STAT3 mediates resistance to MEK inhibitor through microRNA miR-17

Cancer Research

Volumn 71, Issue 10, 2011, Pages 3658-3668

  Dai, Bingbing ^a   Meng, Jieru ^a   Peyton, Michael ^b   Girard, Luc ^b   Bornmann, William G ^a   Ji, Lin ^a   Minna, John D ^b   Fang, Bingliang ^a   Roth, Jack A ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CUCURBITACIN; MICRORNA; MICRORNA 17; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; SELUMETINIB; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHEMOSENSITIVITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GROWTH INHIBITION; HUMAN; HUMAN CELL; INHIBITION KINETICS; LUNG NON SMALL CELL CANCER; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TUMOR VOLUME;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR;

EID: 79956105175     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3647     Document Type: Article

References (44)

1. Adjei AA, Cohen RB, Franklin W, Morris C, Wilson D, Molina JR, et al. Phase I pharmacokinetic and pharmacodynamic study of the oral, small-molecule mitogen-activated protein kinase kinase 1/2 inhibitor AZD6244 (ARRY-142886) in patients with advanced cancers. J Clin Oncol 2008;26:2139-46.
2. Rinehart J, Adjei AA, Lorusso PM, Waterhouse D, Hecht JR, Natale RB, et al. Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. J Clin Oncol 2004;22:4456-62. (Pubitemid 41185111)
3. Friday BB, Adjei AA. Advances in targeting the Ras/Raf/MEK/Erk mitogen-activated protein kinase cascade with MEK inhibitors for cancer therapy. Clin Cancer Res 2008;14:342-6. (Pubitemid 351226098)
4. Wang D, Boerner SA, Winkler JD, LoRusso PM. Clinical experience of MEK inhibitors in cancer therapy. Biochim Biophys Acta 2007;1773: 1248-55. (Pubitemid 47161034)
5. Pratilas CA, Taylor BS, Ye Q, Viale A, Sander C, Solit DB, et al. (V600E) BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci U S A 2009;106:4519-24.
6. Solit DB, Garraway LA, Pratilas CA, Sawai A, Getz G, Basso A, et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 2006;439:358-62. (Pubitemid 43128863)
7. Engelman JA, Chen L, Tan X, Crosby K, Guimaraes AR, Upadhyay R, et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008; 14:1351-6.
8. Pratilas CA, Hanrahan AJ, Halilovic E, Persaud Y, Soh J, Chitale D, et al. Genetic predictors of MEK dependence in non-small cell lung cancer. Cancer Res 2008;68:9375-83.
9. Sos ML, Fischer S, Ullrich R, Peifer M, Heuckmann JM, Koker M, et al. Identifying genotype-dependent efficacy of single and combined PI3K- and MAPK-pathway inhibition in cancer. Proc Natl Acad Sci U S A 2009;106:18351-6.
10. Emery CM, Vijayendran KG, Zipser MC, Sawyer AM, Niu L, Kim JJ, et al. MEK1 mutations confer resistance to MEK and B-RAF inhibition. Proc Natl Acad Sci U S A 2009;106:20411-6.
11. Wee S, Jagani Z, Xiang KX, Loo A, Dorsch M, Yao YM, et al. PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res 2009;69:4286-93.
12. Wheeler DL, Dunn EF, Harari PM. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat Rev Clin Oncol 2010;7:493-507
13. Meng J, Peng H, Dai B, Guo W, Wang L, Ji L, et al. High level of AKT activity is associated with resistance to MEK inhibitor AZD6244 (ARRY-142886). Cancer Biol Ther 2009;8:2073-80.
14. Ginsberg M, Czeko E, Muller P, Ren Z, Chen X, Darnell JE Jr. Amino acid residues required for physical and cooperative transcriptional interaction of STAT3 and AP-1 proteins c-Jun and c-Fos. Mol Cell Biol 2007;27:6300-8. (Pubitemid 47435738)
15. Konnikova L, Kotecki M, Kruger MM, Cochran BH. Knockdown of STAT3 expression by RNAi induces apoptosis in astrocytoma cells. BMC Cancer 2003;3:23.
16. Cai D, Shames DS, Raso MG, Xie Y, Kim YH, Pollack JR, et al. Steroid receptor coactivator-3 expression in lung cancer and its role in the regulation of cancer cell survival and proliferation. Cancer Res 2010;70:6477-85.
17. Guo W, Wu S, Liu J, Fang B. Identification of a small molecule with synthetic lethality for K-ras and protein kinase C iota. Cancer Res 2008;68:7403-8.
18. Meng J, Dai B, Fang B, Bekele BN, Bornmann WG, Sun D, et al. Combination treatment with MEK and AKT inhibitors is more effective than each drug alone in human non-small cell lung cancer in vitro and in vivo. PLoS One 2010;5:e14124.
