Evolving treatments in high-risk neuroblastoma

References

• Maris JM, Hogarty MD, Bagatell R, et al. Neuroblastoma. Lancet. 2007;369:2106–2120.
   PubMed Web of Science ®Google Scholar
• London WB, Castleberry RP, Matthay KK, et al. Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children’s Oncology Group. J Clin Oncol. 2005;23:6459–6465.
   Web of Science ®Google Scholar
• Park JR, Bagatell R, London WB, et al. Children’s oncology group’s 2013 blueprint for research: neuroblastoma. Pediatr Blood Cancer. 2013;60:985–993.
   Google Scholar
• Matthay KK, Maris JM, Schleiermacher G, et al. Neuroblastoma. Nat Rev Dis Prim. 2016;2:1-21.
   Web of Science ®Google Scholar
• Irwin MS, Park JR. Neuroblastoma: paradigm for precision medicine. Pediatr Clin North Am. 2015;62:225–256.
   PubMed Web of Science ®Google Scholar
• Cohn SL, Pearson ADJ, London WB, et al. The international neuroblastoma risk group (INRG) classification system: an INRG task force report. J Clin Oncol. 2009;27:289–297.
   Web of Science ®Google Scholar
• Maris JM. Recent advances in neuroblastoma. N Engl J Med. 2010;362:2202–2211.
   PubMed Web of Science ®Google Scholar
• 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;363:1324–1334.
   Web of Science ®Google Scholar
• London WB, Bagatell R, Weigel BJ, et al. Historical time-to-progression (TTP) and progression-free survival (PFS) in relapsed/refractory neuroblastoma modern-era (2002–14) patients from children’s oncology group (COG) early-phase trials. Cancer. 2017;123:4914–4923.
   Web of Science ®Google Scholar
• Peinemann F, Tushabe DA, van Dalen EC, et al. Rapid COJEC versus standard induction therapies for high-risk neuroblastoma. Cochrane Database Syst Rev. 2015;5.
   Web of Science ®Google Scholar
• Amoroso L, Erminio G, Makin G, et al. Topotecan-vincristine-doxorubicin in stage 4 high-risk neuroblastoma patients failing to achieve a complete metastatic response to rapid COJEC: A SIOPEN study. Cancer Res Treat. 2018;50:148–155.
   PubMed Web of Science ®Google Scholar
• Matthay KK, Villablanca JG, Seeger RC, et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis -retinoic acid. N Engl J Med. 1999;341:1165–1173.
   PubMed Web of Science ®Google Scholar
• Berthold F, Boos J, Burdach S, et al. Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: A randomised controlled trial. Lancet Oncol. 2005;6:649–658.
   Web of Science ®Google Scholar
• Ladenstein R, Pötschger U, Pearson ADJ, et al. Busulfan and melphalan versus carboplatin, etoposide, and melphalan as high-dose chemotherapy for high-risk neuroblastoma (HR-NBL1/SIOPEN): an international, randomised, multi-arm, open-label, phase 3 trial. Lancet Oncol. 2017;18:500–514.
   PubMed Web of Science ®Google Scholar
• Park JR, Kreissman SG, London WB, et al. Effect of tandem autologous stem cell transplant vs single transplant on event-free survival in patients with high-risk neuroblastoma: A randomized clinical trial. J Am Med Assoc. 2019;322:746.
   Web of Science ®Google Scholar
• Suh JK, Koh KN, Min SY, et al. Feasibility and effectiveness of treatment strategy of tandem high-dose chemotherapy and autologous stem cell transplantation in combination with 131 I-MIBG therapy for high-risk neuroblastoma. Pediatr Transplant. 2020;24:1-8.
   Web of Science ®Google Scholar
• Sharp SE, Trout AT, Weiss BD, et al. MIBG in neuroblastoma diagnostic imaging and therapy. Radiographics. 2016;36:258–278.
   PubMed Web of Science ®Google Scholar
• Matthay KK, Yanik G, Messina J, et al. Phase II study on the effect of disease sites, age, and prior therapy on response to iodine-131-metaiodobenzylguanidine therapy in refractory neuroblastoma. J Clin Oncol. 2007;25:1054–1060.
