Acetylation of histone H3 prevents resistance development caused by chronic mTOR inhibition in renal cell carcinoma cells

Cancer Letters

Volumn 324, Issue 1, 2012, Pages 83-90

  Juengel, Eva ^a   Dauselt, Anna ^a   Makarević, Jasmina ^a   Wiesner, Christoph ^a   Tsaur, Igor ^a   Bartsch, Georg ^a   Haferkamp, Axel ^a   Blaheta, Roman A ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

HDAC; Histone H3 acetylation; RAD001; Renal cell carcinoma; Resistance development

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA ACTIN; CYCLIN A; CYCLIN B; CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYTOKERATIN 18; EVEROLIMUS; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE H3; HISTONE H4; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE B; PROTEIN P19; PROTEIN P21; PROTEIN P27; S6 KINASE; SMALL INTERFERING RNA; UVOMORULIN; VALPROIC ACID; VIMENTIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL COUNT; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DEDIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG RESPONSE; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INACTIVATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RNA INTERFERENCE;

ACETYLATION; APOPTOSIS; CARCINOMA, RENAL CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; KIDNEY NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIROLIMUS; TOR SERINE-THREONINE KINASES; VALPROIC ACID;

EID: 84864034290     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.05.003     Document Type: Article

References (33)

1. Porta C., Osanto S., Ravaud A., Climent M.A., Vaishampayan U., White D.A., Creel P., Dickow B., Fischer P., Gornell S.S., Meloni F., Motzer R.J. Management of adverse events associated with the use of everolimus in patients with advanced renal cell carcinoma. Eur. J. Cancer 2011, 47:1287-1298.
2. Coppin C., Kollmannsberger C., Le L., Porzsolt F., Wilt T.J. Targeted therapy for advanced renal cell cancer (RCC): a Cochrane systematic review of published randomised trials. BJU Int. 2011, 108:1556-1563.
3. Hudes G., Carducci M., Tomczak P., Dutcher J., Figlin R., Kapoor A., Staroslawska E., Sosman J., McDermott D., Bodrogi I., Kovacevic Z., Lesovoy V., Schmidt-Wolf I.G., Barbarash O., Gokmen E., O'Toole T., Lustgarten S., Moore L., Motzer R.J. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. New Engl. J. Med. 2007, 356:2271-2281.
4. Motzer R.J., Escudier B., Oudard S., Hutson T.E., Porta C., Bracarda S., Grünwald V., Thompson J.A., Figlin R.A., Hollaender N., Kay A., Ravaud A. Phase 3 trial of everolimus for metastatic renal cell carcinoma: final results and analysis of prognostic factors. Cancer 2010, 116:4256-4265.
5. Milella M., Felici A. Biology of metastatic renal cell carcinoma. J. Cancer 2011, 2:369-373.
6. de Jong E., Winkel P., Poelstra K., Prakash J. Anticancer effects of 15d-prostaglandin-J2 in wild-type and doxorubicin-resistant ovarian cancer cells: novel actions on SIRT1 and HDAC. PLoS ONE 2011, 6:e25192.
7. Stronach E.A., Alfraidi A., Rama N., Datler C., Studd J.B., Agarwal R., Guney T.G., Gourley C., Hennessy B.T., Mills G.B., Mai A., Brown R., Dina R., Gabra H. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res. 2011, 71:4412-4422.
8. Juengel E., Engler J., Natsheh I., Jones J., Mickuckyte A., Hudak L., Jonas D., Blaheta R.A. Combining the receptor tyrosine kinase inhibitor AEE788 and the mammalian target of rapamycin (mTOR) inhibitor RAD001 strongly inhibits adhesion and growth of renal cell carcinoma cells. BMC Cancer 2009, 9:161.
9. Jones J., Juengel E., Mickuckyte A., Hudak L., Wedel S., Jonas D., Blaheta R.A. The histone deacetylase inhibitor valproic acid alters growth properties of renal cell carcinoma in vitro and in vivo. J. Cell Mol. Med. 2009, 13:2376-2385.
10. Phung T.L., Ziv K., Dabydeen D., Eyiah-Mensah G., Riveros M., Perruzzi C., Sun J., Monahan-Earley R.A., Shiojima I., Nagy J.A., Lin M.I., Walsh K., Dvorak A.M., Briscoe D.M., Neeman M., Sessa W.C., Dvorak H.F., Benjamin L.E. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 2006, 10:159-170.
11. Stoeltzing O., Meric-Bernstam F., Ellis L.M. Intracellular signaling in tumor and endothelial cells: The expected and, yet again, the unexpected. Cancer Cell 2006, 10:89-91.
12. Nagaprashantha L.D., Vatsyayan R., Singhal J., Lelsani P., Prokai L., Awasthi S., Singhal S.S. 2'-hydroxyflavanone inhibits proliferation, tumor vascularization and promotes normal differentiation in VHL-mutant renal cell carcinoma. Carcinogenesis 2011, 32:568-575.
13. Tsaur I., Makarević J., Hudak L., Juengel E., Kurosch M., Wiesner C., Bartsch G., Harder S., Haferkamp A., Blaheta R.A. The cdk1-cyclin B complex is involved in everolimus triggered resistance in the PC3 prostate cancer cell line. Cancer Lett. 2011, 313:84-90.
