Emerging nitric oxide gas-assisted cancer photothermal treatment

Abstract

Photothermal therapy (PTT) has garnered significant attention in recent years, but the standalone application of PTT still faces limitations that hinder its ability to achieve optimal therapeutic outcomes. Nitric oxide (NO), being one of the most extensively studied gaseous molecules, presents itself as a promising complementary candidate for PTT. In response, various nanosystems have been developed to enable the simultaneous utilization of PTT and NO-mediated gas therapy (GT), with the integration of photothermal agents (PTAs) and thermally-sensitive NO donors being the prevailing approach. This combination seeks to leverage the synergistic effects of PTT and GT while mitigating the potential risks associated with gas toxicity through the use of a single laser irradiation. Furthermore, additional internal or external stimuli have been employed to trigger NO release when combined with different types of PTAs, thereby further enhancing therapeutic efficacy. This comprehensive review aims to summarize recent advancements in NO gas-assisted cancer photothermal treatment. It commences by providing an overview of various types of NO donors and precursors, including those sensitive to photothermal, light, ultrasound, reactive oxygen species, and glutathione. These NO donors and precursors are discussed in the context of dualmodal PTT/GT. Subsequently, the incorporation of other treatment modalities such as chemotherapy (CHT), photodynamic therapy (PDT), alkyl radical therapy, radiation therapy, and immunotherapy (IT) in the creation of triple-modal therapeutic nanoplatforms is presented. The review further explores tetra-modal therapies, such as PTT/GT/CHT/PDT, PTT/GT/CHT/chemodynamic therapy (CDT), PTT/GT/PDT/IT, PTT/GT/starvation therapy (ST)/IT, PTT/GT/Ca²⁺ overload/IT, PTT/GT/ferroptosis (FT)/IT, and PTT/GT/CDT/IT. Finally, potential challenges and future perspectives concerning these novel paradigms are discussed. This comprehensive review is anticipated to serve as a valuable resource for future studies focused on the development of innovative photothermal/NO-based cancer nanotheranostics.

Keywords

cancer nanotheranostics / gas therapy / nitric oxide / photothermal therapy

References

[1] H. Zhang, H. Zhao, W. Chang, X. Liu, P. Chen, A. Yu, A. Chishti, Y. Zhang, L. Ni, X. Wang, Y. Wei, Tungsten 2023, 5, 225.

[2] Z. Wang, Y. Pan, J. Wu, H. Qi, S. Zhu, Z. Gu, Tungsten 2024, 6, 17.

[3] P. Zhang, Y. Zhu, C. Xiao, X. Chen, Adv. Drug Delivery Rev. 2023, 195, 114725.

[4] S. L. Li, P. Jiang, F. L. Jiang, Y. Liu, Adv. Funct. Mater. 2021, 31, 2100243.

[5] P. Liang, B. Ballou, X. Lv, W. Si, M. P. Bruchez, W. Huang, X. Dong, Adv. Mater. 2021, 33, 2005155.

[6] J. Beik, M. Khateri, Z. Khosravi, S. K. Kamrava, S. Kooranifar, H. Ghaznavi, A. Shakeri-Zadeh, Coord. Chem. Rev. 2019, 387, 299.

[7] M. I. Priester, T. L. Ten Hagen, Adv. Drug Deivery Rev. 2022, 192, 114621.

[8] Z. Zhang, W. Sang, L. Xie, Y. Dai, Coord. Chem. Rev. 2019, 399, 213022.

[9] Z. Mo, M. Qiu, K. Zhao, H. Hu, Q. Xu, J. Cao, Y. Luo, L. Liu, Z. Xu, Z. Xiong, G. Liao, S. Yang, J. Colloid Interface Sci. 2022, 611, 193.

[10] Y. Zou, H. Jin, F. Sun, X. Dai, Z. Xu, S. Yang, G. Liao, ACS Appl. Nano Mater. 2018, 1, 2294.

[11] Y. Zou, F. Sun, C. Liu, C. Yu, M. Zhang, Q. He, Y. Xiong, Z. Xu, S. Yang, G. Liao, Chem. Eng. J. 2019, 357, 237.

[12] H. Zhu, B. Li, C. Y. Chan, B. L. Q. Ling, J. Tor, X. Y. Oh, W. Jiang, E. Ye, Z. Li, X. J. Loh, Adv. Drug Delivery Rev. 2022, 192, 114644.

[13] Z. Mo, X. Pan, X. Pan, L. Ye, H. Hu, Q. Xu, X. Hu, Z. Xu, J. Xiong, G. Liao, S. Yang, J. Mater. Chem. B 2022, 10, 8760.

[14] Z. Lv, S. He, Y. Wang, X. Zhu, Adv. Healthcare Mater. 2021, 10, 2001806.

[15] Y. Zhao, B.-Q. Chen, R. K. Kankala, S.-B. Wang, A.-Z. Chen, ACS Biomater. Sci. Eng. 2020, 6, 4799.

[16] M. Wu, X. Niu, R. Zhang, Z. P. Xu, Adv. Drug Delivery Rev. 2022, 187, 114360.

[17] H. Zhu, L. Gou, C. Li, X. Fu, Y. Weng, L. Chen, B. Fang, L. Shuai, G. Liao, Device 2024, 2, 100283.

[18] Y. Chen, B. Sun, X. Jiang, Z. Yuan, S. Chen, P. Sun, Q. Fan, W. Huang, J. Mater. Chem. B. 2021, 9, 1002.

