Niclosamide overcomes acquired resistance to erlotinib through suppression of STAT3 in non-small cell lung cancer

Molecular Cancer Therapeutics

Volumn 12, Issue 10, 2013, Pages 2200-2212

  Li, Rui ^a   Hu, Zhongliang ^a   Sun, Shi Yong ^a   Chen, Zhuo G ^a   Owonikoko, Taofeek K ^a   Sica, Gabriel L ^a   Ramalingam, Suresh S ^a   Curran, Walter J ^a   Khuri, Fadlo R ^a   Deng, Xingming ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ERLOTINIB; JANUS KINASE 2; MESSENGER RNA; NICLOSAMIDE; PHOSPHATASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN PTPMEG2; STAT3 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PATIENT; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENCY; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

APOPTOSIS; BCL-X PROTEIN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; NICLOSAMIDE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84885228492     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0095     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62: 10-29.
2. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin 2007;57: 43-66.
3. da Cunha Santos G, Shepherd FA, Tsao MS. EGFR mutations and lung cancer. Annu Rev Pathol 2011;6: 49-69.
4. Gridelli C, Maione P, Bareschino MA, Schettino C, Sacco PC, Ambrosio R, et al. Erlotinib in the treatment of non-small cell lung cancer: current status and future developments. Anticancer Res 2010;30: 1301-10.
5. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005;2:e73.
6. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, et al.EGFRmutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005;352: 786-92.
7. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011;3: 75ra26.
8. Yu HA, Arcila ME, Rekhtman N, Sima CS, Zakowski MF, Pao W, et al. Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancers. Clin Cancer Res 2013;19: 2240-7.
9. Arcila ME, Oxnard GR, Nafa K, Riely GJ, Solomon SB, Zakowski MF, et al. Rebiopsy of lung cancer patients with acquired resistance to EGFR inhibitors and enhanced detection of the T790M mutation using a locked nucleic acid-based assay. Clin Cancer Res 2011; 17: 1169-80.
10. Fan W, Tang Z, Yin L, Morrison B, Hafez-Khayyata S, Fu P, et al. METindependent lung cancer cells evading EGFR kinase inhibitors are therapeutically susceptible to BH3 mimetic agents. Cancer Res 2011; 71: 4494-505.
11. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, Savino R, et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999;10: 105-15.
12. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao YX, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;99: 295-303.
13. Alas S, Bonavida B. Rituximab inactivates signal transducer and activation of transcription 3 (STAT3) activity in B-non-Hodgkin's lymphoma through inhibition of the interleukin 10 autocrine/paracrine loop and results in down-regulation of Bcl-2 and sensitization to cytotoxic drugs. Cancer Res 2001;61: 5137-44.
14. Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, Bateman T, et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 2009;15: 91-102.
15. Lee H, Deng J, Kujawski M, Yang C, Liu Y, Herrmann A, et al. STAT3- induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat Med 2010;16: 1421-8.
16. Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Kloppel G, et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 2011;19: 456-69.
17. Gao SP, Mark KG, Leslie K, Pao W, Motoi N, Gerald WL, et al. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 2007;117: 3846-56.
18. Haura EB, Zheng Z, Song L, Cantor A, Bepler G. Activated epidermal growth factor receptor-Stat-3 signaling promotes tumor survival in vivo in non-small cell lung cancer. Clin Cancer Res 2005; 11: 8288-94.
19. Bharti AC, Donato N, Aggarwal BB. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J Immunol 2003;171: 3863-71.
20. Inghirami G, Chiarle R, Simmons WJ, Piva R, Schlessinger K, Levy DE. New and old functions of STAT3: a pivotal target for individualized treatment of cancer. Cell Cycle 2005;4: 1131-3.
21. Su F, Ren F, Rong Y, Wang Y, Geng Y, Feng M, et al. Protein tyrosine phosphatase Meg2 dephosphorylates signal transducer and activator of transcription 3 and suppresses tumor growth in breast cancer. Breast Cancer Res 2012;14:R38.
22. Ren XM, Duan L, HeQA, Zhang Z, Zhou Y,WuDH, et al. Identification of niclosamide as a new small-molecule inhibitor of the STAT3 signaling pathway. Acs Med Chem Lett 2010;1: 454-9.
