Camptothecin and cisplatin upregulate ABCG2 and MRP2 expression by activating the ATM/NF-κB pathway in lung cancer cells

Ke,Shi   Zhong; Ni,Xiao  Yan; Zhang,Yue  Hua; Wang,Yi  Nan; Wu,Bin; Gao,Feng  Guang

doi:10.3892/ijo.2013.1805

Camptothecin and cisplatin upregulate ABCG2 and MRP2 expression by activating the ATM/NF-κB pathway in lung cancer cells

Authors:
- Shi Zhong Ke
- Xiao Yan Ni
- Yue Hua Zhang
- Yi Nan Wang
- Bin Wu
- Feng Guang Gao
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Affiliations: Department of Immunology, Basic Medicine Science, Medical College, Xiamen University, Xiamen 361005, P.R. China, Department of Pharmacology, Affiliated Renji Hospital of Shanghai Jiao Tong University, Shanghai 200030, P.R. China
Published online on: February 1, 2013 https://doi.org/10.3892/ijo.2013.1805
Pages: 1289-1296

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Abstract

Multidrug resistance (MDR) formation is an important problem in lung cancer chemotherapy. Our study showed that both camptothecin and cisplatin could not only induce ATM and NF-κB activation but also upregulate expression of the MDR-related genes ABCG2, MRP2 in NCI-H446 cells. Moreover, camptothecin and cisplatin-induced ABCG2 and MRP2 upregulation could be impaired by ATM and NF-κB inhibitors, indicating a relationship between ATM, NF-κB activation and MDR formation in lung cancer chemotherapy. Our study indicates that ATM may serve as a potential molecular target for MDR formation in lung cancer chemotherapy.