[19] G. Liao, C. Li, S. Liu, B. Fang, H. Yang, Phys. Rep. 2022, 983, 1,

[20] C. Li, B. Cheng, H. Lu, G. Ding, Z. Jiang, G. Liao, Inorg. Chem. 2023, 62, 6843.

[21] Z. Qin, M. Qiu, Q. Zhang, S. Yang, G. Liao, Z. Xiong, Z. Xu, J. Mater. Chem. B. 2021, 9, 8882.

[22] L. Zhang, G. Oudeng, F. Wen, G. Liao, Biomater. Res. 2022, 26, 61.

[23] B. Chang, J. Chen, J. Bao, K. Dong, S. Chen, Z. Cheng, Adv. Drug Delivery Rev. 2023, 192, 114637.

[24] K. Yang, S. Zhao, B. Li, B. Wang, M. Lan, X. Song, Coord. Chem. Rev. 2022, 454, 214330.

[25] P. Wang, B. Chen, Y. Zhan, L. Wang, J. Luo, J. Xu, L. Zhan, Z. Li, Y. Liu, J. Wei, Pharmaceutics 2022, 14, 2279.

[26] W. Fan, B. Yung, P. Huang, X. Chen, Chem. Rev. 2017, 117, 13566.

[27] Y. Cao, Q. Ren, R. Hao, Z. Sun, Mater. Des. 2022, 214, 110391.

[28] X. Yao, B. Yang, J. Xu, Q. He, W. Yang, View 2022, 3, 20200185.

[29] Q. Jin, Y. Deng, F. Jia, Z. Tang, J. Ji, Adv. Ther. 2018, 1, 1800084.

[30] C. Szabo, Nat. Rev. Drug Discovery 2016, 15, 185.

[31] Y. Opoku-Damoah, R. Zhang, H. T. Ta, Z. P. Xu, Exploration 2022, 2, 20210181.

[32] L. Chen, S.-F. Zhou, L. Su, J. Song, ACS Nano 2019, 13, 10887.

[33] Y.-Z. Jing, S.-J. Li, Z.-J. Sun, J. Mater. Chem. B 2021, 9, 8541.

[34] W. Xu, L. Z. Liu, M. Loizidou, M. Ahmed, I. G. Charles, Cell Res. 2002, 12, 311.

[35] B. Li, P. Ji, S. Y. Peng, P. Pan, D. W. Zheng, C. X. Li, Y. X. Sun, X. Z. Zhang, Adv. Mater. 2020, 32, 2000376.

[36] Z. Yang, H. Chen, Nano Res. 2023, 16, 3924.

[37] J. An, Y.-G. Hu, C. Li, X.-L. Hou, K. Cheng, B. Zhang, R.-Y. Zhang, D.-Y. Li, S.-J. Liu, B. Liu, Biomaterials 2020, 230, 119636.

[38] X. Sun, R.-Y. Zhang, F. Zhang, X.-L. Hou, K. Cheng, C.-Q. Li, X.-T. Xie, Z.-T. Zhong, B. Zhang, X.-Q. Yang, J. Colloid Interface Sci. 2022, 621, 77.

[39] Y. Chen, L. Fang, W. Zhou, J. Chang, X. Zhang, C. He, C. Chen, R. Yan, Y. Yan, Y. Lu, J. Nanobiotechnol. 2021, 19, 246.

[40] R. Liu, Y. Peng, L. Lu, S. Peng, T. Chen, M. Zhan, J. Nanobiotechnol. 2021, 19, 443.

[41] Y. Zhao, X. Ouyang, Y. Peng, S. Peng, Pharmaceutics 2021, 13, 1917.

[42] Y. Wu, G. Deng, K. Jiang, H. Wang, Z. Song, H. Han, Biomaterials 2021, 268, 120588.

[43] M. Wu, Z. Lu, K. Wu, C. Nam, L. Zhang, J. Guo, J. Mater. Chem. B 2021, 9, 7063.

[44] G. Jin, Z. Gao, Y. Liu, J. Zhao, H. Ou, F. Xu, D. Ding, Adv. Healthcare Mater. 2021, 10, 2001550.

[45] T. Shang, J. Li, S. Wu, H. Wu, F. Zhang, G. Liao, H. Xiao, L. Huang, L. Chen, Chem. Eng. J. 2023, 478, 147509.

[46] S. Paul, S. Pan, A. Mukherjee, P. De, Mol. Pharm. 2021, 18, 3181.

[47] C. Ji, J. Si, Y. Xu, W. Zhang, Y. Yang, X. He, H. Xu, X. Mou, H. Ren, H. Guo, Theranostics 2021, 11, 8587.

[48] J. C. Pieretti, M. T. Pelegrino, A. Boudier, A. B. Seabra, Mater. Adv. 2021, 2, 7530.

[49] Y. Ding, Y. Ma, C. Du, C. Wang, T. Chen, Y. Wang, J. Wang, Y. Yao, C.-M. Dong, Acta. Biomater. 2021, 123, 335.

[50] M. Wan, Y. Zhao, H. Li, X. Zou, L. Sun, J. Colloid Interface Sci. 2023, 632, 19.

[51] H. Yin, X. Guan, H. Lin, Y. Pu, Y. Fang, W. Yue, B. Zhou, Q. Wang, Y. Chen, H. Xu, Adv. Sci. 2020, 7, 1901954.

