DNA Nanostructures-Based In Situ Cancer Vaccines: Mechanisms and Applications
Bingyu Lin
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorYanfei Liu
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorQiwen Chen
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorMingfeng Li
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorLishang Xu
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorQianqian Chen
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorYifu Tan
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorCorresponding Author
Zhenbao Liu
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
E-mail: [email protected]
Search for more papers by this authorBingyu Lin
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorYanfei Liu
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorQiwen Chen
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorMingfeng Li
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorLishang Xu
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorQianqian Chen
Department of Pharmaceutical Engineering, College of Chemistry and Chemical Engineering, Central South University, Changsha, Hunan, 410083 P. R. China
Search for more papers by this authorYifu Tan
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
Search for more papers by this authorCorresponding Author
Zhenbao Liu
Department of Pharmaceutics, Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, Hunan, 410013 P. R. China
E-mail: [email protected]
Search for more papers by this authorAbstract
Current tumor vaccines suffer from inadequate immune responsive due to the insufficient release of tumor antigens, low tumor infiltration, and immunosuppressive microenvironment. DNA nanostructures with their ability to precisely engineer, controlled release, biocompatibility, and the capability to augment the immunogenicity of tumor microenvironment, have gained significant attention for their potential to revolutionize vaccine designing. This review summarizes various applications of DNA nanostructures in the construction of in situ cancer vaccines, which can generate tumor-associated antigens directly from damaged tumors for cancer immune-stimulation. The mechanisms and components of cancer vaccines are listed, the specific strategies for constructing in situ vaccines using DNA nanostructures are explored and their underlying mechanisms of action are elucidated. The immunogenic cell death (ICD) induced by chemotherapeutic agents, photothermal therapy (PTT), photodynamic therapy (PDT), and radiation therapy (RT) and the related cancer vaccines building strategies are systematically summarized. The applications of different DNA nanostructures in various cancer immunotherapy are elaborated, which exerts precise, long-lasting, and robust immune responses. The current challenges and future prospectives are proposed. This review provides a holistic understanding of the evolving role of DNA nanostructures for in situ vaccine development.
Conflict of Interest
The authors declare no conflict of interest.
References
- 1D. Sun, H. Li, M. Cao, S. He, L. Lei, J. Peng, W. Chen, Cancer Biol. Med. 2020, 17, 879.
- 2S. Lesch, S. Gill, Blood Adv 2021, 5, 3709.
- 3P. Kandra, R. Nandigama, B. Eul, M. Huber, S. Kobold, W. Seeger, F. Grimminger, R. Savai, Front Immunol 2022, 13, 903562.
- 4J. H. Park, M. B. Geyer, R. J. Brentjens, Blood 2016, 127, 3312.
- 5J. P. Murad, D. Tilakawardane, A. K. Park, L. S. Lopez, C. A. Young, J. Gibson, Y. Yamaguchi, H. J. Lee, K. T. Kennewick, B. J. Gittins, W. C. Chang, C. P. Tran, C. Martinez, A. M. Wu, R. E. Reiter, T. B. Dorff, S. J. Forman, S. J. Priceman, Mol. Ther. 2021, 29, 2335.
- 6M. J. Lin, J. Svensson-Arvelund, G. S. Lubitz, A. Marabelle, I. Melero, B. D. Brown, J. D. Brody, Nature Cancer 2022, 3, 911.
- 7N. Gong, M. G. Alameh, R. El-Mayta, L. Xue, D. Weissman, M. J. Mitchell, Nat Rev Drug Discov 2024, 23, 607.
- 8Q. Hu, H. Li, L. Wang, H. Gu, C. Fan, Chem. Rev. 2018, 119, 6459.
- 9X. An, Z. Chen, Y. Luo, P. Yang, Z. Yang, T. Ji, Y. Chi, S. Wang, R. Zhang, Z. Wang, J. Li, Adv. Sci. (Weinh) 2024, 11, 2403158.
- 10J. Dong, I. Willner, Angew Chem Int Ed Engl 2023, 62, 202307898.
- 11Y. Liu, Y. Hu, Y. Tan, Q. Chen, Z. Liu, Chin. Chem. Lett. 2024, 110289.
- 12S. Dey, C. Fan, K. V. Gothelf, J. Li, C. Lin, L. Liu, N. Liu, M. A. D. Nijenhuis, B. Saccà, F. C. Simmel, H. Yan, P. Zhan, Nat Rev Methods Primers 2021, 1, 13.
- 13F. Li, J. Tang, J. Geng, D. Luo, D. Yang, Prog. Polym. Sci. 2019, 98, 101163.
- 14Y. Ouyang, P. Zhang, I. Willner, Angew Chem Int Ed Engl 2024, 63, 202411118.
- 15J. I. Cutler, E. Auyeung, C. A. Mirkin, J. Am. Chem. Soc. 2012, 134, 1376.
- 16K. Mohri, M. Nishikawa, N. Takahashi, T. Shiomi, N. Matsuoka, K. Ogawa, M. Endo, K. Hidaka, H. Sugiyama, Y. Takahashi, Y. Takakura, ACS Nano 2012, 6, 5931.
