2,258
Views
38
CrossRef citations to date
0
Altmetric
Original Research

Anti-GD2 mAb and Vorinostat synergize in the treatment of neuroblastoma

, , , , , , , , , & show all
Article: e1164919 | Received 16 Nov 2015, Accepted 08 Mar 2016, Published online: 08 Jun 2016

References

  • Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet 2007; 369:2106-20; PMID:17586306; http://dx.doi.org/10.1016/S0140-6736(07)60983-0
  • Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D, Gerbing RB, London WB, Villablanca JG. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children's oncology group study. J Clin Oncol 2009; 27:1007-13; PMID:19171716; http://dx.doi.org/10.1200/JCO.2007.13.8925
  • Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363:1324-34; PMID:20879881; http://dx.doi.org/10.1056/NEJMoa0911123
  • Tarek N, Le Luduec JB, Gallagher MM, Zheng J, Venstrom JM, Chamberlain E, Modak S, Heller G, Dupont B, Cheung NK et al. Unlicensed NK cells target neuroblastoma following anti-GD2 antibody treatment. J Clin Invest 2012; 122:3260-70; PMID:22863621; http://dx.doi.org/10.1172/JCI62749
  • Cheung NK, Cheung IY, Kramer K, Modak S, Kuk D, Pandit-Taskar N, Chamberlain E, Ostrovnaya I, Kushner BH. Key role for myeloid cells: Phase II results of anti-G antibody 3F8 plus granulocyte-macrophage colony-stimulating factor for chemoresistant osteomedullary neuroblastoma. Int J Cancer 2014; 135(9):2199-205; PMID:24644014; http://dx.doi.org/10.1002/ijc.28851
  • Kroesen M, Lindau D, Hoogerbrugge P, Adema GJ. Immunocombination therapy for high-risk neuroblastoma. Immunotherapy 2012; 4:163-74; PMID:22394368; http://dx.doi.org/10.2217/imt.11.169
  • Khan O, La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 2012; 90:85-94; PMID:22124371; http://dx.doi.org/10.1038/icb.2011.100
  • Bolden JE, Shi W, Jankowski K, Kan CY, Cluse L, Martin BP, MacKenzie KL, Smyth GK, Johnstone RW. HDAC inhibitors induce tumor-cell-selective pro-apoptotic transcriptional responses. Cell Death Dis 2013; 4:e519; PMID:23449455; http://dx.doi.org/10.1038/cddis.2013.9
  • Nalabothula N, Carrier F. Cancer cells' epigenetic composition and predisposition to histone deacetylase inhibitor sensitization. Epigenomics 2011; 3:145-55; PMID:21743813; http://dx.doi.org/10.2217/epi.11.12
  • Muhlethaler-Mottet A, Meier R, Flahaut M, Bourloud KB, Nardou K, Joseph JM, Gross N. Complex molecular mechanisms cooperate to mediate histone deacetylase inhibitors anti-tumour activity in neuroblastoma cells. Mol Cancer 2008; 7:55; PMID:18549473; http://dx.doi.org/10.1186/1476-4598-7-55
  • Condorelli F, Gnemmi I, Vallario A, Genazzani AA, Canonico PL. Inhibitors of histone deacetylase (HDAC) restore the p53 pathway in neuroblastoma cells. Br J Pharmacol 2008; 153:657-68; PMID:18059320; http://dx.doi.org/10.1038/sj.bjp.0707608
  • Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, Breslow R, Pavletich NP. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 1999; 401:188-93; PMID:10490031; http://dx.doi.org/10.1038/43710
  • Duvic M, Vu J. Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 2007; 16:1111-20; PMID:17594194; http://dx.doi.org/10.1517/13543784.16.7.1111
  • 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 Clin Oncol 2010; 28:3623-9; PMID:20606092; http://dx.doi.org/10.1200/JCO.2009.25.9119
  • Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med 1985; 313:1111-6; PMID:4047115; http://dx.doi.org/10.1056/NEJM198510313131802
  • Jacobs JF, van Bokhoven H, van Leeuwen FN, Hulsbergen-van de Kaa CA, de Vries IJ, Adema GJ, Hoogerbrugge PM, de Brouwer AP. Regulation of MYCN expression in human neuroblastoma cells. BMC Cancer 2009; 9:239; PMID:19615087; http://dx.doi.org/10.1186/1471-2407-9-239