23. Li Y, Fan S, Koo J, Yue P, Chen ZG, Owonikoko TK, et al. Elevated expression of eukaryotic translation initiation factor 4E is associated with proliferation, invasion and acquired resistance to erlotinib in lung cancer. Cancer Biol Ther 2012;13: 272-80.
24. Ito T, Deng X, Carr B, May WS. Bcl-2 phosphorylation required for antiapoptosis function. J Biol Chem 1997;272: 11671-3.
25. Huang S, Okumura K, Sinicrope FA. BH3 mimetic obatoclax enhances TRAIL-mediated apoptosis in human pancreatic cancer cells. Clin Cancer Res 2009;15: 150-9.
26. Sun SY, Yue P, Dawson MI, Shroot B, Michel S, Lamph WW, et al. Differential effects of synthetic nuclear retinoid receptor-selective retinoids on the growth of human non-small cell lung carcinoma cells. Cancer Res 1997;57: 4931-9.
27. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc 2006;1: 1112-6.
28. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, et al. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 2005;65: 7052-8.
29. Wang X, Yue P, Kim YA, Fu H, Khuri FR, Sun SY. Enhancing mammalian target of rapamycin (mTOR)-targeted cancer therapy by preventing mTOR/raptor inhibition-initiated, mTOR/rictor-independent Akt activation. Cancer Res 2008;68: 7409-18.
30. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005;435: 677-81.
31. Liu AW, Cai J, Zhao XL, Jiang TH, He TF, Fu HQ, et al. ShRNA-targeted MAP4K4 inhibits hepatocellular carcinoma growth. Clin Cancer Res 2011;17: 710-20.
32. Liu Y, Sun SY, Owonikoko TK, Sica GL, Curran WJ, Khuri FR, et al. Rapamycin induces Bad phosphorylation in association with its resistance to human lung cancer cells. Mol Cancer Ther 2012;11: 45-56.
33. Xing Y, Chaudry Q, Shen C, Kong KY, Zhau HE, Chung LW, et al. Bioconjugated quantum dots for multiplexed and quantitative immunohistochemistry. Nat Protoc 2007;2: 1152-65.
34. Xu J, Muller S, Nannapaneni S, Pan L, Wang Y, Peng X, et al. Comparison of quantum dot technology with conventional immunohistochemistry in examining aldehyde dehydrogenase 1A1 as a potential biomarker for lymph node metastasis of head and neck cancer. Eur J Cancer 2012;48: 1682-91.
35. Huang DH, Su L, Peng XH, Zhang H, Khuri FR, Shin DM, et al. Quantum dot-based quantification revealed differences in subcellular localization of EGFR and E-cadherin between EGFR-TKI sensitive and insensitive cancer cells. Nanotechnology 2009;20: 225102.
36. Wang X, Hawk N, Yue P, Kauh J, Ramalingam SS, Fu H, et al. Overcoming mTOR inhibition-induced paradoxical activation of survival signaling pathways enhances mTOR inhibitors' anticancer efficacy. Cancer Biol Ther 2008;7: 1952-8.
37. Gandhi J, Zhang J, Xie Y, Soh J, Shigematsu H, Zhang W, et al. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS ONE 2009;4:e4576.
38. Nguyen KS, Kobayashi S, Costa DB. Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancers dependent on the epidermal growth factor receptor pathway. Clin Lung Cancer 2009;10: 281-9.
39. Sack U, Walther W, Scudiero D, Selby M, Kobelt D, Lemm M, et al. Novel effect of antihelminthic Niclosamide on S100A4-mediated metastatic progression in colon cancer. J Natl Cancer Inst 2011;103: 1018-36.
40. Huang DH, Peng XH, Su L, Wang DS, Khuri FR, Shin DM, et al. Comparison and optimization of multiplexed quantum Dot-based immunohistofluorescence. Nano Res 2010;3: 61-8.
41. Engelman JA, Janne PA. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in nonsmall cell lung cancer. Clin Cancer Res 2008;14: 2895-9.
42. Yoshida T, Zhang G, Haura EB. Targeting epidermal growth factor receptor: central signaling kinase in lung cancer. Biochem Pharmacol 2010;80: 613-23.
43. Lateef M, Zargar SA, Khan AR, Nazir M, Shoukat A. Successful treatment of niclosamide- and praziquantel-resistant beef tapeworm infection with nitazoxanide. Int J Infect Dis 2008;12: 80-2.
44. Weinbach EC, Garbus J. Mechanism of action of reagents that uncouple oxidative phosphorylation. Nature 1969;221: 1016-8.
45. Merschjohann K, Steverding D. In vitro trypanocidal activity of the antihelminthic drug niclosamide. Exp Parasitol 2008;118: 637-40.
46. Jin Y, Lu Z, Ding K, Li J, Du X, Chen C, et al. Antineoplastic mechanisms of niclosamide in acute myelogenous leukemia stem cells: inactivation of the NF-kappaB pathway and generation of reactive oxygen species. Cancer Res 2010;70: 2516-27.
47. Smith AM, Gao X, Nie S. Quantum dot nanocrystals for in vivo molecular and cellular imaging. Photochem Photobiol 2004;80: 377-85.
48. Whaley SR, English DS, Hu EL, Barbara PF, Belcher AM. Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 2000;405: 665-8.
49. Luo G, Long J, Zhang B, Liu C, Ji S, Xu J, et al. Quantum dots in cancer therapy. Expert Opin Drug Deliv 2012;9: 47-58.