[52] X. Yi, Q.-Y. Duan, F.-G. Wu, Research 2021, 2021, 9816594.

[53] X. Huang, Y. Lu, M. Guo, S. Du, N. Han, Theranostics 2021, 11, 7546.

[54] Z. Yan, Z. Liu, H. Zhang, X. Guan, H. Xu, J. Zhang, Q. Zhao, S. Wang, Acta Biomater. 2023, 174, 1,

[55] N. Yang, C. Cao, H. Li, Y. Hong, Y. Cai, X. Song, W. Wang, X. Mou, X. Dong, Small Struct. 2021, 2, 2100110.

[56] Z. Li, X. Lai, S. Fu, L. Ren, H. Cai, H. Zhang, Z. Gu, X. Ma, K. Luo, Adv. Sci. 2022, 9, 2201734.

[57] W. Li, J. Yang, L. Luo, M. Jiang, B. Qin, H. Yin, C. Zhu, X. Yuan, J. Zhang, Z. Luo, Nat. Commun. 2019, 10, 3349.

[58] H. Zhang, M. Xie, H. Chen, S. Bavi, M. Sohail, R. Bavi, Environ. Chem. Lett. 2021, 19, 149.

[59] D. Liang, G. Kuang, X. Chen, J. Lu, L. Shang, W. Sun, Smart Med. 2023, 2, e20230016.

[60] A. B. Seabra, J. C. Pieretti, B. de Melo Santana, M. Horue, G. R. Tortella, G. R. Castro, Int. J. Pharm. 2023, 630, 122465.

[61] A. C. Midgley, Y. Wei, Z. Li, D. Kong, Q. Zhao, Adv. Mater. 2020, 32, 1805818.

[62] G. Liao, F. He, Q. Li, L. Zhong, R. Zhao, H. Che, H. Gao, B. Fang, Prog. Mater. Sci. 2020, 112, 100666.

[63] S. M. Andrabi, N. S. Sharma, A. Karan, S. S. Shahriar, B. Cordon, B. Ma, J. Xie, Adv. Sci. 2023, 10, 2303259.

[64] W. Fan, B. C. Yung, X. Chen, Angew. Chem. Int. Ed. 2018, 57, 8383.

[65] E. Hays, B. Bonavida, Antioxidants 2019, 8, 407.

[66] S. Shuwen, Acta Laser Biol. Sin. 2021, 30, 392.

[67] Y. Qian, R. Kumar, M. K. Chug, H. Massoumi, E. J. Brisbois, ACS Appl. Mater. Interfaces 2021, 13, 52250.

[68] O. K. Nag, K. Lee, M. H. Stewart, E. Oh, J. B. Delehanty, Ther. Delivery 2022, 13, 403.

[69] S. Liu, G. Li, D. Ma, Adv. Ther. 2022, 5, 2100227.

[70] D. Gao, S. Asghar, R. Hu, S. Chen, R. Niu, J. Liu, Z. Chen, Y. Xiao, Acta Pharm. Sin. B. 2023, 13, 1498.

[71] L. Qin, H. Gao, Asian J. Pharm. Sci. 2019, 14, 380.

[72] Y. Yang, Z. Huang, L.-L. Li, Nanoscale 2021, 13, 444.

[73] W. Huang, J. Zhang, L. Luo, Y. Yu, T. Sun, ACS Biomater. Sci. Eng. 2022, 9, 139.

[74] Z. Zhao, X. Shan, H. Zhang, X. Shi, P. Huang, J. Sun, Z. He, C. Luo, S. Zhang, J. Controlled Release 2023, 362, 151.

[75] Z. Wang, A. Jin, Z. Yang, W. Huang, ACS Nano 2023, 17, 8935.

[76] Y. Li, B. Yoon, A. Dey, J. H. Park, J. Controlled Release 2022, 352, 179.

[77] H. Yu, L.-X. Cui, N. Huang, Z.-L. Yang, Med. Gas Res. 2019, 9, 184.

[78] J. Lu, L. Cai, Y. Dai, Y. Liu, F. Zuo, C. Ni, M. Shi, J. Li, Chem. Rec. 2021, 21, 781.

[79] X. Cui, Z. Liang, J. Lu, X. Wang, F. Jia, Q. Hu, X. Xiao, X. Deng, Y. Wu, W. Sheng, Nanoscale 2021, 13, 13375.

[80] M. Chang, Z. Hou, M. Wang, D. Wen, C. Li, Y. Liu, Y. Zhao, J. Lin, Angew. Chem., Int. Ed. 2022, 61, e202209245.

[81] M. Chang, Z. Hou, M. Wang, C. Yang, R. Wang, F. Li, D. Liu, T. Peng, C. Li, J. Lin, Angew. Chem., Int. Ed. 2021, 60, 12971.

[82] G. Gao, X. Sun, G. Liang, Adv. Funct. Mater. 2021, 31, 2100738.

[83] X. Huang, Y. Zhong, Y. Li, X. Zhou, L. Yang, B. Zhao, J. Zhou, H. Qiao, D. Huang, H. Qian, ACS Appl. Mater. Interfaces 2022, 14, 37466.

[84] Z. Wang, F. Rong, Z. Li, W. Li, K. Kaur, Y. Wang, Chem. Eng. J. 2023, 452, 139297.