  • Weiss WA, Aldape K, Mohapatra G, Feuerstein BG, Bishop JM. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J 1997; 16:2985-95; PMID:9214616; http://dx.doi.org/10.1093/emboj/16.11.2985
  • Teitz T, Stanke JJ, Federico S, Bradley CL, Brennan R, Zhang J, Johnson MD, Sedlacik J, Inoue M, Zhang ZM et al. Preclinical models for neuroblastoma: establishing a baseline for treatment. PLoS One 2011; 6:e19133; PMID:21559450; http://dx.doi.org/10.1371/journal.pone.0019133
  • Kroesen M, Nierkens S, Ansems M, Wassink M, Orentas RJ, Boon L, den Brok MH, Hoogerbrugge PM, Adema GJ. A transplantable TH-MYCN transgenic tumor model in C57Bl/6 mice for preclinical immunological studies in neuroblastoma. Int J Cancer 2014; 134:1335-45; PMID:24038106; http://dx.doi.org/10.1002/ijc.28463
  • Carlson LM, Rasmuson A, Idborg H, Segerstrom L, Jakobsson PJ, Sveinbjornsson B, Kogner P. Low-dose aspirin delays an inflammatory tumor progression in vivo in a transgenic mouse model of neuroblastoma. Carcinogenesis 2013; 34:1081-8; PMID:23349014; http://dx.doi.org/10.1093/carcin/bgt009
  • Santilli G, Piotrowska I, Cantilena S, Chayka O, D'Alicarnasso M, Morgenstern DA, Himoudi N, Pearson K, Anderson J, Thrasher AJ et al. Polyphenon [corrected] E enhances the antitumor immune response in neuroblastoma by inactivating myeloid suppressor cells. Clin Cancer Res 2013; 19:1116-25; PMID:23322899; http://dx.doi.org/10.1158/1078-0432.CCR-12-2528
  • Movahedi K, Laoui D, Gysemans C, Baeten M, Stange G, Van den Bossche J, Mack M, Pipeleers D, In't Veld P, De Baetselier P et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 2010; 70:5728-39; PMID:20570887; http://dx.doi.org/10.1158/0008-5472.CAN-09-4672
  • Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, Pamer EG, Li MO. The cellular and molecular origin of tumor-associated macrophages. Science 2014; 344:921-5; PMID:24812208; http://dx.doi.org/10.1126/science.1252510
  • Lu T, Ramakrishnan R, Altiok S, Youn JI, Cheng P, Celis E, Pisarev V, Sherman S, Sporn MB, Gabrilovich D. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest 2011; 121:4015-29; PMID:21911941; http://dx.doi.org/10.1172/JCI45862
  • Kroesen M, Gielen P, Brok IC, Armandari I, Hoogerbrugge PM, Adema GJ. HDAC inhibitors and immunotherapy; a double edged sword? Oncotarget 2014; 5:6558-72; PMID:25115382; http://dx.doi.org/10.18632/oncotarget.2289
  • Kroesen M, Nierkens S, Ansems M, Wassink M, Orentas RJ, Boon L, den Brok MH, Hoogerbrugge PM, Adema GJ. A transplantable TH-MYCN transgenic tumor model in C57Bl/6 mice for preclinical immunological studies in neuroblastoma. Int J Cancer 2014; 134:1335-45; PMID:24038106; http://dx.doi.org/10.1002/ijc.28463
  • Furukawa K, Aixinjueluo W, Kasama T, Ohkawa Y, Yoshihara M, Ohmi Y, Tajima O, Suzumura A, Kittaka D. Disruption of GM2/GD2 synthase gene resulted in overt expression of 9-O-acetyl GD3 irrespective of Tis21. J Neurochem 2008; 105:1057-66; PMID:18194438; http://dx.doi.org/10.1111/j.1471-4159.2008.05232.x
  • Suzuki Y, Yanagisawa M, Ariga T, Yu RK. Histone acetylation-mediated glycosyltransferase gene regulation in mouse brain during development. J Neurochem 2011; 116:874-80; PMID:21214566; http://dx.doi.org/10.1111/j.1471-4159.2010.07042.x
  • Leidi M, Gotti E, Bologna L, Miranda E, Rimoldi M, Sica A, Roncalli M, Palumbo GA, Introna M, Golay J. M2 macrophages phagocytose rituximab-opsonized leukemic targets more efficiently than m1 cells in vitro. J Immunol 2009; 182:4415-22; PMID:19299742; http://dx.doi.org/10.4049/jimmunol.0713732
