Dendritic Cell-Based and Other Vaccination Strategies for Pediatric Cancer

Sévérine de Bruijn, Sébastien Anguille, Joris Verlooy, Evelien L Smits, Viggo F van Tendeloo, Maxime de Laere, Koenraad Norga, Zwi N Berneman, Eva Lion, Sévérine de Bruijn, Sébastien Anguille, Joris Verlooy, Evelien L Smits, Viggo F van Tendeloo, Maxime de Laere, Koenraad Norga, Zwi N Berneman, Eva Lion

Abstract

Dendritic cell-based and other vaccination strategies that use the patient's own immune system for the treatment of cancer are gaining momentum. Most studies of therapeutic cancer vaccination have been performed in adults. However, since cancer is one of the leading causes of death among children past infancy in the Western world, the hope is that this form of active specific immunotherapy can play an important role in the pediatric population as well. Since children have more vigorous and adaptable immune systems than adults, therapeutic cancer vaccines are expected to have a better chance of creating protective immunity and preventing cancer recurrence in pediatric patients. Moreover, in contrast to conventional cancer treatments such as chemotherapy, therapeutic cancer vaccines are designed to specifically target tumor cells and not healthy cells or tissues. This reduces the likelihood of side effects, which is an important asset in this vulnerable patient population. In this review, we present an overview of the different therapeutic cancer vaccines that have been studied in the pediatric population, with a main focus on dendritic cell-based strategies. In addition, new approaches that are currently being investigated in clinical trials are discussed to provide guidance for further improvement and optimization of pediatric cancer vaccines.

Keywords: dendritic cells; immunotherapy; pediatric cancer; tumor vaccination.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Mechanistic principles of anti-cancer vaccination. The most important types of tumor vaccines are dendritic cell (DC), tumor cell (TC), and peptide vaccines. The common mechanism of action for all tumor vaccines is the induction of tumor antigen-specific cytotoxic T-lymphocytes (CTLs). These CTLs are capable of recognizing and killing TCs that express tumor antigen fragments, designated peptides, on their cell surface in the context of major histocompatibility complex (MHC) molecules. The recognition of the peptide/MHC is conferred by the T-cell receptor (TCR). (A) DCs are professional antigen-presenting cells (APCs) and are thus highly equipped to induce tumor antigen-specific CTLs. DCs, either from autologous or allogeneic origin, can be loaded with antigenic material through different ways (e.g., by pulsing with peptides, or with TC lysates). These tumor-antigen loaded DCs are usually administered in combination with immune adjuvants for improved immune stimulation. (B) Autologous or allogeneic TCs, inactivated (inact.) by lysis, can also be used in combination with immune adjuvants to induce tumor antigen-specific CTLs, which are in turn capable of killing TCs that express the corresponding tumor antigenic peptide(s). (C) Peptides, administered together with immune adjuvants, are also being used for therapeutic cancer vaccination purposes. Peptide vaccine-based approaches rely on the presence of functionally competent APCs in vivo for effective stimulation of a CTL immune response.

References

    1. National Cancer Institute A Snapshot of Adolescent and Young Adult Cancers. [(accessed on 1 September 2019)]; Available online: .
    1. Cancer Research UK Young People’s Cancer Statistics. [(accessed on 1 September 2019)]; Available online: .
    1. Siegel R.L., Miller K.D., Jemal A. Cancer statistics, 2019. CA Cancer J. Clin. 2019;69:7–34. doi: 10.3322/caac.21551.
    1. Hegde M., Moll A.J., Byrd T.T., Louis C.U., Ahmed N. Cellular immunotherapy for pediatric solid tumors. Cytotherapy. 2015;17:3–17. doi: 10.1016/j.jcyt.2014.05.019.
    1. Choi D.K., Helenowski I., Hijiya N. Secondary malignancies in pediatric cancer survivors: Perspectives and review of the literature. Int. J. Cancer. 2014;135:1764–1773. doi: 10.1002/ijc.28991.
