The histone deacetylase inhibitor Suberoylanilide Hydroxamic Acid (SAHA) as a therapeutic agent in rhabdomyosarcoma

References

• Breitfeld PP, Meyer WH. Rhabdomyosarcoma: new windows of opportunity. Oncologist. 2005;10:518–527. doi: 10.1634/theoncologist.10-7-518.
   PubMedGoogle Scholar
• Huh WW, Skapek SX. Childhood rhabdomyosarcoma: new insight on biology and treatment. Curr Oncol Rep. 2010;12:402–410. doi: 10.1007/s11912-010-0130-3.
   Google Scholar
• Saab R, Spunt SL, Skapek SX. Myogenesis and rhabdomyosarcoma the Jekyll and Hyde of skeletal muscle. Curr Top Dev Biol. 2011;94:197–234. doi: 10.1016/b978-0-12-380916-2.00007-3.
   PubMedGoogle Scholar
• Tombolan L, Poli E, Martini P, Zin A, Millino C, Pacchioni B, Celegato B, Bisogno G, Romualdi C, Rosolen A. Global DNA methylation profiling uncovers distinct methylation patterns of protocadherin alpha4 in metastatic and non-metastatic rhabdomyosarcoma. BMC Cancer. 2016;16:886. doi:10.1186/s12885-016-2936-3.
   Google Scholar
• Ramaglia M, D'Angelo V, Iannotta A, Di Pinto D, Pota E, Affinita MC, Donofrio V, Errico ME, Lombardi A, Indolfi C. High EZH2 expression is correlated to metastatic disease in pediatric soft tissue sarcomas. Cancer Cell Int. 2016;16:59. doi:10.1186/s12935-016-0338-x.
   Google Scholar
• Vella S, Pomella S, Leoncini PP, Colletti M, Conti B, Marquez VE, Strillacci A, Roma J, Gallego S, Milano GM. MicroRNA-101 is repressed by EZH2 and its restoration inhibits tumorigenic features in embryonal rhabdomyosarcoma. Clin Epigenetics. 2015;7:82.doi:10.1186/s13148-015-0107-z.
   Google Scholar
• Böhm M, Wachtel M, Marques JG, Streiff N, Laubscher D, Nanni P, Mamchaoui K, Santoro R, Schäfer BW. Helicase CHD4 is an epigenetic coregulator of PAX3-FOXO1 in alveolar rhabdomyosarcoma. J Clin Invest. 2016;126:4237–4249. doi:10.1172/JCI85057.
   Google Scholar
• Mahoney SE, Yao Z, Keyes CC, Tapscott SJ, Diede SJ. Genome-wide DNA methylation studies suggest distinct DNA methylation patterns in pediatric embryonal and alveolar rhabdomyosarcomas. Epigenetics. 2012;7:400–408. doi: 10.4161/epi.19463.
   PubMedGoogle Scholar
• Sun X, Guo W, Shen JK, Mankin HJ, Hornicek FJ, Duan Z. Rhabdomyosarcoma: advances in Molecular and Cellular Biology. Sarcoma. 2015:232010. doi:10.1155/2015/232010.
   Google Scholar
• Seki M, Nishimura R, Yoshida K, Shimamura T, Shiraishi Y, Sato Y, Kato M, Chiba K, Tanaka H, Hoshino N. Integrated genetic and epigenetic analysis defines novel molecular subgroups in rhabdomyosarcoma. Nat Commun. 2015;6:7557. doi:10.1038/ncomms8557.
   Google Scholar
• Sun W, Chatterjee B, Wang Y, Stevenson HS, Edelman DC, Meltzer PS, Barr FG. Distinct methylation profiles characterize fusion-positive and fusion-negative rhabdomyosarcoma. Mod Pathol. 2015;28(9):1214–1224. doi:10.1038/modpathol.2015.82.
   Web of Science ®Google Scholar
• Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer. 2006;6(38–51). doi: 10.1038/nrc1779.
