2,119
Views
48
CrossRef citations to date
0
Altmetric
Research Paper

Berberine reverses lapatinib resistance of HER2-positive breast cancer cells by increasing the level of ROS

, , , , , & show all
Pages 925-934 | Received 28 Dec 2015, Accepted 03 Jul 2016, Published online: 22 Aug 2016

References

  • Jeffrey SS, Lonning PE, Hillner BE. Genomics-based prognosis and therapeutic prediction in breast cancer. J Natl Compr Canc Net 2005; 3:291-300; PMID:16002001
  • Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244:707-12; PMID:2470152; http://dx.doi.org/10.1126/science.2470152
  • Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001; 2:127-37; PMID:11252954; http://dx.doi.org/10.1038/35052073
  • Arteaga CL, Sliwkowski MX, Osborne CK, Perez EA, Puglisi F, Gianni L. Treatment of HER2-positive breast cancer: current status and future perspectives. Nat Rev Clin Oncol 2012; 9:16-32; PMID:22124364; http://dx.doi.org/10.1038/nrclinonc.2011.177
  • Higa GM, Abraham J. Lapatinib in the treatment of breast cancer. Exp Rev Anticancer Ther 2007; 7:1183-92; PMID:17892419; http://dx.doi.org/10.1586/14737140.7.9.1183
  • Wood ER, Truesdale AT, McDonald OB, Yuan D, Hassell A, Dickerson SH, Ellis B, Pennisi C, Horne E, Lackey K, et al. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res 2004; 64:6652-9; PMID:15374980; http://dx.doi.org/10.1158/0008-5472.CAN-04-1168
  • Dai CL, Tiwari AK, Wu CP, Su XD, Wang SR, Liu DG, Ashby CR Jr, Huang Y, Robey RW, Liang YJ, et al. Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2. Cancer Res 2008; 68:7905-14; PMID:18829547; http://dx.doi.org/10.1158/0008-5472.CAN-08-0499
  • Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, Untch M, Rusnak DW, Spehar G, Mullin RJ, et al. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res 2006; 66:1630-9; PMID:16452222; http://dx.doi.org/10.1158/0008-5472.CAN-05-1182
  • Xia W, Mullin RJ, Keith BR, Liu LH, Ma H, Rusnak DW, Owens G, Alligood KJ, Spector NL. Anti-tumor activity of GW572016: a dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene 2002; 21:6255-63; PMID:12214266; http://dx.doi.org/10.1038/sj.onc.1205794
  • Rusnak DW, Lackey K, Affleck K, Wood ER, Alligood KJ, Rhodes N, Keith BR, Murray DM, Knight WB, Mullin RJ, et al. The effects of the novel, reversible epidermal growth factor receptor/ErbB-2 tyrosine kinase inhibitor, GW2016, on the growth of human normal and tumor-derived cell lines in vitro and in vivo. Mol Cancer Ther 2001; 1:85-94; PMID:12467226
  • Campone M, Juin P, Andre F, Bachelot T. Resistance to HER2 inhibitors: is addition better than substitution? Rationale for the hypothetical concept of drug sedimentation. Crit Rev Oncol/Hematol 2011; 78:195-205; PMID:20684884; http://dx.doi.org/10.1016/j.critrevonc.2010.04.012
  • Imanshahidi M, Hosseinzadeh H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother Res 2008; 22:999-1012; PMID:18618524; http://dx.doi.org/10.1002/ptr.2399
  • Singhal KC. Anthelmintic activity of berberine hydrochloride against Syphacia obvelata in mice. Indian J Exp Biol 1976; 14:345-7; PMID:1033150
  • Tang J, Feng Y, Tsao S, Wang N, Curtain R, Wang Y. Berberine and Coptidis rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations. J Ethnopharmacol 2009; 126:5-17; PMID:19686830; http://dx.doi.org/10.1016/j.jep.2009.08.009
  • Kim S, Han J, Lee SK, Choi MY, Kim J, Lee J, Jung SP, Kim JS, Kim JH, Choe JH, et al. Berberine suppresses the TPA-induced MMP-1 and MMP-9 expressions through the inhibition of PKC-alpha in breast cancer cells. J Surg Res 2012; 176:e21-9; PMID:22381172; http://dx.doi.org/10.1016/j.jss.2011.11.1041
  • Kim JB, Ko E, Han W, Shin I, Park SY, Noh DY. Berberine diminishes the side population and ABCG2 transporter expression in MCF-7 breast cancer cells. Planta medica 2008; 74:1693-700; PMID:18951337; http://dx.doi.org/10.1055/s-0028-1088313
  • Kim DW, Ahan SH, Kim TY. Enhancement of Arsenic Trioxide (As(2)O(3))- Mediated Apoptosis Using Berberine in Human Neuroblastoma SH-SY5Y Cells. J Korean Neurosurg Soc 2007; 42:392-9; PMID:19096576; http://dx.doi.org/10.3340/jkns.2007.42.5.392
