Nanomedicine-Combined Immunotherapy for Cancer

Shigao      Huang; Qi      Zhao
Abstract

Background: Immunotherapy for cancer includes Chimeric Antigen Receptor (CAR)-T cells, CAR-natural Killer (NK) cells, PD1, and the PD-L1 inhibitor. However, the proportion of patients who respond to cancer immunotherapy is not satisfactory. Concurrently, nanotechnology has experienced a revolution in cancer diagnosis and therapy. There are few clinically approved nanoparticles that can selectively bind and target cancer cells and incorporate molecules, although many therapeutic nanocarriers have been approved for clinical use. There are no systematic reviews outlining how nanomedicine and immunotherapy are used in combination to treat cancer.
Objective: This review aims to illustrate how nanomedicine and immunotherapy can be used for cancer treatment to overcome the limitations of the low proportion of patients who respond to cancer immunotherapy and the rarity of nanomaterials in clinical use.
Methods: A literature review of MEDLINE, PubMed / PubMed Central, and Google Scholar was performed. We performed a structured search of literature reviews on nanoparticle drug-delivery systems, which included photodynamic therapy, photothermal therapy, photoacoustic therapy, and immunotherapy for cancer. Moreover, we detailed the advantages and disadvantages of the various nanoparticles incorporated with molecules to discuss the challenges and solutions associated with cancer treatment.
Conclusion: This review identified the advantages and disadvantages associated with improving health care and outcomes. The findings of this review confirmed the importance of nanomedicinecombined immunotherapy for improving the efficacy of cancer treatment. It may become a new way to develop novel cancer therapeutics using nanomaterials to achieve synergistic anticancer immunity.
Keywords: Cancer immunotherapy, CAR-NK cells, drug delivery, nanomedicine, synergistic effect, (CAR)-T cells.
[1] 
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin.,  2019, 69(1), 7-34.
[http://dx.doi.org/10.3322/caac.21551] [PMID:  30620402] 
[2] 
Huang, S.; Dang, Y.; Li, F.; Wei, W.; Ma, Y.; Qiao, S.; Wang, Q. Biological intensity-modulated radiotherapy plus neoadjuvant chemotherapy for multiple peritoneal metastases of ovarian cancer: A case report. Oncol. Lett.,  2015, 9(3), 1239-1243.
[http://dx.doi.org/10.3892/ol.2014.2820] [PMID:  25663890] 
[3] 
Zhu, L.; Li, P.; Gao, D.; Liu, J.; Liu, Y.; Sun, C.; Xu, M.; Chen, X.; Sheng, Z.; Wang, R.; Yuan, Z.; Cai, L.; Ma, Y.; Zhao, Q. pH-sensitive loaded retinal/indocyanine green micelles as an “all-in-one” theranostic agent for multi-modal imaging in vivo guided cellular senescence-photothermal synergistic therapy. Chem. Commun. (Camb.),  2019, 55(44), 6209-6212.
[http://dx.doi.org/10.1039/C9CC02567G] [PMID:  31073580] 
[4] 
Gao, H.X.; Huang, S.G.; Du, J.F.; Zhang, X.C.; Jiang, N.; Kang, W.X.; Mao, J.; Zhao, Q. Comparison of prognostic indices in NSCLC patients with brain metastases after radiosurgery. Int. J. Biol. Sci.,  2018, 14(14), 2065-2072.
[http://dx.doi.org/10.7150/ijbs.28608] [PMID:  30585269] 
[5] 
GBD 2015 Risk Factors Collaborators. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet,  2016, 388(10053), 1659-1724.
[http://dx.doi.org/10.1016/S0140-6736(16)31679-8] [PMID:  27733284] 
[6] 
Ahmed, M.; Cheng, M.; Zhao, Q.; Goldgur, Y.; Cheal, S.M.; Guo, H.F.; Larson, S.M.; Cheung, N.K. Humanized affinity-matured monoclonal antibody 8H9 has potent antitumor activity and binds to FG loop of tumor antigen B7-H3. J. Biol. Chem.,  2015, 290(50), 30018-30029.
[http://dx.doi.org/10.1074/jbc.M115.679852] [PMID:  26487718] 
[7] 
Chen, Z.; Liu, J.; Chu, D.; Shan, Y.; Ma, G.; Zhang, H.; Zhang, X.D.; Wang, P.; Chen, Q.; Deng, C.; Chen, W.; Dimitrov, D.S.; Zhao, Q. A dual-specific IGF-I/II human engineered antibody domain inhibits IGF signaling in breast cancer cells. Int. J. Biol. Sci.,  2018, 14(7), 799-806.
[http://dx.doi.org/10.7150/ijbs.25928] [PMID:  29910690] 
[8] 
Feng, Y.; Zhao, Q.; Chen, W.; Wang, Y.; Crowder, K.; Dimitrov, D.S. A new bispecific antibody targeting non-overlapping epitopes on IGF2: design, in vitro characterization and pharmacokinetics in macaques. Exp. Mol. Pathol.,  2014, 97(3), 359-367.
