ABT-263 enhances sorafenib-induced apoptosis associated with Akt activity and the expression of Bax and p21(CIP1/WAF1) in human cancer cells

British Journal of Pharmacology

Volumn 171, Issue 13, 2014, Pages 3182-3195

  Li, Jingru ^a   Chen, Yicheng ^a   Wan, Jiali ^a   Liu, Xin ^a   Yu, Chunrong ^a   Li, Wenhua ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

ABT 263; cancer; combination therapy; sorafenib

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; NAVITOCLAX; PROTEIN BAX; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SORAFENIB; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; NICOTINAMIDE; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CELL MEMBRANE DEPOLARIZATION; CELL VIABILITY; CLONOGENESIS; COLON CANCER; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SAFETY; ENZYME ACTIVITY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VOLUME; TUMOR XENOGRAFT; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; METABOLISM; NEOPLASMS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANILINE COMPOUNDS; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DRUG SYNERGISM; HUMANS; IN SITU NICK-END LABELING; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SULFONAMIDES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902202963     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12659     Document Type: Article

References (50)

1. Adams JM, Cory S, (2007). The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, Peters JA, Harmar AJ, and CGTP Collaborators (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Catalytic receptors. Br J Pharmacol 170: 1676-1705.
3. Bai D, Ueno L, Vogt PK, (2009). Akt-mediated regulation of NFkappaB and the essentialness of NFkappaB for the oncogenicity of PI3K and Akt. Int J Cancer 125: 2863-2870.
4. Bayir H, Kagan VE, (2008). Bench-to-bedside review: mitochondrial injury, oxidative stress and apoptosis-there is nothing more practical than a good theory. Crit Care 12: 206.
5. Bhattacharya S, Guo H, Ray RM, Johnson LR, (2007). Basic helix-loop-helix protein E47-mediated p21Waf1/Cip1 gene expression regulates apoptosis of intestinal epithelial cells. Biochem J 407: 243-254.
6. Blatt NB, Boitano AE, Lyssiotis CA, Opipari AW Jr, Glick GD, (2009). Bz-423 superoxide signals B cell apoptosis via Mcl-1, Bak, and Bax. Biochem Pharmacol 78: 966-973.
7. Casar B, Arozarena I, Sanz-Moreno V, Pinto A, Agudo-Ibanez L, Marais R, et al. (2009). Ras subcellular localization defines extracellular signal-regulated kinase 1 and 2 substrate specificity through distinct utilization of scaffold proteins. Mol Cell Biol 29: 1338-1353.
8. Chen KF, Tai WT, Liu TH, Huang HP, Lin YC, Shiau CW, et al. (2010). Sorafenib overcomes TRAIL resistance of hepatocellular carcinoma cells through the inhibition of STAT3. Clin Cancer Res 16: 5189-5199.
9. Dasmahapatra G, Yerram N, Dai Y, Dent P, Grant S, (2007). Synergistic interactions between vorinostat and sorafenib in chronic myelogenous leukemia cells involve Mcl-1 and p21CIP1 down-regulation. Clin Cancer Res 13: 4280-4290.
10. Ding H, Han C, Guo D, Wang D, Duan W, Chen CS, et al. (2008). Sensitivity to the non-COX inhibiting celecoxib derivative, OSU03012, is p21(WAF1/CIP1) dependent. Int J Cancer 123: 2931-2938.
11. Fecteau JF, Bharati IS, O'Hayre M, Handel TM, Kipps TJ, Messmer D, (2012). Sorafenib-induced apoptosis of chronic lymphocytic leukemia cells is associated with downregulation of RAF and myeloid cell leukemia sequence 1 (Mcl-1). Mol Med 18: 19-28.