19. Blaskovich MA, Sun J, Cantor A, Turkson J, Jove R, Sebti SM. Discovery of JSI-124 (cucurbitacin I), a selective Janus kinase/signal transducer and activator of transcription 3 signaling pathway inhibitor with potent antitumor activity against human and murine cancer cells in mice. Cancer Res 2003;63:1270-9. (Pubitemid 36348705)
20. Cragg MS, Jansen ES, Cook M, Harris C, Strasser A, Scott CL. Treatment of B-RAF mutant human tumor cells with a MEK inhibitor requires Bim and is enhanced by a BH3 mimetic. J Clin Invest 2008;118:3651-9.
21. Yang JY, Chang CJ, Xia W, Wang Y, Wong KK, Engelman JA, et al. Activation of FOXO3a is sufficient to reverse mitogen-activated protein/ extracellular signal-regulated kinase kinase inhibitor chemoresistance in human cancer. Cancer Res 2010;70:4709-18.
22. Meng J, Fang B, Liao Y, Chresta CM, Smith PD, Roth JA. Apoptosis induction by MEK inhibition in human lung cancer cells is mediated by Bim. PLoS One 2010;5:e13026.
23. Sunters A, Fernández de Mattos S, Stahl M, Brosens JJ, Zoumpoulidou G, Saunders CA, et al. FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 2003;278:49795-805. (Pubitemid 37548813)
24. Sheridan C, Brumatti G, Martin SJ. Oncogenic B-RafV600E inhibits apoptosis and promotes ERK-dependent inactivation of Bad and Bim. J Biol Chem 2008;283:22128-35.
25. Brock M, Trenkmann M, Gay RE, Michel BA, Gay S, Fischler M, et al. Interleukin-6 modulates the expression of the bone morphogenic protein receptor type II through a novel STAT3-microRNA cluster 17/92 pathway. Circ Res 2009;104:1184-91.
26. Dry JR, Pavey S, Pratilas CA, Harbron C, Runswick S, Hodgson D, et al. Transcriptional pathway signatures predict MEK addiction and response to selumetinib (AZD6244). Cancer Res 2010;70:2264-73.
27. Zhang Y, Turkson J, Carter-Su C, Smithgall T, Levitzki A, Kraker A, et al. Activation of Stat3 in v-Src-transformed fibroblasts requires cooperation of Jak1 kinase activity. J Biol Chem 2000;275:24935-44. (Pubitemid 30626601)
28. Giese B, Au-Yeung CK, Herrmann A, Diefenbach S, Haan C, Küster A, et al. Long term association of the cytokine receptor gp130 and the Janus kinase Jak1 revealed by FRAP analysis. J Biol Chem 2003; 278:39205-13. (Pubitemid 37221824)
29. Novotny-Diermayr V, Lin B, Gu L, Cao X. Modulation of the interleukin-6 receptor subunit glycoprotein 130 complex and its signaling by LMO4 interaction. J Biol Chem 2005;280:12747-57.
30. Yoon YK, Kim HP, Han SW, Oh do Y, Im SA, Bang YJ, et al. KRAS mutant lung cancer cells are differentially responsive to MEK inhibitor due to AKT or STAT3 activation: implication for combinatorial approach. Mol Carcinog 2010;49:353-62.
31. Darnell JE. Validating Stat3 in cancer therapy. Nat Med 2005;11: 595-6.
32. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009;9:798-809.
33. Wang YF, Jiang CC, Kiejda KA, Gillespie S, Zhang XD, Hersey P. Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin Cancer Res 2007;13:4934-42. (Pubitemid 47294802)
34. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 1999;96:857-68. (Pubitemid 29165088)
35. Obsil T, Obsilova V. Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene 2008;27:2263-75. (Pubitemid 351501778)
36. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, et al. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 2008;10:138-48. (Pubitemid 351194043)
37. O'Reilly LA, Kruse EA, Puthalakath H, Kelly PN, Kaufmann T, Huang DC, et al. MEK/ERK-mediated phosphorylation of Bim is required to ensure survival of T and B lymphocytes during mitogenic stimulation. J Immunol 2009;183:261-9.
38. Ewings KE, Wiggins CM, Cook SJ. Bim and the pro-survival Bcl-2 proteins: opposites attract, ERK repels. Cell Cycle 2007;6:2236-40. (Pubitemid 47547699)
39. Mu P, Han YC, Betel D, Yao E, Squatrito M, Ogrodowski P, et al. Genetic dissection of the miR-17-92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev 2009;23:2806-11.
40. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008;132:875-86. (Pubitemid 351312807)
41. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 2008;9:405-14. (Pubitemid 351405110)
42. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005;65:9628-32. (Pubitemid 41541436)
43. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL, et al. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2010;70: 5184-93.
44. Zhou M, Liu Z, Zhao Y, Ding Y, Liu H, Xi Y, et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem 2010;285:21496-507.