[http://dx.doi.org/10.1016/j.yexmp.2014.09.007] [PMID:  25220345] 
[9] 
Zhu, Z.; Qin, H.R.; Chen, W.; Zhao, Q.; Shen, X.; Schutte, R.; Wang, Y.; Ofek, G.; Streaker, E.; Prabakaran, P.; Fouda, G.G.; Liao, H.X.; Owens, J.; Louder, M.; Yang, Y.; Klaric, K.A.; Moody, M.A.; Mascola, J.R.; Scott, J.K.; Kwong, P.D.; Montefiori, D.; Haynes, B.F.; Tomaras, G.D.; Dimitrov, D.S. Cross-reactive HIV-1-neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J. Virol.,  2011, 85(21), 11401-11408.
[http://dx.doi.org/10.1128/JVI.05312-11] [PMID:  21880764] 
[10] 
Zhao, Q.; Ahmed, M.; Guo, H.F.; Cheung, I.Y.; Cheung, N.K. Alteration of electrostatic surface potential enhances affinity and tumor killing properties of anti-ganglioside GD2 monoclonal antibody hu3F8. J. Biol. Chem.,  2015, 290(21), 13017-13027.
[http://dx.doi.org/10.1074/jbc.M115.650903] [PMID:  25851904] 
[11] 
Chen, W.; Feng, Y.; Gong, R.; Zhu, Z.; Wang, Y.; Zhao, Q.; Dimitrov, D.S. Engineered single human CD4 domains as potent HIV-1 inhibitors and components of vaccine immunogens. J. Virol.,  2011, 85(18), 9395-9405.
[http://dx.doi.org/10.1128/JVI.05119-11] [PMID:  21715496] 
[12] 
Chen, W.; Feng, Y.; Zhao, Q.; Zhu, Z.; Dimitrov, D.S. Human monoclonal antibodies targeting nonoverlapping epitopes on insulin-like growth factor II as a novel type of candidate cancer therapeutics. Mol. Cancer Ther.,  2012, 11(7), 1400-1410.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0172] [PMID:  22553356] 
[13] 
Zhao, Q.; Feng, Y.; Zhu, Z.; Dimitrov, D.S. Human monoclonal antibody fragments binding to insulin-like growth factors I and II with picomolar affinity. Mol. Cancer Ther.,  2011, 10(9), 1677-1685.
[http://dx.doi.org/10.1158/1535-7163.MCT-11-0281] [PMID:  21750218] 
[14] 
Zhao, Q.; Tran, H.; Dimitrov, D.S.; Cheung, N.K. A dual-specific anti-IGF-1/IGF-2 human monoclonal antibody alone and in combination with temsirolimus for therapy of neuroblastoma. Int. J. Cancer,  2015, 137(9), 2243-2252.
[http://dx.doi.org/10.1002/ijc.29588] [PMID:  25924852] 
[15] 
Schwab, C.L.; English, D.P.; Roque, D.M.; Pasternak, M.; Santin, A.D. Past, present and future targets for immunotherapy in ovarian cancer. Immunotherapy,  2014, 6(12), 1279-1293.
[http://dx.doi.org/10.2217/imt.14.90] [PMID:  25524384] 
[16] 
Sharma, P.; Wagner, K.; Wolchok, J.D.; Allison, J.P. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat. Rev. Cancer,  2011, 11(11), 805-812.
[http://dx.doi.org/10.1038/nrc3153] [PMID:  22020206] 
[17] 
Ayoub, N.M.; Al-Shami, K.M.; Yaghan, R.J. Immunotherapy for HER2-positive breast cancer: recent advances and combination therapeutic approaches. Breast Cancer (Dove Med. Press),  2019, 11, 53-69.
[http://dx.doi.org/10.2147/BCTT.S175360] [PMID:  30697064] 
[18] 
El Chaer, F.; Holtzman, N.G.; Sausville, E.A.; Law, J.Y.; Lee, S.T.; Duong, V.H.; Baer, M.R.; Koka, R.; Singh, Z.N.; Hardy, N.M.; Emadi, A. Relapsed philadelphia chromosome-positive pre-B-ALL after CD19-Directed CAR-T cell therapy successfully treated with combination of blinatumomab and ponatinib. Acta Haematol.,  2019, 141(2), 107-110.
[http://dx.doi.org/10.1159/000495558] [PMID:  30695783] 
[19] 
Gauthier, J. Traitement par cellules CAR-T: état des lieux de leur utilisation aux États-Unis en 2018. Bull. Cancer,  2018, 105(Suppl. 2), S214-S217.
[http://dx.doi.org/10.1016/S0007-4551(19)30052-9] [PMID:  30686360] 
[20] 
Rosenblatt, J.; Avigan, D. Cellular immunotherapy for multiple myeloma. Cancer J.,  2019, 25(1), 38-44.
[http://dx.doi.org/10.1097/PPO.0000000000000356] [PMID:  30694858] 
[21] 
von Roemeling, C.; Jiang, W.; Chan, C.K.; Weissman, I.L.; Kim, B.Y.S. Breaking down the barriers to precision cancer nanomedicine. Trends Biotechnol.,  2017, 35(2), 159-171.