  • Grugan KD, McCabe FL, Kinder M, Greenplate AR, Harman BC, Ekert JE, van Rooijen N, Anderson GM, Nemeth JA, Strohl WR et al. Tumor-associated macrophages promote invasion while retaining Fc-dependent anti-tumor function. J Immunol 2012; 189:5457-66; PMID:23105143; http://dx.doi.org/10.4049/jimmunol.1201889
  • Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12:253-68; PMID:22437938; http://dx.doi.org/10.1038/nri3175
  • Canioni D, Salles G, Mounier N, Brousse N, Keuppens M, Morchhauser F, Lamy T, Sonet A, Rousselet MC, Foussard C et al. High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol 2008; 26:440-6; PMID:18086798; http://dx.doi.org/10.1200/JCO.2007.12.8298
  • Petricevic B, Laengle J, Singer J, Sachet M, Fazekas J, Steger G, Bartsch R, Jensen-Jarolim E, Bergmann M. Trastuzumab mediates antibody-dependent cell-mediated cytotoxicity and phagocytosis to the same extent in both adjuvant and metastatic HER2/neu breast cancer patients. J Transl Med 2013; 11:307; PMID:24330813; http://dx.doi.org/10.1186/1479-5876-11-307
  • Braster R, O'Toole T, van Egmond M. Myeloid cells as effector cells for monoclonal antibody therapy of cancer. Methods 2014; 65:28-37; PMID:23811299; http://dx.doi.org/10.1016/j.ymeth.2013.06.020
  • Haile LA, Gamrekelashvili J, Manns MP, Korangy F, Greten TF. CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J Immunol 2010; 185:203-10; PMID:20525890; http://dx.doi.org/10.4049/jimmunol.0903573
  • Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-802; PMID:18832739; http://dx.doi.org/10.4049/jimmunol.181.8.5791
  • Ferris RL, Jaffee EM, Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J Clin Oncol 2010; 28:4390-9; PMID:20697078; http://dx.doi.org/10.1200/JCO.2009.27.6360
  • Galluzzi L, Vacchelli E, Fridman WH, Galon J, Sautes-Fridman C, Tartour E, Zucman-Rossi J, Zitvogel L, Kroemer G. Trial Watch: Monoclonal antibodies in cancer therapy. Oncoimmunology 2012; 1:28-37; PMID:22720209; http://dx.doi.org/10.4161/onci.1.1.17938
  • Simon T, Hero B, Faldum A, Handgretinger R, Schrappe M, Klingebiel T, Berthold F. Long-term outcome of high-risk neuroblastoma patients after immunotherapy with antibody ch14.18 or oral metronomic chemotherapy. BMC Cancer 2011; 11:21; PMID:21244693; http://dx.doi.org/10.1186/1471-2407-11-21
  • Hahn CK, Ross KN, Warrington IM, Mazitschek R, Kanegai CM, Wright RD, Kung AL, Golub TR, Stegmaier K. Expression-based screening identifies the combination of histone deacetylase inhibitors and retinoids for neuroblastoma differentiation. Proc Natl Acad Sci U S A 2008; 105:9751-6; PMID:18607002; http://dx.doi.org/10.1073/pnas.0710413105
  • Liu T, Tee AE, Porro A, Smith SA, Dwarte T, Liu PY, Iraci N, Sekyere E, Haber M, Norris MD et al. Activation of tissue transglutaminase transcription by histone deacetylase inhibition as a therapeutic approach for Myc oncogenesis. Proc Natl Acad Sci U S A 2007; 104:18682-7; PMID:18003922; http://dx.doi.org/10.1073/pnas.0705524104
  • Lodrini M, Oehme I, Schroeder C, Milde T, Schier MC, Kopp-Schneider A, Schulte JH, Fischer M, De Preter K, Pattyn F et al. MYCN and HDAC2 cooperate to repress miR-183 signaling in neuroblastoma. Nucleic Acids Res 2013; 41:6018-33; PMID:23625969; http://dx.doi.org/10.1093/nar/gkt346
  • Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 2013; 138:105-15; PMID:23216602; http://dx.doi.org/10.1111/imm.12036
  • Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, Porrett PM, Li B, Turka LA, Olson EN, Greene MI et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 2007; 13:1299-307; PMID:17922010; http://dx.doi.org/10.1038/nm1652
  • Akimova T, Ge G, Golovina T, Mikheeva T, Wang L, Riley JL, Hancock WW. Histone/protein deacetylase inhibitors increase suppressive functions of human FOXP3+ Tregs. Clin Immunol 2010; 136:348-63; PMID:20478744; http://dx.doi.org/10.1016/j.clim.2010.04.018
