Conjugated oligo (phenylene vinylene) covalently linked porphyrin for sonodynamic therapy

Abstract

Sonodynamic therapy (SDT) is garnering considerable attention as a promising treatment for deep-seated tumors because of its strong tissue penetration ability, non-invasiveness, and controllability. However, the SDT efficiency of traditional sonosensitizers including porphyrins and their derivatives are limited due to their poor water dissolubility, high aggregation, and low reactive oxygen species (ROS) production efficiency. Consequently, it is crucial to develop novel sonosensitizers with high yields of ROS, outstanding water solubility, and good biocompatibility. Herein, we constructed a new platform for SDT based on unimolecular porphyrin derivatives OPV-C₃-TPP. The probe OPV-C₃-TPP was synthesized by covalently linking conjugated oligomers (OPV) with 5, 10, 15, 20-tetra (4-aminophenyl) porphyrin (TAPP). The introduction of OPV greatly improves the water solubility of the porphyrins and reduces the self-aggregation of the porphyrins. In addition, OPV-C₃-TPP has good intramolecular energy transfer efficiency, thus enhancing the yield of ROS. The experimental results show that OPV-C₃-TPP exhibits excellent ROS generation capacity under ultrasound (US) irradiation, which leads to apoptosis and necrosis of tumor cells. In vivo tumor growth is also significantly inhibited in the OPV-C₃-TPP + US group, exhibiting better SDT effects than TAPP. Therefore, the unimolecular OPV-C₃-TPP can be used as a potential sonosensitizer, providing a promising SDT for deep-tissue tumors.

Keywords

antitumor agents / conjugated oligomer / porphyrin / sensitizers / sonodynamic therapy

References

[1] R. L. Siegel, K. D. Miller, H. E. Fuchs, A. Jemal, CA Cancer J. Clin. 2021, 71, 7.

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

[3] J. C. Li, S. Q. Wang, F. Fontana, C. Tapeinos, M. A. Shahbazi, H. J. Han, H. A. Santos, Bioact. Mater. 2023, 23, 471.

[4] H. J. Ma, R. X. Li, H. B. Meng, M. Tian, X. H. Zhang, Y. L. Liu, L. Li, J. Y. Yuan, Y. Wei, Small 2023, 19, 2204778.

[5] Z. Q. Zhang, Z. N. Lu, Q. Yuan, C. Zhang, Y. L. Tang, J. Mater. Chem. B 2021, 9, 2240.

[6] M. Yang, H. Zhao, Z. Q. Zhang, Q. Yuan, Q. Feng, X. R. Duan, S. Wang, Y. L. Tang, Chem. Sci. 2021, 12, 11515.

[7] A. G. Niculescu, A. M. Grumezescu, Appl. Sci. 2021, 11, 3626.

[8] N. Yumita, R. Nishigaki, K. Umemura, S. Umemura, Jpn. J. Cancer Res. 1989, 80, 219.

[9] S. Liang, X. R. Deng, P. A. Ma, Z. Y. Cheng, J. Lin, Adv. Mater. 2020, 32, 2003214.

[10] X. H. Lin, J. B. Song, X. Y. Chen, H. H. Yang, Angew. Chem., Int. Ed. 2020, 59, 14212.

[11] R. Canaparo, F. Foglietta, N. Barbero, L. Serpe, Adv. Drug Delivery Rev. 2022, 189, 114495.

[12] Z. R. Gong, Z. F. Dai, Adv. Sci. 2021, 8, 2002178.

[13] Y. Zhang, X. Q. Zhang, H. C. Yang, L. Yu, Y. J. Xu, A. Sharma, P. Yin, X. Y. Li, J. S. Kim, Y. Sun, Chem. Soc. Rev. 2021, 50, 11227.

[14] Y. Pu, H. Yin, C. Dong, H. Xiang, W. Wu, B. Zhou, D. Du, Y. Chen, H. Xu, Adv. Mater. 2021, 33, e2104641.

[15] Y. Tang, E. Pang, P. Zhu, Q. Tan, S. Zhao, B. Wang, C. Yao, X. Song, M. Lan, Smart Mol. 2024, 2, e20240003.

[16] Y. X. He, S. H. Liu, J. Yin, J. Yoon, Coord. Chem. Rev. 2021, 429, 213610.

[17] S. Son, J. H. Kim, X. W. Wang, C. L. Zhang, S. A. Yoon, J. Shin, A. Sharma, M. H. Lee, L. Cheng, J. S. Wu, J. S. Kim, Chem. Soc. Rev. 2020, 49, 3244.

[18] T. Xu, S. J. Zhao, C. W. Lin, X. L. Zheng, M. H. Lan, Nano Res. 2020, 13, 2898.

[19] Z. Y. Cao, G. T. Yuan, L. L. Zeng, L. Bai, X. Liu, M. X. Wu, R. L. Sun, Z. T. Chen, Y. Jiang, Q. Y. Gao, Y. X. Chen, Y. L. Zhang, Y. Pan, J. F. Wang, ACS Nano 2022, 16, 10608.

[20] Y. Harada, K. Ogawa, Y. Irie, H. Endo, L. B. Feril, T. Uemura, K. Tachibana, J. Controlled Release 2011, 149, 190.

[21] X. Tan, J. T. Huang, Y. Q. Wang, S. S. He, L. Jia, Y. H. Zhu, K. Y. Pu, Y. Zhang, X. L. Yang, Angew. Chem., Int. Ed. 2021, 60, 14051.

[22] X. W. Wang, X. Y. Zhong, L. X. Bai, J. Xu, F. Gong, Z. L. Dong, Z. J. Yang, Z. J. Zeng, Z. Liu, L. Cheng, J. Am. Chem. Soc. 2020, 142, 6527.