[http://dx.doi.org/10.1016/j.tibtech.2016.07.006] [PMID:  27492049] 
[22] 
Wang, Y.; Jiang, Y.; Ding, S.; Li, J.; Song, N.; Ren, Y.; Hong, D.; Wu, C.; Li, B.; Wang, F.; He, W.; Wang, J.; Mei, Z.; Mei, Z. Small molecule inhibitors reveal allosteric regulation of USP14 via steric blockade. Cell Res.,  2018, 28(12), 1186-1194.
[http://dx.doi.org/10.1038/s41422-018-0091-x] [PMID:  30254335] 
[23] 
Hodgins, N.O.; Wang, J.T.; Al-Jamal, K.T. Nano-technology based carriers for nitrogen-containing bisphosphonates delivery as sensitisers of γδ T cells for anticancer immunotherapy. Adv. Drug Deliv. Rev.,  2017, 114, 143-160.
[http://dx.doi.org/10.1016/j.addr.2017.07.003] [PMID:  28694026] 
[24] 
Dong, P.; Rakesh, K.P.; Manukumar, H.M.; Mohammed, Y.H.E.; Karthik, C.S.; Sumathi, S.; Mallu, P.; Qin, H.L. Innovative nano-carriers in anticancer drug delivery-a comprehensive review. Bioorg. Chem.,  2019, 85, 325-336.
[http://dx.doi.org/10.1016/j.bioorg.2019.01.019] [PMID:  30658232] 
[25] 
Liu, Y.; Tan, H.X.; Koutsakos, M.; Jegaskanda, S.; Esterbauer, R.; Tilmanis, D.; Aban, M.; Kedzierska, K.; Hurt, A.C.; Kent, S.J.; Wheatley, A.K. Cross-lineage protection by human antibodies binding the influenza B hemagglutinin. Nat. Commun.,  2019, 10(1), 324.
[http://dx.doi.org/10.1038/s41467-018-08165-y] [PMID:  30659197] 
[26] 
Miyaho, R.N.; Nakagawa, S.; Hashimoto-Gotoh, A.; Naka-ya, Y.; Shimode, S.; Sakaguchi, S.; Yoshikawa, R.; Takahashi, M.U.; Miyazawa, T. Corrigendum to “Suscepti-bility of domestic animals to pseudotype virus bearing RD-114 virus envelope protein”. Gene,  2019, 690, 137.
[http://dx.doi.org/10.1016/j.gene.2019.01.002] [PMID:  30658857] 
[27] 
Zayed, D.G.; Ebrahim, S.M.; Helmy, M.W.; Khattab, S.N.; Bahey-El-Din, M.; Fang, J.Y.; Elkhodairy, K.A.; Elzoghby, A.O. Combining hydrophilic chemotherapy and hydrophobic phytotherapy via tumor-targeted albumin-QDs nano-hybrids: covalent coupling and phospholipid complexation approaches. J. Nanobiotechnology,  2019, 17(1), 7.
[http://dx.doi.org/10.1186/s12951-019-0445-7] [PMID:  30660179] 
[28] 
Damanik, F.F.R.; Spadolini, G.; Rotmans, J.; Farè, S.; Moroni, L. Biological activity of human mesenchymal stromal cells on polymeric electrospun scaffolds. Biomater. Sci.,  2019, 7(3), 1088-1100.
[http://dx.doi.org/10.1039/C8BM00693H] [PMID:  30633255] 
[29] 
Hsieh, Y.H.; Chuang, W.C.; Yu, K.H.; Jheng, C.P.; Lee, C.I. Sequential photodynamic therapy with phthalocyanine encapsulated chitosan-tripolyphosphate nanoparticles and flucytosine treatment against candida tropicalis. Pharmaceutics,  2019, 11(1)E16
[http://dx.doi.org/10.3390/pharmaceutics11010016] [PMID:  30621174] 
[30] 
Hu, W.; Zhou, W.; Lei, X.; Zhou, P.; Zhang, M.; Chen, T.; Zeng, H.; Zhu, J.; Dai, S.; Yang, S.; Yang, S. Lowtemperature in situ amino functionalization of TiO2 nanoparticles sharpens electron management achieving over 21% efficient planar perovskite solar cells. Advanced materials (Deerfield Beach, Fla.), 2019, 31(8)e1806095.
[http://dx.doi.org/10.1002/adma.201806095] 
[31] 
Kim, K.O.; Lee, D.; Hiep, N.T.; Song, J.H.; Lee, H.J.; Lee, D.; Kang, K.S. Protective effect of phenolic compounds isolated from mugwort (artemisia argyi) against contrast-induced apoptosis in kidney epithelium cell line LLC-PK1. Molecules,  2019, 24(1)E195
[http://dx.doi.org/10.3390/molecules24010195] [PMID:  30621054] 
[32] 
Li, P.; Mainville, M.; Zhang, Y.; Leclerc, M.; Sun, B.; Izquierdo, R.; Ma, D. Air-processed, stable organic solar cells with high power conversion efficiency of 7.41. Nano Micro Small.,  2019, 15(7)e1804671
[http://dx.doi.org/10.1002/smll.201804671] 
[33] 
Lin, K.Y.; Chung, C.H.; Ciou, J.S.; Su, P.F.; Wang, P.W.; Shieh, D.B.; Wang, T.C. Molecular damage and responses of oral keratinocyte to hydrogen peroxide. BMC Oral Health,  2019, 19(1), 10.