- 17M. Wang, X. Li, F. He, J. Li, H. H. Wang, Z. Nie, ChemBioChem 2022, 23, 202200119.
- 18V. Schijns, D. Majhen, P. van der Ley, A. Thakur, A. Summerfield, R. Berisio, C. Nativi, A. Fernández-Tejada, C. Alvarez-Dominguez, S. Gizurarson, A. Zamyatina, A. Molinaro, C. Rosano, Ž. Jakopin, I. Gursel, S. McClean, Pharmaceutics 2021, 13, 501.
- 19M. Ghattas, G. Dwivedi, M. Lavertu, M. G. Alameh, Vaccines (Basel) 2021, 9, 1490.
- 20Y. Ding, Z. Li, A. Jaklenec, Q. Hu, Adv Drug Deliv Rev 2021, 179, 113914.
- 21E. W. Roberts, M. L. Broz, M. Binnewies, M. B. Headley, A. E. Nelson, D. M. Wolf, T. Kaisho, D. Bogunovic, N. Bhardwaj, M. F. Krummel, Cancer Cell 2016, 30, 324.
- 22a) J. M. Curtsinger, M. F. Mescher, Curr. Opin. Immunol. 2010, 22, 333; b) W. Cui, N. S. Joshi, A. Jiang, S. M. Kaech, Vaccine 2009, 27, 2177.
- 23T. Inoue, T. Kurosaki, Nat. Rev. Immunol. 2024, 24, 5.
- 24a) C. Cui, J. Wang, E. Fagerberg, P. M. Chen, K. A. Connolly, M. Damo, J. F. Cheung, T. Mao, A. S. Askari, S. Chen, B. Fitzgerald, G. G. Foster, S. C. Eisenbarth, H. Zhao, J. Craft, N. S. Joshi, Cell 2021, 184, 6101; b) R. A. M. Rossetti, N. P. C. Lorenzi, K. Yokochi, M. Rosa, L. Benevides, P. F. R. Margarido, E. C. Baracat, J. P. Carvalho, L. L. Villa, A. P. Lepique, PLoS One 2018, 13, 0199034; c) S. Hong, Z. Zhang, H. Liu, M. Tian, X. Zhu, Z. Zhang, W. Wang, X. Zhou, F. Zhang, Q. Ge, B. Zhu, H. Tang, Z. Hua, B. Hou, Immunity 2018, 49, 695.
- 25a) M. Saxena, S. H. van der Burg, C. J. M. Melief, N. Bhardwaj, Nat. Rev. Cancer 2021, 21, 360; b) J. Liu, M. Fu, M. Wang, D. Wan, Y. Wei, X. Wei, J. Hematol. Oncol. 2022, 15, 28.
- 26O. Kepp, G. Cerrato, A. Sauvat, G. Kroemer, Oncoimmunology 2022, 11, 2131227.
- 27R. Alzeibak, T. A. Mishchenko, N. Y. Shilyagina, I. V. Balalaeva, M. V. Vedunova, D. V. Krysko, J Immunother Cancer 2021, 9.
- 28D. V. Krysko, A. D. Garg, A. Kaczmarek, O. Krysko, P. Agostinis, P. Vandenabeele, Nat. Rev. Cancer 2012, 12, 860.
- 29G. Kroemer, C. Galassi, L. Zitvogel, L. Galluzzi, Nat. Immunol. 2022, 23, 487.
- 30L. Galluzzi, A. Buque, O. Kepp, L. Zitvogel, G. Kroemer, Nat. Rev. Immunol. 2017, 17, 97.
- 31a) D. Garg, D. Nowis, J. Golab, P. Vandenabeele, D. V. Krysko, P. Agostinis, Biochim. Biophys. Acta 2010, 1805, 53; b) L. Apetoh, F. Ghiringhelli, A. Tesniere, M. Obeid, C. Ortiz, A. Criollo, G. Mignot, M. C. Maiuri, E. Ullrich, P. Saulnier, H. Yang, S. Amigorena, B. Ryffel, F. J. Barrat, P. Saftig, F. Levi, R. Lidereau, C. Nogues, J.-P. Mira, A. Chompret, V. Joulin, F. Clavel-Chapelon, J. Bourhis, F. André, S. Delaloge, T. Tursz, G. Kroemer, L. Zitvogel, Nat. Med. 2007, 13, 1050; c) P. Scaffidi, T. Misteli, M. E. Bianchi, Nature 2002, 418, 191.
- 32F. Ghiringhelli, L. Apetoh, A. Tesniere, L. Aymeric, Y. Ma, C. Ortiz, K. Vermaelen, T. Panaretakis, G. Mignot, E. Ullrich, J. L. Perfettini, F. Schlemmer, E. Tasdemir, M. Uhl, P. Génin, A. Civas, B. Ryffel, J. Kanellopoulos, J. Tschopp, F. André, R. Lidereau, N. M. McLaughlin, N. M. Haynes, M. J. Smyth, G. Kroemer, L. Zitvogel, Nat. Med. 2009, 15, 1170.