[23] R. R. Zhou, M. Q. Chang, M. J. Shen, Y. Cong, Y. Chen, Y. Wang, Adv. Sci. 2023, 10, 2301764.

[24] J. Ouyang, L. Deng, W. S. Chen, J. P. Sheng, Z. J. Liu, L. Q. Wang, Y. N. Liu, Chem. Commun. 2018, 54, 2874.

[25] F. Wang, B. Y. Wang, W. You, G. Chen, Y. Z. You, Nano Res. 2022, 15, 9223.

[26] T. T. Wu, Y. Liu, Y. Cao, Z. H. Liu, Adv. Mater. 2022, 34, 2110364.

[27] X. J. Xing, S. J. Zhao, T. Xu, L. Huang, Y. Zhang, M. H. Lan, C. W. Lin, X. L. Zheng, P. F. Wang, Coord. Chem. Rev. 2021, 445, 214087.

[28] M. H. Lan, S. J. Zhao, W. M. Liu, C. S. Lee, W. J. Zhang, P. F. Wang, Adv. Healthcare Mater. 2019, 8, 1900132.

[29] A. Q. Ma, H. Q. Chen, Y. H. Cui, Z. Y. Luo, R. J. Liang, Z. H. Wu, Z. Chen, T. Yin, J. Ni, M. B. Zheng, L. T. Cai, Small 2019, 15, 1804028.

[30] Z. L. Dong, L. Z. Feng, Y. Hao, Q. G. Li, M. C. Chen, Z. J. Yang, H. Zhao, Z. Liu, Chem 2020, 6, 1391.

[31] T. Chen, W. W. Zeng, Y. Q. Liu, M. Yu, C. Y. Huang, Z. Q. Shi, C. C. Lin, J. Tang, L. Mei, M. Y. Wu, Small 2022, 18, 2202964.

[32] T. Y. Tong, H. Q. Lei, S. Q. Zhang, D. G. Jiang, Y. P. Guan, C. Y. Xing, H. K. Chen, X. W. Yang, Y. Kang, J. Pang, Adv. Healthcare Mater. 2022, 11, 2201472.

[33] Y. T. Zhao, Z. Q. Zhang, Z. N. Lu, H. Wang, Y. L. Tang, ACS Appl. Mater. Interfaces 2019, 11, 38467.

[34] Y. Chen, Q. Tan, Y. Tang, E. Pang, R. Peng, M. Lan, D. Bai, Biomater. Sci. 2024, 12, 1864.

[35] P. Huang, X. Q. Qian, Y. Chen, L. D. Yu, H. Lin, L. Y. Wang, Y. F. Zhu, J. L. Shi, J. Am. Chem. Soc. 2017, 139, 1275.

[36] H. Q. Chen, L. L. Liu, A. Q. Ma, T. Yin, Z. Chen, R. J. Liang, Y. Z. Qiu, M. B. Zheng, L. T. Cai, Biomaterials 2021, 269, 120639.

[37] H. Xu, N. Yu, J. L. Zhang, Z. J. Wang, P. Geng, M. Wen, M. Q. Li, H. J. Zhang, Z. G. Chen, Biomaterials 2020, 257, 120239.

[38] M. Wen, N. Yu, S. W. Wu, M. M. Huang, P. Qiu, Q. Ren, M. F. Zhu, Z. G. Chen, Bioact. Mater. 2022, 18, 242.

[39] Q. H. Feng, W. X. Zhang, X. M. Yang, Y. Z. Li, Y. W. Hao, H. L. Zhang, L. Hou, Z. Z. Zhang, Adv. Healthcare Mater. 2018, 7, 1700957.

[40] P. H. Zhao, Y. L. Wu, X. Y. Li, L. L. Feng, L. Zhang, B. Y. Zheng, M. R. Ke, J. D. Huang, Angew. Chem., Int. Ed. 2022, 61, e202113506.

[41] C. T. Deng, M. C. Zheng, S. P. Han, Y. J. Wang, J. Q. Xin, O. Aras, L. Cheng, F. F. An, Adv. Funct. Mater. 2023, 33, 2300348.

[42] X. Qu, F. Yin, M. M. Pei, Q. Chen, Y. Y. Zhang, S. W. Lu, X. L. Zhang, Z. Y. Liu, X. Y. Li, H. R. Chen, Y. Zhang, H. L. Qin, ACS Nano 2023, 17, 11466.

[43] X. R. Song, Q. Zhang, M. Q. Chang, L. Ding, H. Huang, W. Feng, T. M. Xu, Y. Chen, Adv. Mater. 2023, 35, 2212259.

[44] F. F. Yang, J. Dong, Z. F. Li, Z. H. Wang, ACS Nano 2023, 17, 4102.

[45] H. R. Lin, H. T. Bai, Z. W. Yang, Q. Shen, M. Y. Li, Y. M. Huang, F. T. Lv, S. Wang, Chem. Commun. 2022, 58, 7232.

[46] H. Sun, K. S. Schanze, ACS Appl. Mater. Interfaces 2022, 14, 20506.

[47] Y. Y. Wu, C. Y. Shi, G. B. Wang, H. Sun, S. Y. Yin, J. Mater. Chem. B 2022, 10, 2995.

[48] Z. L. Zeng, C. Zhang, S. S. He, J. T. Li, K. Y. Pu, Adv. Mater. 2022, 34, 2203246.

[49] X. Wang, M. Wu, H. Z. Li, J. L. Jiang, S. S. Zhou, W. Z. Chen, C. Xie, X. Zhen, X. Q. Jiang, Adv. Sci. 2022, 9, 2104125.

RIGHTS & PERMISSIONS

2024 The Author(s). Smart Molecules published by John Wiley & Sons Australia, Ltd on behalf of Dalian University of Technology.