The histone deacetylase inhibitor SAHA acts in synergism with fenretinide and doxorubicin to control growth of rhabdoid tumor cells

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Kerl, Kornelius ^a   Ries, David ^b   Unland, Rebecca ^a   Borchert, Christiane ^a   Moreno, Natalia ^b   Hasselblatt, Martin ^a   Jürgens, Heribert ^a   Kool, Marcel ^c   Görlich, Dennis ^b   Eveslage, Maria ^b   Jung, Manfred ^d   Meisterernst, Michael ^b   Frühwald, Michael ^a,e  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e KLINIKUM AUGSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; DOXORUBICIN; FENRETINIDE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITOR; LIPOCORTIN 5; M 344; MYC PROTEIN; PROPIDIUM IODIDE; RETINOBLASTOMA PROTEIN; RNA; TAMOXIFEN; TRICHOSTATIN A; UNCLASSIFIED DRUG; VORINOSTAT; ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE; HYDROXAMIC ACID;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL ASSAY; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL LINE; CELL PROLIFERATION; CHEMOSENSITIZATION; CONTROLLED STUDY; DRUG POTENTIATION; DRUG TARGETING; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RHABDOID TUMOR; STEM CELL; WESTERN BLOTTING; DNA MICROARRAY; DRUG EFFECTS; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; DOXORUBICIN; DRUG SYNERGISM; FENRETINIDE; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RHABDOID TUMOR;

EID: 84878818288     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-286     Document Type: Article

References (50)

1. Sakuma T, Uzawa K, Onda T, Shiiba M, Yokoe H, Shibahara T, Tanzawa H. Aberrant expression of histone deacetylase 6 in oral squamous cell carcinoma. Int J Oncol 2006, 29(1):117-124.
2. Wilson AJ, Byun DS, Popova N, Murray LB, L'Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006, 281(19):13548-13558. 10.1074/jbc.M510023200, 16533812.
3. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006, 6(1):38-51. 10.1038/nrc1779, 16397526.
4. Camphausen K, Cerna D, Scott T, Sproull M, Burgan WE, Cerra MA, Fine H, Tofilon PJ. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer 2005, 114(3):380-386. 10.1002/ijc.20774, 15578701.
5. Dowdy SC, Jiang S, Zhou XC, Hou X, Jin F, Podratz KC, Jiang SW. Histone deacetylase inhibitors and paclitaxel cause synergistic effects on apoptosis and microtubule stabilization in papillary serous endometrial cancer cells. Mol Cancer Ther 2006, 5(11):2767-2776. 10.1158/1535-7163.MCT-06-0209, 17121923.
6. Kim IA, Shin JH, Kim IH, Kim JH, Kim JS, Wu HG, Chie EK, Ha SW, Park CI, Kao GD. Histone deacetylase inhibitor-mediated radiosensitization of human cancer cells: class differences and the potential influence of p53. Clin Cancer Res 2006, 12(3 Pt 1):940-949.
7. Dokmanovic M, Marks PA. Prospects: histone deacetylase inhibitors. J Cell Biochem 2005, 96(2):293-304. 10.1002/jcb.20532, 16088937.
8. Rasheed WK, Johnstone RW, Prince HM. Histone deacetylase inhibitors in cancer therapy. Expert OpinInvestig Drugs 2007, 16(5):659-678.
9. Furchert SE, Lanvers-Kaminsky C, Juurgens H, Jung M, Loidl A, Fruhwald MC. Inhibitors of histone deacetylases as potential therapeutic tools for high-risk embryonal tumors of the nervous system of childhood. Int J Cancer 2007, 120(8):1787-1794. 10.1002/ijc.22401, 17230517.
10. Muhlisch J, Schwering A, Grotzer M, Vince GH, Roggendorf W, Hagemann C, Sorensen N, Rickert CH, Osada N, Jurgens H, et al. Epigenetic repression of RASSF1A but not CASP8 in supratentorial PNET (sPNET) and atypical teratoid/rhabdoid tumors (AT/RT) of childhood. Oncogene 2006, 25(7):1111-1117. 10.1038/sj.onc.1209137, 16186793.