[http://dx.doi.org/10.1186/s12903-018-0694-0] [PMID:  30634966] 
[34] 
Salminen, A.T.; Zhang, J.; Madejski, G.R.; Khire, T.S.; Waugh, R.E.; McGrath, J.L.; Gaborski, T.R. Ultrathin dual-scale nano- and microporous membranes for vascular transmigration models. Small,  2019, 15(6)e1804111
[http://dx.doi.org/10.1002/smll.201804111]] 
[35] 
Shamloo, A.; Forouzandehmehr, M. Personalised deposition maps for micro- and nanoparticles targeting an atherosclerotic plaque: attributions to the receptor-mediated adsorption on the inflamed endothelial cells. Biomech. Model. Mechanobiol.,  2019, 18(3), 813-828.
[http://dx.doi.org/10.1007/s10237-018-01116-y] [PMID:  30617526] 
[36] 
Waisman, A.; Lukas, D.; Clausen, B.E.; Yogev, N. Dendritic cells as gatekeepers of tolerance. Semin. Immunopathol.,  2017, 39(2), 153-163.
[http://dx.doi.org/10.1007/s00281-016-0583-z] [PMID:  27456849] 
[37] 
Dudek, A.M.; Martin, S.; Garg, A.D.; Agostinis, P. Immature, semi-mature, and fully mature dendritic cells: toward a dc-cancer cells interface that augments anticancer immunity. Front. Immunol.,  2013, 4, 438.
[http://dx.doi.org/10.3389/fimmu.2013.00438] [PMID:  24376443] 
[38] 
Conniot, J.; Silva, J.M.; Fernandes, J.G.; Silva, L.C.; Gaspar, R.; Brocchini, S.; Florindo, H.F.; Barata, T.S. Cancer immunotherapy: nanodelivery approaches for immune cell targeting and tracking. Front Chem.,  2014, 2, 105.
[http://dx.doi.org/10.3389/fchem.2014.00105] [PMID:  25505783] 
[39] 
Wang, L.; Huang, S.; Dang, Y.; Li, M.; Bai, W.; Zhong, Z.; Zhao, H.; Li, Y.; Liu, Y.; Wu, M. Cord blood-derived cytokine-induced killer cellular therapy plus radiation therapy for esophageal cancer: a case report. Medicine (Baltimore),  2014, 93(28)e340
[http://dx.doi.org/10.1097/MD.0000000000000340] [PMID:  25526496] 
[40] 
Newick, K.; O’Brien, S.; Moon, E.; Albelda, S.M. CAR T cell therapy for solid tumors. Annu. Rev. Med.,  2017, 68, 139-152.
[http://dx.doi.org/10.1146/annurev-med-062315-120245] [PMID:  27860544] 
[41] 
Liu, J.; Zhou, G.; Zhang, L.; Zhao, Q. Building potent chimeric antigen receptor T cells with CRISPR genome editing. Front. Immunol.,  2019, 10, 456.
[http://dx.doi.org/10.3389/fimmu.2019.00456] [PMID:  30941126] 
[42] 
Wilkins, O.; Keeler, A.M.; Flotte, T.R. CAR T-cell therapy: progress and prospects. Hum. Gene Ther. Methods,  2017, 28(2), 61-66.
[http://dx.doi.org/10.1089/hgtb.2016.153] [PMID:  28330372] 
[43] 
Rose, S.; First-ever, C.A.R. T-cell therapy approved in U.S. Cancer Discov.,  2017, 7(10), OF1.
[http://dx.doi.org/10.1158/2159-8290.CD-NB2017-126] [PMID:  28887358] 
[44] 
Shimabukuro-Vornhagen, A.; Gödel, P.; Subklewe, M.; Stemmler, H.J.; Schlößer, H.A.; Schlaak, M.; Kochanek, M.; Böll, B.; von Bergwelt-Baildon, M.S. Cytokine release syndrome. J. Immunother. Cancer,  2018, 6, 56.
[http://dx.doi.org/10.1186/s40425-018-0343-9] [PMID:  29907163] 
[45] 
Teachey, D.T.; Rheingold, S.R.; Maude, S.L.; Zugmaier, G.; Barrett, D.M.; Seif, A.E.; Nichols, K.E.; Suppa, E.K.; Kalos, M.; Berg, R.A.; Fitzgerald, J.C.; Aplenc, R.; Gore, L.; Grupp, S.A. Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood,  2013, 121(26), 5154-5157.
