Induction of autophagy contributes to crizotinib resistance in ALK-positive lung cancer

Cancer Biology and Therapy

Volumn 15, Issue 5, 2014, Pages 570-577

  Ji, Cheng ^a,b   Zhang, Li ^a   Cheng, Yan ^a   Patel, Raj ^a   Wu, Hao ^a   Zhang, Yi ^a   Wang, Mian ^a   Ji, Shundong ^a   Belani, Chandra P ^a   Yang, Jin Ming ^a   Ren, Xingcong ^a  

^a PENN STATE CANCER INSTITUTE   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

ALK; Autophagy; Crizotinib; Drug resistance; Lung cancer

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; CHLOROQUINE; CRIZOTINIB; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; ANTINEOPLASTIC AGENT; MTOR PROTEIN, HUMAN; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER INHIBITION; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; LUNG CANCER CELL LINE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL LINE, TUMOR; CHLOROQUINE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICE, NUDE; PYRAZOLES; PYRIDINES; RECEPTOR PROTEIN-TYROSINE KINASES; TOR SERINE-THREONINE KINASES;

EID: 84899887245     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.28162     Document Type: Article

References (23)

1. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, Ou SH, Dezube BJ, Jänne PA, Costa DB, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010; 363:1693-703; PMID:20979469; http://dx.doi.org/10.1056/NEJMoa1006448
2. Ou SH, Bazhenova L, Camidge DR, Solomon BJ, Herman J, Kain T, Bang YJ, Kwak EL, Shaw AT, Salgia R, et al. Rapid and dramatic radiographic and clinical response to an ALK inhibitor (crizotinib, PF02341066) in an ALK translocation-positive patient with non-small cell lung cancer. J Thorac Oncol 2010; 5:2044-6; PMID:21102269; http://dx.doi.org/10.1097/JTO.0b013e318200f9ff
3. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, Shapiro GI, Costa DB, Ou SH, Butaney M, et al. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol 2011; 12:1004-12; PMID:21933749; http://dx.doi.org/10.1016/S1470-2045(11)70232-7
4. Shaw AT, Engelman JA. ALK in lung cancer: past, present, and future. J Clin Oncol 2013; 31:1105-11; PMID:23401436; http://dx.doi.org/10.1200/JCO.2012. 44.5353
5. Katayama R, Shaw AT, Khan TM, Mino-Kenudson M, Solomon BJ, Halmos B, Jessop NA, Wain JC, Yeo AT, Benes C, et al. Mechanisms of acquired crizotinib resistance in ALK-rearranged lung Cancers. Sci Transl Med 2012; 4:20ra17; PMID:22277784; http://dx.doi.org/10.1126/scitranslmed.3003316
6. Choi YL, Soda M, Yamashita Y, Ueno T, Takashima J, Nakajima T, Yatabe Y, Takeuchi K, Hamada T, Haruta H, et al.; ALK Lung Cancer Study Group. EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors. N Engl J Med 2010; 363:1734-9; PMID:20979473; http://dx.doi.org/10.1056/NEJMoa1007478
7. Sasaki T, Koivunen J, Ogino A, Yanagita M, Nikiforow S, Zheng W, Lathan C, Marcoux JP, Du J, Okuda K, et al. A novel ALK secondary mutation and EGFR signaling cause resistance to ALK kinase inhibitors. Cancer Res 2011; 71:6051-60; PMID:21791641; http://dx.doi.org/10.1158/0008-5472.CAN-11-1340
8. Tanizaki J, Okamoto I, Okabe T, Sakai K, Tanaka K, Hayashi H, Kaneda H, Takezawa K, Kuwata K, Yamaguchi H, et al. Activation of HER family signaling as a mechanism of acquired resistance to ALK inhibitors in EML4-ALK-positive non-small cell lung cancer. Clin Cancer Res 2012; 18:6219-26; PMID:22843788; http://dx.doi.org/10.1158/1078-0432.CCR-12-0392
9. Doebele RC, Pilling AB, Aisner DL, Kutateladze TG, Le AT, Weickhardt AJ, Kondo KL, Linderman DJ, Heasley LE, Franklin WA, et al. Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer. Clin Cancer Res 2012; 18:1472-82; PMID:22235099; http://dx.doi.org/10.1158/1078- 0432.CCR-11-2906