   PubMed Web of Science ®Google Scholar
• DuBois SG, Matthay KK. Radiolabeled metaiodobenzylguanidine for the treatment of neuroblastoma. Nucl Med Biol. 2008;35:S35-S48.
   PubMed Web of Science ®Google Scholar
• Dubois SG, Matthay KK. 131I-Metaiodobenzylguanidine therapy in children with advanced neuroblastoma. Q J Nucl Med Mol Imaging. 2013;57:53–65.
   PubMed Web of Science ®Google Scholar
• Clement SC, van Eck-smit BLF, van Trotsenburg ASP, et al. Long-term follow-up of the thyroid gland after treatment with 131 I-Metaiodobenzylguanidine in children with neuroblastoma: importance of continuous surveillance. Pediatr Blood Cancer. 2013;60:1833–1838.
   PubMed Web of Science ®Google Scholar
• Matthay KK, Reynolds CP, Seeger RC, et al. 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;27:1007–1013.
   Web of Science ®Google Scholar
• Reynolds CP, Wang Y, Melton LJ, et al. Retinoic-acid-resistant neuroblastoma cell lines show altered MYC regulation and high sensitivity to fenretinide. Med Pediatr Oncol. 2000;35:597–602.
   Google Scholar
• Peinemann F, van Dalen EC, Enk H, et al. Retinoic acid postconsolidation therapy for high-risk neuroblastoma patients treated with autologous haematopoietic stem cell transplantation. Cochrane Database Syst Rev. 2017;8.
   Web of Science ®Google Scholar
• Sait S, Modak S. Anti-GD2 immunotherapy for neuroblastoma. Expert Rev Anticancer Ther. 2017;17: 889–904.
   PubMed Web of Science ®Google Scholar
• Pennington B, Ren S, Barton S, et al. Dinutuximab beta for treating neuroblastoma: an evidence review group and decision support unit perspective of a NICE single technology appraisal. Pharmacoeconomics. 2019;37:985–993.
   Web of Science ®Google Scholar
• Heukamp LC, Thor T, Schramm A, et al. Targeted expression of mutated ALK induces neuroblastoma in transgenic mice. Sci Transl Med. 2012;4:141ra91–141ra91.
   PubMed Web of Science ®Google Scholar
• Huang M, Weiss WA. Neuroblastoma and MYCN. Cold Spring Harb Perspect Med. 2013;3:a014415-a014415.
   PubMed Web of Science ®Google Scholar
• Schulte JH, Lindner S, Bohrer A, et al. MYCN and ALKF1174L are sufficient to drive neuroblastoma development from neural crest progenitor cells. Oncogene. 2013;32:1059–1065.
   Web of Science ®Google Scholar
• Sasaki T, Okuda K, Zheng W, et al. The neuroblastoma-associated F1174L ALK mutation causes resistance to an ALK kinase inhibitor in ALK-translocated cancers. Cancer Res. 2010;70:10038–10043.
   Web of Science ®Google Scholar
• Umapathy G, Mendoza-Garcia P, Hallberg B, et al. Targeting anaplastic lymphoma kinase in neuroblastoma. APMIS. 2019;127:288–302.
   PubMed Web of Science ®Google Scholar
• Zhu S, Lee JS, Guo F, et al. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell. 2012;21:362–373.
   PubMed Web of Science ®Google Scholar
• Bosse KR, Maris JM. Advances in the translational genomics of neuroblastoma: from improving risk stratification and revealing novel biology to identifying actionable genomic alterations. Cancer. 2016;122:20-33.
   Web of Science ®Google Scholar
• Bown N, Cotterill S, Łastowska M, et al. Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med. 1999;340:1954–1961.
   PubMed Web of Science ®Google Scholar
• Attiyeh EF, London WB, Mossé YP, et al. Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med. 2005;353:2243–2253.
   PubMed Web of Science ®Google Scholar
• Valentijn LJ, Koster J, Zwijnenburg DA, et al. TERT rearrangements are frequent in neuroblastoma and identify aggressive tumors. Nat Genet. 2015;47:1411–1414.