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1	Tan XL, Moyer AM, Fridley BL, et al: Genetic variation predicting cisplatin cytotoxicity associated with overall survival in lung cancer patients receiving platinum-based chemotherapy. Clin Cancer Res. 17:5801–5811. 2011. View Article : Google Scholar
2	Shinoda C, Maruyama M, Fujishita T, et al: Doxorubicin induces expression of multidrug resistance-associated protein 1 in human small cell lung cancer cell lines by the c-jun N-terminal kinase pathway. Int J Cancer. 117:21–31. 2005. View Article : Google Scholar
3	Spiro SG, Tanner NT, Silvestri GA, et al: Lung cancer: progress in diagnosis, staging and therapy. Respirology. 15:44–50. 2010. View Article : Google Scholar : PubMed/NCBI
4	Yamazaki R, Nishiyama Y, Furuta T, et al: Novel acrylonitrile derivatives, YHO-13177 and YHO-13351, reverse BCRP/ABCG2-mediated drug resistance in vitro and in vivo. Mol Cancer Ther. 10:1252–1263. 2011. View Article : Google Scholar : PubMed/NCBI
5	Kim DH, Sriharsha L, Xu W, et al: Clinical relevance of a pharmacogenetic approach using multiple candidate genes to predict response and resistance to imatinib therapy in chronic myeloid leukemia. Clin Cancer Res. 15:4750–4758. 2009. View Article : Google Scholar
6	Doyle LA and Ross DD: Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene. 22:7340–7358. 2003. View Article : Google Scholar : PubMed/NCBI
7	Robey RW, Medina-Pérez WY, Nishiyama K, et al: Over-expression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells. Clin Cancer Res. 7:145–152. 2001.PubMed/NCBI
8	Candeil L, Gourdier I, Peyron D, et al: ABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan-treated metastases. Int J Cancer. 109:848–854. 2004. View Article : Google Scholar : PubMed/NCBI
9	Diestra JE, Scheffer GL, Catala I, et al: Frequent expression of the multi-drug resistance-associated protein BCRP/MXR/ABCP/ABCG2 in human tumours detected by the BXP-21 monoclonal antibody in paraffin-embedded material. J Pathol. 198:213–219. 2002. View Article : Google Scholar
10	Turne JG, Gump JL, Zhang C, et al: ABCG2 expression, function and promoter methylation in human multiple myeloma. Blood. 108:3881–3889. 2006. View Article : Google Scholar : PubMed/NCBI
11	Yamasaki M, Makino T, Masuzawa T, et al: Role of multidrug resistance protein 2 (MRP2) in chemoresistance and clinical outcome in oesophageal squamous cell carcinoma. Br J Cancer. 104:707–713. 2011. View Article : Google Scholar : PubMed/NCBI
12	Chen ZS and Tiwari AK: Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J. 278:3226–3245. 2011. View Article : Google Scholar : PubMed/NCBI
13	Spanswick VJ, Lowe HL, Newton C, et al: Evidence for different mechanisms of ‘unhooking’ for melphalan and cisplatin-induced DNA interstrand cross-links in vitro and in clinical acquired resistant tumour samples. BMC Cancer. 12:4362012.
14	Gaudio E, Spizzo R, Paduano F, et al: Tcl1 interacts with ATM and enhances NF-κB activation in hematologic malignancies. Blood. 119:180–187. 2012.PubMed/NCBI
15	Svirnovski AI, Serhiyenka TF, Kustanovich AM, Khlebko PV, Fedosenko VV, Taras IB and Bakun AV: DNA-PK, ATM and MDR proteins inhibitors in overcoming fludarabine resistance in CLL cells. Exp Oncol. 32:258–262. 2010.PubMed/NCBI
16	Bae JB, Mukhopadhyay SS, Liu L, et al: Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links. Oncogene. 27:5045–5056. 2008. View Article : Google Scholar : PubMed/NCBI
17	Bakkenist CJ and Kastan MB: DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421:499–506. 2003. View Article : Google Scholar : PubMed/NCBI
18	Karin M and Greten FR: NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 5:749–759. 2005. View Article : Google Scholar : PubMed/NCBI
19	Lin Y, Bai L, Chen W and Xu S: The NF-kappaB activation pathways, emerging molecular targets for cancer prevention and therapy. Expert Opin Ther Targets. 14:45–55. 2010. View Article : Google Scholar : PubMed/NCBI
20	Campbell KJ, O’Shea JM and Perkins ND: Differential regulation of NF-kappaB activation and function by topoisomerase II inhibitors. BMC Cancer. 6:1012006. View Article : Google Scholar : PubMed/NCBI
21	Melisi D and Chiao PJ: NF-kappa B as a target for cancer therapy. Expert Opin Ther Targets. 11:133–144. 2007. View Article : Google Scholar : PubMed/NCBI
22	Konstantinopoulos PA, Fountzilas E, Pillay K, et al: Carboplatin-induced gene expression changes in vitro are prognostic of survival in epithelial ovarian cancer. BMC Med Genomics. 1:592008. View Article : Google Scholar : PubMed/NCBI