    1. Guinipero T., Finn O.J. Cancer vaccines: Emphasis on pediatric cancers. Curr. Pharm. Des. 2010;16:292–299. doi: 10.2174/138161210790170148.
    1. Anguille S., Smits E.L., Bryant C., Van Acker H.H., Goossens H., Lion E., Fromm P.D., Hart D.N., Van Tendeloo V.F., Berneman Z.N. Dendritic cells as pharmacological tools for cancer immunotherapy. Pharmacol. Rev. 2015;67:731–753. doi: 10.1124/pr.114.009456.
    1. Anguille S., Smits E.L., Lion E., van Tendeloo V.F., Berneman Z.N. Clinical use of dendritic cells for cancer therapy. Lancet Oncol. 2014;15:e257–e267. doi: 10.1016/S1470-2045(13)70585-0.
    1. Mackall C.L., Merchant M.S., Fry T.J. Immune-based therapies for childhood cancer. Nat. Rev. Clin. Oncol. 2014;11:693–703. doi: 10.1038/nrclinonc.2014.177.
    1. Melief C.J., van Hall T., Arens R., Ossendorp F., van der Burg S.H. Therapeutic cancer vaccines. J. Clin. Investig. 2015;125:3401–3412. doi: 10.1172/JCI80009.
    1. Ceppi F., Beck-Popovic M., Bourquin J.P., Renella R. Opportunities and challenges in the immunological therapy of pediatric malignancy: A concise snapshot. Eur. J. Pediatr. 2017;176:1163–1172. doi: 10.1007/s00431-017-2982-0.
    1. Galluzzi L., Vacchelli E., Bravo-San Pedro J.M., Buque A., Senovilla L., Baracco E.E., Bloy N., Castoldi F., Abastado J.P., Agostinis P., et al. Classification of current anticancer immunotherapies. Oncotarget. 2014;5:12472–12508. doi: 10.18632/oncotarget.2998.
    1. Banchereau J., Palucka K. Immunotherapy: Cancer vaccines on the move. Nat. Rev. Clin. Oncol. 2018;15:9–10. doi: 10.1038/nrclinonc.2017.149.
    1. Van Acker H.H., Versteven M., Lichtenegger F.S., Roex G., Campillo-Davo D., Lion E., Subklewe M., Van Tendeloo V.F., Berneman Z.N., Anguille S. Dendritic cell-based immunotherapy of acute myeloid leukemia. J. Clin. Med. 2019;8:579. doi: 10.3390/jcm8050579.
    1. Capitini C.M., Mackall C.L., Wayne A.S. Immune-based therapeutics for pediatric cancer. Expert Opin. Biol. Ther. 2010;10:163–178. doi: 10.1517/14712590903431022.
    1. McDowell K.A., Hank J.A., DeSantes K.B., Capitini C.M., Otto M., Sondel P.M. NK cell-based immunotherapies in pediatric oncology. J. Pediatr. Hematol. Oncol. 2015;37:79–93. doi: 10.1097/MPH.0000000000000303.
    1. Wayne A.S., Capitini C.M., Mackall C.L. Immunotherapy of childhood cancer: From biologic understanding to clinical application. Curr. Opin. Pediatr. 2010;22:2–11. doi: 10.1097/MOP.0b013e3283350d3e.
    1. Fangusaro J. Pediatric high grade glioma: A review and update on tumor clinical characteristics and biology. Front. Oncol. 2012;2:105. doi: 10.3389/fonc.2012.00105.
    1. Guo C., Manjili M.H., Subjeck J.R., Sarkar D., Fisher P.B., Wang X.Y. Therapeutic cancer vaccines: Past, present, and future. Adv. Cancer Res. 2013;119:421–475.
    1. Liu J.K. Anti-cancer vaccines—A one-hit wonder? Yale J. Biol. Med. 2014;87:481–489.
    1. Khatua S., Sadighi Z.S., Pearlman M.L., Bochare S., Vats T.S. Brain tumors in children—Current therapies and newer directions. Indian J. Pediatr. 2012;79:922–927. doi: 10.1007/s12098-012-0689-9.