11. Thiemann M, Oertel S, Ehemann V, Weichert W, Stenzinger A, Bischof M, Weber KJ, Perez RL, Haberkorn U, Kulozik AE, et al. In vivo efficacy of the histone deacetylase inhibitor suberoylanilidehydroxamic acid in combination with radiotherapy in a malignant rhabdoid tumor mouse model. RadiatOncol 2012, 7:52.
12. Biegel JA. Molecular genetics of atypical teratoid/rhabdoid tumor. Neurosurg Focus 2006, 20(1):E11.
13. Versteege I, Sevenet N, Lange J, Rousseau-Merck MF, Ambros P, Handgretinger R, Aurias A, Delattre O. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 1998, 394(6689):203-206. 10.1038/28212, 9671307.
14. Sultan I, Qaddoumi I, Rodriguez-Galindo C, Nassan AA, Ghandour K, Al-Hussaini M. Age, stage, and radiotherapy, but not primary tumor site, affects the outcome of patients with malignant rhabdoid tumors. Pediatr Blood Cancer 2010, 54(1):35-40. 10.1002/pbc.22285, 19798737.
15. Kieran MW, Roberts CW, Chi SN, Ligon KL, Rich BE, Macconaill LE, Garraway LA, Biegel JA. Absence of oncogenic canonical pathway mutations in aggressive pediatric rhabdoid tumors. Pediatr Blood Cancer 2012, 59(7):1155-1157. 10.1002/pbc.24315, 22997201.
16. Hasselblatt M, Isken S, Linge A, Eikmeier K, Jeibmann A, Oyen F, Nagel I, Richter J, Bartelheim K, Kordes U, et al. High-resolution genomic analysis suggests the absence of recurrent genomic alterations other than SMARCB1 aberrations in atypical teratoid/rhabdoid tumors. Genes Chromosomes Cancer 2013, 52(2):185-190. 10.1002/gcc.22018, 23074045.
17. Versteege I, Medjkane S, Rouillard D, Delattre O. A key role of the hSNF5/INI1 tumour suppressor in the control of the G1-S transition of the cell cycle. Oncogene 2002, 21(42):6403-6412. 10.1038/sj.onc.1205841, 12226744.
18. Tsikitis M, Zhang Z, Edelman W, Zagzag D, Kalpana GV. Genetic ablation of Cyclin D1 abrogates genesis of rhabdoid tumors resulting from Ini1 loss. ProcNatlAcadSci U S A 2005, 102(34):12129-12134.
19. Jagani Z, Mora-Blanco EL, Sansam CG, McKenna ES, Wilson B, Chen D, Klekota J, Tamayo P, Nguyen PT, Tolstorukov M, et al. Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway. Nat Med 2010, 16(12):1429-1433. 10.1038/nm.2251, 21076395.
20. Zhang ZK, Davies KP, Allen J, Zhu L, Pestell RG, Zagzag D, Kalpana GV. Cell cycle arrest and repression of cyclin D1 transcription by INI1/hSNF5. Mol Cell Biol 2002, 22(16):5975-5988. 10.1128/MCB.22.16.5975-5988.2002, 133966, 12138206.
21. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, Cho YJ, Koellhoffer EC, Pomeroy SL, Orkin SH, Roberts CW. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 2010, 18(4):316-328. 10.1016/j.ccr.2010.09.006, 2957473, 20951942.
22. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
23. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008, 40(5):499-507. 10.1038/ng.127, 2912221, 18443585.
24. Vernell R, Helin K, Muller H. Identification of target genes of the p16INK4A-pRB-E2F pathway. J Biol Chem 2003, 278(46):46124-46137. 10.1074/jbc.M304930200, 12923195.
25. Birks DK, Donson AM, Patel PR, Dunham C, Muscat A, Algar EM, Ashley DM, Kleinschmidt-Demasters BK, Vibhakar R, Handler MH, et al. High expression of BMP pathway genes distinguishes a subset of atypical teratoid/rhabdoid tumors associated with shorter survival. Neuro Oncol 2012, 13(12):1296-1307.
26. Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, Foster AC, Zlotnik A. Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 2006, 7(2):67-80. 10.1007/s10048-006-0032-6, 16572319.
27. Takami Y, Nishi R, Nakayama T. Histone H1 variants play individual roles in transcription regulation in the DT40 chicken B cell line. BiochemBiophys Res Commun 2000, 268(2):501-508.
28. Hezroni H, Sailaja BS, Meshorer E. Pluripotency-related, valproic acid (VPA)-induced genome-wide histone H3 lysine 9 (H3K9) acetylation patterns in embryonic stem cells. J Biol Chem 2011, 286(41):35977-35988. 10.1074/jbc.M111.266254, 3195619, 21849501.
29. Knipstein JA, Birks DK, Donson AM, Alimova I, Foreman NK, Vibhakar R. Histone deacetylase inhibition decreases proliferation and potentiates the effect of ionizing radiation in atypical teratoid/rhabdoid tumor cells. Neuro Oncol 2012, 14(2):175-183. 10.1093/neuonc/nor208, 3266389, 22156471.
30. Qiu L, Burgess A, Fairlie DP, Leonard H, Parsons PG, Gabrielli BG. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. MolBiol Cell 2000, 11(6):2069-2083.
31. Zain J, O'Connor OA. Targeting histone deacetyalses in the treatment of B- and T-cell malignancies. Invest New Drugs 2010, 28(Suppl 1):S58-S78. 3003796, 21132350.
32. Betz BL, Strobeck MW, Reisman DN, Knudsen ES, Weissman BE. Re-expression of hSNF5/INI1/BAF47 in pediatric tumor cells leads to G1 arrest associated with induction of p16ink4a and activation of RB. Oncogene 2002, 21(34):5193-5203. 10.1038/sj.onc.1205706, 12149641.
33. Alarcon-Vargas D, Zhang Z, Agarwal B, Challagulla K, Mani S, Kalpana GV. Targeting cyclin D1, a downstream effector of INI1/hSNF5, in rhabdoid tumors. Oncogene 2006, 25(5):722-734. 10.1038/sj.onc.1209112, 16302003.
34. Dragnev KH, Pitha-Rowe I, Ma Y, Petty WJ, Sekula D, Murphy B, Rendi M, Suh N, Desai NB, Sporn MB, et al. Specific chemopreventive agents trigger proteasomal degradation of G1 cyclins: implications for combination therapy. Clin Cancer Res 2004, 10(7):2570-2577. 10.1158/1078-0432.CCR-03-0271, 15073138.
35. Fleming AJ, Hukin J, Rassekh R, Fryer C, Kim J, Stemmer-Rachamimov A, Birks DK, Huang A, Yip S, Dunham C. Atypical TeratoidRhabdoid Tumors (ATRTs): The British Columbia's Children's Hospital's Experience, 1986-2006. Brain Pathol 2012, 22(5):625-635. 10.1111/j.1750-3639.2011.00561.x, 22188464.
36. Lee RS, Stewart C, Carter SL, Ambrogio L, Cibulskis K, Sougnez C, Lawrence MS, Auclair D, Mora J, Golub TR, et al. A remarkably simple genome underlies highly malignant pediatric rhabdoid cancers. J Clin Invest 2012, 122(8):2983-2988. 10.1172/JCI64400, 3408754, 22797305.
37. McKenna ES, Tamayo P, Cho YJ, Tillman EJ, Mora-Blanco EL, Sansam CG, Koellhoffer EC, Pomeroy SL, Roberts CW. Epigenetic inactivation of the tumor suppressor BIN1 drives proliferation of SNF5-deficient tumors. Cell Cycle 2012, 11(10):1956-1965. 10.4161/cc.20280, 3359122, 22544318.
38. Watanabe M, Adachi S, Matsubara H, Imai T, Yui Y, Mizushima Y, Hiraumi Y, Watanabe K, Kamitsuji Y, Toyokuni SY, et al. Induction of autophagy in malignant rhabdoid tumor cells by the histone deacetylase inhibitor FK228 through AIF translocation. Int J Cancer 2009, 124(1):55-67. 10.1002/ijc.23897, 18821579.
