Arsenic trioxide overcomes rapamycin-induced feedback activation of akt and erk signaling to enhance the anti-tumor effects in breast cancer

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Guilbert, Cynthia ^a   Annis, Matthew G ^b   Dong, Zhifeng ^b   Siegel, Peter M ^b   Miller Jr , Wilson H ^a,c   Mann, Koren K ^a,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTINEOPLASTIC AGENTS; ARSENICALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEEDBACK, PHYSIOLOGICAL; HUMANS; MICE; OXIDES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84893590883     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085995     Document Type: Article

References (45)

1. Motzer RJ, Escudier B, Oudard S, Hutson TE, Porta C et al. (2008) Efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial. Lancet 372: 449-456. doi:10.1016/S0140-6736(08)61039-9. PubMed: 18653228.
2. Awada A, Cardoso F, Fontaine C, Dirix L, De Grève J et al. (2008) The oral mTOR inhibitor RAD001 (everolimus) in combination with letrozole in patients with advanced breast cancer: results of a phase I study with pharmacokinetics. Eur J Cancer 44: 84-91. doi:10.1016/j.ejca. 2007.10.003. PubMed: 18039566.
3. Yee KW, Zeng Z, Konopleva M, Verstovsek S, Ravandi F et al. (2006) Phase I/II study of the mammalian target of rapamycin inhibitor everolimus (RAD001) in patients with relapsed or refractory hematologic malignancies. Clin Cancer Res 12: 5165-5173. doi: 10.1158/1078-0432.CCR-06-0764. PubMed: 16951235. (Pubitemid 44453345)
4. Wiza C, Nascimento EB, Ouwens DM (2012) Role of PRAS40 in Akt and mTOR signaling in health and disease. Am J Physiol Endocrinol Metab 302: E1453-E1460. doi:10.1152/ajpendo.00660.2011. PubMed: 22354785.
5. Guertin DA, Sabatini DM (2007) Defining the role of mTOR in cancer. Cancer Cell 12: 9-22. doi:10.1016/j.ccr.2007.05.008. PubMed: 17613433. (Pubitemid 47001784)
6. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB et al. (2006) mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 66: 1500-1508. doi: 10.1158/0008-5472.CAN-05-2925. PubMed: 16452206. (Pubitemid 43259931)
7. Tabernero J, Rojo F, Calvo E, Burris H, Judson I et al. (2008) Dose-and schedule-dependent inhibition of the mammalian target of rapamycin pathway with everolimus: a phase I tumor pharmacodynamic study in patients with advanced solid tumors. J Clin Oncol 26: 1603-1610. doi:10.1200/JCO.2007.14.5482. PubMed: 18332469.
8. Park HS, Kim MS, Huh SH, Park J, Chung J et al. (2002) Akt (protein kinase B) negatively regulates SEK1 by means of protein phosphorylation. J Biol Chem 277: 2573-2578. doi:10.1074/jbc.M110299200. PubMed: 11707464. (Pubitemid 34953281)
9. Kim AH, Khursigara G, Sun X, Franke TF, Chao MV (2001) Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol 21: 893-901. doi:10.1128/MCB. 21.3.893-901.2001. PubMed: 11154276.
10. Song JJ, Lee YJ (2005) Dissociation of Akt1 from its negative regulator JIP1 is mediated through the ASK1-MEK-JNK signal transduction pathway during metabolic oxidative stress: a negative feedback loop. J Cell Biol 170: 61-72. doi:10.1083/jcb.200502070. PubMed: 15998799. (Pubitemid 40994096)
11. Tamburini J, Chapuis N, Bardet V, Park S, Sujobert P et al. (2008) Mammalian target of rapamycin (mTOR) inhibition activates phosphatidylinositol 3-kinase/Akt by up-regulating insulin-like growth factor-1 receptor signaling in acute myeloid leukemia: rationale for therapeutic inhibition of both pathways. Blood 111: 379-382. doi: 10.1182/blood-2007-03-080796. PubMed: 17878402.
12. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101. doi:10.1126/science.1106148. PubMed: 15718470. (Pubitemid 40262113)
13. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP et al. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168. doi:10.1016/j.molcel.2006.03.029. PubMed: 16603397.
14. Ma L, Teruya-Feldstein J, Bonner P, Bernardi R, Franz DN et al. (2007) Identification of S664 TSC2 phosphorylation as a marker for extracellular signal-regulated kinase mediated mTOR activation in tuberous sclerosis and human cancer. Cancer Res 67: 7106-7112. doi: 10.1158/0008-5472.CAN-06-4798. PubMed: 17671177. (Pubitemid 47206537)
15. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J (2004) Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci U S A 101: 13489-13494. doi:10.1073/pnas.0405659101. PubMed: 15342917. (Pubitemid 39238430)
16. Carracedo A, Ma L, Teruya-Feldstein J, Rojo F, Salmena L et al. (2008) Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest 118: 3065-3074. PubMed: 18725988.