    1. Wells E.M., Packer R.J. Pediatric brain tumors. Continuum (Minneap Minn) 2015;21:373–396. doi: 10.1212/01.CON.0000464176.96311.d1.
    1. Mallhi K., Lum L.G., Schultz K.R., Yankelevich M. Hematopoietic cell transplantation and cellular therapeutics in the treatment of childhood malignancies. Pediatr. Clin. N. Am. 2015;62:257–273. doi: 10.1016/j.pcl.2014.10.001.
    1. Lion E., Smits E.L., Berneman Z.N., Van Tendeloo V.F. NK cells: Key to success of DC-based cancer vaccines? Oncologist. 2012;17:1256–1270. doi: 10.1634/theoncologist.2011-0122.
    1. Van Acker H.H., Anguille S., Van Tendeloo V.F., Lion E. Empowering gamma delta T cells with antitumor immunity by dendritic cell-based immunotherapy. Oncoimmunology. 2015;4:e1021538. doi: 10.1080/2162402X.2015.1021538.
    1. Caruso D.A., Orme L.M., Neale A.M., Radcliff F.J., Amor G.M., Maixner W., Downie P., Hassall T.E., Tang M.L., Ashley D.M. Results of a phase 1 study utilizing monocyte-derived dendritic cells pulsed with tumor RNA in children and young adults with brain cancer. Neuro Oncol. 2004;6:236–246. doi: 10.1215/S1152851703000668.
    1. Himoudi N., Wallace R., Parsley K.L., Gilmour K., Barrie A.U., Howe K., Dong R., Sebire N.J., Michalski A., Thrasher A.J., et al. Lack of T-cell responses following autologous tumour lysate pulsed dendritic cell vaccination, in patients with relapsed osteosarcoma. Clin. Transl. Oncol. 2012;14:271–279. doi: 10.1007/s12094-012-0795-1.
    1. Lasky J.L., 3rd, Panosyan E.H., Plant A., Davidson T., Yong W.H., Prins R.M., Liau L.M., Moore T.B. Autologous tumor lysate-pulsed dendritic cell immunotherapy for pediatric patients with newly diagnosed or recurrent high-grade gliomas. Anticancer Res. 2013;33:2047–2056.
    1. Felzmann T., Witt V., Wimmer D., Ressmann G., Wagner D., Paul P., Huttner K., Fritsch G. Monocyte enrichment from leukapharesis products for the generation of DCs by plastic adherence, or by positive or negative selection. Cytotherapy. 2003;5:391–398. doi: 10.1080/14653240310003053.
    1. Barth R.J., Jr., Mule J.J., Spiess P.J., Rosenberg S.A. Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. J. Exp. Med. 1991;173:647–658. doi: 10.1084/jem.173.3.647.
    1. Mohme M., Neidert M.C., Regli L., Weller M., Martin R. Immunological challenges for peptide-based immunotherapy in glioblastoma. Cancer Treat. Rev. 2014;40:248–258. doi: 10.1016/j.ctrv.2013.08.008.
    1. de Vries I.J., Lesterhuis W.J., Barentsz J.O., Verdijk P., van Krieken J.H., Boerman O.C., Oyen W.J., Bonenkamp J.J., Boezeman J.B., Adema G.J., et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol. 2005;23:1407–1413. doi: 10.1038/nbt1154.
    1. Hegde M., Bielamowicz K.J., Ahmed N. Novel approaches and mechanisms of immunotherapy for glioblastoma. Discov. Med. 2014;17:145–154.
    1. Tuyaerts S., Aerts J.L., Corthals J., Neyns B., Heirman C., Breckpot K., Thielemans K., Bonehill A. Current approaches in dendritic cell generation and future implications for cancer immunotherapy. Cancer Immunol. Immunother. 2007;56:1513–1537. doi: 10.1007/s00262-007-0334-z.
