Efficacy and epigenetic interactions of novel DNA hypomethylating agent guadecitabine (SGI-110) in preclinical models of hepatocellular carcinoma

References

• Gores GJ. Decade in review-hepatocellular carcinoma: HCC-subtypes, stratification and sorafenib. Nat Rev Gastroenterol Hepatol 2014; 11(11):645-7; PMID:25245016; http://dx.doi.org/10.1038/nrgastro.2014.157
   PubMed Web of Science ®Google Scholar
• Sheedfar F, Di Biase S, Koonen D, Vinciguerra M. Liver diseases and aging: friends or foes? Aging Cell 2013; 12(6):950-4; PMID:23815295; http://dx.doi.org/10.1111/acel.12128
   PubMed Web of Science ®Google Scholar
• Borghesan M, Fusilli, C, Rappa, F, Panebianco, C, Rizzo, G, Oben, JA, Mazzoccoli, G, Faulkes, C, Pata, I, Agodi, A, et al. DNA Hypomethylation and Histone Variant macroH2A1 synergistically attenuate chemotherapy-induced senescence to promote hepatocellular carcinoma progression. Cancer Res 2016; 76(3):594-606; PMID:26772755; http://dx.doi.org/10.1158/0008-5472.CAN-15-1336
   PubMed Web of Science ®Google Scholar
• Revill K, Wang T, Lachenmayer A, Kojima K, Harrington A, Li J, Hoshida Y, Llovet JM, Powers S. Genome-wide methylation analysis and epigenetic unmasking identify tumor suppressor genes in hepatocellular carcinoma. Gastroenterol 2013; 145(6):1424-35 e1-25; PMID:24012984; http://dx.doi.org/10.1053/j.gastro.2013.08.055
   PubMed Web of Science ®Google Scholar
• Villanueva A, Portela A, Sayols S, Battiston C, Hoshida Y, Mendez-Gonzalez J, Imbeaud S, Letouzé E, Hernandez-Gea V, Cornella H, et al. DNA methylation-based prognosis and epidrivers in hepatocellular carcinoma. Hepatol 2015; 61(6):1945-56; PMID:25645722; http://dx.doi.org/10.1002/hep.27732
   PubMed Web of Science ®Google Scholar
• Borghesan M, Mazzoccoli G, Sheedfar F, Oben J, Pazienza V, Vinciguerra M. Histone variants and lipid metabolism. Biochem Soc Trans 2014; 42(5):1409-13; PMID:25233423; http://dx.doi.org/10.1042/BST20140119
   PubMed Web of Science ®Google Scholar
• Rappa F, Greco A, Podrini C, Cappello F, Foti M, Bourgoin L, Peyrou M, Marino A, Scibetta N, Williams R, et al. Immunopositivity for histone macroH2A1 isoforms marks steatosis-associated hepatocellular carcinoma. PLoS One 2013; 8(1):e54458; PMID:23372727; http://dx.doi.org/10.1371/journal.pone.0054458
   PubMedGoogle Scholar
• Cantarino N, Douet J, Buschbeck M. MacroH2A–an epigenetic regulator of cancer. Cancer Lett 2013; 336(2):247-52; PMID:23531411; http://dx.doi.org/10.1016/j.canlet.2013.03.022
   PubMed Web of Science ®Google Scholar
• Barzily-Rokni M, Friedman N, Ron-Bigger S, Isaac S, Michlin D, Eden A. Synergism between DNA methylation and macroH2A1 occupancy in epigenetic silencing of the tumor suppressor gene p16(CDKN2A). Nucleic Acids Res 2011; 39(4):1326-35; PMID:21030442; http://dx.doi.org/10.1093/nar/gkq994
   PubMed Web of Science ®Google Scholar
• Venturelli S, Berger A, Weiland T, Essmann F, Waibel M, Nuebling T, Häcker S, Schenk M, Schulze-Osthoff K, Salih HR, et al. Differential induction of apoptosis and senescence by the DNA methyltransferase inhibitors 5-azacytidine and 5-aza-2′-deoxycytidine in solid tumor cells. Mol Cancer Ther 2013; 12(10):2226-36; PMID:23924947; http://dx.doi.org/10.1158/1535-7163.MCT-13-0137
   PubMed Web of Science ®Google Scholar
• Venturelli S, Berger A, Weiland T, Zimmermann M, Hacker S, Peter C, Wesselborg S, Königsrainer A, Weiss TS, Gregor M, et al. Dual antitumour effect of 5-azacytidine by inducing a breakdown of resistance-mediating factors and epigenetic modulation. Gut 2011; 60(2):156-65; PMID:21106551; http://dx.doi.org/10.1136/gut.2010.208041
   PubMed Web of Science ®Google Scholar
• Venturelli S, Armeanu S, Pathil A, Hsieh CJ, Weiss TS, Vonthein R, Wehrmann M, Gregor M, Lauer UM, Bitzer M. Epigenetic combination therapy as a tumor-selective treatment approach for hepatocellular carcinoma. Cancer 2007; 109(10):2132-41; PMID:17407132; http://dx.doi.org/10.1002/cncr.22652
   PubMed Web of Science ®Google Scholar
• Kuang Y, El-Khoueiry A, Taverna P, Ljungman M, Neamati N. Guadecitabine (SGI-110) priming sensitizes hepatocellular carcinoma cells to oxaliplatin. Mol Oncol 2015; 9(9):1799-814; PMID:26160429; http://dx.doi.org/10.1016/j.molonc.2015.06.002
   PubMed Web of Science ®Google Scholar
• Jueliger S, Lyons J, Azab M, Taverna P. SGI-110, a novel second generation DNA hypomethylating agent, enhances sorafenib activity and alters the methylation signature of HCC cell lines. EORTC-AACR- NCI Symposium on Molecular Targets and Cancer Therapeutics Dublin, Ireland 2012.