[85] S. Ghalei, S. Hopkins, M. Douglass, M. Garren, A. Mondal, H. Handa, J. Colloid Interface Sci. 2021, 590, 277.

[86] C. D. Workman, S. Hopkins, J. Pant, M. Goudie, H. Handa, ACS Biomater. Sci. Eng. 2021, 7, 5279.

[87] P. Liu, Y. Wang, Y. Liu, F. Tan, J. Li, N. Li, Theranostics 2020, 10, 6774.

[88] Q. Gao, X. Zhang, W. Yin, D. Ma, C. Xie, L. Zheng, X. Dong, L. Mei, J. Yu, C. Wang, Small 2018, 14, 1802290.

[89] W. Wu, Y. Yang, Z. Liang, X. Song, Y. Huang, L. Qiu, X. Qiu, S. Yu, W. Xue, Nanoscale. 2021, 13, 11169.

[90] W. Liu, F. Semcheddine, Z. Guo, H. Jiang, X. Wang, Nanomaterials 2022, 12, 1348.

[91] D. J. Suchyta, M. H. Schoenfisch, Mol. Pharm. 2015, 12, 3569.

[92] S. T. Gregg, Q. Yuan, R. E. Morris, B. Xiao, Mater. Today Commun. 2017, 12, 95.

[93] Y. Wo, E. J. Brisbois, R. H. Bartlett, M. E. Meyerhoff, Biomater. Sci. 2016, 4, 1161.

[94] G. Liao, L. Zhang, C. Li, S.-Y. Liu, B. Fang, H. Yang, Matter 2022, 5, 3341.

[95] C. You, Y. Li, Y. Dong, L. Ning, Y. Zhang, L. Yao, F. Wang, ACS Biomater. Sci. Eng. 2020, 6, 1535.

[96] C. Wu, D. Wang, M. Cen, L. Cao, Y. Ding, J. Wang, X. Yuan, Y. Wang, T. Chen, Y. Yao, Chem. Commun. 2020, 56, 14491.

[97] X. Zhang, J. Du, Z. Guo, J. Yu, Q. Gao, W. Yin, S. Zhu, Z. Gu, Y. Zhao, Adv. Sci. 2019, 6, 1801122.

[98] K. Huang, Z. Li, J. Lin, G. Han, P. Huang, Chem. Soc. Rev. 2018, 47, 5109.

[99] Y. Wu, W. Xiong, Z. Wang, Y. Wang, K.-y. Sun, X. Song, Z. Lv, W. Xu, W. Zhong, X. Zou, Chem. Eng. J. 2022, 427, 131925.

[100] L. Zeng, L. Huang, G. Han, Adv. Drug Delivery Rev. 2022, 189, 114479.

[101] H. Li, Y. Kim, H. Jung, J. Y. Hyun, I. Shin, Chem. Soc. Rev. 2022, 51, 8957.

[102] Z. Ding, Y. Gu, C. Zheng, Y. Gu, J. Yang, D. Li, Y. Xu, P. Wang, Coord. Chem. Rev. 2022, 464, 214564.

[103] L.-X. Yang, Y.-C. Liu, C.-H. Cho, Y.-R. Chen, C.-S. Yang, Y.-L. Lu, Z. Zhang, Y.-T. Tsai, Y.-C. Chin, J. Yu, J. Nanobiotechnol. 2022, 20, 311.

[104] Z. Fang, J. Zhang, Z. Shi, L. Wang, Y. Liu, J. Wang, J. Jiang, D. Yang, H. Bai, B. Peng, Adv. Mater. 2023, 35, 2301901.

[105] J. Li, R. Jiang, Q. Wang, X. Li, X. Hu, Y. Yuan, X. Lu, W. Wang, W. Huang, Q. Fan, Biomaterials 2019, 217, 119304.

[106] C.-G. Wu, J.-L. Liang, X. Wang, X. Zhou, X. Cai, J. Xu, M. Wang, W.-B. Wang, D. Ma, W. Xue, Sci. China Chem. 2021, 64, 1796.

[107] N. L. Fry, P. K. Mascharak, Acc. Chem. Res. 2011, 44, 289.

[108] C. Ji, X. Zheng, S. Li, C. Liu, M. Yin, ACS Appl. Mater. Interfaces 2023, 15, 34427.

[109] X. Huang, F. Xu, H. Hou, J. Hou, Y. Wang, S. Zhou, Nano Res. 2019, 12, 1361.

[110] Y. Bao, Y. Ge, M. Wu, Z. Mao, J. Ye, W. Tong, Adv. Sci. 2023, 10, 2302278.

[111] Z. Zhang, H. Yan, W. Cao, S. Xie, P. Ran, K. Wei, X. Li, ACS Nano 2023, 17, 16089.

[112] Y. Zhao, D. Shi, L. Guo, M. Shang, X. Sun, D. Meng, S. Xiao, X. Wang, J. Li, J. Nanobiotechnol. 2023, 21, 35.

[113] Y. Feng, H. Zhang, X. Xie, Y. Chen, G. Yang, X. Wei, N. Li, M. Li, T. Li, X. Qin, Mater. Today Bio 2022, 14, 100288.

[114] M. Sun, Y. Sang, Q. Deng, Z. Liu, J. Ren, X. Qu, Nano Res. 2022, 15, 5273.