    1. Benitez-Ribas D., Cabezon R., Florez-Grau G., Molero M.C., Puerta P., Guillen A., Paco S., Carcaboso A.M., Santa-Maria Lopez V., Cruz O., et al. Immune response generated with the administration of autologous dendritic cells pulsed with an allogenic tumoral cell-lines lysate in patients with newly diagnosed diffuse intrinsic pontine glioma. Front. Oncol. 2018;8:127. doi: 10.3389/fonc.2018.00127.
    1. Dagher R., Long L.M., Read E.J., Leitman S.F., Carter C.S., Tsokos M., Goletz T.J., Avila N., Berzofsky J.A., Helman L.J., et al. Pilot trial of tumor-specific peptide vaccination and continuous infusion interleukin-2 in patients with recurrent Ewing sarcoma and alveolar rhabdomyosarcoma: An inter-institute NIH study. Med. Pediatr. Oncol. 2002;38:158–164. doi: 10.1002/mpo.1303.
    1. Mackall C.L., Rhee E.H., Read E.J., Khuu H.M., Leitman S.F., Bernstein D., Tesso M., Long L.M., Grindler D., Merino M., et al. A pilot study of consolidative immunotherapy in patients with high-risk pediatric sarcomas. Clin. Cancer Res. 2008;14:4850–4858. doi: 10.1158/1078-0432.CCR-07-4065.
    1. Krishnadas D.K., Shusterman S., Bai F., Diller L., Sullivan J.E., Cheerva A.C., George R.E., Lucas K.G. A phase I trial combining decitabine/dendritic cell vaccine targeting MAGE-A1, MAGE-A3 and NY-ESO-1 for children with relapsed or therapy-refractory neuroblastoma and sarcoma. Cancer Immunol. Immunother. 2015;64:1251–1260. doi: 10.1007/s00262-015-1731-3.
    1. Saito S., Yanagisawa R., Yoshikawa K., Higuchi Y., Koya T., Yoshizawa K., Tanaka M., Sakashita K., Kobayashi T., Kurata T., et al. Safety and tolerability of allogeneic dendritic cell vaccination with induction of Wilms tumor 1-specific T cells in a pediatric donor and pediatric patient with relapsed leukemia: A case report and review of the literature. Cytotherapy. 2015;17:330–335.
    1. Shah N.N., Loeb D.M., Khuu H., Stroncek D., Ariyo T., Raffeld M., Delbrook C., Mackall C.L., Wayne A.S., Fry T.J. Induction of immune response after allogeneic Wilms’ tumor 1 dendritic cell vaccination and donor lymphocyte infusion in patients with hematologic malignancies and post-transplantation relapse. Biol. Blood Marrow Transplant. 2016;22:2149–2154. doi: 10.1016/j.bbmt.2016.08.028.
    1. Hashii Y., Sato E., Ohta H., Oka Y., Sugiyama H., Ozono K. WT1 peptide immunotherapy for cancer in children and young adults. Pediatr. Blood Cancer. 2010;55:352–355. doi: 10.1002/pbc.22522.
    1. Hashii Y., Sato-Miyashita E., Matsumura R., Kusuki S., Yoshida H., Ohta H., Hosen N., Tsuboi A., Oji Y., Oka Y., et al. WT1 peptide vaccination following allogeneic stem cell transplantation in pediatric leukemic patients with high risk for relapse: Successful maintenance of durable remission. Leukemia. 2012;26:530–532. doi: 10.1038/leu.2011.226.
    1. Anguille S., Fujiki F., Smits E.L., Oji Y., Lion E., Oka Y., Berneman Z.N., Sugiyama H. Identification of a Wilms’ tumor 1-derived immunogenic CD4(+) T-cell epitope that is recognized in the context of common Caucasian HLA-DR haplotypes. Leukemia. 2013;27:748–750. doi: 10.1038/leu.2012.248.
    1. Anguille S., Van Tendeloo V.F., Berneman Z.N. Leukemia-associated antigens and their relevance to the immunotherapy of acute myeloid leukemia. Leukemia. 2012;26:2186–2196. doi: 10.1038/leu.2012.145.