- 33a) M. Obeid, A. Tesniere, F. Ghiringhelli, G. M. Fimia, L. Apetoh, J.-L. Perfettini, M. Castedo, G. Mignot, T. Panaretakis, N. Casares, D. Métivier, N. Larochette, P. van Endert, F. Ciccosanti, M. Piacentini, L. Zitvogel, G. Kroemer, Nat. Med. 2007, 13, 54; b) J. Fucikova, R. Spisek, G. Kroemer, L. Galluzzi, Cell Res. 2021, 31, 5.
- 34D. Garg, D. V. Krysko, P. Vandenabeele, P. Agostinis, Cancer Immunol. Immunother. 2012, 61, 215.
- 35Z. Yu, J. Guo, M. Hu, Y. Gao, L. Huang, ACS Nano 2020, 14, 4816.
- 36a) M. Jiang, J. Zeng, L. Zhao, M. Zhang, J. Ma, X. Guan, W. Zhang, Nanoscale 2021, 13, 17218; b) C. Chen, X. Ni, S. Jia, Y. Liang, X. Wu, D. Kong, D. Ding, Adv. Mater. 2019, 31, 1904914.
- 37F. Jin, D. Liu, X. Xu, J. Ji, Y. Du, Int J Nanomedicine 2021, 16, 4693.
- 38J. Fucikova, O. Kepp, L. Kasikova, G. Petroni, T. Yamazaki, P. Liu, L. Zhao, R. Spisek, G. Kroemer, L. Galluzzi, Cell Death Dis. 2020, 11, 1013.
- 39D. Garg, P. Agostinis, Photochem. Photobiol. Sci. 2014, 13, 474.
- 40X. Li, Y. Gao, X. Liu, X. Hu, Y. Li, J. Sun, P. Wang, H. Wu, H. Kim, M. Ramalingam, S. Xie, R. Wang, Front Bioeng Biotechnol 2022, 10, 1005520.
- 41H. S. Han, K. Y. Choi, Biomedicines 2021, 9, 305.
- 42X. Yang, Y. Yang, J. Bian, J. Wei, Z. Wang, Z. Zhou, Z. Li, M. Sun, Nano Today 2021, 38, 101109.
- 43A. Procureur, A. Simonaggio, J.-E. Bibault, S. Oudard, Y.-A. Vano, Cancers 2021, 13, 678.
- 44L. Deng, H. Liang, M. Xu, X. Yang, B. Burnette, A. Arina, X.-D. Li, H. Mauceri, M. Beckett, T. Darga, X. Huang, T. F. Gajewski, Z. J. Chen, Y.-X. Fu, R. R. Weichselbaum, Immunity 2014, 41, 843.
- 45A. Ahmed, S. W. G. Tait, Mol. Oncol. 2020, 14, 2994.
- 46C. Galassi, V. Klapp, T. Yamazaki, L. Galluzzi, Immunol Rev 2023, 321, 20.
- 47T. Liu, P. Pei, W. Shen, L. Hu, K. Yang, Small Methods 2023, 7, 2201401.
- 48E. B. Golden, L. Apetoh, Semin Radiat Oncol 2015, 25, 11.
- 49P. W. Rothemund, Nature 2006, 440, 297.
- 50W. Jiang, J. Li, Z. Lin, J. Guo, J. Ma, Z. Wang, M. Zhang, Y. Wu, Small Struct. 2023, 123, 3976.
- 51A. Doerr, Nat. Methods 2011, 8, 454.
- 52S. M. Douglas, A. H. Marblestone, S. Teerapittayanon, A. Vazquez, G. M. Church, W. M. Shih, Nucleic Acids Res. 2009, 37, 5001.
- 53M. E. Fornace, N. J. Porubsky, N. A. Pierce, ACS Synth. Biol. 2020, 9, 2665.
- 54W. G. Pfeifer, C.-M. Huang, M. G. Poirier, G. Arya, C. E. Castro, Sci. Adv. 2023, 9, eadi0697.
- 55J. Wang, Y. Wei, P. Zhang, Y. Wang, Q. Xia, X. Liu, S. Luo, J. Shi, J. Hu, C. Fan, B. Li, L. Wang, X. Zhou, J. Li, Nano Lett. 2022, 22, 7173.
- 56a) H. Jun, X. Wang, W. P. Bricker, M. Bathe, Nat. Commun. 2019, 10, 5419; b) F. Schneider, FN. Moritz, H. Dietz, Sci. Adv. 2019, 5, 1412.
- 57C. Rossi-Gendron, F. El Fakih, L. Bourdon, K. Nakazawa, J. Finkel, N. Triomphe, L. Chocron, M. Endo, H. Sugiyama, G. Bellot, M. Morel, S. Rudiuk, D. Baigl, Nat. Nanotechnol. 2023, 18, 1311.
- 58Y. C. Zeng, O. J. Young, C. M. Wintersinger, F. M. Anastassacos, J. I. MacDonald, G. Isinelli, M. O. Dellacherie, M. Sobral, H. Bai, A. R. Graveline, A. Vernet, M. Sanchez, K. Mulligan, Y. Choi, T. C. Ferrante, D. B. Keskin, G. G. Fell, D. Neuberg, C. J. Wu, D. J. Mooney, I. C. Kwon, J. H. Ryu, W. M. Shih, Nat. Nanotechnol. 2024, 19, 1055.