[115] P. Yu, X. Li, G. Cheng, X. Zhang, D. Wu, J. Chang, S. Wang, Chin. Chem. Lett. 2021, 32, 2127.

[116] W. Fan, N. Lu, P. Huang, Y. Liu, Z. Yang, S. Wang, G. Yu, Y. Liu, J. Hu, Q. He, Angew. Chem., Int. Ed. 2017, 56, 1229.

[117] J. Wu, G. R. Williams, Y. Zhu, T. Hu, H. Wang, W. Zhao, R. Liang, X. Weng, M. Wei, Biomaterials 2021, 273, 120807.

[118] Y. Xiong, C. Xiao, Z. Li, X. Yang, Chem. Soc. Rev. 2021, 50, 6013.

[119] Y. Hu, T. Lv, Y. Ma, J. Xu, Y. Zhang, Y. Hou, Z. Huang, Y. Ding, Nano Lett. 2019, 19, 2731.

[120] L. Du, H. He, Z. Xiao, H. Xiao, Y. An, H. Zhong, M. Lin, X. Meng, S. Han, X. Shuai, Small 2022, 18, 2107732.

[121] J. Li, L. Xie, W. Sang, W. Li, G. Wang, H. Tian, Z. Zhang, J. Liu, Q. Fan, Y. Dai, ChemPhysMater 2022, 1, 51.

[122] H. Sun, Q. Zhang, J. Li, S. Peng, X. Wang, R. Cai, Nano Today 2021, 37, 101073.

[123] N. Zhang, G. Shu, L. Shen, J. Ding, E. Qiao, S. Fang, J. Song, Y. Yang, Z. Zhao, C. Lu, Nano Res. 2022, 15, 5262.

[124] K. Wu, A. Mohsin, W. Q. Zaman, Z. Zhang, W. Guan, M. Chu, Y. Zhuang, M. Guo, J. Nanobiotechnol. 2022, 20, 224.

[125] Y. Ding, Z. Wang, Z. Zhang, Y. Zhao, S. Yang, Y. Zhang, S. Yao, S. Wang, T. Huang, Y. Zhang, Nano Res. 2022, 15, 7304.

[126] R.-T. Li, Y.-D. Zhu, W.-Y. Li, Y.-K. Hou, Y.-M. Zou, Y.-H. Zhao, Q. Zou, W.-H. Zhang, J.-X. Chen, J. Nanobiotechnol. 2022, 20, 212.

[127] L. Zhao, X. Wang, H. Lou, M. Jiang, X. Wu, J. Qin, J. Zhang, X. Guan, W. Li, W. Zhang, J. Colloid Interface Sci. 2022, 624, 734.

[128] S. Liang, G. Liao, W. Zhu, L. Zhang, Biomater. Res. 2022, 26, 32.

[129] Q. Gao, J. Feng, W. Liu, C. Wen, Y. Wu, Q. Liao, L. Zou, X. Sui, T. Xie, J. Zhang, Adv. Drug Del. Rev. 2022, 188, 114445.

[130] M. K. Shim, S. Yang, I.-C. Sun, K. Kim, Adv. Drug Delivery Rev. 2022, 183, 114177.

[131] B. Z. Chen, Y. T. He, Z. Q. Zhao, Y. H. Feng, L. Liang, J. Peng, C. Y. Yang, H. Uyama, M.-A. Shahbazi, X. D. Guo, Adv. Drug Delivery Rev. 2023, 203, 115109.

[132] P. Yadav, S. V. Ambudkar, N. Rajendra Prasad, J. Nanobiotechnol. 2022, 20, 423.

[133] J. Chen, X. Yu, X. Liu, J. Ni, G. Yang, K. Zhang, Nanoscale 2022, 14, 12984.

[134] L. Hu, C. Xiong, G. Wei, Y. Yu, S. Li, X. Xiong, J.-J. Zou, J. Tian, J. Colloid Interface Sci. 2022, 608, 1882.

[135] A. Perez-Potti, M. Rodríguez-Pérez, E. Polo, B. Pelaz, P. Del Pino, Adv. Drug Delivery Rev. 2023, 197, 114829.

[136] L. Wang, Y. Chang, Y. Feng, X. Li, Y. Cheng, H. Jian, X. Ma, R. Zheng, X. Wu, K. Xu, Nano Lett. 2019, 19, 6800.

[137] M. M. Wan, H. Chen, Z. Da Wang, Z. Y. Liu, Y. Q. Yu, L. Li, Z. Y. Miao, X. W. Wang, Q. Wang, C. Mao, Adv. Sci. 2021, 8, 2002525.

[138] Z. Zhang, J. Wang, C. Chen, Adv. Mater. 2013, 25, 3869.

[139] N. S. Rejinold, G. Choi, J.-H. Choy, Coord. Chem. Rev. 2020, 411, 213252.

[140] Y. Huang, J. Zhang, Y. Zhang, L. Shi, X. Qin, B. Lu, Y. Ding, Y. Wang, T. Chen, Y. Yao, Mater. Des. 2021, 211, 110160.

[141] Y. Wang, X. Huang, S. Zhu, L. Li, J. Yang, J. Li, L. Wang, S. Ma, M. Shen, Q. Wu, Chem. Eng. J. 2023, 461, 141816.

[142] J. Yu, R. Zhang, B. Chen, X. Liu, Q. Jia, X. Wang, Z. Yang, P. Ning, Z. Wang, Y. Yang, Adv. Funct. Mater. 2022, 32, 2202857.