39. Algar EM, Muscat A, Dagar V, Rickert C, Chow CW, Biegel JA, Ekert PG, Saffery R, Craig J, Johnstone RW, et al. Imprinted CDKN1C is a tumor suppressor in rhabdoid tumor and activated by restoration of SMARCB1 and histone deacetylase inhibitors. PLoS One 2009, 4(2):e4482. 10.1371/journal.pone.0004482, 2637419, 19221586.
40. Paternot S, Bockstaele L, Bisteau X, Kooken H, Coulonval K, Roger PP. Rb inactivation in cell cycle and cancer: the puzzle of highly regulated activating phosphorylation of CDK4 versus constitutively active CDK-activating kinase. Cell Cycle 2010, 9(4):689-699. 10.4161/cc.9.4.10611, 20107323.
41. Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S, Bouffet E, Clifford SC, Hawkins CE, French P, et al. Medulloblastoma comprises four distinct molecular variants. J ClinOncol 2011, 29(11):1408-1414.
42. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, Holcomb T, Stinson J, Gould SE, Coleman B, et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N Engl J Med 2009, 361(12):1173-1178. 10.1056/NEJMoa0902903, 19726761.
43. Villablanca JG, London WB, Naranjo A, McGrady P, Ames MM, Reid JM, McGovern RM, Buhrow SA, Jackson H, Stranzinger E, et al. Phase II study of oral capsular 4-hydroxyphenylretinamide (4-HPR/fenretinide) in pediatric patients with refractory or recurrent neuroblastoma: a report from the Children's Oncology Group. Clin Cancer Res 2011, 17(21):6858-6866. 10.1158/1078-0432.CCR-11-0995, 3207022, 21908574.
44. Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 2007, 5(10):981-989. 10.1158/1541-7786.MCR-07-0324, 17951399.
45. Marks PA, Richon VM, Breslow R, Rifkind RA. Histone deacetylase inhibitors as new cancer drugs. CurrOpinOncol 2001, 13(6):477-483.
46. Garcia-Manero G, Tambaro FP, Bekele NB, Yang H, Ravandi F, Jabbour E, Borthakur G, Kadia TM, Konopleva MY, Faderl S, et al. Phase II trial of vorinostat with idarubicin and cytarabine for patients with newly diagnosed acute myelogenous leukemia or myelodysplastic syndrome. J ClinOncol 2012, 30(18):2204-2210.
47. Ramaswamy B, Fiskus W, Cohen B, Pellegrino C, Hershman DL, Chuang E, Luu T, Somlo G, Goetz M, Swaby R, et al. Phase I-II study of vorinostat plus paclitaxel and bevacizumab in metastatic breast cancer: evidence for vorinostat-induced tubulin acetylation and Hsp90 inhibition in vivo. Breast Cancer Res Treat 2012, 132(3):1063-1072. 10.1007/s10549-011-1928-x, 3486521, 22200869.
48. Walter RB, Medeiros BC, Powell BL, Schiffer CA, Appelbaum FR, Estey EH. Phase II trial of vorinostat and gemtuzumabozogamicin as induction and post-remission therapy in older adults with previously untreated acute myeloid leukemia. Haematologica 2012, 97(5):739-742. 10.3324/haematol.2011.055822, 3342977, 22133771.
49. Friday BB, Anderson SK, Buckner J, Yu C, Giannini C, Geoffroy F, Schwerkoske J, Mazurczak M, Gross H, Pajon E, et al. Phase II trial of vorinostat in combination with bortezomib in recurrent glioblastoma: a north central cancer treatment group study. Neuro Oncol 2012, 14(2):215-221. 10.1093/neuonc/nor198, 3266383, 22090453.
50. Fouladi M, Park JR, Stewart CF, Gilbertson RJ, Schaiquevich P, Sun J, Reid JM, Ames MM, Speights R, Ingle AM, et al. Pediatric phase I trial and pharmacokinetic study of vorinostat: a Children's Oncology Group phase I consortium report. J ClinOncol 2010, 28(22):3623-3629.