- 59E.-C. Wamhoff, L. Ronsard, J. Feldman, G. A. Knappe, B. M. Hauser, A. Romanov, J. B. Case, S. Sanapala, E. C. Lam, K. J. S. Denis, J. Boucau, A. K. Barczak, A. B. Balazs, M. S. Diamond, A. G. Schmidt, D. Lingwood, M. Bathe, Nat. Commun. 2024, 15, 795.
- 60R. Veneziano, T. J. Moyer, M. B. Stone, E. C. Wamhoff, B. J. Read, S. Mukherjee, T. R. Shepherd, J. Das, W. R. Schief, D. J. Irvine, M. Bathe, Nat. Nanotechnol. 2020, 15, 716.
- 61a) A. Suma, E. Poppleton, M. Matthies, P. Šulc, F. Romano, A. A. Louis, J. P. K. Doye, C. Micheletti, L. Rovigatti, J. Comput. Chem. 2019, 40, 2586; b) H. Jun, T. R. Shepherd, K. Zhang, W. P. Bricker, S. Li, W. Chiu, M. Bathe, ACS Nano 2019, 13, 2083; c) X. Wang, H. Jun, M. Bathe, J Am Chemical Soc 2022, 144, 4403.
- 62X. Chen, Q. Wang, J. Peng, Q. Long, H. Yu, Z. Li, ACS Appl Materials & Interfaces 2018, 10, 24344.
- 63F. Praetorius, B. Kick, K. L. Behler, M. N. Honemann, D. Weuster-Botz, H. Dietz, Nature 2017, 552, 84.
- 64X. Jian, X. Feng, Y. Luo, F. Li, J. Tan, Y. Yin, Y. Liu, Front Bioeng Biotechnol 2021, 9, 661409.
- 65Y. Xing, E. Cheng, Y. Yang, P. Chen, T. Zhang, Y. Sun, Z. Yang, D. Liu, Adv. Mater. 2011, 23, 1117.
- 66Y. Huang, W. Xu, G. Liu, L. Tian, Chem Commun (Camb) 2017, 53, 3038.
- 67a) C. Yao, R. Zhang, J. Tang, D. Yang, Nat. Protoc. 2021, 16, 5460; b) D. Wang, J. Duan, J. Liu, H. Yi, Z. Zhang, H. Song, Y. Li, K. Zhang, Adv. Healthcare Mater. 2023, 12, 2203031.
- 68L. Yue, S. Wang, V. Wulf, I. Willner, Nat. Commun. 2019, 10, 4774.
- 69W. C. Liao, S. Lilienthal, J. S. Kahn, M. Riutin, Y. S. Sohn, R. Nechushtai, I. Willner, Chem. Sci. 2017, 8, 3362.
- 70T. Uzumcu, O. Guney, O. Okay, Polymer 2016, 100, 169.
- 71P. P. He, X. Du, Y. Cheng, Q. Gao, C. Liu, X. Wang, Y. Wei, Q. Yu, W. Guo, Small 2022, 18, 2200263.
- 72Y. Hu, J. Y. Ying, Small 2023, 19, 2205909.
- 73L. Peng, M. You, Q. Yuan, C. Wu, D. Han, Y. Chen, Z. Zhong, J. Xue, W. Tan, J. Am. Chem. Soc. 2012, 134, 12302.
- 74C. Wang, M. Fadeev, J. Zhang, M. Vázquez-González, G. Davidson-Rozenfeld, H. Tian, I. Willner, Chem. Sci. 2018, 9, 7145.
- 75C. Li, M. J. Rowland, Y. Shao, T. Cao, C. Chen, H. Jia, X. Zhou, Z. Yang, O. A. Scherman, D. Liu, Adv. Mater. 2015, 27, 3298.
- 76Z.-H. Yang, J. Yin, L. Xin, Y. Li, Y. Huang, R. Yuan, Y. Zhuo, Chin. Chem. Lett. 2024, 35, 109558.
- 77R. P. Goodman, I. A. T. Schaap, C. F. Tardin, C. M. Erben, R. M. Berry, C. F. Schmidt, T. AJ, Science 2005, 310, 1661.
- 78a) S. Li, T. Tian, T. Zhang, X. Cai, Y. Lin, Mater. Today 2019, 24, 57; b) T. Zhang, T. Tian, R. Zhou, S. Li, W. Ma, Y. Zhang, N. Liu, S. Shi, Q. Li, X. Xie, Y. Ge, M. Liu, Q. Zhang, S. Lin, X. Cai, Y. Lin, Nat. Protoc. 2020, 15, 2728.
- 79W. Wang, M. Lin, W. Wang, Z. Shen, Z.-S. Wu, Bioact Mater 2024, 33, 279.
- 80L. Gao, L. Liu, Y. Tian, Q. Yang, P. Wu, C. Fan, Q. Zhao, F. Li, Anal. Chem. 2021, 93, 7045.
- 81S. N. Barnaby, T. L. Sita, S. H. Petrosko, A. H. Stegh, C. A. Mirkin, Cancer Treat Res 2015, 166, 23.
