Comparing histone deacetylase inhibitor responses in genetically engineered mouse lung cancer models and a window of opportunity trial in patients with lung cancer

Molecular Cancer Therapeutics

Volumn 12, Issue 8, 2013, Pages 1545-1555

  Ma, Tian ^a   Galimberti, Fabrizio ^a   Erkmen, Cherie P ^b   Memoli, Vincent ^c,e,f   Chinyengetere, Fadzai ^a   Sempere, Lorenzo ^d   Beumer, Jan H ^g,h   Anyang, Bean N ^g   Nugent, William ^b   Johnstone, David ^b   Tsongalis, Gregory J ^c   Kurie, Jonathan M ⁱ   Li, Hua ^a   Di Renzo, James ^a,e,f   Guo, Yongli ^a   Freemantle, Sarah J ^a   Dragnev, Konstantin H ^d,e,f   Dmitrovsky, Ethan ^a,d,e,f  

^a Departments of Pharmacology and Toxicology   (United States)

^b Departments of Surgery   (United States)

^c Departments of Pathology   (United States)

^d Departments of Medicine   (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

^f DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^g UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^h UNIVERSITY OF PITTSBURGH   (United States)

ⁱ UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN E; K RAS PROTEIN; PROTEIN P27; PROTEIN P53; VORINOSTAT;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PATIENT; CANCER SURGERY; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG BLOOD LEVEL; FEMALE; HISTONE ACETYLATION; HUMAN; HUMAN CELL; INFLAMMATION; LUNG CANCER; MALE; MOUSE; MULTIMODALITY CANCER THERAPY; NECROSIS; NONHUMAN; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; TREATMENT RESPONSE; TUMOR BIOPSY;

AGED; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D1; CYCLIN E; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LUNG NEOPLASMS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEOPLASM STAGING; ONCOGENE PROTEINS;

EID: 84882267461     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0933     Document Type: Article

