117
Views
7
CrossRef citations to date
0
Altmetric
Original Research

Dinutuximab Synergistically Enhances the Cytotoxicity of Natural Killer Cells to Retinoblastoma Through the Perforin-Granzyme B Pathway

, , , ORCID Icon, ORCID Icon, , ORCID Icon & show all
Pages 3903-3920 | Published online: 08 May 2020

References

  • Dyer MA. Lessons from retinoblastoma: implications for cancer, development, evolution, and regenerative medicine. Trends Mol Med. 2016;22(10):863–876. doi:10.1016/j.molmed.2016.07.01027567287
  • Truong B, Green AL, Friedrich P, Ribeiro KB, Rodriguez-Galindo C. Ethnic, racial, and socioeconomic disparities in retinoblastoma. JAMA Pediatr. 2015;169(12):1096–1104. doi:10.1001/jamapediatrics.2015.236026436436
  • Rajeshuni N, Whittemore AS, Ludwig CA, Mruthyunjaya P, Moshfeghi DM. Racial, ethnic, and socioeconomic disparities in retinoblastoma enucleation: a population-based study, SEER 18 2000-2014. Am J Ophthalmol. 2019. doi:10.1016/j.ajo.2019.04.015
  • Dimaras H, Kimani K, Dimba EA, et al. Retinoblastoma. Lancet. 2012;379(9824):1436–1446. doi:10.1016/S0140-6736(11)61137-922414599
  • Asnaghi L, White DT, Key N, et al. ACVR1C/SMAD2 signaling promotes invasion and growth in retinoblastoma. Oncogene. 2019;38(12):2056–2075. doi:10.1038/s41388-018-0543-230401983
  • Chen M, Luo C, Zhao J, Devarajan G, Xu H. Immune regulation in the aging retina. Prog Retin Eye Res. 2019;69:159–172. doi:10.1016/j.preteyeres.2018.10.00330352305
  • Park DY, Lee J, Kim J, et al. Plastic roles of pericytes in the blood-retinal barrier. Nat Commun. 2017;8:15296. doi:10.1038/ncomms1529628508859
  • Suzuki M, Cheung NK. Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin Ther Tar. 2015;19(3):349–362. doi:10.1517/14728222.2014.986459
  • Durbas M, Horwacik I, Boratyn E, Kamycka E, Rokita H. GD2 ganglioside specific antibody treatment downregulates PI3K/Akt/mTOR signaling network in human neuroblastoma cell lines. Int J Oncol. 2015;47(3):1143–1159. doi:10.3892/ijo.2015.307026134970
  • Julien S, Bobowski M, Steenackers A, Le Bourhis X, Delannoy P. How do gangliosides regulate RTKs signaling? Cells. 2013;2(4):751–767. doi:10.3390/cells204075124709879
  • Iwasawa T, Zhang P, Ohkawa Y, et al. Enhancement of malignant properties of human glioma cells by ganglioside GD3/GD2. Int J Oncol. 2018;52(4):1255–1266. doi:10.3892/ijo.2018.426629436609
  • Battula VL, Shi Y, Evans KW, et al. Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis. J Clin Invest. 2012;122(6):2066–2078. doi:10.1172/JCI5973522585577
  • Liang YJ, Ding Y, Levery SB, Lobaton M, Handa K, Hakomori SI. Differential expression profiles of glycosphingolipids in human breast cancer stem cells vs. cancer non-stem cells. Proc Natl Acad Sci U S A. 2013;110(13):4968–4973. doi:10.1073/pnas.130282511023479608
  • Portoukalian J, David MJ, Gain P, Richard M. Shedding of GD2 ganglioside in patients with retinoblastoma. Int J Cancer. 1993;53(6):948–951. doi:10.1002/ijc.29105306148473052
  • Cheung NK, Cheung IY, Kramer K, et al. Key role for myeloid cells: Phase II results of anti-G(D2) antibody 3F8 plus granulocyte-macrophage colony-stimulating factor for chemoresistant osteomedullary neuroblastoma. Int J Cancer. 2014;135(9):2199–2205. doi:10.1002/ijc.2885124644014