[143] Z. Meng, H. Xue, T. Wang, B. Chen, X. Dong, L. Yang, J. Dai, X. Lou, F. Xia, J. Nanobiotechnol. 2022, 20, 344.

[144] K. Zhou, S. Wang, L. Xu, H. Li, Y. Wang, Z. Qiu, G. Zhang, Z. Zhao, B. Z. Tang, Matter. 2023, 6, 3449.

[145] J. Zhu, J. Tian, C. Yang, J. Chen, L. Wu, M. Fan, X. Cai, Small 2021, 17, 2101495.

[146] M. Xia, Y. Yan, H. Pu, X. Du, J. Liang, Y. Sun, J. Zheng, Y. Yuan, Chem. Eng. J. 2022, 442, 136295.

[147] S.-S. Wan, J.-Y. Zeng, H. Cheng, X.-Z. Zhang, Biomaterials 2018, 185, 51.

[148] M. Ding, K. Shao, L. Wu, Y. Jiang, B. Cheng, L. Wang, J. Shi, X. Kong, Biomater. Sci. 2021, 9, 5824.

[149] Z. Yuan, C. Lin, Y. He, B. Tao, M. Chen, J. Zhang, P. Liu, K. Cai, ACS Nano 2020, 14, 3546.

[150] D. Jiang, T. Yue, G. Wang, C. Wang, C. Chen, H. Cao, Y. Gao, New J. Chem. 2020, 44, 162.

[151] J. Zhu, W. Wang, X. Wang, L. Zhong, X. Song, W. Wang, Y. Zhao, X. Dong, Adv. Healthcare Mater. 2021, 10, 2002038.

[152] Q. Wang, Y. Dai, J. Xu, J. Cai, X. Niu, L. Zhang, R. Chen, Q. Shen, W. Huang, Q. Fan, Adv. Funct. Mater. 2019, 29, 1901480.

[153] B. Liu, C. Li, G. Chen, B. Liu, X. Deng, Y. Wei, J. Xia, B. Xing, P. A. Ma, J. Lin, Adv. Sci. 2017, 4, 1600540.

[154] J. Mou, T. Lin, F. Huang, H. Chen, J. Shi, Biomaterials 2016, 84, 13.

[155] H. Shi, C. F. Xiong, L. J. Zhang, H. C. Cao, R. Wang, P. Pan, H. Y. Guo, T. Liu, Adv. Healthcare Mater. 2023, 12, 2300012.

[156] L. Sun, J. Wang, J. Liu, L. Li, Z. P. Xu, Small Struct. 2021, 2, 2000112.

[157] K. Wang, L. Jiang, L. Qiu, Acta Biomater. 2022, 140, 506.

[158] X. Zheng, W. Sun, M. Ju, J. Wu, H. Huang, B. Shen, Biomater. Sci. 2022, 10, 4681.

[159] R. Zhou, X. Zeng, H. Zhao, Q. Chen, P. Wu, Coord. Chem. Rev. 2022, 452, 214306.

[160] R. V. Huis in ’t Veld, J. Heuts, S. Ma, L. J. Cruz, F. A. Ossendorp, M. J. Jager, Pharmaceutics 2023, 15, 330.

[161] W. Guo, T. Wang, C. Huang, S. Ning, Q. Guo, W. Zhang, H. Yang, D. Zhu, Q. Huang, H. Qian, Nano Res. 2022, 16, 782.

[162] D. Ma, W. Chen, L. Wang, R. Han, K. Tang, Colloids Surf., B 2023, 222, 113060.

[163] S. Zhang, M. Li, J. Wang, Y. Zhou, P. Dai, M. Zhao, W. Lv, S. Liu, Q. Zhao, Bioconjugate Chem. 2023, 34, 1327.

[164] Y. Wang, X. Huang, Y. Tang, J. Zou, P. Wang, Y. Zhang, W. Si, W. Huang, X. Dong, Chem. Sci. 2018, 9, 8103.

[165] Y. Wang, Y. Wen, Y. Qu, Z. Pei, Y. Pei, J. Colloid Interface Sci. 2022, 615, 386.

[166] P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne, M. Barberi-Heyob, Theranostics 2015, 5, 1030.

[167] S. Batooei, A. Khajeali, R. Khodadadi, J. P. Islamian, J. Drug Delivery Sci. Technol. 2020, 56, 101576.

[168] S. Her, D. A. Jaffray, C. Allen, Adv. Drug Delivery Rev. 2017, 109, 84.

[169] Y. Wu, K. Zhu, X. Zhang, W. Du, J. Song, H. Yang, Adv. Drug Delivery Rev. 2023, 194, 114710.

[170] J. Wang, X. Tan, X. Pang, L. Liu, F. Tan, N. Li, ACS Appl. Mater. Interfaces 2016, 8, 24331.

[171] M. Zhou, Y. Chen, M. Adachi, X. Wen, B. Erwin, O. Mawlawi, S. Y. Lai, C. Li, Biomaterials 2015, 57, 41.

[172] Y. J. Lin, C. C. Chen, D. Nguyen, H. R. Su, K. J. Lin, H. L. Chen, Y. J. Hu, P. L. Lai, H. W. Sung, Small 2020, 16, 2000655.

[173] W. Fan, W. Bu, Z. Zhang, B. Shen, H. Zhang, Q. He, D. Ni, Z. Cui, K. Zhao, J. Bu, Angew. Chem., Int. Ed. 2015, 54, 14026.