- 82R. J. Banga, N. Chernyak, S. P. Narayan, S. T. Nguyen, C. A. Mirkin, J. Am. Chem. Soc. 2014, 136, 9866.
- 83S. Mahajan, A. H. Stegh, Cancers (Basel) 2022, 14, 1615.
- 84E. Callmann, L. E. Cole, C. D. Kusmierz, Z. Huang, D. Horiuchi, C. A. Mirkin, Proc Natl Acad Sci U S A 2020, 117, 17543.
- 85S. Wang, L. Qin, G. Yamankurt, K. Skakuj, Z. Huang, P. C. Chen, D. Dominguez, A. Lee, B. Zhang, C. A. Mirkin, Proc Natl Acad Sci U S A 2019, 116, 10473.
- 86C. E. Callmann, C. D. Kusmierz, J. W. Dittmar, L. Broger, C. A. Mirkin, ACS Cent. Sci. 2021, 7, 892.
- 87Z. Huang, C. E. Callmann, S. Wang, M. K. Vasher, M. Evangelopoulos, S. H. Petrosko, C. A. Mirkin, ACS Cent. Sci. 2022, 8, 692.
- 88J. R. Ferrer, J. A. Wertheim, C. A. Mirkin, Bioconjug Chem 2019, 30, 944.
- 89Y. Hao, Y. Li, L. Song, Z. Deng, J. Am. Chem. Soc. 2021, 143, 3065.
- 90a) C. H. Kapadia, J. R. Melamed, E. S. Day, BioDrugs 2018, 32, 297; b) Z. Tao, H. Zhang, S. Wu, J. Zhang, Y. Cheng, L. Lei, Y. Qin, H. Wei, C.-Y. Yu, Nanoscale 2024, 16, 4392.
- 91K. Mohri, M. Nishikawa, Y. Takahashi, Y. Takakura, Eur. J. Pharm. Sci. 2014, 58, 26.
- 92S. Rattanakiat, M. Nishikawa, H. Funabashi, D. Luo, Y. Takakura, Biomaterials 2009, 30, 5701.
- 93Y. H. Roh, R. C. H. Ruiz, S. Peng, J. B. Lee, D. Luo, Chem. Soc. Rev. 2011, 40, 5730.
- 94K. Mohri, M. Nishikawa, N. Takahashi, T. Shiomi, N. Matsuoka, K. Ogawa, M. Endo, K. Hidaka, H. Sugiyama, Y. Takahashi, Y. Takakura, ACS Nano 2012, 6, 5931.
- 95S. Uno, M. Nishikawa, K. Mohri, Y. Umeki, N. Matsuzaki, Y. Takahashi, H. Fujita, N. Kadowaki, Y. Takakura, Nanomedicine 2014, 10, 765.
- 96T. Yata, Y. Takahashi, M. Tan, K. Hidaka, H. Sugiyama, M. Endo, Y. Takakura, M. Nishikawa, Sci. Rep. 2015, 5, 14979.
- 97a) J. K. Tian, M. L. Zhao, Y. M. Song, X. Zhong, R. Yuan, Y. Zhuo, Anal. Chem. 2021, 93, 13928; b) J. Zhang, Y. Guo, F. Ding, G. Pan, X. Zhu, C. Zhang, Angew Chem Int Ed Engl 2019, 58, 13794; c) Y. Han, Y. Wu, F. Wang, G. Li, J. Wang, X. Wu, A. Deng, X. Ren, X. Wang, J. Gao, Z. Shi, L. Bai, J. Su, Bioact Mater 2024, 35, 1; d) Y. Zhang, M. Lin, J. Yao, X. Xu, Chem Commun (Camb) 2024, 60, 3721.
- 98Y. Bian, Z. Zhou, G. Li, S.-D. Liu, S. Li, Z. Gao, W. Kang, SSRN Electronic Journal 2023, 380, 133402.
- 99a) N. Stephanopoulos, ChemBioChem 2019, 20, 2191; b) J. Hahn, S. F. Wickham, W. M. Shih, S. D. Perrault, ACS Nano 2014, 8, 8765.
- 100V. Linko, A. Keller, Small 2023, 19, 2301935.
- 101H. Shirota, D. Tross, D. M. Klinman, Vaccines (Basel) 2015, 3, 390.
- 102D. Verthelyi, K. J. Ishii, M. Gursel, F. Takeshita, D. M. Klinman, J. Immunol. 2001, 166, 2372.
- 103D. M. Klinman, Nat. Rev. Immunol. 2004, 4, 249.
- 104M. Luchner, S. Reinke, A. Milicic, Pharmaceutics 2021, 13, 142.
- 105a) M. Krieg, A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, D. M. Klinman, Nature 1995, 374, 546; b) T. Adamus, M. Kortylewski, Contemp Oncol (Pozn) 2018, 22, 56.
- 106M. Swiecki, M. Colonna, Nat. Rev. Immunol. 2015, 15, 471.
- 107A. H. Dalpke, K. Heeg, Int J Med Microbiol 2004, 294, 345.
- 108a) C. Bode, G. Zhao, F. Steinhagen, T. Kinjo, D. M. Klinman, Expert Rev. Vaccines 2011, 10, 499; b) N. Kayraklioglu, B. Horuluoglu, D. M. Klinman, Methods Mol Biol 2021, 2197, 51.