  • Shen H, Tang Y, Xu X, Tang H. Detection of the GD2+/CD56+/CD45- immunophenotype by flow cytometry in cerebrospinal fluids from a patient with retinoblastoma. Pediatr Hematol Oncol. 2013;30(1):30–32. doi:10.3109/08880018.2012.73709423126274
  • Laurent VE, Sampor C, Solernou V, et al. Detection of minimally disseminated disease in the cerebrospinal fluid of children with high-risk retinoblastoma by reverse transcriptase-polymerase chain reaction for GD2 synthase mRNA. Eur J Cancer. 2013;49(13):2892–2899. doi:10.1016/j.ejca.2013.04.02123721779
  • Laurent VE, Otero LL, Vazquez V, et al. Optimization of molecular detection of GD2 synthase mRNA in retinoblastoma. Mol Med Rep. 2010;3(2):253–259. doi:10.3892/mmr_0000024821472230
  • Chantada GL, Rossi J, Casco F, et al. An aggressive bone marrow evaluation including immunocytology with GD2 for advanced retinoblastoma. J Pediatr Hematol Oncol. 2006;28(6):369–373. doi:10.1097/00043426-200606000-0000916794505
  • Ho WL, Hsu WM, Huang MC, Kadomatsu K, Nakagawara A. Protein glycosylation in cancers and its potential therapeutic applications in neuroblastoma. J Hematol Oncol. 2016;9(1):100. doi:10.1186/s13045-016-0334-627686492
  • Yu AL, Gilman AL, Ozkaynak MF, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363(14):1324–1334. doi:10.1056/NEJMoa091112320879881
  • Navid F, Sondel PM, Barfield R, et al. Phase I trial of a novel anti-GD2 monoclonal antibody, Hu14.18K322A, designed to decrease toxicity in children with refractory or recurrent neuroblastoma. J Clin Oncol. 2014;32(14):1445–1452. doi:10.1200/JCO.2013.50.442324711551
  • Ladenstein R, Poetschger U, Gray J, et al. Toxicity and outcome of anti-GD2 antibody ch14.18/CHO in front-line, high-risk patients with neuroblastoma: final results of the Phase III immunotherapy randomisation (HR-NBL1/SIOPEN trial). J Clin Oncol. 2016;34(15_suppl):10500. doi:10.1200/JCO.2016.34.15_suppl.10500
  • Furman WL, Shulkin BL, Federico SM, et al. Early response rates and Curie scores at end of induction: an update from a phase II study of an anti-GD2 monoclonal antibody (mAb) with chemotherapy (CT) in newly diagnosed patients (pts) with high-risk (HR) neuroblastoma (NB). J Clin Oncol. 2017;35(15_suppl):10534. doi:10.1200/JCO.2017.35.15_suppl.10534
  • Mody R, Naranjo A, Van Ryn C, et al. Irinotecan–temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): an open-label, randomised, Phase 2 trial. Lancet Oncol. 2017;18(7):946–957. doi:10.1016/S1470-2045(17)30355-828549783
  • Dhillon S. Dinutuximab: first global approval. Drugs. 2015;75(8):923–927. doi:10.1007/s40265-015-0399-525940913
  • Lopez-Soto A, Gonzalez S, Smyth MJ, Galluzzi L. Control of metastasis by NK cells. Cancer Cell. 2017;32(2):135–154. doi:10.1016/j.ccell.2017.06.00928810142
  • Romain G, Senyukov V, Rey-Villamizar N, et al. Antibody Fc engineering improves frequency and promotes kinetic boosting of serial killing mediated by NK cells. Blood. 2014;124(22):3241–3249. doi:10.1182/blood-2014-04-56906125232058
  • Paul P, Picard C, Sampol E, et al. Genetic and functional profiling of CD16-dependent natural killer activation identifies patients at higher risk of cardiac allograft vasculopathy. Circulation. 2018;137(10):1049–1059. doi:10.1161/CIRCULATIONAHA.117.03043529097449