23	Wu ZH, Shi Y, Tibbetts RS and Miyamoto S: Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli. Science. 311:1141–1146. 2006. View Article : Google Scholar : PubMed/NCBI
24	Hu SX, Sui HX, Jin HJ, et al: Lipopolysaccharide and dose of nicotine determine the effects of nicotine on murine bone marrow-derived dendritic cells. Mol Med Rep. 5:1005–1010. 2012.PubMed/NCBI
25	Zhang L and Yu H: Neuroprotective effects of salidroside against beta-amyloid-induced oxidative stress in SH-SY5Y human neuroblastoma cells. Neurochem Int. 57:547–555. 2010. View Article : Google Scholar
26	Buhrmann C, Mobasheri A, Busch F, Aldinger C, Stahlmann R, Montaseri A and Shakibaei M: Curcumin modulates nuclear factor kappaB (NF-kappaB)-mediated inflammation in human tenocytes in vitro: role of the phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem. 286:28556–28566. 2011. View Article : Google Scholar
27	Dioum EM, Osborne JK, Goetsch S, Russell J, Schneider JW and Cobb MH: A small molecule differentiation inducer increases insulin production by pancreatic β cells. Proc Natl Acad Sci USA. 108:20713–20718. 2011.PubMed/NCBI
28	Jin HJ, Li HT, Sui HX, Xue MQ, Wang YN, Wang JX and Gao FG: Nicotine stimulated bone marrow-derived dendritic cells could augment HBV specific CTL priming by activating PI3K-Akt pathway. Immunol Lett. 146:40–49. 2012. View Article : Google Scholar : PubMed/NCBI
29	Heo JI, Oh SJ, Kho, et al: ATM mediates interdependent activation of p53 and ERK through formation of a ternary complex with p-p53 and p-ERK in response to DNA damage. Mol Biol Rep. 39:8007–8014. 2012. View Article : Google Scholar : PubMed/NCBI
30	Ai L, Skehan RR, Saydi J, Lin T and Brown KD: Ataxia-telangiectasia, mutated (ATM)/nuclear factor κ light chain enhancer of activated B cells (NF-κB) signaling controls basal and DNA damage-induced transglutaminase 2 expression. J Biol Chem. 287:18330–18341. 2012.
31	Togashi H, Sasaki M, Frohman E, et al: Neuronal (type I) nitric oxide synthase regulates nuclear factor κB activity and immunologic (type II) nitric oxide synthase expression. Proc Natl Acad Sci USA. 94:2676–2680. 1997.
32	Tenopoulou M, Kurz T, Doulias PT, Galaris D and Brunk UT: Does the calcein-AM method assay the total cellular ‘labile iron pool’ or only a fraction of it? Biochem J. 403:261–266. 2007.
33	Zolner AE, Abdou I, Ye R, et al: Phosphorylation of polynucleotide kinase/phosphatase by DNA-dependent protein kinase and ataxia-telangiectasia mutated regulates its association with sites of DNA damage. Nucleic Acids Res. 39:9224–9237. 2011. View Article : Google Scholar
34	Alexande A, Cai SL, Kim J, et al: ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA. 107:4153–4158. 2010. View Article : Google Scholar : PubMed/NCBI
35	Korita PV, Wakai T, Shirai Y, et al: Multidrug resistance associated protein 2 determines the efficacy of cisplatin in patients with hepatocellular carcinoma. Oncol Rep. 23:965–972. 2010.PubMed/NCBI
36	Yasui K, Mihara S, Zhao C, et al: Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res. 64:1403–1410. 2004. View Article : Google Scholar : PubMed/NCBI
37	Cho S, Lu M, He X, Ee PL, Bhat U, Schneider E, Miele L and Beck WT: Notch1 regulates the expression of the multidrug resistance gene ABCC1/MRP1 in cultured cancer cells. Proc Natl Acad Sci USA. 108:20778–20783. 2011. View Article : Google Scholar : PubMed/NCBI
38	Bram EE, Stark M, Raz S and Assaraf YG: Chemotherapeutic drug-induced ABCG2 promoter demethylation as a novel mechanism of acquired multidrug resistance. Neoplasia. 11:1359–1370. 2009.PubMed/NCBI
39	Yang Y, Xia F, Hermance N, et al: A cytosolic ATM/NEMO/RIP1 complex recruits TAK1 to mediate the NF-kappaB and p38 mitogen-activated protein kinase (MAPK)/MAPK-activated protein 2 responses to DNA damage. Mol Cell Biol. 31:2774–2786. 2011. View Article : Google Scholar : PubMed/NCBI
40	Miyamoto S: Nuclear initiated NF-κB signaling: NEMO and ATM take center stage. Cell Res. 21:116–130. 2011.
41	Wu ZH and Miyamoto S: Induction of a pro-apoptotic ATM-NF-κB pathway and its repression by ATR in response to replication stress. EMBO J. 27:1963–1973. 2008.
42	Ling J, Kang Y, Zhao R, et al: Kras^G12D-induced IKK2/β/NF-ϰB activation by IL-1α and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell. 21:105–120. 2012.
43	Li F and Sethi G: Targeting transcription factor NF-κB to overcome chemoresistance and radioresistance in cancer therapy. Biochim Biophys Acta. 1805:167–180. 2010.