   Google Scholar
• Coral S, Parisi G, Nicolay HJ, Colizzi F, Danielli R, Fratta E, Covre A, Taverna P, Sigalotti L, Maio M. Immunomodulatory activity of SGI-110, a 5-aza-2′-deoxycytidine-containing demethylating dinucleotide. Cancer Immunol Immunother 2013; 62(3):605-14; PMID:23138873; http://dx.doi.org/10.1007/s00262-012-1365-7
   PubMed Web of Science ®Google Scholar
• Issa JP, Roboz G, Rizzieri D, Jabbour E, Stock W, O'Connell C, Yee K, Tibes R, Griffiths EA, Walsh K, et al. Safety and tolerability of guadecitabine (SGI-110) in patients with myelodysplastic syndrome and acute myeloid leukaemia: a multicentre, randomised, dose-escalation phase 1 study. Lancet Oncol 2015; 16(9):1099-110; PMID:26296954; http://dx.doi.org/10.1016/S1470-2045(15)00038-8
   PubMed Web of Science ®Google Scholar
• Srivastava P, Paluch BE, Matsuzaki J, James SR, Collamat-Lai G, Karbach J, Nemeth MJ, Taverna P, Karpf AR, Griffiths EA. Immunomodulatory action of SGI-110, a hypomethylating agent, in acute myeloid leukemia cells and xenografts. Leuk Res 2014; 38(11):1332-41; PMID:25260825; http://dx.doi.org/10.1016/j.leukres.2014.09.001
   PubMed Web of Science ®Google Scholar
• McCarthy H, Wierda WG, Barron LL, Cromwell CC, Wang J, Coombes KR, Rangel R, Elenitoba-Johnson KS, Keating MJ, Abruzzo LV. High expression of activation-induced cytidine deaminase (AID) and splice variants is a distinctive feature of poor-prognosis chronic lymphocytic leukemia. Blood 2003; 101(12):4903-8; PMID:12586616; http://dx.doi.org/10.1182/blood-2002-09-2906
   PubMed Web of Science ®Google Scholar
• Ebrahem Q, Mahfouz RZ, Ng KP, Saunthararajah Y. High cytidine deaminase expression in the liver provides sanctuary for cancer cells from decitabine treatment effects. Oncotarget 2012; 3(10):1137-45; PMID:23087155; http://dx.doi.org/10.18632/oncotarget.597
   PubMed Web of Science ®Google Scholar
• Maio M, Covre A, Fratta E, Di Giacomo AM, Taverna P, Natali PG, Coral S, Sigalotti L. Molecular pathways: At the crossroads of cancer epigenetics and immunotherapy. Clin Cancer Res 2015; 21(18):4040-7; PMID:26374074; http://dx.doi.org/10.1158/1078-0432.CCR-14-2914
   PubMed Web of Science ®Google Scholar
• Savona MR, Malcovati L, Komrokji R, Tiu RV, Mughal TI, Orazi A, Kiladjian JJ, Padron E, Solary E, Tibes R, et al. An international consortium proposal of uniform response criteria for myelodysplastic/myeloproliferative neoplasms (MDS/MPN) in adults. Blood 2015; 125(12):1857-65; PMID:25624319; http://dx.doi.org/10.1182/blood-2014-10-607341
   PubMed Web of Science ®Google Scholar
• El-Khoueiry AM, Bekali-Saab M, Kim T, Denlinger R, Goel CS, Gupta R, Jueliger S, Dua S, Oganesian R, Keer A, editor Single Agent Activity Of The Second-Generation Hypomethylating Agent, SGI-110, In Patients With Hepatocellular Carcinoma (HCC) After Progression On Sorafenib. 9th ILCA Annual Conference; 2015
   Google Scholar
• Podrini C, Borghesan M, Greco A, Pazienza V, Mazzoccoli G, Vinciguerra M. Redox homeostasis and epigenetics in non-alcoholic fatty liver disease (NAFLD). Curr Pharm Des 2013; 19(15):2737-46; PMID:23092327; http://dx.doi.org/10.2174/1381612811319150009.