  • Modak S, Le Luduec JB, Cheung IY, et al. Adoptive immunotherapy with haploidentical natural killer cells and Anti-GD2 monoclonal antibody m3F8 for resistant neuroblastoma: results of a phase I study. Oncoimmunology. 2018;7(8):e1461305. doi:10.1080/2162402X.2018.146130530221057
  • Tran HC, Wan Z, Sheard MA, et al. TGFbetaR1 blockade with galunisertib (LY2157299) enhances anti-neuroblastoma activity of the anti-GD2 antibody dinutuximab (ch14.18) with natural killer cells. Clin Cancer Res. 2017;23(3):804–813. doi:10.1158/1078-0432.CCR-16-174327756784
  • Kim S, Poursine-Laurent J, Truscott SM, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–713. doi:10.1038/nature0384716079848
  • Wang W, Erbe AK, Hank JA, Morris ZS, Sondel PM. NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy. Front Immunol. 2015;6:368. doi:10.3389/fimmu.2015.0036826284063
  • Erbe AK, Wang W, Carmichael L, et al. Neuroblastoma patients’ KIR and KIR-Ligand genotypes influence clinical outcome for dinutuximab-based immunotherapy: a report from the children’s oncology group. Clin Cancer Res. 2018;24(1):189–196. doi:10.1158/1078-0432.CCR-17-176728972044
  • Delgado DC, Hank JA, Kolesar J, et al. Genotypes of NK cell KIR receptors, their ligands, and Fcgamma receptors in the response of neuroblastoma patients to Hu14.18-IL2 immunotherapy. Cancer Res. 2010;70(23):9554–9561. doi:10.1158/0008-5472.CAN-10-221120935224
  • Boyiadzis M, Agha M, Redner RL, et al. Phase 1 clinical trial of adoptive immunotherapy using “off-the-shelf” activated natural killer cells in patients with refractory and relapsed acute myeloid leukemia. Cytotherapy. 2017;19(10):1225–1232. doi:10.1016/j.jcyt.2017.07.00828864289
  • Tonn T, Schwabe D, Klingemann HG, et al. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy. 2013;15(12):1563–1570. doi:10.1016/j.jcyt.2013.06.01724094496
  • Arai S, Meagher R, Swearingen M, et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy. 2008;10(6):625–632. doi:10.1080/1465324080230187218836917
  • Maki G, Klingemann HG, Martinson JA, Tam YK. Factors regulating the cytotoxic activity of the human natural killer cell line, NK-92. J Hematother Stem Cell Res. 2001;10(3):369–383. doi:10.1089/15258160175028897511454312
  • Spadoni I, Fornasa G, Rescigno M. Organ-specific protection mediated by cooperation between vascular and epithelial barriers. Nat Rev Immunol. 2017;17(12):761–773. doi:10.1038/nri.2017.10028869253
  • Chen X, Kunda PE, Lin J, et al. SYK-targeted dendritic cell-mediated cytotoxic T lymphocytes enhance the effect of immunotherapy on retinoblastoma. J Cancer Res Clin Oncol. 2018;144(4):675–684. doi:10.1007/s00432-018-2584-x29372378
  • Liu Q, Wang Y, Wang H, Liu Y, Liu T, Kunda PE. Tandem therapy for retinoblastoma: immunotherapy and chemotherapy enhance cytotoxicity on retinoblastoma by increasing apoptosis. J Cancer Res Clin Oncol. 2013;139(8):1357–1372. doi:10.1007/s00432-013-1448-723689539
  • Mitra M, Kandalam M, Harilal A, et al. EpCAM is a putative stem marker in retinoblastoma and an effective target for T-cell-mediated immunotherapy. Mol Vis. 2012;18.