   PubMed Web of Science ®Google Scholar
• Hertwig F, Peifer M, Fischer M. Telomere maintenance is pivotal for high-risk neuroblastoma. Cell Cycle. 2016;15:311–312.
   PubMed Web of Science ®Google Scholar
• Yu EY, Cheung IY, Feng Y, et al. Telomere trimming and DNA damage as signatures of high risk neuroblastoma. Neoplasia (United States). 2019;21:689–701.
   Google Scholar
• Suzuki M, Cheung NKV. Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin Ther Targets. 2015;19:349–362.
   PubMed Web of Science ®Google Scholar
• Modak S, Cheung NKV. Disialoganglioside directed immunotherapy of neuroblastoma. Cancer Invest. 2007;25:67–77.
   PubMed Web of Science ®Google Scholar
• Sadelain M, Brentjens R, Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3:388–398.
   PubMed Web of Science ®Google Scholar
• Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118:6050–6056.
   PubMed Web of Science ®Google Scholar
• Thomas S, Straathof K, Himoudi N, et al. An optimized GD2-targeting retroviral cassette for more potent and safer cellular therapy of neuroblastoma and other cancers. PLoS One. 2016;11:e0152196.
   Web of Science ®Google Scholar
• DeRenzo C, Krenciute G, Gottschalk S. The landscape of CAR T cells beyond acute lymphoblastic leukemia for pediatric solid tumors. Am Soc Clin Oncol Educ B. 2018;830–837. DOI:10.1200/EDBK_200773
   PubMedGoogle Scholar
• Asgharzadeh S, Salo JA, Ji L, et al. Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol. 2012;30:3525–3532.
   PubMed Web of Science ®Google Scholar
• Kushner BH, Cheung IY, Modak S, et al. Phase i trial of a bivalent gangliosides vaccine in combination with β-glucan for high-risk neuroblastoma in second or later remission. Clin Cancer Res. 2014;20:1375–1382.
   Web of Science ®Google Scholar
• Becker R, Eichler MK, Jennemann R, et al. Phase I clinical trial on adjuvant active immunotherapy of human gliomas with GD2-conjugate. Br J Neurosurg. 2002;16:269–275.
   PubMed Web of Science ®Google Scholar
• Mond JJ, Lees A, Snapper CM. T cell-independent antigens type 2. Annu Rev Immunol. 1995;13:655–692.
   PubMed Web of Science ®Google Scholar
• Bhattacharya-Chatterjee M, Chatterjee SK, Foon KA. Anti-idiotype vaccine against cancer. Immunol Lett. 2000;74:51–58.
   PubMed Web of Science ®Google Scholar
• Herlyn D, Somasundaram R, Li W, et al. Anti-idiotype cancer vaccines: past and future. Cancer Immunol Immunother. 1996;43:65–76.
   PubMed Web of Science ®Google Scholar
• Eger C, Siebert N, Seidel D, et al. Generation and characterization of a human/mouse chimeric GD2-mimicking anti-idiotype antibody ganglidiximab for active immunotherapy against neuroblastoma. PLoS One. 2016;11:e0150479.
   PubMed Web of Science ®Google Scholar
• Van Heek-Romanowski R, Ptter S, Trarbach T, et al. Disialoganglioside GD2 loss following monoclonal antibody therapy is rare in neuroblastoma. Med Pediatr Oncol. 2001;36:197–198.
   PubMedGoogle Scholar
• Schumacher-Kuckelkorn R, Volland R, Gradehandt A, et al. Lack of immunocytological GD2 expression on neuroblastoma cells in bone marrow at diagnosis, during treatment, and at recurrence. Pediatr Blood Cancer. 2017;64:46–56.
   PubMed Web of Science ®Google Scholar
• Terzic T, Cordeau M, Herblot S, et al. Expression of disialoganglioside (GD2) in neuroblastic tumors: a prognostic value for patients treated with anti-GD2 immunotherapy. Pediatr Dev Pathol. 2018;21:355–362.