17. Mi R, Ma J, Zhang D, Li L, Zhang H (2009) Efficacy of combined inhibition of mTOR and ERK/MAPK pathways in treating a tuberous sclerosis complex cell model. J Genet Genomics 36: 355-361. doi: 10.1016/S1673-8527(08)60124-1. PubMed: 19539245.
18. Serra V, Scaltriti M, Prudkin L, Eichhorn PJ, Ibrahim YH et al. (2011) PI3K inhibition results in enhanced HER signaling and acquired ERK dependency in HER2-overexpressing breast cancer. Oncogene 30: 2547-2557. doi:10.1038/onc. 2010.626. PubMed: 21278786.
19. Mann KK, Colombo M, Miller WH Jr. (2008) Arsenic trioxide decreases AKT protein in a caspase-dependent manner. Mol Cancer Ther 7: 1680-1687. doi:10.1158/1535-7163.MCT-07-2164. PubMed: 18566239.
20. Kasukabe T, Okabe-Kado J, Haranosono Y, Kato N, Honma Y (2013) Inhibition of rapamycin-induced Akt phosphorylation by cotylenin A correlates with their synergistic growth inhibition of cancer cells. Int J Oncol 42: 767-775. PubMed: 23255002.
21. Xue P, Hou Y, Zhang Q, Woods CG, Yarborough K et al. (2011) Prolonged inorganic arsenite exposure suppresses insulin-stimulated AKT S473 phosphorylation and glucose uptake in 3T3-L1 adipocytes: involvement of the adaptive antioxidant response. Biochem Biophys Res Commun 407: 360-365. doi:10.1016/j.bbrc.2011.03.024. PubMed: 21396911.
22. Hardin JA, Sherr DH, DeMaria M, Lopez PA (1992) A simple fluorescence method for surface antigen phenotyping of lymphocytes undergoing DNA fragmentation. J Immunol Methods 154: 99-107. doi: 10.1016/0022-1759(92)90217-H. PubMed: 1401949.
23. Mehrara E, Forssell-Aronsson E, Ahlman H, Bernhardt P (2007) Specific growth rate versus doubling time for quantitative characterization of tumor growth rate. Cancer Res 67: 3970-3975. doi: 10.1158/0008-5472.CAN-06-3822. PubMed: 17440113. (Pubitemid 46762187)
24. Holliday DL, Speirs V (2011) Choosing the right cell line for breast cancer research. Breast Cancer Res 13: 215. doi:10.1186/bcr2889. PubMed: 21884641.
25. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N et al. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15: 6541-6551. PubMed: 8978681. (Pubitemid 26413787)
26. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J et al. (2009) An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 284: 8023-8032. doi:10.1074/jbc.M900301200. PubMed: 19150980.
27. Mosley JD, Poirier JT, Seachrist DD, Landis MD, Keri RA (2007) Rapamycin inhibits multiple stages of c-Neu/ErbB2 induced tumor progression in a transgenic mouse model of HER2-positive breast cancer. Mol Cancer Ther 6: 2188-2197. doi: 10.1158/1535-7163.MCT-07-0235. PubMed: 17699716. (Pubitemid 47294747)
28. Diaz Z, Laurenzana A, Mann KK, Bismar TA, Schipper HM et al. (2007) Trolox enhances the anti-lymphoma effects of arsenic trioxide, while protecting against liver toxicity. Leukemia 21: 2117-2127. doi:10.1038/sj.leu.2404891. PubMed: 17690699. (Pubitemid 47430453)
29. Yardley DA (2013) Combining mTOR Inhibitors with Chemotherapy and Other Targeted Therapies in Advanced Breast Cancer: Rationale, Clinical Experience, and Future Directions. Breast Cancer (Auckl) 7: 7-22. PubMed: 23492649.
30. Mondesire WH, Jian W, Zhang H, Ensor J, Hung MC et al. (2004) Targeting mammalian target of rapamycin synergistically enhances chemotherapy-induced cytotoxicity in breast cancer cells. Clin Cancer Res 10: 7031-7042. doi:10.1158/1078-0432.CCR-04-0361. PubMed: 15501983. (Pubitemid 39383055)
31. Campone M, Levy V, Bourbouloux E, Berton Rigaud D, Bootle D et al. (2009) Safety and pharmacokinetics of paclitaxel and the oral mTOR inhibitor everolimus in advanced solid tumours. Br J Cancer 100: 315-321. doi:10.1038/sj.bjc.6604851. PubMed: 19127256.
32. Huober J, Fasching PA, Hanusch C, Rezai M, Eidtmann H et al. (2013) Neoadjuvant chemotherapy with paclitaxel and everolimus in breast cancer patients with non-responsive tumours to epirubicin/cyclophosphamide (EC)+/-bevacizumab - Results of the randomised GeparQuinto study (GBG 44). Eur J Cancer.
