JNK signaling mediates epha2-Dependent tumor cell proliferation, motility, and cancer stem cell-Like properties in non-Small cell lung cancer

Cancer Research

Volumn 74, Issue 9, 2014, Pages 2444-2454

  Song, Wenqiang ^a,b   Ma, Yufang ^c   Wang, Jialiang ^c,d   Brantley Sieders, Dana ^b   Chen, Jin ^a,b,d,e,f  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Department of Medicine   (United States)

^c Departments of Neurological Surgery   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^e Cell and Developmental Biology   (United States)

^f VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; EPHA2 PROTEIN; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPHA2 GENE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR XENOGRAFT;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTHRACENES; CARCINOGENESIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, EPHA2; TUMOR BURDEN;

EID: 84900007107     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2136     Document Type: Article

References (43)

1. Brantley-Sieders DM. Clinical relevance of Ephs and ephrins in cancer: lessons from breast, colorectal, and lung cancer profiling. Semin Cell Dev Biol 2012;23:102-8.
2. Pasquale EB. Eph receptors and ephrins in cancer: bidirectional signaling and beyond. Nat Rev Cancer 2010;10:165-80.
3. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signaling. Nat Rev Mol Cell Biol 2002;3:475.
4. Pasquale EB. Developmental Cell Biology: Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 2005;6:462-75. (Pubitemid 40780558)
5. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008;133:38-52. (Pubitemid 351442996)
6. Larsen AB, PedersenMW,Stockhausen MT, Grandal MV, van Deurs B, Poulsen HS. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol Cancer Res 2007;5:283-93. (Pubitemid 46569779)
7. Brantley-Sieders DM, Zhuang G, Hicks D, Fang WB, Hwang Y, Cates JM, et al. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J Clin Invest 2008;118:64-78.
8. Kinch MS, Moore MB, Harpole DHJ. Predictive value of the EphA2 receptor tyrosine kinase in lung cancer recurrence and survival. Clin Cancer Res 2003;9:613-8. (Pubitemid 36182592)
9. Brannan JM, Dong W, Prudkin L, Behrens C, Lotan R, Bekele BN, et al. Expression of the receptor tyrosine kinase EphA2 is increased in smokers and predicts poor survival in non-small cell lung cancer. Clin Cancer Res 2009;15:4423-30.
10. Faoro L, Singleton PA, Cervantes GM, Lennon FE, Choong NW, Kanteti R, et al. EphA2 mutation in lung squamous cell carcinoma promotes increased cell survival, cell invasion, focal adhesions, and mTOR activation. J Biol Chem 2010;285:18575-85.
11. Brannan JM, Sen B, Saigal B, Prudkin L, Behrens C, Solis L, et al. EphA2 in the early pathogenesis and progression of non-small cell lung cancer. Cancer Prev Res 2009;2:1039-49.
12. Brantley DM, Cheng N, Thompson EJ, Lin Q, Brekken RA, Thorpe PE, et al. Soluble EphA receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 2002;21:7011-26. (Pubitemid 35252975)
13. Brantley-Sieders DM, Jiang A, Sarma K, Badu-Nkansah A, Walter DL, Shyr Y, et al. Eph/ephrin profiling in human breast cancer reveals significant associations between expression level and clinical outcome. PLoS ONE 2011;6:e24426.
14. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opi Cell Biol 2007;19:142-9. (Pubitemid 46386399)
15. Chen F. JNK-induced apoptosis, compensatory growth, and cancer stem cells. Cancer Res 2012;72:379-86.
16. Hess P, Pihan G, Sawyers CL, Flavell RA, Davis RJ. Survival signaling mediated by c-Jun NH(2)-terminal kinase in transformed B lymphoblasts. Nat Genet 2002;32:201-5. (Pubitemid 34977219)
17. Durbin AD, Somers GR, Forrester M, Pienkowska M, Hannigan GE, Malkin D. JNK1 determines the oncogenic or tumor-suppressiveactivity of the integrin-linked kinase in human rhabdomyosarcoma. J Clin Invest 2009;119:1558-70.
18. Khatlani TS, Wislez M, Sun M, Srinivas H, Iwanaga K, Ma L, et al. c-Jun N-terminal kinase is activated in non-small-cell lung cancer and promotes neoplastic transformation in human bronchial epithelial cells. Oncogene 2007;26:2658-66. (Pubitemid 46632007)
