D-type neuropeptide decorated AIEgen/RENP hybrid nanoprobes with light-driven ROS generation ability for NIR-II fluorescence imaging-guided through-skull photodynamic therapy of gliomas

Abstract

Glioma is one of the most common malignant tumors of the central nervous system, leading high mortality rates in human. Aggregation-induced emission (AIE) photosensitizers-based photodynamic therapy (PDT) has emerged as a promising therapeutic strategy for least-invasive treatment of glioma, which involves local irradiation of the tumor using an external near-infrared (NIR) laser. Unfortunately, most AIE photosensitizers suffered from poorly penetration of the visible light excitation, bad spatiotemporal resolution in deep tissues and low efficient blood-brain barrier (BBB) crossing ability, which greatly limited the clinical practice of AIE photosensitizers for especially deep-seated brain tumor treatment. In this work, we developed a multifunctional NIR-driven theranostic agent through hybrid of AIE photosensitizers TIND with rare-earth doping nanoparticles (RENPs) NaGdF₄:Nd/Yb/Tm with up/down dual-mode conversion luminescence. The theranostic agent was further decorated with D-type neuropeptide ^DNPY for crossing BBB and targeting glioma. Under the 808-nm light irradiation, the down-conversion NIR-II luminescence could indicate the position glioma and the upconversion NIR-I luminescence could trigger the AIE photosensitizers producing reactive oxygen species to inhibit orthotopic glioma tumor growth in situ. These results demonstrate that the integration of Dtype neuropeptide, AIE photosensitizers and RENPs could be promising candidates for in vivo NIR-II fluorescence image-guided through-skull PDT treatments of brain tumors.

Keywords

aggregation-induced emission / D-type neuropeptide / glioma / photodynamic therapy / rare-earth doping nanoparticles

References

[1] J. T. Huse, E. C. Holland, Nat. Rev. Cancer 2010, 10, 319.

[2] D. N. Louis, A. Perry, P. Wesseling, D. J. Brat, I. A. Cree, D. Figarella-Branger, C. Hawkins, H. K. Ng, S. M. Pfister, G. Reifenberger, R. Soffietti, A. von Deimling, D. W. Ellison, Neuro-Oncology 2021, 23, 1231.

[3] R. L. Siegel, K. D. Miller, H. E. Fuchs, A. Jemal, CA Cancer J. Clin. 2022, 72, 7.

[4] N. Sanai, M. S. Berger, Neurosurgery 2008, 62, 753.

[5] H. S. Friedman, T. Kerby, H. Calvert, Clin. Cancer Res. 2000, 6, 2585.

[6] A. Omuro, L. M. DeAngelis, JAMA 2013, 310, 1842.

[7] N. A. O Bush, S. M. Chang, M. S. Berger, Neurosurg. Rev. 2017, 40, 1.

[8] K. J. Langen, N. Galldiks, E. Hattingen, N. J. Shah, Nat. Rev. Neurosci. 2017, 13, 279.

[9] X. Li, J. F. Lovell, J. Yoon, X. Chen, Nat. Rev. Clin. Oncol. 2020, 17, 657.

[10] J. Chen, T. Fan, Z. Xie, Q. Zeng, P. Xue, T. Zheng, Y. Chen, X. Luo, H. Zhang, Biomaterials 2020, 237, 119827.

[11] W. Fan, P. Huang, X. Chen, Chem. Soc. Rev. 2016, 45, 6488.

[12] J. Ni, Y. Wang, H. Zhang, J. Z. Sun, B. Z. Tang, Molecules 2021, 26, 268.

[13] S. Wang, X. Wang, L. Yu, M. Sun, Photodiagnosis Photodyn. Ther. 2021, 34, 102254.

[14] S. D. Xu, Y. Y. Yuan, X. L. Cai, C. J. Zhang, F. Hu, J. Liang, G. X. Zhang, D. Q. Zhang, B. Liu, Chem. Sci. 2015, 6, 5824.

[15] X. Z. Zhao, J. P. Liu, J. L. Fan, H. Chao, X. J. Peng, Chem. Soc. Rev. 2021, 50, 4185.

[16] K. Wanderi, Z. Cui, Exploration 2022, 2, 20210097.

[17] J. Lv, Y. Xing, X. Li, X. Du, Exploration 2022, 2, 20210162.

[18] D. Mao, F. Hu, Z. G. Yi, K. Kenry, S. D. Xu, S. Q. Yan, Z. C. Luo, W. B. Wu, Z. H. Wang, D. L. Kong, X. G. Liu, B. Liu, Sci. Adv. 2020, 6, eabb2712.