[174] F. Zhang, S. Liu, N. Zhang, Y. Kuang, W. Li, S. Gai, F. He, A. Gulzar, P. Yang, Nanoscale 2020, 12, 19293.

[175] C. Zhao, H. Deng, X. Chen, Adv. Drug Delivery Rev. 2022, 188, 114456.

[176] R. S. Riley, C. H. June, R. Langer, M. J. Mitchell, Nat. Rev. Drug Discovery 2019, 18, 175.

[177] J. Li, X. Gao, Y. Wang, T. Xia, Y. Zhao, H. Meng, Matter 2022, 5, 1162.

[178] B. Xu, Y. Cui, W. Wang, S. Li, C. Lyu, S. Wang, W. Bao, H. Wang, M. Qin, Z. Liu, Adv. Mater. 2020, 32, 2003563.

[179] A. S. Mikhail, R. Morhard, M. Mauda-Havakuk, M. Kassin, A. Arrichiello, B. J. Wood, Adv. Drug Delivery Rev. 2023, 202, 115083.

[180] S. Gao, X. Yang, J. Xu, N. Qiu, G. Zhai, ACS Nano 2021, 15, 12567.

[181] Q. Chen, M. Chen, Z. Liu, Chem. Soc. Rev. 2019, 48, 5506.

[182] S. Zhang, J. Wang, Z. Kong, X. Sun, Z. He, B. Sun, C. Luo, J. Sun, Biomaterials 2022, 282, 121433.

[183] J. Li, W. Cai, J. Yu, S. Zhou, X. Li, Z. He, D. Ouyang, H. Liu, Y. Wang, Biomaterials 2022, 287, 121651.

[184] J. Guo, Y. Zou, L. Huang, Small Methods 2023, 7, 2201307.

[185] Y. Pan, L. Liu, L. Rao, X. Chen, Matter 2022, 5, 1367.

[186] N. Wang, J.-Y. Fang, Trends Microbiol. 2023, 31, 159.

[187] Y. Gao, D. Bi, R. Xie, M. Li, J. Guo, H. Liu, X. Guo, J. Fang, T. Ding, H. Zhu, Signal Transduction Targeted Ther. 2021, 6, 398.

[188] Y. Xin, Y. Yu, M. Su, X. Li, M. Elsabahy, H. Gao, J. Controlled Release 2023, 359, 69.

[189] D. Chowell, L. G. Morris, C. M. Grigg, J. K. Weber, R. M. Samstein, V. Makarov, F. Kuo, S. M. Kendall, D. Requena, N. Riaz, Science 2018, 359, 582.

[190] Z. Meng, Y. Zhang, X. Zhou, J. Ji, Z. Liu, Adv. Drug Delivery Rev. 2022, 182, 114107.

[191] P. Jiang, S. Gu, D. Pan, J. Fu, A. Sahu, X. Hu, Z. Li, N. Traugh, X. Bu, B. Li, Nat. Med. 2018, 24, 1550.

[192] Y. Li, H. Qian, X. Huang, X. Zhou, B. Zhao, L. Yang, J. Chen, H. Qiao, D. Huang, Y. Zhong, Nano Today 2022, 42, 101381.

[193] M. Li, M. Zhao, Y. Zhang, M. Ding, N. Yu, S. Peng, X. Shi, J. Li, Nano Today 2023, 50, 101833.

[194] Y. Xie, M. Wang, Y. Qian, L. Li, Q. Sun, M. Gao, C. Li, Small 2023, 19, 2303596.

[195] Z. Su, H. Xu, Y. Zhang, H. Zhang, H. Zhang, Y. Bao, X. Wu, R. Yan, G. Tan, Z. Wang, J. Mater. Chem. B 2023, 11, 4211.

[196] S. Hao, J. Zuo, H. Huang, W. Li, H. Guo, M. Liu, H. Zhu, H. Sun, J. Mater. Chem. B 2023, 11, 1739.

[197] Z. Liu, Y. Zhong, X. Zhou, X. Huang, J. Zhou, D. Huang, Y. Li, Z. Wang, B. Dong, H. Qiao, Biomaterials 2021, 277, 121118.

[198] L. Jiang, K. Wang, L. Qiu, Asian J. Pharm. Sci. 2022, 17, 924.

[199] H. Cheng, Y. He, J. Lu, Z. Yan, L. Song, Y. Mao, D. Di, Y. Gao, Q. Zhao, S. Wang, J. Colloid Interface Sci. 2023, 639, 249.

[200] R. K. Kankala, Adv. Drug Delivery Rev. 2022, 186, 114270.

[201] J. Yang, W. Qi, L. Wang, L. He, C. Ou, C. Xu, D. He, L. Deng, Acta Biomater. 2024, 176, 379.

[202] B. Niu, K. Liao, Y. Zhou, T. Wen, G. Quan, X. Pan, C. Wu, Biomaterials 2021, 277, 121110.

[203] L. Zhang, Z. Yang, W. He, J. Ren, C.-Y. Wong, J. Colloid Interface Sci. 2021, 599, 543.

[204] Y. Shi, Y. Shi, Z. Wang, J. Zhang, R. Hao, G. Zhang, X. Zhao, L. Zeng, Chem. Eng. J. 2023, 453, 139885.