- 109V. J. Schüller, S. Heidegger, N. Sandholzer, P. C. Nickels, N. A. Suhartha, S. Endres, C. Bourquin, T. Liedl, ACS Nano 2011, 5, 9696.
- 110J. Li, H. Pei, B. Zhu, L. Liang, M. Wei, Y. He, N. Chen, D. Li, Q. Huang, C. Fan, ACS Nano 2011, 5, 8783.
- 111S. Ohtsuki, N. Matsuzaki, K. Mohri, M. Endo, T. Emura, K. Hidaka, H. Sugiyama, Y. Takahashi, K. Ishiyama, N. Kadowaki, Y. Takakura, M. Nishikawa, Nucleic Acid Ther. 2015, 25, 245.
- 112M. Tan, N. Makiguchi, K. Kusamori, S. Itakura, Y. Takahashi, Y. Takakura, M. Nishikawa, Biotechnol. J. 2024, 19, 2300308.
- 113K. Mohri, E. Kusuki, S. Ohtsuki, N. Takahashi, M. Endo, K. Hidaka, H. Sugiyama, Y. Takahashi, Y. Takakura, M. Nishikawa, Biomacromolecules 2015, 16, 1095.
- 114D. L. Burdette, K. M. Monroe, K. Sotelo-Troha, J. S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa, R. E. Vance, Nature 2011, 478, 515.
- 115Q. R. Wu, X. Peng, X. D. Zhou, Sichuan Da Xue Xue Bao Yi Xue Ban 2022, 53, 1098.
- 116O. Demaria, A. De Gassart, S. Coso, N. Gestermann, J. Di Domizio, L. Flatz, O. Gaide, O. Michielin, P. Hwu, T. V. Petrova, F. Martinon, R. L. Modlin, D. E. Speiser, M. Gilliet, Proc Natl Acad Sci U S A 2015, 112, 15408.
- 117L. Zhang, Y. Wang, J. Karges, D. Tang, H. Zhang, K. Zou, J. Song, H. Xiao, Adv. Mater. 2023, 35, 2210267.
- 118N. Samson, A. Ablasser, Nat Cancer 2022, 3, 1452.
- 119M. D. Castro Eiro, K. Hioki, L. Li, M. E. P. Wilmsen, C. H. Kiernan, I. Brouwers-Haspels, M. van Meurs, M. Zhao, H. de Wit, D. G. B. Grashof, H. J. G. van de Werken, Y. M. Mueller, C. Schliehe, B. Temizoz, K. Kobiyama, K. J. Ishii, P. D. Katsikis, J. Immunol. 2024, 212, 455.
- 120B. Temizoz, E. Kuroda, K. Ohata, N. Jounai, K. Ozasa, K. Kobiyama, T. Aoshi, K. J. Ishii, Eur. J. Immunol. 2015, 45, 1159.
- 121a) K. K. Short, S. M. Miller, L. Walsh, V. Cybulski, H. Bazin, J. T. Evans, D. Burkhart, J Control Release 2019, 315, 186; b) B. B. Kocabas, K. Almacioglu, E. A. Bulut, G. Gucluler, G. Tincer, D. Bayik, M. Gursel, I. Gursel, J Control Release 2020, 328, 587.
- 122B. Temizoz, K. Hioki, S. Kobari, N. Jounai, T. Kusakabe, M. S. J. Lee, C. Coban, E. Kuroda, K. J. Ishii, Int. Immunol. 2022, 34, 353.
- 123W. Liu, J. Xing, X. Tang, X. Sheng, H. Chi, W. Zhan, Front Immunol 2022, 13, 881753.
- 124M. G. Tovey, C. Lallemand, Methods Mol Biol 2010, 626, 287.
- 125J. Sun, M. Pan, F. Liu, W. Yu, W. Wang, F. Mo, S. Yu, Y. Zhou, X. Liu, ACS Mater. Lett. 2020, 2, 1606.
- 126Z. Zhang, M. Lu, Y. Qin, W. Gao, L. Tao, W. Su, J. Zhong, Front Immunol 2021, 12, 672356.
- 127Y. Zhang, H. Xu, L. Jiang, Z. Liu, C. Lian, X. Ding, C. Wan, N. Liu, Y. Wang, Z. Yu, L. Zhu, F. Yin, Z. Li, ACS Nano 2022, 16, 19509.
- 128S. Liu, Q. Jiang, X. Zhao, R. Zhao, Y. Wang, Y. Wang, J. Liu, Y. Shang, S. Zhao, T. Wu, Y. Zhang, G. Nie, B. Ding, Nat. Mater. 2021, 20, 421.
- 129X. Liu, Y. Xu, T. Yu, C. Clifford, Y. Liu, H. Yan, Y. Chang, Nano Lett. 2012, 12, 4254.
- 130J. O. Jin, H. Kim, Y. H. Huh, A. Herrmann, M. Kwak, J Control Release 2019, 315, 76.
- 131Y. Hu, S. Gao, H. Lu, S. Tan, F. Chen, Y. Ke, J. Y. Ying, Nano Lett. 2023, 23, 9778.