12. Gautier F, Guillemin Y, Cartron PF, Gallenne T, Cauquil N, Le Diguarher T, et al. (2011). Bax activation by engagement with, then release from, the BH3 binding site of Bcl-xL. Mol Cell Biol 31: 832-844.
13. Gong K, Li W, (2011). Shikonin, a Chinese plant-derived naphthoquinone, induces apoptosis in hepatocellular carcinoma cells through reactive oxygen species: a potential new treatment for hepatocellular carcinoma. Free Radic Biol Med 51: 2259-2271.
14. Gong K, Chen C, Zhan Y, Chen Y, Huang Z, Li W, (2012). Autophagy-related gene 7 (ATG7) and reactive oxygen species/extracellular signal-regulated kinase regulate tetrandrine-induced autophagy in human hepatocellular carcinoma. J Biol Chem 287: 35576-35588.
15. Hoeferlin LA, Oleinik NV, Krupenko NI, Krupenko SA, (2011). Activation of p21-dependent G1/G2 Arrest in the absence of DNA damage as an antiapoptotic response to metabolic stress. Genes Cancer 2: 889-899.
16. Li X, Wang J, Ye Z, Li JC, (2012). Oridonin up-regulates expression of P21 and induces autophagy and apoptosis in human prostate cancer cells. Int J Biol Sci 8: 901-912.
17. Liu C, Gong K, Mao X, Li W, (2011a). Tetrandrine induces apoptosis by activating reactive oxygen species and repressing Akt activity in human hepatocellular carcinoma. Int J Cancer 129: 1519-1531.
18. Liu L, Cao Y, Chen C, Zhang X, McNabola A, Wilkie D, et al. (2006). Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 66: 11851-11858.
19. Liu Q, Mier JW, Panka DJ, (2011b). Differential modulatory effects of GSK-3beta and HDM2 on sorafenib-induced AIF nuclear translocation (programmed necrosis) in melanoma. Mol Cancer 10: 115.
20. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
21. Loor G, Kondapalli J, Schriewer JM, Chandel NS, Vanden Hoek TL, Schumacker PT, (2010). Menadione triggers cell death through ROS-dependent mechanisms involving PARP activation without requiring apoptosis. Free Radic Biol Med 49: 1925-1936.
22. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
23. Meng XW, Lee SH, Dai H, Loegering D, Yu C, Flatten K, et al. (2007). Mcl-1 as a buffer for proapoptotic Bcl-2 family members during TRAIL-induced apoptosis: a mechanistic basis for sorafenib (Bay 43-9006)-induced TRAIL sensitization. J Biol Chem 282: 29831-29846.
24. Nguyen TK, Jordan N, Friedberg J, Fisher RI, Dent P, Grant S, (2010). Inhibition of MEK/ERK1/2 sensitizes lymphoma cells to sorafenib-induced apoptosis. Leuk Res 34: 379-386.
25. Panka DJ, Wang W, Atkins MB, Mier JW, (2006). The Raf inhibitor BAY 43-9006 (Sorafenib) induces caspase-independent apoptosis in melanoma cells. Cancer Res 66: 1611-1619.
26. Park MA, Reinehr R, Haussinger D, Voelkel-Johnson C, Ogretmen B, Yacoub A, et al. (2010). Sorafenib activates CD95 and promotes autophagy and cell death via Src family kinases in gastrointestinal tumor cells. Mol Cancer Ther 9: 2220-2231.
27. Pasdois P, Parker JE, Griffiths EJ, Halestrap AP, (2011). The role of oxidized cytochrome c in regulating mitochondrial reactive oxygen species production and its perturbation in ischaemia. Biochem J 436: 493-505.
28. Plastaras JP, Kim SH, Liu YY, Dicker DT, Dorsey JF, McDonough J, et al. (2007). Cell cycle dependent and schedule-dependent antitumor effects of sorafenib combined with radiation. Cancer Res 67: 9443-9454.
29. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N, (2010). RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464: 427-430.
30. Rahmani M, Davis EM, Bauer C, Dent P, Grant S, (2005). Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 280: 35217-35227.