19. Nitta RT, Del Vecchio CA, Chu AH, Mitra SS, Godwin AK, Wong AJ. The role of the c-Jun N-terminal kinase 2-a-isoform in non-small cell lung carcinoma tumorigenesis. Oncogene 2011;30:234-44.
20. Lei K, Nimnual A, Zong WX, Kennedy NJ, Flavell RA, Thompson CB, et al. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol Cell Biol 2002;22:4929-42. (Pubitemid 34620425)
21. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer 2012;12:133-43.
22. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8:755-68.
23. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B, et al. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 2010;70: 9937-48.
24. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009;7:330-8.
25. Chen J. Regulation of tumor initiation and metastatic progression by Eph receptor tyrosine kinases. Adv Cancer Res 2012;114:1-20.
26. Miao H, Li DQ, Mukherjee A, Guo H, Petty A, Cutter J, et al. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 2009;16:9-20.
27. Miao H, Wei B-R, Peehl DM, Li Q, Alexandrou T, Schelling JR, et al.Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nature Cell Biol 2001;13:527-30. (Pubitemid 32422092)
28. Fujishita T, Aoki M, Taketo MM. JNK signaling promotes intestinaltumorigenesis through activation of mTOR complex 1 in Apc(D716) mice. Gastroenterology 2011;140:1556-63.
29. Marinissen MJ, Chiariello M, Tanos T, Bernard O, Narumiya S, Gutkind JS. The small GTP-binding protein RhoA regulates c-jun by a ROCKJNK signaling axis. Mol Cell 2004;14:29-41. (Pubitemid 38469907)
30. Coso OA, Chiariello M, Yu JC, Teramoto H, Crespo P, Xu N, et al. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995;81:1137-46.
31. Vaught D, Chen J, Brantley-Sieders DM. Regulation of mammary gland branching morphogenesis by EphA2 receptor tyrosine kinase. Mol Biol Cell 2009;20:2572-81.
32. Fang WB, Ireton RC, Zhuang G, Takahashi T, Reynolds A, Chen J. Overexpression of EPHA2 receptor destabilizes adherens junctions via a RhoA-dependent mechanism. J Cell Sci 2008;121: 358-68. (Pubitemid 351356707)
33. Parri M, Taddei ML, Bianchini F, Calorini L, Chiarugi P. EphA2 reexpression prompts invasion of melanoma cells shifting from mesenchymal to amoeboid-like motility style. Cancer Res 2009;69: 2072-81.
34. Fuchs SY, Dolan L, Davis RJ, Ronai Z. Phosphorylation-dependent targeting of c-Jun ubiquitination by Jun N-kinase. Oncogene 1996; 13:1531-5. (Pubitemid 26354201)
35. Nie D, Di Nardo A, Han JM, Baharanyi H, Kramvis I, Huynh T, et al.Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat Neurosci 2010;13:163-72.
36. Yang NY, Fernandez C, Richter M, Xiao Z, Valencia F, Tice DA, et al. Crosstalk of the EphA2 receptor with a serine/threonine phosphatase suppresses the Akt-mTORC1 pathway in cancer cells. Cell Signal 2011;23:201-12.
37. Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009;10:307-18.
38. Chen J, Nachebeh A, Scherer C, Ganju P, Reith A, Bronson R, et al. Germline inactivation of the murine Eck receptor tyrosine kinase byretroviral insertion. Oncogene 1996;12:979-88. (Pubitemid 26104440)
39. Orsulic S, Kemler R. Expression of Eph receptors and ephrins is differentially regulated by E-cadherin. J Cell Sci 2000;113 (Pt 10):1793-802. (Pubitemid 30333128)
40. Binda E, Visioli A, Giani F, Lamorte G, Copetti M, Pitter KL, et al. The EphA2 receptor drives self-renewal and tumorigenicity in stem-liketumor- propagating cells from human glioblastomas. Cancer Cell 2012; 22:765-80.
41. Zhang T, Inesta-Vaquera F, Niepel M, Zhang J, Ficarro SB, Machleidt T, et al. Discovery of potent and selective covalent inhibitors of JNK.Chem Biol 2012;19:140-54.
42. Wykosky J, Debinski W. The EphA2 receptor and ephrinA1 ligand insolid tumors: function and therapeutic targeting. Mol Cancer Res 2008;6:1795-806.
43. Noberini R, Lamberto I, Pasquale EB. Targeting Eph receptors with peptides and small molecules: progress and challenges. Semin CellDev Biol 2012;23:51-7.