FoxO transcription factors promote AKT Ser473 phosphorylation and renal tumor growth in response to pharmacologic inhibition of the PI3K-AKT pathway

Cancer Research

Volumn 74, Issue 6, 2014, Pages 1682-1693

  Lin, Aifu ^a   Piao, Hai Long ^a   Zhuang, Li ^a   Sarbassov, Dos D ^a,b   Ma, Li ^a,b   Gan, Boyi ^a,b  

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

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DACTOLISIB; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RICTOR PROTEIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE ARREST; CONTROLLED STUDY; EMBRYO; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEEDBACK SYSTEM; FOXO GENE; FOXO L GENE; FOXO1 GENE; FOXO3 GENE; FOXO4 L GENE; GENE; GENE SILENCING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; KIDNEY TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, RENAL CELL; CARRIER PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; IMIDAZOLES; KIDNEY NEOPLASMS; MICE; MICE, NUDE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; QUINOLINES; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84896512807     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1729     Document Type: Article

References (40)

1. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002; 296:1655-7. (Pubitemid 34579158)
2. Laplante M, Sabatini DM. mTOR Signaling in Growth Control and Disease. Cell 2012;149:274-93.
3. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell 2007;129:1261-74. (Pubitemid 46962095)
4. Huang J, Manning BD. The TSC1-TSC2 complex: a molecular switchboard controlling cell growth. Biochem J 2008;412:179-90. (Pubitemid 351758225)
5. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 2005;24: 7410-25. (Pubitemid 41637981)
6. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004;117:421-6. (Pubitemid 38610228)
7. Zhang Y, Gan B, Liu D, Paik JH. FoxO family members in cancer. Cancer Biol Ther 2011;12:253-9.
8. Eijkelenboom A, Burgering BM. FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 2013;14: 83-97.
9. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004;304:554. (Pubitemid 38541907)
10. Cully M, You H, Levine AJ, Mak TW. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer 2006;6:184-92. (Pubitemid 43292562)
11. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 2003;4: 257-62. (Pubitemid 37329790)
12. Salmena L, Carracedo A, Pandolfi PP. Tenets of PTEN tumor suppression. Cell 2008;133:403-14. (Pubitemid 351622014)
13. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013;499: 43-9.
14. Linehan WM, Zbar B. Focus on kidney cancer. Cancer Cell 2004; 6:223-8. (Pubitemid 39222035)
15. Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet 2009;373:1119-32.
16. Robb VA, Karbowniczek M, Klein-Szanto AJ, Henske EP. Activation of the mTOR signaling pathway in renal clear cell carcinoma. J Urol 2007; 177:346-52. (Pubitemid 44879483)
17. Pantuck AJ, Seligson DB, Klatte T, Yu H, Leppert JT, Moore L, et al. Prognostic relevance of the mTOR pathway in renal cell carcinoma: implications for molecular patient selection for targeted therapy. Cancer 2007;109:2257-67. (Pubitemid 46801555)
18. Gan B, Lim C, Chu G, Hua S, Ding Z, Collins M, et al. FoxOs enforce a progression checkpoint to constrain mTORC1-Activated renal tumorigenesis. Cancer Cell 2010;18:472-84.
19. Atkins MB, Hidalgo M, Stadler WM, Logan TF, Dutcher JP, Hudes GR, et al. Randomized phase II study of multiple dose levels of CCI-779, a novel mammalian target of rapamycin kinase inhibitor, in patients with advanced refractory renal cell carcinoma. J Clin Oncol 2004;22: 909-18. (Pubitemid 41103603)
20. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A, et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007;356:2271-81. (Pubitemid 46849157)
21. Motzer RJ, Escudier B, Oudard S, Hutson TE, Porta C, Bracarda S, et al. Efficacy of everolimus in advanced renal cell carcinoma: a doubleblind, randomised, placebo-controlled phase III trial. Lancet 2008;372: 449-56.
22. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 2007;12:9-22. (Pubitemid 47001784)
23. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004;18:1926-45. (Pubitemid 39071573)
24. Um SH, D'Alessio D, Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 2006;3:393-402. (Pubitemid 43811780)
25. Bhaskar PT, Hay N. The two TORCs and Akt. Dev Cell 2007;12: 487-502. (Pubitemid 46523652)
26. Manning BD. Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol 2004;167:399-403. (Pubitemid 39489047)
27. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006;66:1500-8. (Pubitemid 43259931)
28. Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006;441:424-30. (Pubitemid 44050136)
29. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 2009;9:550-62.
30. Cho DC, Cohen MB, Panka DJ, Collins M, Ghebremichael M, Atkins MB, et al. The efficacy of the novel dual PI3-kinase/mTOR inhibitor NVP-BEZ235 compared with rapamycin in renal cell carcinoma. Clin Cancer Res 2010;16:3628-38.
31. Maira SM, Stauffer F, Brueggen J, Furet P, Schnell C, Fritsch C, et al. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther 2008;7:1851-63.
32. Carver BS, Chapinski C, Wongvipat J, Hieronymus H, Chen Y, Chandarlapaty S, et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 2011;19:575-86.
33. Serra V, Scaltriti M, Prudkin L, Eichhorn PJ, Ibrahim YH, Chandarlapaty S, et al. PI3K inhibition results in enhanced HER signaling and acquired ERK dependency in HER2-overexpressing breast cancer. Oncogene 2011;30:2547-57.
34. 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.
35. Serra V, Markman B, Scaltriti M, Eichhorn PJ, Valero V, Guzman M, et al. NVP-BEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Res 2008;68:8022-30.
36. Chandarlapaty S, Sawai A, Scaltriti M, Rodrik-Outmezguine V, Grbovic-Huezo O, Serra V, et al. AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 2011;19:58-71.
37. Muranen T, Selfors LM, Worster DT, Iwanicki MP, Song L, Morales FC, et al. Inhibition of PI3K/mTOR leads to adaptive resistance in matrixattached cancer cells. Cancer Cell 2012;21:227-39.
38. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-101. (Pubitemid 40262113)
39. Chen CC, Jeon SM, Bhaskar PT, Nogueira V, Sundararajan D, Tonic I, et al. FoxOs inhibit mTORC1 and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev Cell 2010;18:592-604.
40. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007;128:309-23. (Pubitemid 46123514)