31. Ramakrishnan V, Timm M, Haug JL, Kimlinger TK, Wellik LE, Witzig TE, et al. (2010). Sorafenib, a dual Raf kinase/vascular endothelial growth factor receptor inhibitor has significant anti-myeloma activity and synergizes with common anti-myeloma drugs. Oncogene 29: 1190-1202.
32. Ramanathan A, Schreiber SL, (2009). Direct control of mitochondrial function by mTOR. Proc Natl Acad Sci U S A 106: 22229-22232.
33. Rosato RR, Almenara JA, Coe S, Grant S, (2007). The multikinase inhibitor sorafenib potentiates TRAIL lethality in human leukemia cells in association with Mcl-1 and cFLIPL down-regulation. Cancer Res 67: 9490-9500.
34. Shi J, Zhou Y, Huang HC, Mitchison TJ, (2011). Navitoclax (ABT-263) accelerates apoptosis during drug-induced mitotic arrest by antagonizing Bcl-xL. Cancer Res 71: 4518-4526.
35. Shoemaker AR, Mitten MJ, Adickes J, Ackler S, Refici M, Ferguson D, et al. (2008). Activity of the Bcl-2 family inhibitor ABT-263 in a panel of small cell lung cancer xenograft models. Clin Cancer Res 14: 3268-3277.
36. Singhal SS, Sehrawat A, Sahu M, Singhal P, Vatsyayan R, Rao Lelsani PC, et al. (2010). Rlip76 transports sunitinib and sorafenib and mediates drug resistance in kidney cancer. Int J Cancer 126: 1327-1338.
37. Tan N, Malek M, Zha J, Yue P, Kassees R, Berry L, et al. (2011). Navitoclax enhances the efficacy of taxanes in non-small cell lung cancer models. Clin Cancer Res 17: 1394-1404.
38. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, et al. (2008). ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 68: 3421-3428.
39. Vitiello PF, Wu YC, Staversky RJ, O'Reilly MA, (2009). p21(Cip1) protects against oxidative stress by suppressing ER-dependent activation of mitochondrial death pathways. Free Radic Biol Med 46: 33-41.
40. Vogler M, Dinsdale D, Dyer MJ, Cohen GM, (2009). Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 16: 360-367.
41. Vogler M, Furdas SD, Jung M, Kuwana T, Dyer MJ, Cohen GM, (2010). Diminished sensitivity of chronic lymphocytic leukemia cells to ABT-737 and ABT-263 due to albumin binding in blood. Clin Cancer Res 16: 4217-4225.
42. Wang G, Zhan Y, Wang H, Li W, (2012). ABT-263 sensitizes TRAIL-resistant hepatocarcinoma cells by downregulating the Bcl-2 family of anti-apoptotic protein. Cancer Chem Pharmacol 69: 799-805.
43. Wei G, Wang M, Hyslop T, Wang Z, Carr BI, (2010). Vitamin K enhancement of sorafenib-mediated HCC cell growth inhibition in vitro and in vivo. Int J Cancer 127: 2949-2958.
44. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA, et al. (2006). Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov 5: 835-844.
45. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. (2004). BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 64: 7099-7109.
46. Wilson WH, O'Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, Leonard JP, et al. (2010). Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol 11: 1149-1159.
47. Yamaguchi R, Janssen E, Perkins G, Ellisman M, Kitada S, Reed JC, (2011). Efficient elimination of cancer cells by deoxyglucose-ABT-263/737 combination therapy. PLoS ONE 6: e24102.
48. Yang F, Brown C, Buettner R, Hedvat M, Starr R, Scuto A, et al. (2010). Sorafenib induces growth arrest and apoptosis of human glioblastoma cells through the dephosphorylation of signal transducers and activators of transcription 3. Mol Cancer Ther 9: 953-962.
49. Youle RJ, Strasser A, (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
50. Zhang W, Konopleva M, Ruvolo VR, McQueen T, Evans RL, Bornmann WG, et al. (2008). Sorafenib induces apoptosis of AML cells via Bim-mediated activation of the intrinsic apoptotic pathway. Leukemia 22: 808-818.