References (48)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: The impact of eliminating socioeconomic and racial disparity on premature deaths. CA Cancer J Clin 2011;61:212-36.
2. Garcia M, Jemal A, Ward E, Center MM, Hao Y, Siegel RL, et al. Global cancer facts & figures 2007. Atlanta, GA: American Cancer Society, 2007.
3. Lonardo F, Rusch V, Langenfeld J, Dmitrovsky E, Klimstra DS. Overexpression of cyclins D1 and E is frequent in bronchial preneoplasia and precedes squamous cell carcinoma development. Cancer Res 1999;59:2470-6.
4. Ratschiller D, Heighway J, Gugger M, Kappeler A, Pirnia F, Schmid RA, et al. Cyclin D1 overexpression in bronchial epithelia of patients with lung cancer is associated with smoking and predicts survival. J Clin Oncol 2003;21:2085-93.
5. Betticher DC, Heighway J, Hasleton PS, Altermatt HJ, Ryder WD, Cerny T, et al. Prognostic significance of CCND1 (cyclin D1) overexpression in primary resected non-small-cell lung cancer. Br J Cancer 1996;73:294-300.
6. Fukuse T, Hirata T, Naiki H, Hitomi S, Wada H. Prognostic significance of cyclin E overexpression in resected non-small cell lung cancer. Cancer Res 2000;60:242-4.
7. Mishina T, Dosaka-Akita H, Hommura F, Nishi M, Kojima T, Ogura S, et al. Cyclin E expression, a potential prognostic marker for non-small cell lung cancers. Clin Cancer Res 2000;6:11-6.
8. Freemantle SJ, Liu X, Feng Q, Galimberti F, Blumen S, Sekula D, et al. Cyclin degradation for cancer therapy and chemoprevention. J Cell Biochem 2007;102:869-77.
9. Dragnev KH, Pitha-Rowe I, Ma Y, Petty WJ, Sekula D, Murphy B, et al. Specific chemopreventive agents trigger proteasomal degradation of G1 cyclins: Implications for combination therapy. Clin Cancer Res 2004;10:2570-7.
10. Papadimitrakopoulou VA, Izzo J, Mao L, Keck J, Hamilton D, Shin DM, et al. Cyclin D1 and p16 alterations in advanced premalignant lesions of the upper aerodigestive tract: Role in response to chemoprevention and cancer development. Clin Cancer Res 2001;7: 3127-34.
11. Boyle JO, Langenfeld J, Lonardo F, Sekula D, Reczek P, Rusch V, et al. Cyclin D1 proteolysis: A retinoid chemoprevention signal in normal, immortalized, and transformed human bronchial epithelial cells. J Natl Cancer Inst 1999;91:373-9.
12. Langenfeld J, Kiyokawa H, Sekula D, Boyle J, Dmitrovsky E. Posttranslational regulation of cyclin D1 by retinoic acid: A chemoprevention mechanism. Proc Natl Acad Sci USA 1997;94: 12070-4.
13. Petty WJ, Dragnev KH, Memoli VA, Ma Y, Desai NB, Biddle A, et al. Epidermal growth factor receptor tyrosine kinase inhibition represses cyclin D1 in aerodigestive tract cancers. Clin Cancer Res 2004;10: 7547-54.
14. Dragnev KH, Ma T, Cyrus J, Galimberti F, Memoli V, Busch A, et al. Bexarotene plus erlotinib suppress lung carcinogenesis independent of KRAS mutations in two clinical trials and transgenic models. Cancer Prev Res 2011;4:818-28.
15. Dragnev KH, Petty WJ, Shah SJ, Lewis LD, Black CC,Memoli V, et al. A proof-of-principle clinical trial of bexarotene in patients with non-small cell lung cancer. Clin Cancer Res 2007;13:1794-800.
16. Ma Y, Fiering S, Black C, Liu X, Yuan Z, Memoli VA, et al. Transgenic cyclin E triggers dysplasia and multiple pulmonary adenocarcinomas. Proc Natl Acad Sci USA 2007;104:4089-94.
17. Freemantle SJ, Dmitrovsky E. Cyclin E transgenic mice: Discovery tools for lung cancer biology, therapy and prevention. Cancer Prev Res 2010;3:1513-8.
18. Liu X, Sempere LF, Galimberti F, Freemantle SJ, Black C, Dragnev KH, et al. Uncovering growth-suppressive microRNAs in lung cancer. Clin Cancer Res 2009;15:1177-83.
19. Galimberti F, Thompson SL, Liu X, Li H, Memoli V, Green SR, et al. Targeting the cyclin E-Cdk-2 complex represses lung cancer growth by triggering anaphase catastrophe. Clin Cancer Res 2010;16:109-20.
20. Liu X, Sempere LF, Ouyang H, Memoli VA, Andrew AS, Luo Y, et al. MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest 2010;120:1298-309.
21. Galimberti F, Busch AM, Chinyengetere F, Ma T, Sekula D, Memoli V, et al. Response to smoothened inhibition in diverse epithelial cancers that lack smoothened or patched 1 mutations. Int J Oncol 2012;41: 1751-61.
22. Marks PA. Discovery and development of SAHA as an anti-cancer agent. Oncogene 2007;26:1351-6.
23. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: Molecular mechanisms of action. Oncogene 2007;26:5541-52.
24. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009;27:5459-68.
25. Schrump DS. Cytotoxicity mediated by histone deacetylase inhibitors in cancer cells: Mechanisms and potential clinical implications. Clin Cancer Res 2009;14:3947-57.
26. Senese S, Zaragoza K, Minardi S, Muradore I, Ronzoni S, Passafaro A, et al. Role for histone deacetylase 1 in human tumor cell proliferation. Mol Cell Biol 2007;27:4784-95.
27. Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, et al. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 1999;401:188-93.
28. Miyanaga P, Gemma A, Noro R, Kataoka K, Matsuda K, Nara M, et al. Antitumor activity of histone deacetylase inhibitors in non-small cell lung cancer cells: Development of a molecular predictive model. Mol Cancer Ther 2008;7:1923-30.
29. Traynor AM, Dubey S, Eickhoff JC, Kolesar JM, Schell K, Huie MS, et al. Vorinostat (NSC# 701852) in patients with relapsed non-small cell lung cancer: A Wisconsin Oncology Network phase II study. J Thorac Oncol 2009;4:522-6.
30. Vansteenkiste J, Van Cutsem E, Dumez H, Chen C, Ricker JL, Randolph SS, et al. Early phase II trial of oral vorinostat in relapsed or refractory breast, colorectal, or non-small cell lung cancer. Invest New Drugs 2008;26:483-8.
31. Ramalingam SS, Parise RA, Ramanathan RK, Lagattuta TF, Musguire LA, Stoller RG, et al. Phase I and pharmacokinetic study of vorinostat, a histone deacetylase inhibitor in combination with carboplatin and paclitaxel for advanced solid malignancies. Clin Cancer Res 2007;13:3605-10.
32. Ramalingam SS, Maitland ML, Frankel P, Argiris AE, Koczywas M, Gitlitz B, et al. Carboplatin and paclitaxel in combination with either vorinostat or placebo in first-line therapy of advanced non-small cell lung cancer. J Clin Oncol 2010;28:56-62.
33. Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, Goodall GJ, et al. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 2009;23:2140-51.
34. Wislez M, Spencer ML, Izzo JG, Juroske DM, Balhara K, Cody KK, et al. Inhibition of mammalian target of rapamycin reverses alveolar epithelial neoplasia induced by oncogenic k-ras. Cancer Res 2005;65: 3226-35.
35. Guo Y, Dolinko AV, Chinyengetere F, Stanton B, Bomberger JM, Demidenko E, et al. Blockade of the ubiquitin protease UBP43 destabilizes transcription factor PML/RARa and inhibits the growth of acute promyelocytic leukemia. Cancer Res 2010;70: 9875-85.
36. Clopper C, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 1934;26:404-13.
37. Parise RA, Holleran JL, Beumer JH, Ramalingam S, Egorin MJ. A liquid chromatography-electrospray ionization tandem mass spectrometric assay for quantitation of the histone deacetylase inhibitor, vorinostat (suberoylanilide hydroxamic acid, SAHA), and its metabolites in human serum. J Chromatogr B Analyt Technol Biomed Life Sci 2006;840: 108-15.
38. Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A, et al. Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered micro-RNA expression in solid tumors. Clin Cancer Res 2010;16: 4246-55.
39. Kelly WK, Richon VM, O'Connor O, Curley T, MacGregor-Curtelli B, Tong W, et al. Phase I clinical trial of histone deacetylase inhibitor: Suberoylanilide hydroxamic acid administered intravenously. Clin Cancer Res 2003;9:3578-88.
40. Komatsu N, Kawamata N, Takeuchi S, Yin D, Chien W, Miller CW, et al. SAHA, a HDAC inhibitor, has profound anti-growth activity against non-small cell lung cancer cells. Oncol Rep 2006;15:187-91.
41. Desai D, Das A, Cohen L, el-Bayoumy K, Amin S. Chemopreventive efficacy of suberoylanilide hydroxamic acid (SAHA) against 4-(methylnitrosamino)-1-(3- pyridyl)-1-butanone (NNK)-induced lung tumorigenesis in female A/J mice. Anticancer Res 2003;23:499-503.
42. Singh M, Murriel CL, Johnson L. Genetically engineered mouse models: Closing the gap between preclinical data and trial outcomes. Cancer Res 2012;72:2695-700.
43. Chen Z, Cheng K, Walton Z, Wang Y, Ebi H, Shimamura T, et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 2012;483:613-7.
44. Robey RW, Chakraborty AR, Basseville A, Luchencko V, Bahr J, Zhan A, et al. Histone deacetylase inhibitors: Emerging mechanisms of resistance. Mol Pharm 2011;6:2021-31.
45. Hauswald S, Duque-Afonso J, Wagner MM, Schertl FM, Lubbert M, Peschel C, et al. Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin Cancer Res 2009;15:3705-15.
46. Vrana J, Decker R, Johnson C, Wang Z, Jarvis W, Richon V, et al. Induction of apoptosis in U937 human leukemia cells by suberoylanilide hydroxamic acid (SAHA) proceeds through pathways that are regulated by Bcl-2/Bcl-XL, c-Jun, and p21CIP1, but independent of p53. Oncogene 1999;18:7016-25.
47. Yazbeck VY, Buglio D, Georgakis GV, Li Y, Iwado E, Romaguera JE, et al. Temsirolimus downregulates p21 without altering cyclin D1 expression and induces autophagy and synergizes with vorinostat in mantle cell lymphoma. Exp Hematol 2008;36:443-50.
48. Luchenko VL, Salcido CD, Zhang Y, Agama K, Komlodi-Pasztor E, Murphy RF, et al. Schedule-dependent synergy of histone deacetylase inhibitors with DNA damaging agents in small cell lung cancer. Cell Cycle 2011;10:3119-28.