   PubMedGoogle Scholar
• Furchert SE, Lanvers-Kaminsky C, Juürgens H, Jung M, Loidl A, Frühwald 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. doi:10.1002/ijc.22401.
   Web of Science ®Google Scholar
• Dokmanovic M, Marks PA. Prospects: histone deacetylase inhibitors. J Cell Biochem. 2005;96:293–304. doi: 10.1002/jcb.20532.
   PubMedGoogle Scholar
• Rasheed WK, Johnstone RW, Prince HM. Histone deacetylase inhibitors in cancer therapy. Expert Opin Investig Drugs. 2007;16:659–678. doi: 10.1517/13543784.16.5.659.
   PubMedGoogle Scholar
• Morera L, Lübbert M, Jung M. Targeting histone methyltransferases and demethylases in clinical trials for cancer therapy. Clin Epigenetics. 2016;8:57. doi: 10.1186/s13148-016-0223-4.
   PubMedGoogle Scholar
• McCabe MT, Mohammad HP, Barbash O, Kruger RG. Targeting Histone Methylation in Cancer. Cancer J. 2017;23(292–301). doi: 10.1097/PPO.0000000000000283.
   PubMedGoogle Scholar
• Faleiro I, Leão R, Binnie A, de Mello RA, Maia AT, Castelo-Branco P. Epigenetic therapy in urologic cancers: an update on clinical trials. Oncotarget. 2017;8(7):12484–12500. doi:10.18632/oncotarget.14226.
   Google Scholar
• Damaskos C, Garmpis N, Valsami S, Kontos M, Spartalis E, Kalampokas T, Kalampokas E, Athanasiou A, Moris D, Daskalopoulou A. Histone Deacetylase Inhibitors: an Attractive Therapeutic Strategy Against Breast Cancer. Anticancer Res. 2017;37(1):35–46. doi:10.21873/anticanres.11286.
   Web of Science ®Google Scholar
• Tang F, Choy E, Tu C, Hornicek F, Duan Z. Therapeutic applications of histone deacetylase inhibitors in sarcoma. Cancer Treat Rev. 2017;59:33–45. doi: 10.1016/j.ctrv.2017.06.006.
   PubMedGoogle Scholar
• Bannister AJ, Miska EA. Regulation of gene expression by transcription factor acetylation. Cell Mol Life Sci. 57;2000:1184–1192.
   PubMed Web of Science ®Google Scholar
• Johnstone RW. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov. 2002;1:287–299. doi: 10.1038/nrd772.
   PubMedGoogle Scholar
• Galanis E, Jaeckle KA, Maurer MJ, Reid JM, Ames MM, Hardwick JS, Reilly JF, Loboda A, Nebozhyn M, Fantin VR. Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J Clinical Oncology: Official Journal Am Soc Clin Oncol. 2009;27(12):2052–2058. doi:10.1200/JCO.2008.19.0694.
   Google Scholar
• Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene. 2007;26:1351–1356. doi: 10.1038/sj.onc.1210204.
   Google Scholar
• Fakih MG, Fetterly G, Egorin MJ, Muindi JR, Espinoza-Delgado I, Zwiebel JA, Litwin A, Holleran JL, Wang K, Diasio RB. A phase I, pharmacokinetic, and pharmacodynamic study of two schedules of vorinostat in combination with 5-fluorouracil and leucovorin in patients with refractory solid tumors. Clin Cancer Res. 2010;16(14):3786-3794. doi:10.1158/1078-0432.CCR-10-0547.
   Web of Science ®Google Scholar
• Heinicke U, Fulda S. Chemosensitization of rhabdomyosarcoma cells by the histone deacetylase inhibitor SAHA. Cancer Lett. 2014;351:50–58. doi: 10.1016/j.canlet.2014.04.021.
   PubMedGoogle Scholar
• Vleeshouwer-Neumann T, Phelps M, Bammler TK, MacDonald JW, Jenkins I, Chen EY. Histone Deacetylase Inhibitors Antagonize Distinct Pathways to Suppress Tumorigenesis of Embryonal Rhabdomyosarcoma. PloS one. 2015;10(12):e0144320. doi:10.1371/journal.pone.0144320.