   PubMed Web of Science ®Google Scholar
• Balis FM, Busch CM, Desai AV, et al. The ganglioside GD2 as a circulating tumor biomarker for neuroblastoma. Pediatr Blood Cancer. 2020;67:1-6.
   Web of Science ®Google Scholar
• Valentino L, Moss T, Olson E, et al. Shed tumor gangliosides and progression of human neuroblastoma. Blood. 1990;75:1564–1567.
   PubMed Web of Science ®Google Scholar
• Federico SM, McCarville MB, Shulkin BL, et al. A pilot trial of humanized anti-GD2 monoclonal antibody (hu14.18K322A) with chemotherapy and natural killer cells in children with recurrent/refractory neuroblastoma. Clin Cancer Res. 2017;23:6441–6449.
   PubMed Web of Science ®Google Scholar
• Furman WL, Federico SM, McCarville MB, et al. A phase II trial of Hu14.18K322A in combination with induction chemotherapy in children with newly diagnosed high-risk neuroblastoma. Clin Cancer Res. 2019;25:6320–6328.
   PubMed Web of Science ®Google Scholar
• van den Bijgaart RJE, Kroesen M, Wassink M, et al. Combined sialic acid and histone deacetylase (HDAC) inhibitor treatment up-regulates the neuroblastoma antigen GD2. J Biol Chem. 2019;294:4437–4449.
   PubMed Web of Science ®Google Scholar
• Rettig I, Koeneke E, Trippel F, et al. Selective inhibition of HDAC8 decreases neuroblastoma growth in vitro and in vivo and enhances retinoic acid-mediated differentiation. Cell Death Dis. 2015;6:e1657-e1657.
   PubMed Web of Science ®Google Scholar
• Thompson PA, Drissi R, Muscal JA, et al. A phase I trial of imetelstat in children with refractory or recurrent solid tumors: A children’s oncology group phase I consortium study (ADVL1112). Clin Cancer Res. 2013;19:6578–6584.
   Web of Science ®Google Scholar
• Salloum R, Hummel TR, Kumar SS, et al. A molecular biology and phase II study of imetelstat (GRN163L) in children with recurrent or refractory central nervous system malignancies: a pediatric brain tumor consortium study. J Neurooncol. 2016;129:443–451.
   PubMed Web of Science ®Google Scholar
• Johnsen JI, Dyberg C, Fransson S, et al. Molecular mechanisms and therapeutic targets in neuroblastoma. Pharmacol Res. 2018;131:164–176.
   PubMed Web of Science ®Google Scholar
• Bassiri H, Benavides A, Haber M, et al. Translational development of difluoromethylornithine (DFMO) for the treatment of neuroblastoma. Transl Pediatr. 2015;4:226–238.
   PubMed Web of Science ®Google Scholar
• LoGiudice N, Le L, Abuan I, et al. Alpha-difluoromethylornithine, an irreversible inhibitor of polyamine biosynthesis, as a therapeutic strategy against hyperproliferative and infectious diseases. Med Sci. 2018;6:1-17.
   Google Scholar
• Hogarty MD, Norris MD, Davis K, et al. ODC1 is a critical determinant of MYCN oncogenesis and a therapeutic target in neuroblastoma. Cancer Res. 2008;68:9735–9745.
   PubMed Web of Science ®Google Scholar
• Sholler GLS, Gerner EW, Bergendahl G, et al. A phase I trial of DFMO targeting polyamine addiction in patients with relapsed/refractory neuroblastoma. PLoS One. 2015;10:1-20.
   Web of Science ®Google Scholar
• Puissant A, Frumm SM, Alexe G, et al. Targeting MYCN in neuroblastoma by BET bromodomain inhibition. Cancer Discov. 2013;3:308–323.
   PubMed Web of Science ®Google Scholar
• Lee S, Rellinger EJ, Kim KW, et al. Bromodomain and extraterminal inhibition blocks tumor progression and promotes differentiation in neuroblastoma. Surg (United States). 2015;158:819-826.