[19] Y. Guan, H. G. Lu, W. Li, Y. D. Zheng, Z. Jiang, J. L. Zou, H. Gao, ACS Appl. Mater. Interfaces 2017, 9, 26731.

[20] Q. Xin, H. Ma, H. Wang, X. Zhang, Exploration 2023, 3, 20210473.

[21] F. Li, Y. Du, J. Liu, H. Sun, J. Wang, R. Li, D. Kim, T. Hyeon, D. Ling, Adv. Mater. 2018, 30, 1802808.

[22] G. Jin, R. He, Q. Liu, M. Lin, Y. Dong, K. Li, B. Z. Tang, B. Liu, F. Xu, Theranostics 2019, 9, 246.

[23] P. L. Kubben, K. J. ter Meulen, O. Schijns, M. P. ter Laak-Poort, J. J. van Overbeeke, H. van Santbrink, Lancet Oncol. 2011, 12, 1062.

[24] W. Chen, J. Nucl. Med. 2007, 48, 1468.

[25] P. Beard, Interface Focus 2011, 1, 602.

[26] L. Z. Zhao, J. Y. Zhu, Y. J. Cheng, Z. J. Xiong, Y. Q. Tang, L. L. Guo, X. Y. Shi, J. H. Zhao, ACS Appl. Mater. Interfaces 2015, 7, 19798.

[27] Y. Wu, F. Zhang, View 2020, 1, 20200068.

[28] Z. Hu, C. Fang, B. Li, Z. Zhang, C. Cao, M. Cai, S. Su, X. Sun, X. Shi, C. Li, T. Zhou, Y. Zhang, C. Chi, P. He, X. Xia, Y. Chen, S. S. Gambhir, Z. Cheng, J. Tian, Nat. Biomed. Eng. 2020, 4, 259.

[29] F. Wang, H. Wan, Z. Ma, Y. Zhong, Q. Sun, Y. Tian, L. Qu, H. Du, M. Zhang, L. Li, H. Ma, J. Luo, Y. Liang, W. J. Li, G. Hong, L. Liu, H. Dai, Nat. Methods 2019, 16, 545.

[30] S. Zhu, R. Tian, A. L. Antaris, X. Chen, H. Dai, Adv. Mater. 2019, 31, 1900321.

[31] Y. Zhong, Z. Ma, S. Zhu, J. Yue, M. Zhang, A. L. Antaris, J. Yuan, R. Cui, H. Wan, Y. Zhou, W. Wang, N. F. Huang, J. Luo, Z. Hu, H. Dai, Nat. Commun. 2017, 8, 737.

[32] Y. Zhong, Z. Ma, F. Wang, X. Wang, Y. Yang, Y. Liu, X. Zhao, J. Li, H. Du, M. Zhang, Q. Cui, S. Zhu, Q. Sun, H. Wan, Y. Tian, Q. Liu, W. Wang, K. C. Garcia, H. Dai, Nat. Biotech. 2019, 37, 1322.

[33] H. Li, X. Wang, X. Li, S. Zeng, G. Chen, Chem. Mater. 2020, 32, 3365.

[34] L. Youbin, M. Jiang, Z. Xue, S. Zeng, Theranostics 2020, 10, 6875.

[35] R. Daneman, Ann. Neurol. 2012, 72, 648.

[36] Y. Chen, L. Liu, Adv. Drug Delivery Rev. 2012, 64, 640.

[37] X. Wei, C. Zhan, Q. Shen, W. Fu, C. Xie, J. Gao, C. Peng, P. Zheng, W. Lu, Angew. Chem. Int. Ed. 2015, 54, 3023.

[38] Y. Li, Y. Pan, Y. Wang, Z. Jiang, O. U. Akakuru, M. Li, X. Zhang, B. Yuan, J. Xing, L. Luo, D. Larhammar, A. Wu, J. Li, Nano Today 2022, 44, 101465.

[39] Q. Chen, C. Wang, L. Cheng, W. W. He, Z. Cheng, Z. Liu, Biomaterials 2014, 35, 2915.

[40] A. Douplik, G. Saiko, I. Schelkanova, V. V. Tuchin, Lasers for Medical Applications, 2013, Sawston, UK: Woodhead Publishing.

[41] X. Xu, G. Deng, Z. Sun, Y. Luo, J. Liu, X. Yu, Y. Zhao, P. Gong, G. Liu, P. Zhang, F. Pan, L. Cai, B. Z. Tang, Adv. Mater. 2021, 33, 2102322.

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2023 2023 The Authors. Aggregate published by SCUT, AIEI, and John Wiley & Sons Australia, Ltd.