   Web of Science ®Google Scholar
• Hedrick E, Crose L, Linardic CM, Safe S. Histone Deacetylase Inhibitors Inhibit Rhabdomyosarcoma by Reactive Oxygen Species-Dependent Targeting of Specificity Protein Transcription Factors. Mol Cancer Ther. 2015;14:2143–2153. doi: 10.1158/1535-7163.MCT-15-0148.
   PubMedGoogle Scholar
• Kutko MC, Glick RD, Butler LM, Coffey DC, Rifkind RA, Marks PA, Richon VM, LaQuaglia MP. Histone deacetylase inhibitors induce growth suppression and cell death in human rhabdomyosarcoma in vitro. Clin Cancer Res. 2003;9(15):5749–5755
   Web of Science ®Google Scholar
• Hinson AR, Jones R, Crose LE, Belyea BC, Barr FG, Linardic CM. Human rhabdomyosarcoma cell lines for rhabdomyosarcoma research: utility and pitfalls. Front Oncol. 2013;3:(183. doi:10.3389/fonc.2013.00183.
   Google Scholar
• Ramalingam SS, Parise RA, Ramanathan RK, Ramananthan RK, Lagattuta TF, Musguire LA, Stoller RG, Potter DM, Argiris AE, Zwiebel JA. 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(12):3605–3610. doi:10.1158/1078-0432.CCR-07-0162.
   Web of Science ®Google Scholar
• Fujiwara Y, Yamamoto N, Yamada Y, Yamada K, Otsuki T, Kanazu S, Iwasa T, Hardwick JS, Tamura T. Phase I and pharmacokinetic study of vorinostat (suberoylanilide hydroxamic acid) in Japanese patients with solid tumors. Cancer Sci. 2009;100(9):1728–1734. doi:10.1111/j.1349-7006.2009.01237.x.
   Web of Science ®Google Scholar
• Muscal JA, Scorsone KA, Zhang L, Ecsedy JA, Berg SL. Additive effects of vorinostat and MLN8237 in pediatric leukemia, medulloblastoma, and neuroblastoma cell lines. Invest New Drugs. 2013;31:39–45. doi: 10.1007/s10637-012-9831-9.
   PubMedGoogle Scholar
• Hummel TR, Wagner L, Ahern C, Fouladi M, Reid JM, McGovern RM, Ames MM, Gilbertson RJ, Horton T, Ingle AM. A pediatric phase 1 trial of vorinostat and temozolomide in relapsed or refractory primary brain or spinal cord tumors: a Children’s Oncology Group phase 1 consortium study. Pediatric Blood & Cancer. 2013;60(9):1452–1457. doi:10.1002/pbc.24541.
   Web of Science ®Google Scholar
• Phelps MP, Bailey JN, Vleeshouwer-Neumann T, Chen EY. CRISPR screen identifies the NCOR/HDAC3 complex as a major suppressor of differentiation in rhabdomyosarcoma. Proc Natl Acad Sci U S A. 2016;113:15090–15095. doi: 10.1073/pnas.1610270114.
   Google Scholar
• Roos WP, Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Letters. 2013;332:237–248. doi: 10.1016/j.canlet.2012.01.007.
   PubMedGoogle Scholar
• Chun P. Histone deacetylase inhibitors in hematological malignancies and solid tumors. Arch Pharm Res. 2015;38:933–949. doi: 10.1007/s12272-015-0571-1.
   Google Scholar
• Ewald JA, Desotelle JA, Wilding G, Jarrard DF. Therapy-induced senescence in cancer. Journal of the National Cancer Institute. 2010;102:1536–1546. doi: 10.1093/jnci/djq364.
   PubMedGoogle Scholar
• Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995;92(20):9363–9367.
   Web of Science ®Google Scholar
• Freund A, Laberge RM, Demaria M, Lamin CJ. B1 loss is a senescence-associated biomarker. Mol Biol Cell. 2012;23:2066–2075. doi: 10.1091/mbc.E11-10-0884.
