Resistance to selumetinib (AZD6244) in colorectal cancer cell lines is mediated by p70s6K and RPS6 activation

Neoplasia (United States)

Volumn 16, Issue 10, 2014, Pages 845-860

  Grasso, Silvina ^a   Tristante, Elena ^b   Saceda, Miguel ^a,c   Carbonell, Pablo ^b   Mayor López, Leticia ^b   Carballo Santana, Mar ^b   Carrasco García, Estefanía ^a,d   Rocamora Reverte, Lourdes ^a,e   García Morales, Pilar ^a,c   Carballo, Fernando ^b   Ferragut, José A ^a   Martínez Lacaci, Isabel ^a,b  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

^c HOSPITAL GENERAL UNIVERSITARIO DE ELCHE   (Spain)

^d BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^e INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84934282290     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.08.011     Document Type: Article

References (42)

1. ObrandDI and Gordon PH (1997). Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum 40, 15-24.
2. Wagner AD, Arnold D, Grothey AA, Haerting J, and Unverzagt S (2009). Antiangiogenic therapies for metastatic colorectal cancer. Cochrane Database Syst Rev 3, 1-78 (CD005392).
3. Downward J (2003). Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3, 11-22.
4. Lievre A, Rouleau E, Buecher B, and Mitry E (2010). Clinical significance of BRAF mutations in colorectal cancer. Bull Cancer 97, 1441-1452.
5. Arrington AK, Heinrich EL, Lee W, Duldulao M, Patel S, Sanchez J, Garcia-Aguilar J, and Kim J (2012). Prognostic and predictive roles of KRAS mutation in colorectal cancer. Int J Mol Sci 13, 12153-12168.
6. Peyssonnaux C and Eychene A (2001). The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell 93, 53-62.
7. Hoshino R, Chatani Y, Yamori T, Tsuruo T, Oka H, Yoshida O, Shimada Y, Ari-i S, Wada H, and Fujimoto J, et al (1999). Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene 18, 813-822.
8. Ohren JF, Chen H, Pavlovsky A, Whitehead C, Zhang E, Kuffa P, Yan C, McConnell P, Spessard C, and Banotai C, et al (2004). Structures of human MAP kinase kinase 1 (MEK1) and MEK2 describe novel noncompetitive kinase inhibition. Nat Struct Mol Biol 11, 1192-1197.
9. Matallanas D, Birtwistle M, Romano D, Zebisch A, Rauch J, and von KA Kolch W (2011). Raf family kinases: old dogs have learned new tricks. GenesCancer 2, 232-260.
10. Niault TS and Baccarini M (2010). Targets of Raf in tumorigenesis. Carcinogenesis 31, 1165-1174.
11. Catalanotti F, Solit DB, Pulitzer MP, Berger MF, Scott SN, Iyriboz T, Lacouture ME, Panageas KS, Wolchok JD, and Carvajal RD, et al (2013). Phase II trial of MEK inhibitor selumetinib (AZD6244, ARRY-142886) in patients with BRAFV600E/K-mutated melanoma. Clin Cancer Res 19, 2257-2264.
12. Kirkwood JM, Bastholt L, Robert C, Sosman J, Larkin J, Hersey P, MiddletonM, Cantarini M, Zazulina V, and Kemsley K, et al (2012). Phase II, open-label, randomized trial of the MEK1/2 inhibitor selumetinib as monotherapy versus temozolomide in patients with advanced melanoma. Clin Cancer Res 18, 555-567.
13. Yeh TC, Marsh V, Bernat BA, Ballard J, Colwell H, Evans RJ, Parry J, Smith D, Brandhuber BJ, and Gross S, et al (2007). Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogen-activated protein kinase kinase 1/2 inhibitor. Clin Cancer Res 13, 1576-1583.