  • Liu J, He C, Zhou K, Wang J, Kang JX. Coptis extracts enhance the anticancer effect of estrogen receptor antagonists on human breast cancer cells. Biochem Biophys Res Commun 2009; 378:174-8; PMID:19000652; http://dx.doi.org/10.1016/j.bbrc.2008.10.169
  • Formentini L, Sanchez-Arago M, Sanchez-Cenizo L, Cuezva JM. The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol Cell 2012; 45:731-42; PMID:22342343; http://dx.doi.org/10.1016/j.molcel.2012.01.008
  • Gnocchi D, Leoni S, Incerpi S, Bruscalupi G. 3,5,3′-triiodothyronine (T3) stimulates cell proliferation through the activation of the PI3K/Akt pathway and reactive oxygen species (ROS) production in chick embryo hepatocytes. Steroids 2012; 77:589-95; PMID:22366194; http://dx.doi.org/10.1016/j.steroids.2012.01.022
  • Lenaz G. Mitochondria and reactive oxygen species. Which role in physiology and pathology? Adv Exp Med Biol 2012; 942:93-136; PMID:22399420; http://dx.doi.org/10.1007/978-94-007-2869-1_5
  • Kuo PL, Chen CY, Hsu YL. Isoobtusilactone A induces cell cycle arrest and apoptosis through reactive oxygen species/apoptosis signal-regulating kinase 1 signaling pathway in human breast cancer cells. Cancer Res 2007; 67:7406-20; PMID:17671211; http://dx.doi.org/10.1158/0008-5472.CAN-07-1089
  • Xie J, Xu Y, Huang X, Chen Y, Fu J, Xi M, Wang L. Berberine-induced apoptosis in human breast cancer cells is mediated by reactive oxygen species generation and mitochondrial-related apoptotic pathway. Tumour Biol 2015; 36:1279-88; PMID:25352028; http://dx.doi.org/10.1007/s13277-014-2754-7
  • Zhang DD. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 2006; 38:769-89; PMID:17145701; http://dx.doi.org/10.1080/03602530600971974
  • Venugopal R, Jaiswal AK. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc Natl Acad Sci U S A 1996; 93:14960-5; PMID:8962164; http://dx.doi.org/10.1073/pnas.93.25.14960
  • Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T, Harada T, Yamamoto M. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 2001; 59:169-77; PMID:11134556; http://dx.doi.org/10.1093/toxsci/59.1.169
  • Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci U S A 2001; 98:4611-6; PMID:11287661; http://dx.doi.org/10.1073/pnas.081082098
  • Li YJ, Takizawa H, Azuma A, Kohyama T, Yamauchi Y, Takahashi S, Yamamoto M, Kawada T, Kudoh S, Sugawara I. Disruption of Nrf2 enhances susceptibility to airway inflammatory responses induced by low-dose diesel exhaust particles in mice. Clin Immunol 2008; 128:366-73; PMID:18614404; http://dx.doi.org/10.1016/j.clim.2008.05.005
  • Iizuka T, Ishii Y, Itoh K, Kiwamoto T, Kimura T, Matsuno Y, Morishima Y, Hegab AE, Homma S, Nomura A, et al. Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells 2005; 10:1113-25; PMID:16324149; http://dx.doi.org/10.1111/j.1365-2443.2005.00905.x
  • Aoki Y, Sato H, Nishimura N, Takahashi S, Itoh K, Yamamoto M. Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicol Appl Pharmacol 2001; 173:154-60; PMID:11437637; http://dx.doi.org/10.1006/taap.2001.9176
  • Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci U S A 2001; 98:3410-5; PMID:11248092; http://dx.doi.org/10.1073/pnas.051618798
  • Iida K, Itoh K, Kumagai Y, Oyasu R, Hattori K, Kawai K, Shimazui T, Akaza H, Yamamoto M. Nrf2 is essential for the chemopreventive efficacy of oltipraz against urinary bladder carcinogenesis. Cancer Res 2004; 64:6424-31; PMID:15374950; http://dx.doi.org/10.1158/0008-5472.CAN-04-1906
  • Mao L, Wang H, Qiao L, Wang X. Disruption of Nrf2 enhances the upregulation of nuclear factor-kappaB activity, tumor necrosis factor-alpha, and matrix metalloproteinase-9 after spinal cord injury in mice. Mediators of inflammation 2010; 2010:238321; PMID:20862369; http://dx.doi.org/10.1155/2010/238321
  • Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, Chen W, Yi X, Zheng W, Wondrak GT, et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008; 29:1235-43; PMID:18413364; http://dx.doi.org/10.1093/carcin/bgn095
