Biomimetic Nanoplatform-Mediated Protective Autophagy Blockage Enhancing Sonodynamic and Ca2+-Overload Combined Therapy for Colon Cancer
Yuanru Zhao
Institute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, the People's Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, 530021 China
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYujie Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYan Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYuanyuan Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorZhichao Deng
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorTing Bai
Department of Cardiovascular Medicine, The First Affiliated Hospital, Xi'an Jiaotong University, Xi'an, Shaanxi, 710077 China
Search for more papers by this authorCorresponding Author
Mingxin Zhang
Department of Gastroenterology, The First Affiliated Hospital of Xi'an Medical University, Xi'an, Shaanxi, 710077 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Mingzhen Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Department of Hepatobiliary Surgery, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Jian Song
Institute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, the People's Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, 530021 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorYuanru Zhao
Institute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, the People's Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, 530021 China
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYujie Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYan Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorYuanyuan Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorZhichao Deng
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Search for more papers by this authorTing Bai
Department of Cardiovascular Medicine, The First Affiliated Hospital, Xi'an Jiaotong University, Xi'an, Shaanxi, 710077 China
Search for more papers by this authorCorresponding Author
Mingxin Zhang
Department of Gastroenterology, The First Affiliated Hospital of Xi'an Medical University, Xi'an, Shaanxi, 710077 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Mingzhen Zhang
School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
Department of Hepatobiliary Surgery, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi, 710061 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Jian Song
Institute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, the People's Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, 530021 China
E-mail: [email protected]; [email protected]; [email protected]
Search for more papers by this authorAbstract
The application of a multimodal combination therapy based on a targeted nanodelivery system has been demonstrated to be more valuable in the treatment of cancer. In this work, a hollow polydopamine delivery system (CCC@HP@M) was designed to achieve sonodynamic and calcium-overload combined therapy for colon cancer. The CCC@HP@M exhibits both homologous tumour-targeting ability and pH-responsive drug release properties, enabling the simultaneous targeted delivery of CaO2 nanoparticles/sonosensitizer Ce6/autophagy inhibitor CQ. The CaO2 nanoparticles as calcium agents capable of triggering Ca2+ overload in tumor cells. The oxidative stress produced by sonodynamic therapy is facilitated by the disruption of calcium homeostasis to enhance the effect of Ca2+ overload-induced apoptosis. Furthermore, the O2 produced by CaO2 augments the sensitization of sonodynamic therapy. The autophagy inhibitor CQ can inhibit protective cellular autophagy, which is activated by sonodynamic therapy and Ca2+ overload. Consequently, autophagy blockage can ensure the therapeutic effect of sonodynamic and Ca2+-overload combined therapy for colon cancer. The results of experiments in vitro and in vivo demonstrate that the stimulus-responsive targeted delivery system achieves autophagy blockage augmented sonodynamic and Ca2+-overload combined therapy of colon cancer. This work offers a promising theoretical basis for optimizing combined treatment strategies for tumors and clinical translational applications.
Conflict of Interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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| smtd202402091-sup-0001-SuppMat.docx5 MB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Y. Y. Liu, M. Zhang, W. B. Bu, View 2020, 1, e18.
- 2S. Marchi, C. Giorgi, L. Galluzzi, P. Pinton, Mol. Cell 2020, 78, 1055.
- 3X. Chu, X. W. Jiang, Y. Y. Liu, S. J. Zhai, Y. Q. Jiang, Y. Chen, J. Wu, Y. Wang, Y. L. Wu, X. F. Tao, X. H. He, W. B. Bu, Adv. Funct. Mater. 2021, 31, 2008507.
- 4S. A. Almofty, M. Nawaz, F. Qureshi, R. Al-Mutairi, Int. J. Mol. Sci. 2022, 23, 4777.
- 5X. Z. Ai, L. N. Lyu, Y. Zhang, Y. X. Tang, J. Mu, F. Liu, Y. X. Zhou, Z. H. Zuo, G. Liu, B. G. Xing, Angew. Chem. Int. Ed. 2017, 56, 3031.
- 6M. Xu, J. Li, N. Hanagata, H. Su, H. Chen, D. Fujita, Nanoscale 2013, 5, 4763.
- 7J. Burk, L. Sikk, P. Burk, B. B. Manshian, S. J. Soenen, J. J. Scott-Fordsmand, T. Tamm, K. Tämm, Nanoscale 2018, 10, 21985.
- 8Y. Y. Kao, Y. C. Chen, T. J. Cheng, Y. M. Chiung, P. S. Liu, Toxicol. Sci. 2012, 125, 462.
- 9Y. Zhang, H. Wang, H. Jiang, X. Wang, Nanoscale 2012, 4, 3530.
- 10M. Zhang, R. X. Song, Y. Y. Liu, Z. G. Yi, X. F. Meng, J. W. Zhang, Z. M. Tang, Z. W. Yao, Y. Liu, X. G. Liu, W. B. Bu, Chem 2019, 5, 2171.