[205] H.-L. Zhang, Y. Wang, Q. Tang, B. Ren, S.-P. Yang, J.-G. Liu, J. Inorg. Biochem. 2023, 241, 112133.

[206] Q. Xiang, C. Yang, Y. Luo, F. Liu, J. Zheng, W. Liu, H. Ran, Y. Sun, J. Ren, Z. Wang, Small 2022, 18, 2107809.

[207] Q. Chen, C. Li, Q. Wang, Small Methods 2023, 7, 2201457.

[208] W. Jiang, W. Dong, M. Li, Z. Guo, Q. Wang, Y. Liu, Y. Bi, H. Zhou, Y. Wang, ACS Nano 2022, 16, 3881.

[209] L. Wang, K. Kang, Y. Ma, F. Zhang, W. Guo, K. Yu, K. Wang, F. Qu, H. Lin, Chem. Eng. J. 2022, 444, 136512.

[210] W. Xie, W.-W. Deng, M. Zan, L. Rao, G.-T. Yu, D.-M. Zhu, W.-T. Wu, B. Chen, L.-W. Ji, L. Chen, ACS Nano 2019, 13, 2849.

[211] S. Yu, Z. Chen, X. Zeng, X. Chen, Z. Gu, Theranostics 2019, 9, 8026.

[212] X. Zhang, C. He, Y. Chen, C. Chen, R. Yan, T. Fan, Y. Gai, T. Yang, Y. Lu, G. Xiang, Biomaterials 2021, 275, 120987.

[213] X. He, Y. Hao, B. Chu, Y. Yang, A. Sun, K. Shi, C. Yang, K. Zhou, Y. Qu, H. Li, Nano Today 2021, 39, 101174.

[214] M. Qi, X. Ren, W. Li, Y. Sun, X. Sun, C. Li, S. Yu, L. Xu, Y. Zhou, S. Song, Nano Today 2022, 43, 101447.

[215] M. Wang, D. Wang, Q. Chen, C. Li, Z. Li, J. Lin, Small 2019, 15, 1903895.

[216] X. Huang, K. Ren, Z. Chang, Y. Ye, D. Huang, W. Zhao, L. Yang, Y. Dong, Z. Cao, H. Qiao, Chem. Eng. J. 2022, 430, 132898.

[217] Q. Chen, D. Huo, H. Cheng, Z. Lyu, C. Zhu, B. Guan, Y. Xia, Adv. Healthcare Mater. 2019, 8, 1801113.

[218] C. Cui, R. Merritt, L. Fu, Z. Pan, Acta Pharm. Sin. B 2017, 7, 3.

[219] Q. Sun, B. Liu, R. Zhao, L. Feng, Z. Wang, S. Dong, Y. Dong, S. Gai, H. Ding, P. Yang, ACS Appl. Mater. Interfaces 2021, 13, 44096.

[220] B. Liu, Y. Bian, M. Yuan, Y. Zhu, S. Liu, H. Ding, S. Gai, P. Yang, Z. Cheng, J. Lin, Biomaterials 2022, 289, 121746.

[221] H. Hao, M. Yu, Y. Yi, S. Sun, X. Huang, C. Huang, Y. Liu, W. Huang, J. Wang, J. Zhao, Chem. Eng. J. 2022, 437, 135371.

[222] Z. Shen, J. Song, B. C. Yung, Z. Zhou, A. Wu, X. Chen, Adv. Mater. 2018, 30, 1704007.

[223] C. Liang, X. Zhang, M. Yang, X. Dong, Adv. Mater. 2019, 31, 1904197.

[224] X. Shan, S. Li, B. Sun, Q. Chen, J. Sun, Z. He, C. Luo, J. Controlled Release 2020, 319, 322.

[225] S. Zuo, J. Yu, H. Pan, L. Lu, Biomarker Res. 2020, 8, 50.

[226] G. Lei, L. Zhuang, B. Gan, Nat. Rev. Cancer 2022, 22, 381.

[227] H. Tian, J. Lin, F. Zhu, J. Li, S. Jiang, L. Xie, Y. Li, P. Wang, Z. Hou, J. Mi, Chin. Chem. Lett. 2023, 34, 107577.

[228] M. Lv, Y. Zheng, J. Wu, Z. Shen, B. Guo, G. Hu, Y. Huang, J. Zhao, Y. Qian, Z. Su, Angew. Chem., Int. Ed. 2023, 135, e202312897.

[229] M. He, Y. Song, W. Xu, X. Zhang, C. M. Dong, Adv. Funct. Mater. 2023, 33, 2304216.

[230] H. Tian, Y. Li, J. Lin, F. Zhu, Z. Hou, P. Wang, X. Liu, ACS Mater. Lett. 2023, 5, 2542.

[231] Y. Zhang, Z. Zhou, Z. Gao, X. Li, X. Wang, Z. Zheng, J. Deng, D. Liu, T. Peng, Z. Hou, Chem. Eng. J. 2023, 474, 145677.

[232] Q. Zhang, Y. Wang, F. Liu, Cell. Signal. 2022, 103, 110567.

[233] D. Lavie, A. Ben-Shmuel, N. Erez, R. Scherz-Shouval, Nat. Cancer 2022, 3, 793.

[234] S. Shen, Z. Zhang, H. Huang, J. Yang, X. Tao, Z. Meng, H. Ren, X. Li, Biomater. Res. 2023, 27, 44.

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