  • Li Z, Geng YN, Jiang JD, Kong WJ. Antioxidant and anti-inflammatory activities of berberine in the treatment of diabetes mellitus. Evid-Based Complement Alternat Med 2014; 2014:289264; PMID:24669227; http://dx.doi.org/10.1155/2014/289264
  • Robidoux A, Tang G, Rastogi P, Geyer CE, Jr., Azar CA, Atkins JN, Fehrenbacher L, Bear HD, Baez-Diaz L, Sarwar S, et al. Lapatinib as a component of neoadjuvant therapy for HER2-positive operable breast cancer (NSABP protocol B-41): an open-label, randomised phase 3 trial. Lancet Oncol 2013; 14:1183-92; PMID:24095300; http://dx.doi.org/10.1016/S1470-2045(13)70411-X
  • Liu L, Greger J, Shi H, Liu Y, Greshock J, Annan R, Halsey W, Sathe GM, Martin AM, Gilmer TM. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res 2009; 69:6871-8; PMID:19671800; http://dx.doi.org/10.1158/0008-5472.CAN-08-4490
  • Wang Q, Quan H, Zhao J, Xie C, Wang L, Lou L. RON confers lapatinib resistance in HER2-positive breast cancer cells. Cancer Lett 2013; 340:43-50; PMID:23811285; http://dx.doi.org/10.1016/j.canlet.2013.06.022
  • Brady SW, Zhang J, Seok D, Wang H, Yu D. Enhanced PI3K p110alpha signaling confers acquired lapatinib resistance that can be effectively reversed by a p110alpha-selective PI3K inhibitor. Mol Cancer Ther 2014; 13:60-70; PMID:24249715; http://dx.doi.org/10.1158/1535-7163.MCT-13-0518
  • Chen S, Zhu X, Qiao H, Ye M, Lai X, Yu S, Ding L, Wen A, Zhang J. Protective autophagy promotes the resistance of HER2-positive breast cancer cells to lapatinib. Tumour Biol 2016 Feb; 37(2):2321-31; PMID:26369543; http://dx.doi.org/10.1007/s13277-015-3800-9
  • Tan W, Zhong Z, Wang S, Suo Z, Yang X, Hu X, Wang Y. Berberine Regulated Lipid Metabolism in the Presence of C75, Compound C, and TOFA in Breast Cancer Cell Line MCF-7. Evid-Based Complement Alternative Med 2015; 2015:396035; PMID:26351511; http://dx.doi.org/10.1155/2015/396035
  • Mohanty S, Saha S, Md SHD, Adhikary A, Mukherjee S, Manna A, Chakraborty S, Mazumdar M, Ray P, Das K, et al. ROS-PIASgamma cross talk channelizes ATM signaling from resistance to apoptosis during chemosensitization of resistant tumors. Cell Death Dis 2014; 5:e1021; PMID:24457965; http://dx.doi.org/10.1038/cddis.2013.534
  • Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29:323-33; PMID:11035261; http://dx.doi.org/10.1016/S0891-5849(00)00302-6
  • Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 2004; 7:97-110; PMID:15158766; http://dx.doi.org/10.1016/j.drup.2004.01.004
  • Zhang M, Wang A, Xia T, He P. Effects of fluoride on DNA damage, S-phase cell-cycle arrest and the expression of NF-kappaB in primary cultured rat hippocampal neurons. Toxicol Lett 2008; 179:1-5; PMID:18485627; http://dx.doi.org/10.1016/j.toxlet.2008.03.002
  • Tkachev VO, Menshchikova EB, Zenkov NK. Mechanism of the Nrf2/Keap1/ARE signaling system. Biochem Biokhimiia 2011; 76:407-22; PMID:21585316; http://dx.doi.org/10.1134/S0006297911040031
  • Rada P, Rojo AI, Evrard-Todeschi N, Innamorato NG, Cotte A, Jaworski T, Tobón-Velasco JC, Devijver H, García-Mayoral MF, Van Leuven F, et al. Structural and functional characterization of Nrf2 degradation by the glycogen synthase kinase 3/beta-TrCP axis. Mol Cell Biol 2012; 32:3486-99; PMID:22751928; http://dx.doi.org/10.1128/MCB.00180-12
  • DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K, Mangal D, Yu KH, Yeo CJ, Calhoun ES, et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475:106-9; PMID:21734707; http://dx.doi.org/10.1038/nature10189
  • Matkar S, Sharma P, Gao S, Gurung B, Katona BW, Liao J, Muhammad AB, Kong XC, Wang L, Jin G, et al. An Epigenetic Pathway Regulates Sensitivity of Breast Cancer Cells to HER2 Inhibition via FOXO/c-Myc Axis. Cancer Cell 2015; 28:472-85; PMID:26461093; http://dx.doi.org/10.1016/j.ccell.2015.09.005
  • Zhang J, Cao H, Zhang B, Cao H, Xu X, Ruan H, Yi T, Tan L, Qu R, Song G, et al. Berberine potently attenuates intestinal polyps growth in ApcMin mice and familial adenomatous polyposis patients through inhibition of Wnt signalling. J Cell Mol Med 2013; 17:1484-93; PMID:24015932; http://dx.doi.org/10.1111/jcmm.12119

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.