- 11L. H. Liu, Y. H. Zhang, W. X. Qiu, L. Zhang, F. Gao, B. Li, L. Xu, J. X. Fan, Z. H. Li, X. Z. Zhang, Small 2017, 13, 1701621.
- 12C. C. Huang, W. T. Chia, M. F. Chung, K. J. Lin, C. W. Hsiao, C. Jin, W. H. Lim, C. C. Chen, H. W. Sung, J. Am. Chem. Soc. 2016, 138, 5222.
- 13M. Zhang, R. Song, Y. Liu, Z. Yi, X. Meng, J. Zhang, Z. Tang, Z. Yao, Y. Liu, X. Liu, W. Bu, Chem 2019, 5, 2171.
- 14E. H. Cheteh, M. Augsten, H. Rundqvist, J. Bianchi, V. Sarne, L. Egevad, V. J. Bykov, A. Östman, K. G. Wiman, Cell Death Dis. 2017, 8, e2848.
- 15D. Panja, C. A. Vedeler, M. Schubert, Neuropathol. Appl. Neurobiol. 2019, 45, 141.
- 16S. Orrenius, B. Zhivotovsky, P. Nicotera, Nat. Rev. Mol. Cell Biol. 2003, 4, 552.
- 17Y. Liu, Z. Li, F. Fan, X. Zhu, L. Jia, M. Chen, P. Du, L. Yang, S. Yang, Adv. Sci. 2021, 8, 2102422.
- 18Y. Zhang, X. Q. Zhang, H. C. Yang, L. Yu, Y. Xu, A. Sharma, P. Yin, X. Y. Li, J. S. Kim, Y. Sun, Chem. Soc. Rev. 2021, 50, 11227.
- 19J. Ouyang, Z. M. Tang, N. Farokhzad, N. Kong, N. Y. Kim, C. Feng, S. Blake, Y. F. Xiao, C. Liu, T. Xie, W. Tao, Nano Today 2020, 35, 100949.
- 20L. Sun, X. Wang, F. Gong, K. Yin, W. Zhu, N. Yang, S. Bai, F. Liao, M. Shao, L. Cheng, Theranostics 2021, 11, 9234.
- 21X. Li, L. Gao, L. Zheng, J. Kou, X. Zhu, Y. Jiang, Z. Zhong, J. Dan, H. Xu, Y. Yang, H. Li, S. Shi, W. Cao, Y. Zhao, Y. Tian, L. Yang, Int. J. Nanomed. 2015, 10, 821.
- 22G. Li, H. Lei, Y. Yang, X. Zhong, F. Gong, Y. Gong, Y. Zhou, Y. Zhang, H. Shi, Z. Xiao, Z. Dong, L. Cheng, Adv. Sci. 2022, 9, 2201069.
- 23C. C. Gong, J. M. Zhao, X. D. Meng, Z. Yang, H. F. Dong, Chem. Eng. J. 2022, 435, 135083.
- 24B. Huang, S. Chen, W. Pei, Y. Xu, Z. Jiang, C. Niu, L. Wang, Front. Chem. 2020, 8, 358.
- 25Y. R. Zhao, J. W. Xu, Y. Y. Zhang, F. Wu, W. Zhao, R. Q. Li, Y. Yang, M. Z. Zhang, Y. J. Zhang, C. Guo, Chem. Eng. J. 2023, 472, 144911.
- 26S. Lakkadwala, B. D. Santos Rodrigues, C. Sun, J. Singh, J. Controlled Release. 2019, 307, 247.
- 27J. P. Leung, S. Wu, K. C. Chou, R. Signorell, Nanomaterials 2013, 3, 86.
- 28Y. Bi, R. J. Lee, X. Wang, Y. Sun, M. Wang, L. Li, C. Li, J. Xie, L. Teng, Int. J. Nanomed. 2018, 13, 5811.
- 29W. P. Fan, W. B. Bu, J. L. Shi, Adv. Mater. 2016, 28, 3987.
- 30Y. Y. Lu, Z. J. Li, S. Q. Zhang, T. T. Zhang, Y. J. Liu, L. Zhang, Theranostics 2023, 13, 736.
- 31P. E. Porporato, N. Filigheddu, J. M. B. Pedro, G. Kroemer, L. Galluzzi, Cell Res. 2018, 28, 265.
- 32R. Khalifehzadeh, H. Arami, Adv. Colloid Interface Sci. 2020, 279, 102157.
- 33G. Miao, Y. Zhang, D. Chen, H. Zhang, Mol. Cell 2020, 77, 618.
- 34X. H. Lin, S. Y. Liu, X. Zhang, R. Zhu, S. Chen, X. Y. Chen, J. B. Song, H. H. Yang, Angew. Chem., Int. Ed. 2020, 59, 1682.