33. Baselga J, Campone M, Piccart M, Burris HA 3rd, Rugo HS et al. (2012) Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med 366: 520-529. doi:10.1056/NEJMoa1109653. PubMed: 22149876.
34. Liu N, Tai S, Ding B, Thor RK, Bhuta S et al. (2012) Arsenic trioxide synergizes with everolimus (Rad001) to induce cytotoxicity of ovarian cancer cells through increased autophagy and apoptosis. Endocr Relat Cancer 19: 711-723. doi:10.1530/ERC-12-0150. PubMed: 22919067.
35. Bolt AM, Zhao F, Pacheco S, Klimecki WT (2012) Arsenite-induced autophagy is associated with proteotoxicity in human lymphoblastoid cells. Toxicol Appl Pharmacol 264: 255-261. doi:10.1016/j.taap.2012.08.006. PubMed: 22959463.
36. Bolt AM, Douglas RM, Klimecki WT (2010) Arsenite exposure in human lymphoblastoid cell lines induces autophagy and coordinated induction of lysosomal genes. Toxicol Lett 199: 153-159. doi:10.1016/j.toxlet.2010.08.017. PubMed: 20816728.
37. Huang HS, Liu ZM, Cheng YL (2011) Involvement of glycogen synthase kinase-3beta in arsenic trioxide-induced p21 expression. Toxicol Sci 121: 101-109. doi:10.1093/toxsci/kfr023. PubMed: 21278055.
38. Calvino E, Estan MC, Simon GP, Sancho P, Boyano-Adanez Mdel C et al. (2011) Increased apoptotic efficacy of lonidamine plus arsenic trioxide combination in human leukemia cells. Reactive oxygen species generation and defensive protein kinase (MEK/ERK, Akt/mTOR) modulation. Biochem Pharmacol 82: 1619-1629. doi:10.1016/j.bcp.2011.08.017. PubMed: 21889928. Available online at: doi:10.1016/j.bcp.2011.08.017 Available online at: PubMed: 21889928
39. Estan MC, Calvino E, de Blas E, Boyano-Adanez Mdel C, Mena ML et al. (2012) 2-Deoxy-D-glucose cooperates with arsenic trioxide to induce apoptosis in leukemia cells: involvement of IGF-1R-regulated Akt/mTOR, MEK/ERK and LKB-1/AMPK signaling pathways. Biochem Pharmacol 84: 1604-1616. doi:10.1016/j.bcp.2012.09.022. PubMed: 23041229. Available online at: doi:10.1016/j.bcp.2012.09.022 Available online at: PubMed: 23041229
40. Davison K, Mann KK, Waxman S, Miller WH Jr (2004) JNK activation is a mediator of arsenic trioxide-induced apoptosis in acute promyelocytic leukemia cells. Blood 103: 3496-3502. doi:10.1182/blood-2003-05-1412. PubMed: 14701702. (Pubitemid 38525683)
41. Giafis N, Katsoulidis E, Sassano A, Tallman MS, Higgins LS et al. (2006) Role of the p38 mitogen-activated protein kinase pathway in the generation of arsenic trioxide-dependent cellular responses. Cancer Res 66: 6763-6771. doi:10.1158/0008-5472.CAN-05-3699. PubMed: 16818652. (Pubitemid 44085635)
42. Noh EK, Kim H, Park MJ, Baek JH, Park JH et al. (2010) Gefitinib enhances arsenic trioxide (AS2O3)-induced differentiation of acute promyelocytic leukemia cell line. Leuk Res 34: 1501-1505. doi:10.1016/j.leukres.2010.02.016. PubMed: 20226526.
43. Lunghi P, Costanzo A, Salvatore L, Noguera N, Mazzera L et al. (2006) MEK1 inhibition sensitizes primary acute myelogenous leukemia to arsenic trioxide-induced apoptosis. Blood 107: 4549-4553. doi:10.1182/blood-2005-07- 2829. PubMed: 16467208. (Pubitemid 43801384)
44. Lunghi P, Tabilio A, Lo-Coco F, Pelicci PG, Bonati A (2005) Arsenic trioxide (ATO) and MEK1 inhibition synergize to induce apoptosis in acute promyelocytic leukemia cells. Leukemia 19: 234-244. doi: 10.1038/sj.leu.2403585. PubMed: 15538402. (Pubitemid 40220588)
45. Hoang B, Benavides A, Shi Y, Yang Y, Frost P et al. (2012) The PP242 mammalian target of rapamycin (mTOR) inhibitor activates extracellular signal-regulated kinase (ERK) in multiple myeloma cells via a target of rapamycin complex 1 (TORC1)/eukaryotic translation initiation factor 4E (eIF-4E)/RAF pathway and activation is a mechanism of resistance. J Biol Chem 287: 21796-21805. doi:10.1074/jbc.M111.304626. PubMed: 22556409.