  • Hayashida Y, Kurimoto S, Yamamoto N. Effect of lymphokine-activated killer cells on human retinoblastoma cells (Y-79) in vitro: enhancement of the activity by a polysaccharide preparation, krestin. Biochem Biophys Res Commun. 1991;174(1):107–114. doi:10.1016/0006-291X(91)90492-P1899189
  • Ohashi Y, Sasabe T, Nishida T, Manabe R. Natural killer cells kill human retinoblastoma cells. Jpn J Ophthalmol. 1984;28(4):370–376.6085129
  • Merriam JC, Lyon HS, Char DH. Toxicity of a monoclonal F(ab’)2: ricinA conjugate for retinoblastoma in vitro. Cancer Res. 1984;44(8):3178–3183.6744258
  • Ramtohul P, Denis D, Comet A. Natural course of a retinal metastasis from colon adenocarcinoma. Ophthalmology. 2019;126(6):840. doi:10.1016/j.ophtha.2019.03.03131122361
  • Shields CL, McMahon JF, Atalay HT, Hasanreisoglu M, Shields JA. Retinal metastasis from systemic cancer in 8 cases. JAMA Ophthalmol. 2014;132(11):1303–1308. doi:10.1001/jamaophthalmol.2014.240625033168
  • Horai R, Zarate-Blades CR, Dillenburg-Pilla P, et al. Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site. Immunity. 2015;43(2):343–353. doi:10.1016/j.immuni.2015.07.01426287682
  • Rosenbaum JT, McDevitt HO, Guss RB, Egbert PR. Endotoxin-induced uveitis in rats as a model for human disease. Nature. 1980;286(5773):611–613. doi:10.1038/286611a07402339
  • Fernandez-Diaz AB, Garcia-Medina A, Ferrer-Guillen B, Berrocal A. Eye immune privilege? Nivolumab plus ipilimumab: successful treatment in a patient with cutaneous melanoma and ocular metastases. Melanoma Res. 2019;29(3):345–347. doi:10.1097/CMR.000000000000059131022059
  • Pe’er J, Rowe JM, Frenkel S, Dann EJ. Testicular lymphoma, intraocular (vitreoretinal) lymphoma, and brain lymphoma: involvement of three immunoprivileged sites in one patient. Am J Hematol. 2010;85(8):631–633. doi:10.1002/ajh.2176720658596
  • Yuan X, He X, Li Y, et al. Establishment and genomic characterization of a novel retinoblastoma cell line without RB1 mutation derived from a Han Chinese donor. J Shanghai Jiao Tong Univ. 2018;38:866–873.
  • Fan X, Rai A, Kambham N, et al. Endometrial VEGF induces placental sFLT1 and leads to pregnancy complications. J Clin Invest. 2014;124(11):4941–4952. doi:10.1172/JCI7686425329693
  • Wahl S, Drong A, Lehne B, et al. Epigenome-wide association study of body mass index, and the adverse outcomes of adiposity. Nature. 2017;541(7635):81–86. doi:10.1038/nature2078428002404
  • Olin A, Henckel E, Chen Y, et al. Stereotypic immune system development in newborn children. Cell. 2018;174(5):1277–1292 e1214. doi:10.1016/j.cell.2018.06.04530142345
  • Giugliano S, Petroff MG, Warren BD, et al. Hepatitis C virus sensing by human trophoblasts induces innate immune responses and recruitment of maternal NK cells: potential implications for limiting vertical transmission. J Immunol. 2015;195(8):3737–3747. doi:10.4049/jimmunol.150040926342030
  • Chai P, Jia R, Jia R, et al. Dynamic chromosomal tuning of a novel GAU1 lncing driver at chr12p13.32 accelerates tumorigenesis. Nucleic Acids Res. 2018;46(12):6041–6056. doi:10.1093/nar/gky36629741668
  • Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–15550. doi:10.1073/pnas.050658010216199517