- 132Y. Ishii-Mizuno, Y. Umeki, Y. Onuki, H. Watanabe, Y. Takahashi, Y. Takakura, M. Nishikawa, Int. J. Pharm. 2017, 516, 392.
- 133M. Nishikawa, K. Ogawa, Y. Umeki, K. Mohri, Y. Kawasaki, H. Watanabe, N. Takahashi, E. Kusuki, R. Takahashi, Y. Takahashi, Y. Takakura, J Control Release 2014, 180, 25.
- 134Y. Umeki, K. Mohri, Y. Kawasaki, H. Watanabe, R. Takahashi, Y. Takahashi, Y. Takakura, M. Nishikawa, Adv. Funct. Mater. 2015, 25, 5758.
- 135Y. Qu, R. De Rose, C. J. Kim, J. Zhou, Z. Lin, Y. Ju, S. K. Bhangu, C. Cortez-Jugo, F. Cavalieri, F. Caruso, Angew Chem Int Ed Engl 2023, 62, 202214935.
- 136P. Chen, D. Wang, Y. Wang, L. Zhang, Q. Wang, L. Liu, J. Li, X. Sun, M. Ren, R. Wang, Y. Fang, J. J. Zhao, K. Zhang, Nano Lett. 2022, 22, 4058.
- 137Y. Umeki, M. Saito, K. Kusamori, M. Tsujimura, M. Nishimura, Y. Takahashi, Y. Takakura, M. Nishikawa, J Control Release 2018, 288, 189.
- 138L. Qin, S. Wang, D. Dominguez, A. Long, S. Chen, J. Fan, J. Ahn, K. Skakuj, Z. Huang, A. Lee, C. Mirkin, B. Zhang, Front Immunol 2020, 11, 1333.
- 139G. Zhu, Y. Liu, X. Yang, Y. H. Kim, H. Zhang, R. Jia, H. S. Liao, A. Jin, J. Lin, M. Aronova, R. Leapman, Z. Nie, G. Niu, X. Chen, Nanoscale 2016, 8, 6684.
- 140Z. Hu, D. E. Leet, R. L. Allesøe, G. Oliveira, S. Li, A. M. Luoma, J. Liu, J. Forman, T. Huang, J. B. Iorgulescu, R. Holden, S. Sarkizova, S. H. Gohil, R. A. Redd, J. Sun, L. Elagina, A. Giobbie-Hurder, W. Zhang, L. Peter, Z. Ciantra, S. Rodig, O. Olive, K. Shetty, J. Pyrdol, M. Uduman, P. C. Lee, P. Bachireddy, E. I. Buchbinder, C. H. Yoon, D. Neuberg, et al., Nat. Med. 2021, 27, 515.
- 141G. Zhu, L. Mei, H. D. Vishwasrao, O. Jacobson, Z. Wang, Y. Liu, B. C. Yung, X. Fu, A. Jin, G. Niu, Q. Wang, F. Zhang, H. Shroff, X. Chen, Nat. Commun. 2017, 8, 1482.
- 142Y. Zhang, L. Jiang, S. Huang, C. Lian, H. Liang, Y. Xing, J. Liu, X. Tian, Z. Liu, R. Wang, Y. An, F. Lu, Y. Pan, W. Han, Z. Li, F. Yin, Adv. Sci. (Weinh) 2024, 11, 2307754.
- 143Q. Ni, F. Zhang, Y. Liu, Z. Wang, G. Yu, B. Liang, G. Niu, T. Su, G. Zhu, G. Lu, L. Zhang, X. Chen, Sci. Adv. 2020, 6, eaaw6071.
- 144Y. Shao, Z. Y. Sun, Y. Wang, B. D. Zhang, D. Liu, Y. M. Li, ACS Appl. Mater. Interfaces 2018, 10, 9310.
- 145Y. Kang, W. Zhang, Q. Yu, L. Gao, J. Quan, F. Gu, Y. Wu, Y. Tian, Z. Wu, S. Shao, H. Zhou, S. Duan, Y. Zhou, L. Zhang, X. Gao, H. Tian, W. Yao, Cancer Immunol. Immunother. 2023, 72, 2741.
- 146a) H. Ijäs, B. Shen, A. Heuer-Jungemann, A. Keller, M. A. Kostiainen, T. Liedl, J. A. Ihalainen, V. Linko, Nucleic Acids Res. 2021, 49, 3048; b) Y. Xu, S. W. Huang, Y. Q. Ma, H. M. Ding, Nanoscale Adv 2022, 4, 754.
- 147M. Liu, L. Hao, D. Zhao, J. Li, Y. Lin, ACS Appl. Mater. Interfaces 2022, 14, 38506.
- 148B. Deng, B. Ma, Y. Ma, P. Cao, X. Leng, P. Huang, Y. Zhao, T. Ji, X. Lu, L. Liu, J Nanobiotechnology 2022, 20, 140.
- 149F. Shen, L. Sun, L. Wang, R. Peng, C. Fan, Z. Liu, Nano Lett. 2022, 22, 4509.
- 150H. Wei, Z. Zhao, Y. Wang, J. Zou, Q. Lin, Y. Duan, ACS Appl. Mater. Interfaces 2019, 11, 46479.