   PubMed Web of Science ®Google Scholar
• Saito K, Uebanso T, Maekawa K, Ishikawa M, Taguchi R, Nammo T, Nishimaki-Mogami T, Udagawa H, Fujii M, Shibazaki Y, et al. Characterization of hepatic lipid profiles in a mouse model with nonalcoholic steatohepatitis and subsequent fibrosis. Sci Rep 2015; 5:12466.
   Google Scholar
• Takakura K, Koido S, Fujii M, Hashiguchi T, Shibazaki Y, Yoneyama H, et al. Characterization of non-alcoholic steatohepatitis-derived hepatocellular carcinoma as a human stratification model in mice. Anticancer Res 2014; 34(9):4849-55; PMID:25202066
   PubMed Web of Science ®Google Scholar
• Fang F, Munck J, Tang J, Taverna P, Wang Y, Miller DF, Pilrose J, Choy G, Azab M, Pawelczak KS, et al. The novel, small-molecule DNA methylation inhibitor SGI-110 as an ovarian cancer chemosensitizer. Clin Cancer Res 2014; 20(24):6504-16; PMID:25316809; http://dx.doi.org/10.1158/1078-0432.CCR-14-1553
   PubMed Web of Science ®Google Scholar
• Henikoff S, Smith MM. Histone variants and epigenetics. Cold Spring Harb Perspect Biol 2015; 7(1):a019364; PMID:25561719; http://dx.doi.org/10.1101/cshperspect.a019364
   PubMed Web of Science ®Google Scholar
• Podrini C, Koffas A, Chokshi S, Vinciguerra M, Lelliott CJ, White JK, Adissu HA, Williams R, Greco A. MacroH2A1 isoforms are associated with epigenetic markers for activation of lipogenic genes in fat-induced steatosis. FASEB J 2015; 29(5):1676-87; PMID:25526730; http://dx.doi.org/10.1096/fj.14-262717
   PubMed Web of Science ®Google Scholar
• Novikov L, Park JW, Chen H, Klerman H, Jalloh AS, Gamble MJ. QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol Cell Biol 2011; 31(20):4244-55; PMID:21844227; http://dx.doi.org/10.1128/MCB.05244-11
   PubMed Web of Science ®Google Scholar
• Srivastava P, Paluch BE, Matsuzaki J, James SR, Collamat-Lai G, Taverna P, Karpf AR, Griffiths EA. Immunomodulatory action of the DNA methyltransferase inhibitor SGI-110 in epithelial ovarian cancer cells and xenografts. Epigenetics 2015; 10(3):237-46; PMID:25793777; http://dx.doi.org/10.1080/15592294.2015.1017198
   PubMed Web of Science ®Google Scholar
• Tellez CS, Grimes MJ, Picchi MA, Liu Y, March TH, Reed MD, Oganesian A, Taverna P, Belinsky SA. SGI-110 and entinostat therapy reduces lung tumor burden and reprograms the epigenome. Int J Cancer 2014; 135(9):2223-31; PMID:24668305; http://dx.doi.org/10.1002/ijc.28865
   PubMed Web of Science ®Google Scholar
• Longo VD, Antebi A, Bartke A, Barzilai N, Brown-Borg HM, Caruso C, Curiel TJ, de Cabo R, Franceschi C, Gems D, et al. Interventions to slow aging in humans: Are we ready? Aging Cell 2015; 14(4):497-510; PMID:25902704; http://dx.doi.org/10.1111/acel.12338
   PubMed Web of Science ®Google Scholar
• McKee C, Sigala B, Soeda J, Mouralidarane A, Morgan M, Mazzoccoli G, Rappa F, Cappello F, Cabibi D, Pazienza V, et al. Amphiregulin activates human hepatic stellate cells and is upregulated in non alcoholic steatohepatitis. Sci Rep 2015; 5:8812; PMID:25744849; http://dx.doi.org/10.1038/srep08812
   PubMed Web of Science ®Google Scholar
• Moylan CA, Pang H, Dellinger A, Suzuki A, Garrett ME, Guy CD, Murphy SK, Ashley-Koch AE, Choi SS, Michelotti GA, et al. Hepatic gene expression profiles differentiate presymptomatic patients with mild vs. severe nonalcoholic fatty liver disease. Hepatol 2014; 59(2):471-82; PMID:23913408; http://dx.doi.org/10.1002/hep.26661
