Targeting TBK1 inhibits migration and resistance to MEK inhibitors in mutant NRAS melanoma

Molecular Cancer Research

Volumn 12, Issue 10, 2014, Pages 1509-1519

  Vu, Ha Linh ^a   Aplin, Andrew E ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZ 13102909; BX 795; I KAPPA B KINASE; MITOGEN ACTIVATED PROTEIN KINASE; SELUMETINIB; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; BENZIMIDAZOLE DERIVATIVE; BX795; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NRAS PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PYRIMIDINE DERIVATIVE; TBK1 PROTEIN, HUMAN; THIOPHENE DERIVATIVE;

APOPTOSIS; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; MELANOMA; MELANOMA CELL LINE; ONCOGENE N RAS; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MOLECULARLY TARGETED THERAPY; MUTATION; PATHOLOGY; SKIN NEOPLASMS; TUMOR CELL LINE; TUMOR INVASION;

APOPTOSIS; BENZIMIDAZOLES; CELL LINE, TUMOR; CELL MOVEMENT; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; GTP PHOSPHOHYDROLASES; HUMANS; MELANOMA; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MOLECULAR TARGETED THERAPY; MUTATION; NEOPLASM INVASIVENESS; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINES; SKIN NEOPLASMS; THIOPHENES;

EID: 84907986134     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0204     Document Type: Article

References (46)