    1. Anguille S., Van de Velde A.L., Smits E.L., Van Tendeloo V.F., Juliusson G., Cools N., Nijs G., Stein B., Lion E., Van Driessche A., et al. Dendritic cell vaccination as postremission treatment to prevent or delay relapse in acute myeloid leukemia. Blood. 2017;130:1713–1721. doi: 10.1182/blood-2017-04-780155.
    1. De Vleeschouwer S., Fieuws S., Rutkowski S., Van Calenbergh F., Van Loon J., Goffin J., Sciot R., Wilms G., Demaerel P., Warmuth-Metz M., et al. Postoperative adjuvant dendritic cell-based immunotherapy in patients with relapsed glioblastoma multiforme. Clin. Cancer Res. 2008;14:3098–3104. doi: 10.1158/1078-0432.CCR-07-4875.
    1. Merchant M.S., Bernstein D., Amoako M., Baird K., Fleisher T.A., Morre M., Steinberg S.M., Sabatino M., Stroncek D.F., Venkatasan A.M., et al. Adjuvant immunotherapy to improve outcome in high-risk pediatric sarcomas. Clin. Cancer Res. 2016;22:3182–3191. doi: 10.1158/1078-0432.CCR-15-2550.
    1. Dohnal A.M., Witt V., Hugel H., Holter W., Gadner H., Felzmann T. Phase I study of tumor Ag-loaded IL-12 secreting semi-mature DC for the treatment of pediatric cancer. Cytotherapy. 2007;9:755–770. doi: 10.1080/14653240701589221.
    1. Ridolfi R., Riccobon A., Galassi R., Giorgetti G., Petrini M., Fiammenghi L., Stefanelli M., Ridolfi L., Moretti A., Migliori G., et al. Evaluation of in vivo labelled dendritic cell migration in cancer patients. J. Transl. Med. 2004;2:27. doi: 10.1186/1479-5876-2-27.
    1. Geiger J.D., Hutchinson R.J., Hohenkirk L.F., McKenna E.A., Yanik G.A., Levine J.E., Chang A.E., Braun T.M., Mule J.J. Vaccination of pediatric solid tumor patients with tumor lysate-pulsed dendritic cells can expand specific T cells and mediate tumor regression. Cancer Res. 2001;61:8513–8519.
    1. Rutkowski S., De Vleeschouwer S., Kaempgen E., Wolff J.E., Kuhl J., Demaerel P., Warmuth-Metz M., Flamen P., Van Calenbergh F., Plets C., et al. Surgery and adjuvant dendritic cell-based tumour vaccination for patients with relapsed malignant glioma, a feasibility study. Br. J. Cancer. 2004;91:1656–1662. doi: 10.1038/sj.bjc.6602195.
    1. Suminoe A., Matsuzaki A., Hattori H., Koga Y., Hara T. Immunotherapy with autologous dendritic cells and tumor antigens for children with refractory malignant solid tumors. Pediatr. Transplant. 2009;13:746–753. doi: 10.1111/j.1399-3046.2008.01066.x.
    1. Bai Y., Zheng J.E., Wang N., Cai H.H., Zhai L.N., Wu Y.H., Wang F., Jin R.M., Zhou D.F. Effects of dendritic cell-activated and cytokine-induced killer cell therapy on 22 children with acute myeloid leukemia after chemotherapy. J. Huazhong Univ. Sci. Technol. Med. Sci. 2015;35:689–693. doi: 10.1007/s11596-015-1491-5.
    1. Anguille S., Van Acker H.H., Van den Bergh J., Willemen Y., Goossens H., Van Tendeloo V.F., Smits E.L., Berneman Z.N., Lion E. Interleukin-15 dendritic cells harness NK cell cytotoxic effector function in a contact- and IL-15-dependent manner. PLoS ONE. 2015;10:e0123340. doi: 10.1371/journal.pone.0123340.
    1. Van Elssen C.H., Oth T., Germeraad W.T., Bos G.M., Vanderlocht J. Natural killer cells: The secret weapon in dendritic cell vaccination strategies. Clin. Cancer Res. 2014;20:1095–1103. doi: 10.1158/1078-0432.CCR-13-2302.