   PubMedGoogle Scholar
• Qian Y, Zhang J, Yan B, Chen X. DEC1, a basic helix-loop-helix transcription factor and a novel target gene of the p53 family, mediates p53-dependent premature senescence. J Biol Chem. 2008;283:2896–2905. doi: 10.1074/jbc.M708624200.
   Google Scholar
• Saab R. Cellular senescence: many roads, one final destination. Scientific World Journal. 2010;10:727–741. doi: 10.1100/tsw.2010.68.
   Google Scholar
• Lawlor ER, Thiele CJ. Epigenetic changes in pediatric solid tumors: promising new targets. Clin Cancer Res. 2012;18:2768–2779. doi: 10.1158/1078-0432.CCR-11-1921.
   PubMedGoogle Scholar
• Shern JF, Chen L, Chmielecki J, Wei JS, Patidar R, Rosenberg M, Ambrogio L, Auclair D, Wang J, Song, YK. Comprehensive genomic analysis of rhabdomyosarcoma reveals a landscape of alterations affecting a common genetic axis in fusion-positive and fusion-negative tumors. Cancer Discov. 2014;4(2):216–231. doi:10.1158/2159-8290.CD-13-0639.
   Web of Science ®Google Scholar
• Gryder BE, Yohe ME, Chou HC, Zhang X, Marques J, Wachtel M, Schaefer B, Sen N, Song YK, Gualtieri A. PAX3-FOXO1 Establishes Myogenic Super Enhancers and Confers BET Bromodomain Vulnerability. Cancer Discov. 2017. doi: 10.1158/2159-8290.CD-16-1297.
   Web of Science ®Google Scholar
• Zhu B, Davie JK. New insights into signalling-pathway alterations in rhabdomyosarcoma. Br J Cancer. 2015;112:227–231. doi: 10.1038/bjc.2014.471.
   Google Scholar
• De Los Santos M, Martínez-Iglesias O, Aranda A. Anti-estrogenic actions of histone deacetylase inhibitors in MCF-7 breast cancer cells. Endocr Relat Cancer. 2007;14:1021–1028. doi: 10.1677/ERC-07-0144.
   PubMedGoogle Scholar
• Hrzenjak A, Moinfar F, Kremser ML, Strohmeier B, Petru E, Zatloukal K, Denk H. Histone deacetylase inhibitor vorinostat suppresses the growth of uterine sarcomas in vitro and in vivo. Molecular Cancer. 2010;9:49. doi:10.1186/1476-4598-9-49.
   Google Scholar
• Keller C, Guttridge DC. Mechanisms of impaired differentiation in rhabdomyosarcoma. FEBS J. 2013;280:4323–4334. doi: 10.1111/febs.12421.
   PubMedGoogle Scholar
• Claus R, Lübbert M. Epigenetic targets in hematopoietic malignancies. Oncogene. 2003;22:6489–6496. doi: 10.1038/sj.onc.1206814.
   PubMedGoogle Scholar
• Fazi F, Travaglini L, Carotti D, Palitti F, Diverio D, Alcalay M, McNamara S, Miller WH, Lo Coco F, Pelicci PG. Retinoic acid targets DNA-methyltransferases and histone deacetylases during APL blast differentiation in vitro and in vivo. Oncogene. 2005;24(11):1820–1830. doi:10.1038/sj.onc.1208286.
   Web of Science ®Google Scholar
• Capobianco E, Mora A, La Sala D, Roberti A, Zaki N, Badidi E, Taranta M, Cinti C. Separate and combined effects of DNMT and HDAC inhibitors in treating human multi-drug resistant osteosarcoma HosDXR150 cell line. PloS one. 2014;9(4):e95596. doi:10.1371/journal.pone.0095596.