14. Doberstein K., Wieland A., Lee S.B., Blaheta R.A., Wedel S., Moch H., Schraml P., Pfeilschifter J., Kristiansen G., Gutwein P. L1-CAM expression in ccRCC correlates with shorter patients survival times and confers chemoresistance in renal cell carcinoma cells. Carcinogenesis 2011, 32:262-270.
15. Cho D.C., Cohen M.B., Panka D.J., Collins M., Ghebremichael M., Atkins M.B., Signoretti S., Mier J.W. The efficacy of the novel dual PI3-kinase/mTOR inhibitor NVP-BEZ235 compared with rapamycin in renal cell carcinoma. Clin. Cancer Res. 2010, 16:3628-3638.
16. Wysocki P.J. MTOR in renal cell cancer: modulator of tumor biology and therapeutic target. Expert Rev. Mol. Diagn. 2009, 9:231-241.
17. Le Tourneau C., Faivre S., Serova M., Raymond E. MTORC1 inhibitors: is temsirolimus in renal cancer telling us how they really work. Br. J. Cancer 2008, 99:1197-1203.
18. Kuo S.H., Hsu C.H., Chen L.T., Lu Y.S., Lin C.H., Yeh P.Y., Jeng H.J., Gao M., Yeh K.H., Cheng A.L. Lack of compensatory pAKT activation and eIF4E phosphorylation of lymphoma cells towards mTOR inhibitor, RAD001. Eur. J. Cancer 2011, 47:1244-1257.
19. Johnson N., Bentley J., Wang L.Z., Newell D.R., Robson C.N., Shapiro G.I., Curtin N.J. Pre-clinical evaluation of cyclin-dependent kinase 2 and 1 inhibition in anti-estrogen-sensitive and resistant breast cancer cells. Br. J. Cancer 2010, 102:342-350.
20. Dean J.L., Thangavel C., McClendon A.K., Reed C.A., Knudsen E.S. Therapeutic CDK4/6 inhibition in breast cancer: key mechanisms of response and failure. Oncogene 2010, 29:4018-4032.
21. Araki K., Shimura T., Suzuki H., Tsutsumi S., Wada W., Yajima T., Kobayahi T., Kubo N., Kuwano H. E/N-cadherin switch mediates cancer progression via TGF-β-induced epithelial-to-mesenchymal transition in extrahepatic cholangiocarcinoma. Br. J. Cancer 2011, 105:1885-1893.
22. Novellino L., De Filippo A., Deho P., Perrone F., Pilotti S., Parmiani G., Castelli C. PTPRK negatively regulates transcriptional activity of wild type and mutated oncogenic beta-catenin and affects membrane distribution of beta-catenin/E-cadherin complexes in cancer cells. Cell. Signal. 2008, 20:872-883.
23. Salahshor S., Naidoo R., Serra S., Shih W., Tsao M.S., Chetty R., Woodgett J.R. Frequent accumulation of nuclear E-cadherin and alterations in the Wnt signaling pathway in esophageal squamous cell carcinomas. Mod. Pathol. 2008, 21:271-281.
24. Gervais M.L., Henry P.C., Saravanan A., Burry T.N., Gallie B.L., Jewett M.A., Hill R.P., Evans A.J., Ohh M. Nuclear E-cadherin and VHL immunoreactivity are prognostic indicators of clear-cell renal cell carcinoma. Lab. Invest. 2007, 87:1252-1264.
25. Russell R.C., Ohh M. The role of VHL in the regulation of E-cadherin: a new connection in an old pathway. Cell Cycle 2007, 6:56-59.
26. Sun S.Y., Rosenberg L.M., Wang X., Zhou Z., Yue P., Fu H., Khuri F.R. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res. 2005, 65:7052-7058.
27. O'Reilly K.E., Rojo F., She Q.B., Solit D., Mills G.B., Smith D., Lane H., Hofmann F., Hicklin D.J., Ludwig D.L., Baselga J., Rosen N. MTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 2006, 66:1500-1508.
28. Nishioka C., Ikezoe T., Yang J., Koeffler H.P., Yokoyama A. Blockade of mTOR signaling potentiates the ability of histone deacetylase inhibitor to induce growth arrest and differentiation of acute myelogenous leukemia cells. Leukemia 2008, 22:2159-2168.
29. Martowicz M.L., Meyer M.B., Pike J.W. The mouse RANKL gene locus is defined by a broad pattern of histone H4 acetylation and regulated through distinct distal enhancers. J. Cell. Biochem. 2011, 112:2030-2045.
30. Blais M., Désilets A., Asselin C. Synergy between deacetylase inhibitors and IL-1beta in activation of the serum amyloid A2 gene promoter. DNA Cell Biol. 2005, 24:209-217.
31. Kim N.H., Kim S.N., Kim Y.K. Involvement of HDAC1 in E-cadherin expression in prostate cancer cells; its implication for cell motility and invasion. Biochem. Biophys. Res. Commun. 2011, 404:915-921.
32. El-Khoury V., Breuzard G., Fourré N., Dufer J. The histone deacetylase inhibitor trichostatin A downregulates human MDR1 (ABCB1) gene expression by a transcription-dependent mechanism in a drug-resistant small cell lung carcinoma cell line model. Br. J. Cancer 2007, 97:562-573.
33. Suh Y.A., Lee H.Y., Virmani A., Wong J., Mann K.K., Miller W.H., Gazdar A., Kurie J.M. Loss of retinoic acid receptor beta gene expression is linked to aberrant histone H3 acetylation in lung cancer cell lines. Cancer Res. 2002, 62:3945-3949.