    1. Ardon H., De Vleeschouwer S., Van Calenbergh F., Claes L., Kramm C.M., Rutkowski S., Wolff J.E., Van Gool S.W. Adjuvant dendritic cell-based tumour vaccination for children with malignant brain tumours. Pediatr. Blood Cancer. 2010;54:519–525. doi: 10.1002/pbc.22319.
    1. Hollingsworth R.E., Jansen K. Turning the corner on therapeutic cancer vaccines. NPJ Vaccines. 2019;4:7. doi: 10.1038/s41541-019-0103-y.
    1. Schlom J., Hodge J.W., Palena C., Tsang K.Y., Jochems C., Greiner J.W., Farsaci B., Madan R.A., Heery C.R., Gulley J.L. Therapeutic cancer vaccines. Adv. Cancer Res. 2014;121:67–124.
    1. Maris J.M., Hogarty M.D., Bagatell R., Cohn S.L. Neuroblastoma. Lancet. 2007;369:2106–2120. doi: 10.1016/S0140-6736(07)60983-0.
    1. Dumba M., Jawad N., McHugh K. Neuroblastoma and nephroblastoma: A radiological review. Cancer Imaging. 2015;15:5. doi: 10.1186/s40644-015-0040-6.
    1. Rousseau R.F., Brenner M.K. Vaccine therapies for pediatric malignancies. Cancer J. 2005;11:331–339. doi: 10.1097/00130404-200507000-00009.
    1. Bowman L.C., Grossmann M., Rill D., Brown M., Zhong W.Y., Alexander B., Leimig T., Coustan-Smith E., Campana D., Jenkins J., et al. Interleukin-2 gene-modified allogeneic tumor cells for treatment of relapsed neuroblastoma. Hum. Gene Ther. 1998;9:1303–1311. doi: 10.1089/hum.1998.9.9-1303.
    1. Bowman L., Grossmann M., Rill D., Brown M., Zhong W.Y., Alexander B., Leimig T., Coustan-Smith E., Campana D., Jenkins J., et al. IL-2 adenovector-transduced autologous tumor cells induce antitumor immune responses in patients with neuroblastoma. Blood. 1998;92:1941–1949.
    1. Russell H.V., Strother D., Mei Z., Rill D., Popek E., Biagi E., Yvon E., Brenner M., Rousseau R. A phase 1/2 study of autologous neuroblastoma tumor cells genetically modified to secrete IL-2 in patients with high-risk neuroblastoma. J. Immunother. 2008;31:812–819. doi: 10.1097/CJI.0b013e3181869893.
    1. Russell H.V., Strother D., Mei Z., Rill D., Popek E., Biagi E., Yvon E., Brenner M., Rousseau R. Phase I trial of vaccination with autologous neuroblastoma tumor cells genetically modified to secrete IL-2 and lymphotactin. J. Immunother. 2007;30:227–233. doi: 10.1097/01.cji.0000211335.14385.57.
    1. Rousseau R.F., Haight A.E., Hirschmann-Jax C., Yvon E.S., Rill D.R., Mei Z., Smith S.C., Inman S., Cooper K., Alcoser P., et al. Local and systemic effects of an allogeneic tumor cell vaccine combining transgenic human lymphotactin with interleukin-2 in patients with advanced or refractory neuroblastoma. Blood. 2003;101:1718–1726. doi: 10.1182/blood-2002-08-2493.
    1. Dilloo D., Bacon K., Holden W., Zhong W., Burdach S., Zlotnik A., Brenner M. Combined chemokine and cytokine gene transfer enhances antitumor immunity. Nat. Med. 1996;2:1090–1095. doi: 10.1038/nm1096-1090.
    1. Haining W.N., Cardoso A.A., Keczkemethy H.L., Fleming M., Neuberg D., DeAngelo D.J., Stone R.M., Galinsky I., Silverman L.B., Sallan S.E., et al. Failure to define window of time for autologous tumor vaccination in patients with newly diagnosed or relapsed acute lymphoblastic leukemia. Exp. Hematol. 2005;33:286–294. doi: 10.1016/j.exphem.2004.12.001.