[http://dx.doi.org/10.1182/blood-2013-02-485623] [PMID:  23678006] 
[46] 
Zhang, J.; Zheng, H.; Diao, Y. Natural Killer cells and current applications of chimeric antigen receptor-modified NK-92 cells in tumor immunotherapy. Int. J. Mol. Sci.,  2019, 20(2)E317
[http://dx.doi.org/10.3390/ijms20020317] [PMID:  30646574] 
[47] 
Hu, Y.; Tian, Z.G.; Zhang, C. Chimeric antigen receptor (CAR)-transduced natural killer cells in tumor immunotherapy. Acta Pharmacol. Sin.,  2018, 39(2), 167-176.
[http://dx.doi.org/10.1038/aps.2017.125] [PMID:  28880014] 
[48] 
Mehta, R.S.; Rezvani, K. Chimeric antigen receptor expressing natural killer cells for the immunotherapy of cancer. Front. Immunol.,  2018, 9, 283.
[http://dx.doi.org/10.3389/fimmu.2018.00283] [PMID:  29497427] 
[49] 
Siegler, E.L.; Zhu, Y.; Wang, P.; Yang, L. Off-the-shelf CAR-NK cells for cancer immunotherapy. Cell Stem Cell,  2018, 23(2), 160-161.
[http://dx.doi.org/10.1016/j.stem.2018.07.007] [PMID:  30075127] 
[50] 
Tang, X.; Yang, L.; Li, Z.; Nalin, A.P.; Dai, H.; Xu, T.; Yin, J.; You, F.; Zhu, M.; Shen, W.; Chen, G.; Zhu, X.; Wu, D.; Yu, J. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am. J. Cancer Res.,  2018, 8(6), 1083-1089.
[PMID:  30034945] 
[51] 
Ohta, Y.; Shiina, T.; Lohr, R.L.; Hosomichi, K.; Pollin, T.I.; Heist, E.J.; Suzuki, S.; Inoko, H.; Flajnik, M.F. Primordial linkage of β2-microglobulin to the MHC. J. Immunol.,  2011, 186(6), 3563-3571.
[http://dx.doi.org/10.4049/jimmunol.1003933] [PMID:  21321107] 
[52] 
Loos, M.; Hedderich, D.M.; Friess, H.; Kleeff, J. B7-h3 and its role in antitumor immunity. Clin. Dev. Immunol.,  2010, 2010683875
[http://dx.doi.org/10.1155/2010/683875] [PMID:  21127709] 
[53] 
Xu-Monette, Z.Y.; Zhang, M.; Li, J.; Young, K.H. PD-1/PD-L1 blockade: have we found the key to unleash the antitumor immune response? Front. Immunol.,  2017, 8, 1597.
[http://dx.doi.org/10.3389/fimmu.2017.01597] [PMID:  29255458] 
[54] 
Ma, W.; Gilligan, B.M.; Yuan, J.; Li, T. Current status and perspectives in translational biomarker research for PD-1/PD-L1 immune checkpoint blockade therapy. J. Hematol. Oncol.,  2016, 9(1), 47.
[http://dx.doi.org/10.1186/s13045-016-0277-y] [PMID:  27234522] 
[55] 
Chen, L.; McGowan, P.; Ashe, S.; Johnston, J.; Li, Y.; Hellström, I.; Hellström, K.E. Tumor immunogenicity determines the effect of B7 costimulation on T cell-mediated tumor immunity. J. Exp. Med.,  1994, 179(2), 523-532.
[http://dx.doi.org/10.1084/jem.179.2.523] [PMID:  7507508] 
[56] 
Bu, X.; Yao, Y.; Li, X. Immune checkpoint blockade in breast cancer therapy. Adv. Exp. Med. Biol.,  2017, 1026, 383-402.
[http://dx.doi.org/10.1007/978-981-10-6020-5_18] [PMID:  29282694] 
[57] 
Chen, L.; Linsley, P.S.; Hellström, K.E. Costimulation of T cells for tumor immunity. Immunol. Today,  1993, 14(10), 483-486.
[http://dx.doi.org/10.1016/0167-5699(93)90262-J] [PMID:  7506034] 
[58] 
Altmann, D.M. A nobel prize-worthy pursuit: cancer immunology and harnessing immunity to tumour neoantigens. Immunology,  2018, 155(3), 283-284.
[http://dx.doi.org/10.1111/imm.13008] [PMID:  30320408] 
[59] 
Yu, Z.; Schmaltz, R.M.; Bozeman, T.C.; Paul, R.; Rishel, M.J.; Tsosie, K.S.; Hecht, S.M. Selective tumor cell targeting by the disaccharide moiety of bleomycin. J. Am. Chem. Soc.,  2013, 135(8), 2883-2886.
[http://dx.doi.org/10.1021/ja311090e] [PMID:  23379863] 
[60] 
Chen, Q.; Yang, Y.; Lin, X.; Ma, W.; Chen, G.; Li, W.; Wang, X.; Yu, Z. Platinum(iv) prodrugs with long lipid chains for drug delivery and overcoming cisplatin resistance. Chem. Commun. (Camb.),  2018, 54(42), 5369-5372.