   PubMed Web of Science ®Google Scholar
• Murphy SK, Yang H, Moylan CA, Pang H, Dellinger A, Abdelmalek MF, Garrett ME, Ashley-Koch A, Suzuki A, Tillmann HL, et al. Relationship between methylome and transcriptome in patients with nonalcoholic fatty liver disease. Gastroenterol 2013; 145(5):1076-87; PMID:23916847; http://dx.doi.org/10.1053/j.gastro.2013.07.047
   PubMed Web of Science ®Google Scholar
• Vinciguerra M. Normalization of a NAFLD gene expression signature. Hepatol 2014; 60(4):1445; PMID:24493162; http://dx.doi.org/10.1002/hep.27042
   PubMed Web of Science ®Google Scholar
• Mann DA. Epigenetics in liver disease. Hepatol 2014; 60(4):1418-25; PMID:24633972; http://dx.doi.org/10.1002/hep.27131
   PubMed Web of Science ®Google Scholar
• Benegiamo G, Vinciguerra M, Mazzoccoli G, Piepoli A, Andriulli A, Pazienza V. DNA methyltransferases 1 and 3b expression in Huh-7 cells expressing HCV core protein of different genotypes. Dig Dis Sci 2012; 57(6):1598-603; PMID:22526584; http://dx.doi.org/10.1007/s10620-012-2160-1
   PubMed Web of Science ®Google Scholar
• Bian EB, Huang C, Ma TT, Tao H, Zhang H, Cheng C, Lv XW, Li J. DNMT1-mediated PTEN hypermethylation confers hepatic stellate cell activation and liver fibrogenesis in rats. Toxicol Appl Pharmacol 2012; 264(1):13-22; PMID:22841775; http://dx.doi.org/10.1016/j.taap.2012.06.022
   PubMed Web of Science ®Google Scholar
• Lavelle D, Vaitkus K, Ling Y, Ruiz MA, Mahfouz R, Ng KP, Negrotto S, Smith N, Terse P, Engelke KJ, et al. Effects of tetrahydrouridine on pharmacokinetics and pharmacodynamics of oral decitabine. Blood 2012; 119(5):1240-7; PMID:22160381; http://dx.doi.org/10.1182/blood-2011-08-371690
   PubMed Web of Science ®Google Scholar
• Cervello M, Bachvarov D, Lampiasi N, Cusimano A, Azzolina A, McCubrey JA, Montalto G. Molecular mechanisms of sorafenib action in liver cancer cells. Cell Cycle 2012; 11(15):2843-55; PMID:22801548; http://dx.doi.org/10.4161/cc.21193
   PubMed Web of Science ®Google Scholar
• D'Aronzo M, Vinciguerra M, Mazza T, Panebianco C, Saracino C, Pereira SP, Graziano P, Pazienza V. Fasting cycles potentiate the efficacy of gemcitabine treatment in in vitro and in vivo pancreatic cancer models. Oncotarget 2015; 6(21):18545-57; PMID:26176887; http://dx.doi.org/10.18632/oncotarget.4186
   PubMed Web of Science ®Google Scholar
• Pazienza V, Borghesan M, Mazza T, Sheedfar F, Panebianco C, Williams R, Mazzoccoli G, Andriulli A, Nakanishi T, Vinciguerra M. SIRT1-metabolite binding histone macroH2A1.1 protects hepatocytes against lipid accumulation. Aging (Albany NY) 2014; 6(1):35-47; PMID:24473773; http://dx.doi.org/10.18632/aging.100632
   PubMedGoogle Scholar
• Ripoli M, Barbano R, Balsamo T, Piccoli C, Brunetti V, Coco M, Mazzoccoli G, Vinciguerra M, Pazienza V. Hypermethylated levels of E-cadherin promoter in Huh-7 cells expressing the HCV core protein. Virus Res 2011; 160(1–2):74-81; PMID:21640770; http://dx.doi.org/10.1016/j.virusres.2011.05.014
   PubMed Web of Science ®Google Scholar
• Planavila A, Dominguez E, Navarro M, Vinciguerra M, Iglesias R, Giralt M, Lope-Piedrafita S, Ruberte J, Villarroya F. Dilated cardiomyopathy and mitochondrial dysfunction in Sirt1-deficient mice: a role for Sirt1-Mef2 in adult heart. J Mol Cell Cardiol 2012; 53(4):521-31; PMID:22986367; http://dx.doi.org/10.1016/j.yjmcc.2012.07.019
   PubMed Web of Science ®Google Scholar