14. Davies BR, Logie A,McKay JS, Martin P, Steele S, Jenkins R, Cockerill M,Cartlidge S, and Smith PD (2007). AZD6244 (ARRY-142886), a potent inhibitor of mitogenactivated protein kinase/extracellular signal-regulated kinase kinase 1/2 kinases: mechanism of action in vivo, pharmacokinetic/pharmacodynamic relationship, and potential for combination in preclinical models. Mol Cancer Ther 6, 2209-2219.
15. Carbonell P, Turpin MC, Torres-Moreno D, Molina-Martinez I, Garcia-Solano J, Perez-Guillermo M, and Conesa-Zamora P (2011). Comparison of allelic discrimination by dHPLC, HRM, and TaqMan in the detection of BRAF mutation V600E. J Mol Diagn 13, 467-473.
16. Garcia-Solano J, Conesa-Zamora P, Carbonell P, Trujillo-Santos J, Torres-Moreno DD, Pagan-Gomez I, Rodriguez-Braun E, and Perez-Guillermo M (2012). Colorectal serrated adenocarcinoma shows a different profile of oncogene mutations, MSI status and DNA repair protein expression compared to conventional and sporadic MSI-H carcinomas. Int J Cancer 131, 1790-1799.
17. Berenbaum MC (1981). Criteria for analyzing interactions between biologically active agents. Adv Cancer Res 35, 269-335.
18. Buck E, Eyzaguirre A, Brown E, Petti F, McCormack S, Haley JD, Iwata KK, Gibson NW, and Griffin G (2006). Rapamycin synergizes with the epidermal growth factor receptor inhibitor erlotinib in non-small-cell lung, pancreatic, colon, and breast tumors. Mol Cancer Ther 5, 2676-2684.
19. Huang KT, Chen YH, and Walker AM (2004). Inaccuracies in MTS assays: major distorting effects of medium, serum albumin, and fatty acids. Biotechniques 37, 406-412.
20. Davies CC, Mason J, Wakelam MJ, Young LS, and Eliopoulos AG (2004). Inhibition of phosphatidylinositol 3-kinase- and ERK MAPK-regulated protein synthesis reveals the pro-apoptotic properties of CD40 ligation in carcinoma cells. J Biol Chem 279, 1010-1019.
21. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, and Blenis J (2007). RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282, 14056-14064.
22. Baumann P, Mandl-Weber S, Oduncu F, and Schmidmaier R (2009). The novel orally bioavailable inhibitor of phosphoinositol-3-kinase and mammalian target of rapamycin, NVP-BEZ235, inhibits growth and proliferation in multiple myeloma. Exp Cell Res 315, 485-497.
23. Masuda M, Shimomura M, Kobayashi K, Kojima S, and Nakatsura T (2011). Growth inhibition by NVP-BEZ235, a dual PI3K/mTOR inhibitor, in hepatocellular carcinoma cell lines. Oncol Rep 26, 1273-1279.
24. Leung E, KimJE, RewcastleGW, Finlay GJ, and Baguley BC (2011). Comparison of the effects of the PI3K/mTOR inhibitors NVP-BEZ235 and GSK2126458 on tamoxifen-resistant breast cancer cells. Cancer Biol Ther 11, 938-946.
25. Pearce LR, Alton GR, Richter DT, Kath JC, Lingardo L, Chapman J, Hwang C, and Alessi DR (2010). Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem J 431, 245-255.
26. Farley J, Brady WE, Vathipadiekal V, Lankes HA, Coleman R, Morgan MA, Mannel R, Yamada SD, Mutch D, and Rodgers WH, et al (2013). Selumetinib in women with recurrent low-grade serous carcinoma of the ovary or peritoneum: an open-label, single-arm, phase 2 study. Lancet Oncol 14, 134-140.
27. Patel SP, Lazar AJ, Papadopoulos NE, Liu P, Infante JR, Glass MR, Vaughn CS, LoRusso PM, Cohen RB, and Davies MA, et al (2013). Clinical responses to selumetinib (AZD6244; ARRY-142886)-based combination therapy stratified by gene mutations in patients with metastatic melanoma. Cancer 119, 799-805.