[http://dx.doi.org/10.1039/C8CC02791A] [PMID:  29744485] 
[61] 
Yang, Y.; Wang, X.; Liao, G.; Liu, X.; Chen, Q.; Li, H.; Lu, L.; Zhao, P.; Yu, Z. iRGD-decorated red shift emissive carbon nanodots for tumor targeting fluorescence imaging. J. Colloid Interface Sci.,  2018, 509, 515-521.
[http://dx.doi.org/10.1016/j.jcis.2017.09.007] [PMID:  28923749] 
[62] 
Liu, Y.; Kim, Y.J.; Siriwon, N.; Rohrs, J.A.; Yu, Z.; Wanga, P. Combination drug delivery via multilamellar vesicles enables targeting of tumor cells and tumor vasculature. Biotechnol. Bioeng.,  2018, 115(6), 1403-1415.
[http://dx.doi.org/10.1002/bit.26566] [PMID:  29457630] 
[63] 
Li, S.D.; Chen, Y.C.; Hackett, M.J.; Huang, L. Tumor-targeted delivery of siRNA by self-assembled nano-particles. Mol. Ther.,  2008, 16(1), 163-169.
[http://dx.doi.org/10.1038/sj.mt.6300323] [PMID:  17923843] 
[64] 
Li, S.D.; Chono, S.; Huang, L. Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J. Control. Release,  2008, 126(1), 77-84.
[http://dx.doi.org/10.1016/j.jconrel.2007.11.002] [PMID:  18083264] 
[65] 
Li, S.D.; Huang, L. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol. Pharm.,  2006, 3(5), 579-588.
[http://dx.doi.org/10.1021/mp060039w] [PMID:  17009857] 
[66] 
Li, S.D.; Huang, L. Nanoparticles evading the reticuloendothelial system: role of the supported bilayer. Biochim. Biophys. Acta,  2009, 1788(10), 2259-2266.
[http://dx.doi.org/10.1016/j.bbamem.2009.06.022] [PMID:  19595666] 
[67] 
Iavicoli, I.; Fontana, L.; Nordberg, G. The effects of nanoparticles on the renal system. Crit. Rev. Toxicol.,  2016, 46(6), 490-560.
[http://dx.doi.org/10.1080/10408444.2016.1181047] [PMID:  27195425] 
[68] 
Fontana, L.; Leso, V.; Marinaccio, A.; Cenacchi, G.; Papa, V.; Leopold, K.; Schindl, R.; Bocca, B.; Alimonti, A.; Iavicoli, I. The effects of palladium nanoparticles on the renal function of female Wistar rats. Nanotoxicology,  2015, 9(7), 843-851.
[http://dx.doi.org/10.3109/17435390.2014.980759] [PMID:  25405262] 
[69] 
Iavicoli, I.; Fontana, L.; Bergamaschi, A. The effects of metals as endocrine disruptors. J. Toxicol. Environ. Health B Crit. Rev.,  2009, 12(3), 206-223.
[http://dx.doi.org/10.1080/10937400902902062] [PMID:  19466673] 
[70] 
Saraiva, C.; Praça, C.; Ferreira, R.; Santos, T.; Ferreira, L.; Bernardino, L. Nanoparticle-mediated brain drug delivery: Overcoming blood-brain barrier to treat neurodegenerative diseases. J. Control. Release,  2016, 235, 34-47.
[http://dx.doi.org/10.1016/j.jconrel.2016.05.044] [PMID:  27208862] 
[71] 
Koshkaryev, A.; Sawant, R.; Deshpande, M.; Torchilin, V. Immunoconjugates and long circulating systems: origins, current state of the art and future directions. Adv. Drug Deliv. Rev.,  2013, 65(1), 24-35.
[http://dx.doi.org/10.1016/j.addr.2012.08.009] [PMID:  22964425] 
[72] 
Meerovich, I.; Koshkaryev, A.; Torchilin, V.P. Kinetic and thermodynamic approaches to the drug targeting phenomena. Curr. Drug Discov. Technol.,  2011, 8(4), 287-300.
[http://dx.doi.org/10.2174/157016311798109335] [PMID:  21726187] 
[73] 
Miyata, K.; Oba, M.; Nakanishi, M.; Fukushima, S. Yamasaki, Y Polyplexes from poly(aspartamide) bearing 1,2-diaminoethane side chains induce pH-selective, endosomal membrane destabilization with amplified transfection and negligible cytotoxicit. J. Am. Chem. Soc.,  2008, 130(48), 16287-16294.
[http://dx.doi.org/10.1021/ja804561g]] 
[74] 
Minami, T.; Matsueda, S.; Takedatsu, H.; Tanaka, M.; Noguchi, M.; Uemura, H.; Itoh, K.; Harada, M. Identification of SART3-derived peptides having the potential to induce cancer-reactive cytotoxic T lymphocytes from prostate cancer patients with HLA-A3 supertype alleles. Cancer Immunol. Immunother.,  2007, 56(5), 689-698.