  • Boulagnon C, Ducasse A, Patey M, Diebold MD, Arndt C. Cytopathology of vitreous humor samples in routine practice. Acta Cytol. 2016;60(1):65–73. doi:10.1159/00044457626986556
  • Narumi M, Nishitsuka K, Yamakawa M, Yamashita H. A survey of vitreous cell components performed using liquid-based cytology. Acta Ophthalmol. 2015;93(5):e386–390. doi:10.1111/aos.1262325752226
  • Eagle RC Jr., Shields JA, Donoso L, Milner RS. Malignant transformation of spontaneously regressed retinoblastoma, retinoma/retinocytoma variant. Ophthalmology. 1989;96(9):1389–1395. doi:10.1016/S0161-6420(89)32714-X2780006
  • Yu J, Wu X, Yan J, et al. Anti-GD2/4-1BB chimeric antigen receptor T cell therapy for the treatment of Chinese melanoma patients. J Hematol Oncol. 2018;11(1):1. doi:10.1186/s13045-017-0548-229298689
  • Khosravi A, Shahrabi S, Shahjahani M, Saki N. The bone marrow metastasis niche in retinoblastoma. Cell Oncol (Dordr). 2015;38(4):253–263. doi:10.1007/s13402-015-0232-x26063518
  • Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells - mechanisms of immune surveillance and escape. Nat Rev Clin Oncol. 2017;14(3):155–167. doi:10.1038/nrclinonc.2016.14427644321
  • Su S, Chen J, Yao H, et al. CD10+GPR77+ cancer-associated fibroblasts promote cancer formation and chemoresistance by sustaining cancer stemness. Cell. 2018;172(4):841–856.e816. doi:10.1016/j.cell.2018.01.00929395328
  • Boire A, Zou Y, Shieh J, Macalinao DG, Pentsova E, Massague J. Complement component 3 adapts the cerebrospinal fluid for leptomeningeal metastasis. Cell. 2017;168(6):1101–1113 e1113. doi:10.1016/j.cell.2017.02.02528283064
  • Vadrevu SK, Chintala NK, Sharma SK, et al. Complement c5a receptor facilitates cancer metastasis by altering T-cell responses in the metastatic niche. Cancer Res. 2014;74(13):3454–3465. doi:10.1158/0008-5472.CAN-14-015724786787
  • Bonavita E, Gentile S, Rubino M, et al. PTX3 is an extrinsic oncosuppressor regulating complement-dependent inflammation in cancer. Cell. 2015;160(4):700–714. doi:10.1016/j.cell.2015.01.00425679762
  • Ajona D, Ortiz-Espinosa S, Pio R, Lecanda F. Complement in metastasis: a comp in the camp. Front Immunol. 2019;10:669. doi:10.3389/fimmu.2019.0066931001273
  • Markiewski MM, DeAngelis RA, Benencia F, et al. Modulation of the antitumor immune response by complement. Nat Immunol. 2008;9(11):1225–1235. doi:10.1038/ni.165518820683
  • Medler TR, Murugan D, Horton W, et al. Complement C5a fosters squamous carcinogenesis and limits T cell response to chemotherapy. Cancer Cell. 2018;34(4):561–578 e566. doi:10.1016/j.ccell.2018.09.00330300579
  • Wang Y, Sun SN, Liu Q, et al. Autocrine complement inhibits IL10-dependent T-cell-mediated antitumor immunity to promote tumor progression. Cancer Discov. 2016;6(9):1022–1035. doi:10.1158/2159-8290.CD-15-141227297552
  • Gotthardt D, Putz EM, Straka E, et al. Loss of STAT3 in murine NK cells enhances NK cell-dependent tumor surveillance. Blood. 2014;124(15):2370–2379. doi:10.1182/blood-2014-03-56445025185262
  • Johnson DE, O’Keefe RA, Grandis JR. Targeting the IL-6/JAK/STAT3 signalling axis in cancer. Nat Rev Clin Oncol. 2018;15(4):234–248. doi:10.1038/nrclinonc.2018.829405201