28. Troiani T, Vecchione L, Martinelli E, Capasso A, Costantino S, Ciuffreda LP, Morgillo F, Vitagliano D, D'Aiuto E, and De PR, et al (2012). Intrinsic resistance to selumetinib, a selective inhibitor of MEK1/2, by cAMP-dependent protein kinase A activation in human lung and colorectal cancer cells. Br J Cancer 106, 1648-1659.
29. Garon EB, Finn RS, Hosmer W, Dering J, Ginther C, Adhami S, Kamranpour N, Pitts S, Desai A, and Elashoff D, et al (2010). Identification of common predictive markers of in vitro response to the Mek inhibitor selumetinib (AZD6244; ARRY-142886) in human breast cancer and non-small cell lung cancer cell lines. Mol Cancer Ther 9, 1985-1994.
30. Yang JY, Chang CJ, XiaW,Wang Y, Wong KK, Engelman JA, Du Y, Andreeff M, Hortobagyi GN, and Hung MC (2010). Activation of FOXO3a is sufficient to reverse mitogen-activated protein/extracellular signal-regulated kinase kinase inhibitor chemoresistance in human cancer. Cancer Res 70, 4709-4718.
31. Adjei AA, Cohen RB, Franklin W, Morris C, Wilson D, Molina JR, Hanson LJ, Gore L, Chow L, and Leong S, et al (2008). 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 26, 2139-2146.
32. Solit DB, Garraway LA, Pratilas CA, Sawai A, Getz G, Basso A, Ye Q, Lobo JM, She Y, and Osman I, et al (2006). BRAF mutation predicts sensitivity to MEK inhibition. Nature 439, 358-362.
33. Corcoran RB, Rothenberg SM, Hata AN, Faber AC, Piris A, Nazarian RM, Brown RD, Godfrey JT, Winokur D, and Walsh J, et al (2013). TORC1 suppression predicts responsiveness to RAF and MEK inhibition in BRAFmutant melanoma. Sci Transl Med 5(196), 196ra98.
34. Sebolt-Leopold JS, Dudley DT, Herrera R, Van BK, Wiland A, Gowan RC, Tecle H, Barrett SD, Bridges A, and Przybranowski S, et al (1999). Blockade of theMAP kinase pathway suppresses growth of colon tumors in vivo. NatMed 5, 810-816.
35. Tentler JJ, Nallapareddy S,Tan AC, Spreafico A, Pitts TM,Morelli MP, Selby HM, Kachaeva MI, Flanigan SA, and Kulikowski GN, et al (2010). Identification of predictive markers of response to theMEK1/2 inhibitor selumetinib (AZD6244) in K-ras-mutated colorectal cancer. Mol Cancer Ther 9, 3351-3362.
36. Yeh JJ, Routh ED, Rubinas T, Peacock J, Martin TD, Shen XJ, Sandler RS, Kim HJ, Keku TO, and Der CJ (2009). KRAS/BRAF mutation status and ERK1/2 activation as biomarkers for MEK1/2 inhibitor therapy in colorectal cancer. Mol Cancer Ther 8, 834-843.
37. Balmanno K, Chell SD, Gillings AS, Hayat S, and Cook SJ (2009). Intrinsic resistance to the MEK1/2 inhibitor AZD6244 (ARRY-142886) is associated with weak ERK1/2 signalling and/or strong PI3K signalling in colorectal cancer cell lines. Int J Cancer 125, 2332-2341.
38. Little AS, Balmanno K, Sale MJ, Newman S, Dry JR, Hampson M, Edwards PA, Smith PD, and Cook SJ (2011). Amplification of the driving oncogene, KRAS or BRAF, underpins acquired resistance to MEK1/2 inhibitors in colorectal cancer cells. Sci Signal 4(166), ra17.
39. Meng J,X Peng H,Dai B, Guo W,Wang L, Ji L,Minna JD, ChrestaCM, Smith PD, and Fang B, et al (2009). High level of AKT activity is associated with resistance to MEK inhibitor AZD6244 (ARRY-142886). Cancer Biol Ther 8, 2073-2080.
40. Wee S, Jagani Z, Xiang KX, Loo A, Dorsch M, Yao YM, Sellers WR, Lengauer C, and Stegmeier F (2009). PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res 69, 4286-4293.
41. Samuels Y and Velculescu VE (2004). Oncogenic mutations of PIK3CA in human cancers. Cell Cycle 3, 1221-1224.
42. Zeiser R (2014). Trametinib. Recent Results Cancer Res 201, 241-248.