[http://dx.doi.org/10.1007/s00262-006-0216-9] [PMID:  16937115] 
[75] 
Tang, L.; Zheng, Y.; Melo, M.B.; Mabardi, L.; Castaño, A.P.; Xie, Y.Q.; Li, N.; Kudchodkar, S.B.; Wong, H.C.; Jeng, E.K.; Maus, M.V.; Irvine, D.J. Enhancing T cell therapy through TCR-signaling-responsive nanoparticle drug delivery. Nat. Biotechnol.,  2018, 36(8), 707-716.
[http://dx.doi.org/10.1038/nbt.4181] [PMID:  29985479] 
[76] 
Johnson, L.A.; Scholler, J.; Ohkuri, T.; Kosaka, A.; Patel, P.R.; McGettigan, S.E.; Nace, A.K.; Dentchev, T.; Thekkat, P.; Loew, A.; Boesteanu, A.C.; Cogdill, A.P.; Chen, T.; Fraietta, J.A.; Kloss, C.C.; Posey, A.D., Jr; Engels, B.; Singh, R.; Ezell, T.; Idamakanti, N.; Ramones, M.H.; Li, N.; Zhou, L.; Plesa, G.; Seykora, J.T.; Okada, H.; June, C.H.; Brogdon, J.L.; Maus, M.V. Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma. Sci. Transl. Med.,  2015, 7(275)275ra22
[http://dx.doi.org/10.1126/scitranslmed.aaa4963] [PMID:  25696001] 
[77] 
Klebanoff, C.A.; Finkelstein, S.E.; Surman, D.R.; Lichtman, M.K.; Gattinoni, L.; Theoret, M.R.; Grewal, N.; Spiess, P.J.; Antony, P.A.; Palmer, D.C.; Tagaya, Y.; Rosenberg, S.A.; Waldmann, T.A.; Restifo, N.P. IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc. Natl. Acad. Sci. USA,  2004, 101(7), 1969-1974.
[http://dx.doi.org/10.1073/pnas.0307298101] [PMID:  14762166] 
[78] 
Rosenberg, S.A.; Restifo, N.P. Adoptive cell transfer as personalized immunotherapy for human cancer. Science,  2015, 348(6230), 62-68.
[http://dx.doi.org/10.1126/science.aaa4967] [PMID:  25838374] 
[79] 
Chen, Q.; Xu, L.; Liang, C.; Wang, C.; Peng, R.; Liu, Z. Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat. Commun.,  2016, 7, 13193.
[http://dx.doi.org/10.1038/ncomms13193] [PMID:  27767031] 
[80] 
Deng, R.H.; Qiu, B.; Zhou, P.H. Chitosan/hyaluronic acid/plasmid-DNA nanoparticles encoding interleukin-1 receptor antagonist attenuate inflammation in synoviocytes induced by interleukin-1 beta. J. Mater. Sci. Mater. Med.,  2018, 29(10), 155.
[http://dx.doi.org/10.1007/s10856-018-6160-3] [PMID:  30276528] 
[81] 
Kranz, L.M.; Diken, M.; Haas, H.; Kreiter, S.; Loquai, C.; Reuter, K.C.; Meng, M.; Fritz, D.; Vascotto, F.; Hefesha, H.; Grunwitz, C.; Vormehr, M.; Hüsemann, Y.; Selmi, A.; Kuhn, A.N.; Buck, J.; Derhovanessian, E.; Rae, R.; Attig, S.; Diekmann, J.; Jabulowsky, R.A.; Heesch, S.; Hassel, J.; Langguth, P.; Grabbe, S.; Huber, C.; Türeci, Ö.; Sahin, U. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature,  2016, 534(7607), 396-401.
[http://dx.doi.org/10.1038/nature18300] [PMID:  27281205] 
[82] 
Thomas, S.N.; Vokali, E.; Lund, A.W.; Hubbell, J.A.; Swartz, M.A. Targeting the tumor-draining lymph node with adjuvanted nanoparticles reshapes the anti-tumor immune response. Biomaterials,  2014, 35(2), 814-824.
[http://dx.doi.org/10.1016/j.biomaterials.2013.10.003] [PMID:  24144906] 
[83] 
Qian, Y.; Qiao, S.; Dai, Y.; Xu, G.; Dai, B.; Lu, L.; Yu, X.; Luo, Q.; Zhang, Z. Molecular-targeted immunotherapeutic strategy for melanoma via dual-targeting nanoparticles delivering small interfering RNA to tumor-associated macrophages. ACS Nano,  2017, 11(9), 9536-9549.
[http://dx.doi.org/10.1021/acsnano.7b05465] [PMID:  28858473] 
[84] 
Hu, W.; Mao, A.; Wong, P.; Larsen, A.; Yazaki, P.J.; Wong, J.Y.C.; Shively, J.E. Characterization of 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-n-[methoxy(polyethylene glycerol)-2000] and its complex with doxorubicin using nuclear magnetic resonance spectroscopy and molecular dynamics. Bioconjug. Chem.,  2017, 28(6), 1777-1790.