- 151F. Wang, M. Xie, Y. Huang, Y. Liu, X. Liu, L. Zhu, X. Zhu, Y. Guo, C. Zhang, Angew Chem Int Ed Engl 2024, 63, 202315282.
- 152G. Yuanyuan, Z. Qiushuang, Z. Qiwen, G. Jing, Z. Xinyuan, Y. Haijun, L. Yuehua, Z. Chuan, Sci. Adv. 2022, 8, e2941.
10.1126/sciadv.abn2941 Google Scholar
- 153D. Wang, J. Liu, J. Duan, H. Yi, J. Liu, H. Song, Z. Zhang, J. Shi, K. Zhang, Nat. Commun. 2023, 14, 4511.
- 154S. Yang, J. Wu, Z. Wang, Y. Cheng, R. Zhang, C. Yao, D. Yang, Angew Chem Int Ed Engl 2024, 63, 202319073.
- 155T. Yata, Y. Takahashi, M. Tan, H. Nakatsuji, S. Ohtsuki, T. Murakami, H. Imahori, Y. Umeki, T. Shiomi, Y. Takakura, M. Nishikawa, Biomaterials 2017, 146, 136.
- 156Y. Wu, Q. Li, G. Shim, Y. K. Oh, J Control Release 2021, 330, 540.
- 157Y. Yang, B. Liu, Y. Liu, J. Chen, Y. Sun, X. Pan, J. Xu, S. Xu, Z. Liu, W. Tan, Nano Lett. 2022, 22, 2826.
- 158Y. Xie, H. Li, L. Xu, H. Zou, X. Wang, X. He, Q. Tang, Y. Zhou, X. Zhao, X. Chen, H. Liu, J. Pu, D. Luo, P. Liu, Adv. Mater. 2023, 35, 2208546.
- 159J. Yan, H. Yu, X. Tang, F. Li, Z. Li, Y. Liang, B. He, X. Wang, Y. Sun, Mater. Des. 2023, 226, 111584.
- 160J. Yan, H. Yu, C. Liu, B. Li, D. Wei, B. He, H. Liu, Y. Liang, Y. Sun, F. Ju, Chem. Eng. J. 2024, 481, 148616.
- 161S. Liu, Q. Jiang, X. Zhao, R. Zhao, Y. Wang, Y. Wang, J. Liu, Y. Shang, S. Zhao, T. Wu, Y. Zhang, G. Nie, B. Ding, Nat. Mater. 2020, 20, 421.
- 162Q. Wang, Y. Ma, Z. Lu, H. Yu, Z. Li, ACS Appl. Nano Mater. 2022, 5, 101.
- 163J. Yan, Z. Zhang, X. Zhan, K. Chen, Y. Pu, Y. Liang, B. He, Nanoscale 2021, 13, 9577.
- 164M. Nishikawa, Y. Mizuno, K. Mohri, N. Matsuoka, S. Rattanakiat, Y. Takahashi, H. Funabashi, D. Luo, Y. Takakura, Biomaterials 2011, 32, 488.
- 165D. Wang, J. Liu, J. Duan, Y. Ma, H. Gao, Z. Zhang, J. Liu, J. Shi, K. Zhang, ACS Appl. Mater. Interfaces 2022, 14, 44183.
- 166a) T. Li, H. Sui, T. Zhang, Advances in Nanomaterials-based Cell Biology Research 2021, 7, 191;
10.1007/978-981-16-2666-1_7 Google Scholarb) Y. Wang, T. J. Chen-Mayfield, Z. Li, M. H. Younis, W. Cai, Q. Hu, Adv. Funct. Mater. 2022, 32, 2112273.
- 167J. B. Hall, M. A. Dobrovolskaia, A. K. Patri, S. E. McNeil, Nanomedicine (Lond) 2007, 2, 789.
- 168C. R. Lucas, P. D. Halley, A. A. Chowdury, B. K. Harrington, L. Beaver, R. Lapalombella, A. J. Johnson, E. K. Hertlein, M. A. Phelps, J. C. Byrd, C. E. Castro, Small 2022, 18, 2108063.
- 169Q. Zhang, Q. Jiang, N. Li, L. Dai, Q. Liu, L. Song, J. Wang, Y. Li, J. Tian, B. Ding, Y. Du, ACS Nano 2014, 8, 6633.
- 170Y. Xin, C. Kielar, S. Zhu, C. Sikeler, X. Xu, C. Möser, G. Grundmeier, T. Liedl, A. Heuer-Jungemann, D. M. Smith, A. Keller, Small 2020, 16, 1905959.
- 171a) K. T. Butler, D. W. Davies, H. Cartwright, O. Isayev, A. Walsh, Nature 2018, 559, 547; b) J. Li, T. P. Chiu, R. Rohs, Nat. Commun. 2024, 15, 1243.
- 172F. Gianfelici, IEEE Transactions on Neural Networks 2008, 19, 377.
10.1109/TNN.2008.917504 Google Scholar
- 173M. Ben-Dov, R. Feldman, Text Mining and Information Extraction. Part 6 2010, 809.
- 174J. Schmidhuber, Neural Networks 2015, 61, 85.