Oncol 9:423-430.
34. Piggott L, Omidvar N, Martí Pérez S, Eberl M, and Clarkson RW (2011) Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anti-cancer agent, TRAIL. Breast Cancer Res 13:R88.
35. Rudin D, Li L, Niu N, Kalari KR, Gilbert JA, AmesMM, and Wang L (2011). Gemcitabine Cytotoxicity: Interaction of Efflux and Deamination. J Drug Metab Toxicol 2:1-10.
36. Scholz C, Richter A, Lehmann M, Schulze-Osthoff K, Dörken B, and Daniel PT (2005) Arsenic trioxide induces regulated, death receptor-independent cell death through a Bcl-2-controlled pathway. Oncogene 24:7031-7042.
37. Sève P and Dumontet C (2005) Chemoresistance in non-small cell lung cancer. Curr Med Chem Anticancer Agents 5:73-88.
38. Smith DM, Patel S, Raffoul F, Haller E, Mills GB, and Nanjundan M (2010) Arsenic trioxide induces a beclin-1-independent autophagic pathway via modulation of SnoN/SkiL expression in ovarian carcinoma cells. Cell Death Differ 17:1867-1881.
39. Takeda K, Stagg J, Yagita H, Okumura K, and Smyth MJ (2007) Targeting deathinducing receptors in cancer therapy. Oncogene 26:3745-3757.
40. Tandon RK, Singh DS, Arora RR, Lal P, and Tandon BN (1975) Epidemic dropsy in New Delhi. Am J Clin Nutr 28:883-887.
41. Walker AM, Stevens JJ, Ndebele K, and Tchounwou PB (2010) Arsenic trioxide modulates DNA synthesis and apoptosis in lung carcinoma cells. Int J Environ Res Public Health 7:1996-2007.
42. Wu X, Shi J, Wu Y, Tao Y, Hou J, Meng X, Hu X, Han Y, Jiang W, and Tang S, et al. (2010) Arsenic trioxide-mediated growth inhibition of myeloma cells is associated with an extrinsic or intrinsic signaling pathway through activation of TRAIL or TRAIL receptor 2. Cancer Biol Ther 10:1201-1214.
43. Xu JY, Meng QH, Chong Y, Jiao Y, Zhao L, Rosen EM, and Fan S (2012) Sanguinarine inhibits growth of human cervical cancer cells through the induction of apoptosis. Oncol Rep 28:2264-2270.
44. Zanchi C, Zuco V, Lanzi C, Supino R, and Zunino F (2005) Modulation of survival signaling pathways and persistence of the genotoxic stress as a basis for the synergistic interaction between the atypical retinoid ST1926 and the epidermal growth factor receptor inhibitor ZD1839. Cancer Res 65:2364-2372.
45. Zhang TD, Chen GQ, Wang ZG, Wang ZY, Chen SJ, and Chen Z (2001) Arsenic trioxide, a therapeutic agent for APL. Oncogene 20:7146-7153.
46. Zhao H, Guo W, Peng C, Ji T, and Lu X (2010) Arsenic trioxide inhibits the growth of adriamycin resistant osteosarcoma cells through inducing apoptosis. Mol Biol Rep 37:2509-2515.