10. Katayama R, Khan TM, Benes C, Lifshits E, Ebi H, Rivera VM, Shakespeare WC, Iafrate AJ, Engelman JA, Shaw AT. Therapeutic strategies to overcome crizotinib resistance in non-small cell lung cancers harboring the fusion oncogene EML4- ALK. Proc Natl Acad Sci U S A 2011; 108:7535-40; PMID:21502504; http://dx.doi.org/10.1073/pnas.1019559108
11. Yamada T, Takeuchi S, Nakade J, Kita K, Nakagawa T, Nanjo S, Nakamura T, Matsumoto K, Soda M, Mano H, et al. Paracrine receptor activation by microenvironment triggers bypass survival signals and ALK inhibitor resistance in EML4-ALK lung cancer cells. Clin Cancer Res 2012; 18:3592-602; PMID:22553343; http://dx.doi.org/10.1158/1078-0432.CCR-11-2972
12. Sang J, Acquaviva J, Friedland JC, Smith DL, Sequeira M, Zhang C, Jiang Q, Xue L, Lovly CM, Jimenez JP, et al. Targeted inhibition of the molecular chaperone Hsp90 overcomes ALK inhibitor resistance in non-small cell lung cancer. Cancer Discov 2013; 3:430-43; PMID:23533265; http://dx.doi.org/10.1158/ 2159-8290.CD-12-0440
13. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, Choi HG, Kim J, Chiang D, Thomas R, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res 2008; 14:4275-83; PMID:18594010; http://dx.doi.org/10.1158/1078-0432.CCR-08-0168
14. Takezawa K, Okamoto I, Nishio K, Jänne PA, Nakagawa K. Role of ERK-BIM and STAT3-survivin signaling pathways in ALK inhibitor-induced apoptosis in EML4-ALK-positive lung cancer. Clin Cancer Res 2011; 17:2140-8; PMID:21415216; http://dx.doi.org/10.1158/1078-0432.CCR-10-2798
15. McDermott U, Iafrate AJ, Gray NS, Shioda T, Classon M, Maheswaran S, Zhou W, Choi HG, Smith SL, Dowell L, et al. Genomic alterations of anaplastic lymphoma kinase may sensitize tumors to anaplastic lymphoma kinase inhibitors. Cancer Res 2008; 68:3389-95; PMID:18451166; http://dx.doi.org/10.1158/0008-5472. CAN-07-6186
16. Marzec M, Kasprzycka M, Liu X, El-Salem M, Halasa K, Raghunath PN, Bucki R, Wlodarski P, Wasik MA. Oncogenic tyrosine kinase NPM/ALK induces activation of the rapamycin-sensitive mTOR signaling pathway. Oncogene 2007; 26:5606-14; PMID:17353907; http://dx.doi.org/10.1038/sj.onc.1210346 (Pubitemid 47267838)
17. Hallberg B, Palmer RH. Mechanistic insight into ALK receptor tyrosine kinase in human cancer biology. Nat Rev Cancer 2013; 13:685-700; PMID:24060861; http://dx.doi.org/10.1038/nrc3580
18. Janku F, McConkey DJ, Hong DS, Kurzrock R. Autophagy as a target for anticancer therapy. Nat Rev Clin Oncol 2011; 8:528-39; PMID:21587219; http://dx.doi.org/10.1038/nrclinonc.2011.71
19. Cheng Y, Qiu F, Tashiro S, Onodera S, Ikejima T. ERK and JNK mediate TNFalpha-induced p53 activation in apoptotic and autophagic L929 cell death. Biochem Biophys Res Commun 2008; 376:483-8; PMID:18796294; http://dx.doi.org/10. 1016/j.bbrc.2008.09.018
20. Cagnol S, Chambard JC. ERK and cell death: mechanisms of ERK-induced cell death-apoptosis, autophagy and senescence. FEBS J 2010; 277:2-21; PMID:19843174; http://dx.doi.org/10.1111/j.1742-4658.2009.07366.x
21. Cheng Y, Ren X, Hait WN, Yang JM. Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol Rev 2013; 65:1162-97; PMID:23943849; http://dx.doi.org/10.1124/pr.112.007120
22. Shingu T, Fujiwara K, Bögler O, Akiyama Y, Moritake K, Shinojima N, Tamada Y, Yokoyama T, Kondo S. Inhibition of autophagy at a late stage enhances imatinib-induced cytotoxicity in human malignant glioma cells. Int J Cancer 2009; 124:1060-71; PMID:19048625; http://dx.doi.org/10.1002/ijc.24030
23. Degtyarev M, De Mazière A, Orr C, Lin J, Lee BB, Tien JY, Prior WW, van Dijk S, Wu H, Gray DC, et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 2008; 183:101-16; PMID:18838554; http://dx.doi.org/10.1083/jcb.200801099