   Web of Science ®Google Scholar
• Megiorni F, Camero S, Ceccarelli S, McDowell HP, Mannarino O, Marampon F, Pizer B, Shukla R, Pizzuti A, Marchese C. DNMT3B in vitro knocking-down is able to reverse embryonal rhabdomyosarcoma cell phenotype through inhibition of proliferation and induction of myogenic differentiation. Oncotarget. 2016;7(48):79342–79356. doi:10.18632/oncotarget.12688.
   Google Scholar
• Li ZY, Yang J, Gao X, Lu JY, Zhang Y, Wang K, Cheng MB, Wu NH, Wu Z, Shen YF. Sequential recruitment of PCAF and BRG1 contributes to myogenin activation in 12-O-tetradecanoylphorbol-13-acetate-induced early differentiation of rhabdomyosarcoma-derived cells. J Biol Chem. 2007;282(26):18872–18878. doi:10.1074/jbc.M609448200.
   Web of Science ®Google Scholar
• Carrió E, Suelves M. DNA methylation dynamics in muscle development and disease. Front Aging Neurosci. 2015;7(19). doi: 10.3389/fnagi.2015.00019.
   PubMedGoogle Scholar
• Wolf S, Hagl B, Kappler R. Identification of BMP2 as an epigenetically silenced growth inhibitor in rhabdomyosarcoma. Int J Oncol. 2014;44:1727–1735. doi: 10.3892/ijo.2014.2312.
   PubMedGoogle Scholar
• Walters ZS, Villarejo-Balcells B, Olmos D, Buist TW, Missiaglia E, Allen R, Al-Lazikani B, Garrett MD, Blagg J, Shipley J. JARID2 is a direct target of the PAX3-FOXO1 fusion protein and inhibits myogenic differentiation of rhabdomyosarcoma cells. Oncogene. 2014;33(9):1148–1157. doi:10.1038/onc.2013.46.
   Web of Science ®Google Scholar
• Brinkmann H, Dahler AL, Popa C, Serewko MM, Parsons PG, Gabrielli BG, Burgess AJ, Saunders NA. Histone hyperacetylation induced by histone deacetylase inhibitors is not sufficient to cause growth inhibition in human dermal fibroblasts. J Biol Chem. 2001;276(25):22491–22499. doi:10.1074/jbc.M100206200.
   Web of Science ®Google Scholar
• Chen CS, Weng SC, Tseng PH, Lin HP. Histone acetylation-independent effect of histone deacetylase inhibitors on Akt through the reshuffling of protein phosphatase 1 complexes. J Biol Chem. 2005;280:38879–38887. doi: 10.1074/jbc.M505733200.
   Google Scholar
• Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science. 2001;293:1653–1657. doi: 10.1126/science.1062374.
   Google Scholar
• Li D, Marchenko ND, Moll UM. SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ. 2011;18:1904–1913. doi: 10.1038/cdd.2011.71.
   Google Scholar
• Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 2002;21(24):6820–6831.
   Web of Science ®Google Scholar
• Zalzali H, Harajly M, Abdul-Latif L, El-Chaar N, Dbaibo G, Skapek SX, Saab R. Temporally distinct roles for tumor suppressor pathways in cell cycle arrest and cellular senescence in Cyclin D1-driven tumor. Molecular Cancer. 2012;11:28. doi:10.1186/1476-4598-11-28.
   Web of Science ®Google Scholar
• Basma H, Ghayad SE, Rammal G, Mancinelli A, Harajly M, Ghamloush F, Dweik L, El-Eit R, Zalzali H, Rabeh W. The synthetic retinoid ST1926 as a novel therapeutic agent in rhabdomyosarcoma. Int J Cancer. 2016;138(6):1528–1537. doi:10.1002/ijc.29886.
   Web of Science ®Google Scholar
• Keshelava N, Houghton PJ, Morton CL, Lock RB, Carol H, Keir ST, Maris JM, Reynolds CP, Gorlick R, Kolb EA. Initial testing (stage 1) of vorinostat (SAHA) by the pediatric preclinical testing program. Pediatric Blood & Cancer. 2009;53(3):505–508. doi:10.1002/pbc.21988.
   Web of Science ®Google Scholar