1. Howe HL, WuX, Ries LA, Cokkinides V, Ahmed F, Jemal A, et al. Annual report to the nation on the status of cancer, 1975-2003, featuring cancer among U.S. Hispanic/Latino populations. Cancer 2006;107:1711-42.
2. Miller AJ, Mihm MC Jr. Melanoma. N Engl J Med 2006;355:51-65.
3. Russo AE, Torrisi E, Bevelacqua Y, Perrotta R, Libra M, McCubrey JA, et al. Melanoma: molecular pathogenesis and emerging target therapies (Review). Int J Oncol 2009;34:1481-9.
4. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene 2003;22:3138-51.
5. Gray-Schopfer V, Wellbrock C, Marais R. Melanoma biology and new targeted therapy. Nature 2007;445:851-7.
6. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell 2012;150:251-63.
7. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010;468:973-7.
8. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
9. 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.
10. Kirkwood JM, Bastholt L, Robert C, Sosman J, Larkin J, Hersey P, et al. Phase II, open-label, randomized trial of the MEK1/2 inhibitor selumetinib as monotherapy versus temozolomide in patients with advanced melanoma. Clin Cancer Res 2012;18:555-67.
11. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 2003;3:11-22.
12. Mishra PJ, Ha L, Rieker J, Sviderskaya EV, Bennett DC, Oberst MD, et al. Dissection of RAS downstream pathways in melanomagenesis: a role for Ral in transformation. Oncogene 2010;29:2449-56.
13. Zipfel PA, Brady DC, Kashatus DF, Ancrile BD, Tyler DS, Counter CM. Ral activation promotes melanomagenesis. Oncogene 2010;29:4859-64.
14. Chien Y, Kim S, Bumeister R, Loo YM, Kwon SW, Johnson CL, et al. RalB GTPase-mediated activation of the IkappaB family kinase TBK1 couples innate immune signaling to tumor cell survival. Cell 2006;127:157-70.
15. Bodemann BO, White MA. Ral GTPases and cancer: linchpin support of the tumorigenic platform. Nat Rev Cancer 2008;8:133-40.
16. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009;462:108-12.
17. Ou YH, Torres M, Ram R, Formstecher E, Roland C, Cheng T, et al. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol Cell 2011;41:458-70.
18. Xie X, Zhang D, Zhao B, Lu MK, You M, Condorelli G, et al. IkappaB kinase epsilon and TANK-binding kinase 1 activate AKT by direct phosphorylation. Proc Natl Acad Sci U S A 2011;108:6474-9.
19. Kaplan FM, Kugel CH III, Dadpey N, Shao Y, Abel EV, Aplin AE. SHOC2 and CRAF mediate ERK1/2 reactivation in mutant NRAS-mediated resistance to RAF inhibitor. J Biol Chem 2012;287:41797-807.
20. Abel EV, Aplin AE. FOXD3 is a mutant B-RAF-regulated inhibitor of G (1)-S progression in melanoma cells. Cancer Res 2010;70:2891-900.
21. Lei CQ, Zhong B, Zhang Y, Zhang J, Wang S, Shu HB. Glycogen synthase kinase 3beta regulates IRF3 transcription factor-mediated antiviral response via activation of the kinase TBK1. Immunity 2010;33:878-89.
22. Verhelst K, Verstrepen L, Carpentier I, Beyaert R. IkappaB kinase epsilon (IKKepsilon): a therapeutic target in inflammation and cancer. Biochem Pharmacol 2013;85:873-80.
23. Woodman SE, Trent JC, Stemke-Hale K, Lazar AJ, Pricl S, Pavan GM, et al. Activity of dasatinib against L576P KIT mutant melanoma: molecular, cellular, and clinical correlates. Mol Cancer Ther 2009;8:2079-85.
24. Kishore N, Huynh QK, Mathialagan S, Hall T, Rouw S, Creely D, et al. IKK-i and TBK-1 are enzymatically distinct from the homologous enzyme IKK-2: comparative analysis of recombinant human IKK-i, TBK-1, and IKK-2. J Biol Chem 2002;277:13840-7.
25. Boutin JA. Myristoylation. Cell Signal 1997;9:15-35.
26. Schaller MD, Borgman CA, Parsons JT. Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 1993;13:785-91.
27. Hess AR, Postovit LM, Margaryan NV, Seftor EA, Schneider GB, Seftor RE, et al. Focal adhesion kinase promotes the aggressive melanoma phenotype. Cancer Res 2005;65:9851-60.
28. Smalley KS, Haass NK, Brafford PA, Lioni M, Flaherty KT, Herlyn M. Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases. Mol Cancer Ther 2006;5:1136-44.
29. Fallica B, Maffei JS, Villa S, Makin G, Zaman M. Alteration of cellular behavior and response to PI3K pathway inhibition by culture in 3D collagen gels. PLoS ONE 2012;7:e48024.
30. Feldman RI, Wu JM, Polokoff MA, Kochanny MJ, Dinter H, Zhu D, et al. Novel small molecule inhibitors of 3-phosphoinositide-dependent kinase-1. J Biol Chem 2005;280:19867-74.
31. Clark K, Plater L, Peggie M, Cohen P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J Biol Chem 2009;284:14136-46.
32. Shu C, Sankaran B, Chaton CT, Herr AB, Mishra A, Peng J, et al. Structural insights into the functions of TBK1 in innate antimicrobial immunity. Structure 2013;21:1137-48.
33. Wang T, Block MA, Cowen S, Davies AM, Devereaux E, Gingipalli L, et al. Discovery of azabenzimidazole derivatives as potent, selective inhibitors of TBK1/IKKepsilon kinases. Bioorg Med Chem Lett 2012;22:2063-9.
34. Fedorenko IV, Gibney GT, Smalley KS. NRAS mutant melanoma: biological behavior and future strategies for therapeutic management. Oncogene 2013;32:3009-18.
35. Yang KM, Jung Y, Lee JM, Kim W, Cho JK, Jeong J, et al. Loss of TBK1 induces epithelial-mesenchymal transition in the breast cancer cells by ERalphadownregulation. Cancer Res. 2013Nov 15. [Epubahead of print].
36. Kim JK, Jung Y, Wang J, Joseph J, Mishra A, Hill EE, et al. TBK1 regulates prostate cancer dormancy through mTOR inhibition. Neoplasia 2013;15:1064-74.
37. Stahl JM, Sharma A, Cheung M, Zimmerman M, Cheng JQ, Bosenberg MW, et al. Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res 2004;64:7002-10.
38. Zhu Z, Aref AR, Cohoon TJ, Barbie TU, Imamura Y, Yang S, et al. Inhibition of KRAS-driven tumorigenicity by interruption of an autocrine cytokine circuit. Cancer Discov 2014;4:452-65.
39. Czabanka M, Korherr C, Brinkmann U, Vajkoczy P. Influence of TBK-1 on tumor angiogenesis and microvascular inflammation. Front Biosci 2008;13:7243-9.
40. Stellzig J, Chariot A, Shostak K, Ismail Goktuna S, Renner F, Acker T, et al. Deregulated expression of TANK in glioblastomas triggers protumorigenic ERK1/2 and AKT signaling pathways. Oncogenesis 2013;2:e79.
41. Liu W, Huang YJ, Liu C, Yang YY, Liu H, Cui JG, et al. Inhibition of TBK1 attenuates radiation-induced epithelial-mesenchymal transition of A549 human lung cancer cells via activation of GSK-3beta and repression of ZEB1. Lab Invest 2014;94:362-70.
42. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science 2001;294:1708-12.
43. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 2003;163:583-95.
44. 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.
45. Scortegagna M, Ruller C, Feng Y, Lazova R, Kluger H, Li JL, et al. Genetic inactivation or pharmacological inhibition of Pdk1 delays development and inhibits metastasis of Braf::Pten melanoma. Oncogene. 2013 Sep 16. [Epub ahead of print].
46. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011;39:D945-50.