  • Crusz SM, Balkwill FR. Inflammation and cancer: advances and new agents. Nat Rev Clin Oncol. 2015;12(10):584–596. doi:10.1038/nrclinonc.2015.10526122183
  • Dai HS, Griffin N, Bolyard C, et al. The Fc domain of immunoglobulin is sufficient to bridge NK cells with virally infected cells. Immunity. 2017;47(1):159–170 e110. doi:10.1016/j.immuni.2017.06.01928723548
  • Aranda F, Buque A, Bloy N, et al. Trial watch: adoptive cell transfer for oncological indications. Oncoimmunology. 2015;4(11):e1046673. doi:10.1080/2162402X.2015.104667326451319
  • Vacchelli E, Aranda F, Bloy N, et al. Trial Watch-Immunostimulation with cytokines in cancer therapy. Oncoimmunology. 2016;5(2):e1115942. doi:10.1080/2162402X.2015.111594227057468
  • Alkins R, Burgess A, Kerbel R, Wels WS, Hynynen K. Early treatment of HER2-amplified brain tumors with targeted NK-92 cells and focused ultrasound improves survival. Neuro-Oncology. 2016;18(7):974–981. doi:10.1093/neuonc/nov31826819443
  • Williams BA, Wang XH, Leyton JV, et al. CD16+NK-92 and anti-CD123 monoclonal antibody prolongs survival in primary human acute myeloid leukemia xenografted mice. Haematologica. 2018;103(10):1720–1729. doi:10.3324/haematol.2017.18738529976748
  • Hao X, Li C, Zhang Y, et al. Programmable chemotherapy and immunotherapy against breast cancer guided by multiplexed fluorescence imaging in the second near-infrared window. adv mater. 2018;30(51):e1804437. doi:10.1002/adma.20180443730357938
  • Morvan MG, Lanier LL. NK cells and cancer: you can teach innate cells new tricks. Nat Rev Cancer. 2016;16(1):7–19. doi:10.1038/nrc.2015.526694935
  • Bhatnagar N, Ahmad F, Hong HS, et al. FcgammaRIII (CD16)-mediated ADCC by NK cells is regulated by monocytes and FcgammaRII (CD32). Eur J Immunol. 2014;44(11):3368–3379. doi:10.1002/eji.20144451525100508
  • Muntasell A, Ochoa MC, Cordeiro L, et al. Targeting NK-cell checkpoints for cancer immunotherapy. Curr Opin Immunol. 2017;45:73–81. doi:10.1016/j.coi.2017.01.00328236750
  • Prager I, Liesche C, van Ooijen H, et al. NK cells switch from granzyme B to death receptor-mediated cytotoxicity during serial killing. J Exp Med. 2019;undefined(undefined):undefined.
  • Lee EK, Jo DH, Kim JH, Yu YS, Kim KW, Kim JH. NK cell-associated antigen expression in retinoblastoma animal model. Cancer Inves. 2013;31(1):67–73. doi:10.3109/07357907.2012.743554
  • Poulaki V, Mitsiades CS, McMullan C, et al. Human retinoblastoma cells are resistant to apoptosis induced by death receptors: role of caspase-8 gene silencing. Invest Ophth Vis Sci. 2005;46(1):358–366. doi:10.1167/iovs.04-0324
  • Madigan MC, Penfold PL, King NJ, Billson FA, Conway RM. Immunoglobulin superfamily expression in primary retinoblastoma and retinoblastoma cell lines. Oncol Res. 2002;13(2):103–111.12392158
  • Hagmann M. A trigger of natural (and other) killers. Science. 1999;285(5428):645, 647. doi:10.1126/science.285.5428.64510454908
  • Graves JD, Kordich JJ, Huang TH, et al. Apo2L/TRAIL and the death receptor 5 agonist antibody AMG 655 cooperate to promote receptor clustering and antitumor activity. Cancer Cell. 2014;26(2):177–189. doi:10.1016/j.ccr.2014.04.02825043603