  • Bridle BW, Chen L, Lemay CG, Diallo JS, Pol J, Nguyen A, Capretta A, He R, Bramson JL, Bell JC et al. HDAC inhibition suppresses primary immune responses, enhances secondary immune responses, and abrogates autoimmunity during tumor immunotherapy. Mol Ther 2013; 21:887-94; PMID:23295947; http://dx.doi.org/10.1038/mt.2012.265
  • Cheng P, Corzo CA, Luetteke N, Yu B, Nagaraj S, Bui MM, Ortiz M, Nacken W, Sorg C, Vogl T et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med 2008; 205:2235-49; PMID:18809714; http://dx.doi.org/10.1084/jem.20080132
  • Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, De Baetselier P, Van Ginderachter JA. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233-44; PMID:18272812; http://dx.doi.org/10.1182/blood-2007-07-099226
  • Hamaguchi Y, Xiu Y, Komura K, Nimmerjahn F, Tedder TF. Antibody isotype-specific engagement of Fcgamma receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 2006; 203:743-53; PMID:16520392; http://dx.doi.org/10.1084/jem.20052283
  • Gul N, Babes L, Siegmund K, Korthouwer R, Bogels M, Braster R, Vidarsson G, Ten Hagen TL, Kubes P, van Egmond M. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J Clin Invest 2014; 124:812-23; PMID:24430180; http://dx.doi.org/10.1172/JCI66776
  • Asgharzadeh S, Salo JA, Ji L, Oberthuer A, Fischer M, Berthold F, Hadjidaniel M, Liu CW, Metelitsa LS, Pique-Regi R et al. Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol 2012; 30:3525-32; PMID:22927533; http://dx.doi.org/10.1200/JCO.2011.40.9169
  • McEarchern JA, Oflazoglu E, Francisco L, McDonagh CF, Gordon KA, Stone I, Klussman K, Turcott E, van Rooijen N, Carter P et al. Engineered anti-CD70 antibody with multiple effector functions exhibits in vitro and in vivo antitumor activities. Blood 2007; 109:1185-92; PMID:17038522; http://dx.doi.org/10.1182/blood-2006-07-034017
  • Oflazoglu E, Stone IJ, Gordon KA, Grewal IS, van Rooijen N, Law CL, Gerber HP. Macrophages contribute to the antitumor activity of the anti-CD30 antibody SGN-30. Blood 2007; 110:4370-2; PMID:17909075; http://dx.doi.org/10.1182/blood-2007-06-097014
  • Hubert P, Heitzmann A, Viel S, Nicolas A, Sastre-Garau X, Oppezzo P, Pritsch O, Osinaga E, Amigorena S. Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res 2011; 71:5134-43; PMID:21697279; http://dx.doi.org/10.1158/0008-5472.CAN-10-4222
  • Vo DD, Prins RM, Begley JL, Donahue TR, Morris LF, Bruhn KW, de la Rocha P, Yang MY, Mok S, Garban HJ et al. Enhanced antitumor activity induced by adoptive T-cell transfer and adjunctive use of the histone deacetylase inhibitor LAQ824. Cancer Res 2009; 69:8693-9; PMID:19861533; http://dx.doi.org/10.1158/0008-5472.CAN-09-1456
  • Christiansen AJ, West A, Banks KM, Haynes NM, Teng MW, Smyth MJ, Johnstone RW. Eradication of solid tumors using histone deacetylase inhibitors combined with immune-stimulating antibodies. Proc Natl Acad Sci U S A 2011; 108:4141-6; PMID:21368108; http://dx.doi.org/10.1073/pnas.1011037108
  • Kim DK, Lee JY, Kim JS, Ryu JH, Choi JY, Lee JW, Im GJ, Kim TK, Seo JW, Park HJ et al. Synthesis and biological evaluation of 3-(4-substituted-phenyl)-N-hydroxy-2-propenamides, a new class of histone deacetylase inhibitors. J Med Chem 2003; 46:5745-51; PMID:14667227; http://dx.doi.org/10.1021/jm030377q
  • Kozikowski AP, Tapadar S, Luchini DN, Kim KH, Billadeau DD. Use of the nitrile oxide cycloaddition (NOC) reaction for molecular probe generation: a new class of enzyme selective histone deacetylase inhibitors (HDACIs) showing picomolar activity at HDAC6. J Med Chem 2008; 51:4370-3; PMID:18642892; http://dx.doi.org/10.1021/jm8002894