- 35J. An, Y. G. Hu, K. Cheng, C. Li, X. L. Hou, G. L. Wang, X. S. Zhang, B. Liu, Y. D. Zhao, M. Z. Zhang, Biomaterials 2020, 234, 119761.
- 36Y. J. Zhang, J. J. Zhao, L. M. Zhang, Y. R. Zhao, Y. Y. Zhang, L. L. Cheng, D. Wang, C. Liu, M. X. Zhang, K. L. Fan, M. Z. Zhang, Nano Today 2023, 49, 101798.
- 37Q. X. Zheng, Y. Chen, D. Chen, H. Y. Zhao, Y. Feng, Q. Meng, Y. Zhao, H. Zhang, Cell 2022, 185, 4082.
- 38R. H. Fang, A. V. Kroll, W. Gao, L. Zhang, Adv. Mater. 2018, 30, 1706759.
- 39Z. J. Fang, S. B. Pan, P. Gao, H. G. Sheng, L. J. Li, L. Shi, Y. Q. Zhang, X. Q. Cai, Int. J. Pharm. 2020, 575, 118841.
- 40C. Wang, X. Sun, L. Feng, Z. Liu, Bmemat 2024, 2, 12083.
- 41M. Liang, M. Guo, P. E. Saw, Y. Yao, Int. J. Nanomed. 2022, 17, 2069.
- 42B. Shrestha, L. Wang, H. Zhang, C. Y. Hung, L. Tang, Int. J. Nanomed. 2020, 15, 8109.
- 43M. Gao, Z. Han, X. Zhang, X. Zou, L. Peng, Y. Zhao, L. Sun, Nanomaterials 2022, 12, 2068.
- 44C. C. He, X. J. Zhang, R. C. Yan, P. X. Zhao, Y. Chen, M. S. Li, C. Chen, T. Fan, Y. Lu, C. Wang, F. Wu, R. J. Lee, T. Yang, G. Y. Xiang, Biomater. Sci. 2019, 7, 4260.
- 45M. Mu, H. Chen, R. Fan, Y. Wang, X. Tang, L. Mei, N. Zhao, B. Zou, A. Tong, J. Xu, B. Han, G. Guo, J. Adv. Res. 2021, 34, 29.
- 46Q. Wu, H. Zhang, H. Liu, BMEMat 2023, 1, 12010.
- 47M. Cui, B. Xu, L. Wang, BMEMat 2024, 2, 12043
- 48M. Zhang, C. Xu, L. Wen, M. K. Han, B. Xiao, J. Zhou, Y. Zhang, Z. Zhang, E. Viennois, D. Merlin, Cancer Res. 2016, 76, 7208.
- 49D. Zhang, B. Zhang, L. X. Zhou, J. Zhao, Y. Y. Yan, Y. L. Li, J. M. Zeng, L. L. Wang, B. Yang, N. M. Lin, Acta Pharmacol. Sin. 2016, 37, 1597.
- 50S. Meng, F. Xia, J. Xu, X. Zhang, M. Xue, M. Gu, F. Guo, Y. Huang, H. Qiu, Y. Yang, Chin. Med. J. 2022, 135, 837.
- 51B. Dąbrowska-Bouta, G. Sulkowski, M. Sałek, M. Frontczak-Baniewicz, L. Strużyńska, Int. J. Mol. Sci. 2021, 22, 3067.
- 52D. R. A. Reyes, M. J. Gomes, C. M. Rosa, L. U. Pagan, S. G. Zanati, R. L. Damatto, E. A. Rodrigues, R. F. Carvalho, A. A. H. Fernandes, P. F. Martinez, A. R. R. Lima, M. D. M. Cezar, L. Carvalho, K. Okoshi, M. P. Okoshi, J. Cell. Mol. Med. 2019, 23, 1235.
- 53R. Chai, L. Yu, C. Dong, Y. Yin, S. Wang, Y. Chen, Q. Zhang, Bioact. Mater. 2022, 17, 276.
- 54G. M. Pontes-Quero, L. Benito-Garzón, J. P. Cano, M. R. Aguilar, B. Vázquez-Lasa, Pharmaceutics 2021, 13, 290.
- 55R. L. Siegel, K. D. Miller, H. E. Fuchs, A. Jemal, CA: A Cancer J. Clin. 2021, 71, 7.
- 56S. Marchi, C. Giorgi, L. Galluzzi, P. Pinton, Mol. Cell 2020, 78, 1055.
- 57X. Tan, J. Huang, Y. Wang, S. He, L. Jia, Y. Zhu, K. Pu, Y. Zhang, X. Yang, Angew. Chem., Int. Ed. 2021, 60, 14051.
- 58Z. Zhang, X. Zhang, S. Zhao, C. Dong, W. Feng, L. Yu, L. Ding, Y. Chen, B. Chen, Chem. Eng. J. 2023, 455, 140869.