   Google Scholar
• Henssen A, Althoff K, Odersky A, et al. Targeting MYCN-driven transcription by BET-bromodomain inhibition. Clin Cancer Res. 2016;22:2470–2481.
   PubMed Web of Science ®Google Scholar
• Jin Z, Lu Y, Wu Y, et al. Development of differentiation modulators and targeted agents for treating neuroblastoma. Eur J Med Chem. 2020;207:112818.
   Web of Science ®Google Scholar
• Richards MW, Burgess SG, Poon E, et al. Structural basis of N-Myc binding by Aurora-A and its destabilization by kinase inhibitors. Proc Natl Acad Sci U S A. 2016;113:13726–13731.
   Web of Science ®Google Scholar
• Brockmann M, Poon E, Berry T, et al. Small molecule inhibitors of Aurora-A induce proteasomal degradation of N-Myc in childhood neuroblastoma. Cancer Cell. 2013;24:75–89.
   PubMed Web of Science ®Google Scholar
• Maris JM, Morton CL, Gorlick R, et al. Initial testing of the Aurora kinase a inhibitor MLN8237 by the pediatric preclinical testing program (PPTP). Pediatr Blood Cancer. 2010;55:26-34.
   Google Scholar
• Felgenhauer J, Tomino L, Selich-Anderson J, et al. Dual BRD4 and AURKA inhibition is synergistic against MYCN-amplified and nonamplified neuroblastoma. Neoplasia (United States). 2018;20:965–974.
   Google Scholar
• DuBois SG, Marachelian A, Fox E, et al. Phase I study of the aurora A kinase inhibitor alisertib in combination with irinotecan and temozolomide for patients with relapsed or refractory neuroblastoma: A nant (new approaches to neuroblastoma therapy) trial. J Clin Oncol. 2016;34:1368–1375.
   Web of Science ®Google Scholar
• DuBois SG, Mosse YP, Fox E, et al. Phase II trial of alisertib in combination with irinotecan and temozolomide for patients with relapsed or refractory neuroblastoma. Clin Cancer Res. 2018;24:6142–6149.
   PubMed Web of Science ®Google Scholar
• Guan J, Tucker ER, Wan H, et al. The ALK inhibitor PF-06463922 is effective as a single agent in neuroblastoma driven by expression of ALK and MYCN. DMM Dis Model Mech. 2016;9:941–952.
   PubMed Web of Science ®Google Scholar
• Infarinato NR, Park JH, Krytska K, et al. The ALK/ROS1 inhibitor PF-06463922 overcomes primary resistance to crizotinib in ALK-driven neuroblastoma. Cancer Discov. 2016;6:96–107.
   PubMed Web of Science ®Google Scholar
• Alam MW, Borenäs M, Lind DE, et al. Alectinib, an anaplastic lymphoma kinase inhibitor, abolishes ALK activity and growth in ALK-positive neuroblastoma cells. Front Oncol. 2019;9:1-12.
   Web of Science ®Google Scholar
• Chicard M, Boyault S, Daage LC, et al. Genomic copy number profiling using circulating free tumor DNA highlights heterogeneity in neuroblastoma. Clin Cancer Res. 2016;22:5564–5573.
   PubMed Web of Science ®Google Scholar
• Ou S-HI, Nagasaka M, Zhu VW. Liquid biopsy to identify actionable genomic alterations. Am Soc Clin Oncol Educ B. 2018;978–997. DOI:10.1200/EDBK_199765
   PubMedGoogle Scholar
• Van Roy N, Van Der Linden M, Menten B, et al. Shallow whole genome sequencing on circulating cell-free DNA allows reliable noninvasive copy-number profiling in neuroblastoma patients. Clin Cancer Res. 2017;23:6305–6314.
   PubMed Web of Science ®Google Scholar
• Chicard M, Colmet-Daage L, Clement N, et al. Whole-exome sequencing of cell-free DNA reveals temporo-spatial heterogeneity and identifies treatment-resistant clones in neuroblastoma. Clin Cancer Res. 2018;24:939–949.
   PubMed Web of Science ®Google Scholar