    1. Rousseau R.F., Biagi E., Dutour A., Yvon E.S., Brown M.P., Lin T., Mei Z., Grilley B., Popek E., Heslop H.E., et al. Immunotherapy of high-risk acute leukemia with a recipient (autologous) vaccine expressing transgenic human CD40L and IL-2 after chemotherapy and allogeneic stem cell transplantation. Blood. 2006;107:1332–1341. doi: 10.1182/blood-2005-03-1259.
    1. Pollack I.F., Jakacki R.I., Butterfield L.H., Hamilton R.L., Panigrahy A., Potter D.M., Connelly A.K., Dibridge S.A., Whiteside T.L., Okada H. Antigen-specific immune responses and clinical outcome after vaccination with glioma-associated antigen peptides and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in children with newly diagnosed malignant brainstem and nonbrainstem gliomas. J. Clin. Oncol. 2014;32:2050–2058.
    1. Pollack I.F., Jakacki R.I., Butterfield L.H., Hamilton R.L., Panigrahy A., Normolle D.P., Connelly A.K., Dibridge S., Mason G., Whiteside T.L., et al. Immune responses and outcome after vaccination with glioma-associated antigen peptides and poly-ICLC in a pilot study for pediatric recurrent low-grade gliomas. Neuro Oncol. 2016;18:1157–1168. doi: 10.1093/neuonc/now026.
    1. Sawada A., Inoue M., Kondo O., Yamada-Nakata K., Ishihara T., Kuwae Y., Nishikawa M., Ammori Y., Tsuboi A., Oji Y., et al. Feasibility of cancer immunotherapy with WT1 peptide vaccination for solid and hematological malignancies in children. Pediatr. Blood Cancer. 2016;63:234–241. doi: 10.1002/pbc.25792.
    1. Hirabayashi K., Yanagisawa R., Saito S., Higuchi Y., Koya T., Sano K., Koido S., Okamoto M., Sugiyama H., Nakazawa Y., et al. Feasibility and immune response of WT1 peptide vaccination in combination with OK-432 for paediatric solid tumors. Anticancer Res. 2018;38:2227–2234.
    1. Ceschin R., Kurland B.F., Abberbock S.R., Ellingson B.M., Okada H., Jakacki R.I., Pollack I.F., Panigrahy A. Parametric response mapping of apparent diffusion coefficient as an imaging biomarker to distinguish pseudoprogression from true tumor progression in peptide-based vaccine therapy for pediatric diffuse intrinsic pontine glioma. AJNR Am. J. Neuroradiol. 2015;36:2170–2176. doi: 10.3174/ajnr.A4428.
    1. Hodi F.S., Hwu W.J., Kefford R., Weber J.S., Daud A., Hamid O., Patnaik A., Ribas A., Robert C., Gangadhar T.C., et al. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with pembrolizumab. J. Clin. Oncol. 2016;34:1510–1517. doi: 10.1200/JCO.2015.64.0391.
    1. Garnett-Benson C., Hodge J.W., Gameiro S.R. Combination regimens of radiation therapy and therapeutic cancer vaccines: Mechanisms and opportunities. Semin. Radiat. Oncol. 2015;25:46–53. doi: 10.1016/j.semradonc.2014.07.002.
    1. Dudley M.E., Yang J.C., Sherry R., Hughes M.S., Royal R., Kammula U., Robbins P.F., Huang J., Citrin D.E., Leitman S.F., et al. Adoptive cell therapy for patients with metastatic melanoma: Evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 2008;26:5233–5239. doi: 10.1200/JCO.2008.16.5449.
    1. Versteven M., Van den Bergh J.M.J., Marcq E., Smits E.L.J., Van Tendeloo V.F.I., Hobo W., Lion E. Dendritic cells and programmed death-1 blockade: A joint venture to combat cancer. Front. Immunol. 2018;9:394. doi: 10.3389/fimmu.2018.00394.

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