[http://dx.doi.org/10.1021/acs.bioconjchem.7b00238] [PMID:  28520406] 
[85] 
Huang, S.; Fong, C.I.; Xu, M.; Han, B-n.; Yuan, Z.; Zhao, Q. Nano-loaded natural killer cells as carriers of indocyanine green for synergetic cancer immunotherapy and photothera-py. J. Innov. Opt. Health Sci.,  2019, 12(3)1941002
[http://dx.doi.org/10.1142/S1793545819410025] 
[86] 
Poupot, R.; Goursat, C.; Fruchon, S. Multivalent nanosystems: targeting monocytes/macrophages. Int. J. Nanomedicine,  2018, 13, 5511-5521.
[http://dx.doi.org/10.2147/IJN.S146192] [PMID:  30271144] 
[87] 
Chellat, F.; Merhi, Y.; Moreau, A.; Yahia, L. Therapeutic potential of nanoparticulate systems for macrophage targeting. Biomaterials,  2005, 26(35), 7260-7275.
[http://dx.doi.org/10.1016/j.biomaterials.2005.05.044] [PMID:  16023200] 
[88] 
Kuai, R.; Ochyl, L.J.; Bahjat, K.S.; Schwendeman, A.; Moon, J.J. Designer vaccine nanodiscs for personalized cancer immunotherapy. Nat. Mater.,  2017, 16(4), 489-496.
[http://dx.doi.org/10.1038/nmat4822] [PMID:  28024156] 
[89] 
Ochyl, L.J.; Bazzill, J.D.; Park, C.; Xu, Y.; Kuai, R.; Moon, J.J. PEGylated tumor cell membrane vesicles as a new vaccine platform for cancer immunotherapy. Biomaterials,  2018, 182, 157-166.
[http://dx.doi.org/10.1016/j.biomaterials.2018.08.016] [PMID:  30121425] 
[90] 
Wang, C.; Ye, Y.; Hochu, G.M.; Sadeghifar, H.; Gu, Z. Enhanced cancer immunotherapy by microneedle patch-assisted delivery of anti-PD1 antibody. Nano Lett.,  2016, 16(4), 2334-2340.
[http://dx.doi.org/10.1021/acs.nanolett.5b05030] [PMID:  26999507] 
[91] 
Shimizu, T.; Kishida, T.; Hasegawa, U.; Ueda, Y.; Imanishi, J.; Yamagishi, H.; Akiyoshi, K.; Otsuji, E.; Mazda, O. Nanogel DDS enables sustained release of IL-12 for tumor immunotherapy. Biochem. Biophys. Res. Commun.,  2008, 367(2), 330-335.
[http://dx.doi.org/10.1016/j.bbrc.2007.12.112] [PMID:  18158918] 
[92] 
Furugaki, K.; Cui, L.; Kunisawa, Y.; Osada, K.; Shinkai, K.; Tanaka, M.; Kataoka, K.; Nakano, K. Intraperitoneal administration of a tumor-associated antigen SART3, CD40L, and GM-CSF gene-loaded polyplex micelle elicits a vaccine effect in mouse tumor models. PLoS One,  2014, 9(7)e101854
[http://dx.doi.org/10.1371/journal.pone.0101854] [PMID:  25013909] 
[93] 
Yoshizaki, Y.; Yuba, E.; Sakaguchi, N.; Koiwai, K.; Harada, A.; Kono, K. Potentiation of pH-sensitive polymer-modified liposomes with cationic lipid inclusion as antigen delivery carriers for cancer immunotherapy. Biomaterials,  2014, 35(28), 8186-8196.
[http://dx.doi.org/10.1016/j.biomaterials.2014.05.077] [PMID:  24969637] 
[94] 
He, C.; Duan, X.; Guo, N.; Chan, C.; Poon, C.; Weichselbaum, R.R.; Lin, W. Core-shell nanoscale coordination polymers combine chemotherapy and photodynamic therapy to potentiate checkpoint blockade cancer immunotherapy. Nat. Commun.,  2016, 7, 12499.
[http://dx.doi.org/10.1038/ncomms12499] [PMID:  27530650] 
[95] 
Schmid, D.; Park, C.G.; Hartl, C.A.; Subedi, N.; Cartwright, A.N.; Puerto, R.B.; Zheng, Y.; Maiarana, J.; Freeman, G.J.; Wucherpfennig, K.W.; Irvine, D.J.; Goldberg, M.S. T cell-targeting nanoparticles focus delivery of immunotherapy to improve antitumor immunity. Nat. Commun.,  2017, 8(1), 1747.
[http://dx.doi.org/10.1038/s41467-017-01830-8] [PMID:  29170511] 
[96] 
Wu, L.; Zhang, F.; Wei, Z.; Li, X.; Zhao, H.; Lv, H.; Ge, R.; Ma, H.; Zhang, H.; Yang, B.; Li, J.; Jiang, J. Magnetic delivery of Fe3O4@polydopamine nanoparticle-loaded natural killer cells suggest a promising anticancer treatment. Biomater. Sci.,  2018, 6(10), 2714-2725.
[http://dx.doi.org/10.1039/C8BM00588E] [PMID:  30151523] 
Cite As
Current Medicinal Chemistry

Nanomedicine-Combined Immunotherapy for Cancer

Abstract
