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Research Article

3D magnetic field guided sunflower-like nanocatalytic active swarm targeting patients-derived organoids

Dong Liu1,2,§Ruirui Guo1,2,§Shuangshuang Mao3,§Yanjie Huang1,2Bin Wang1Zijian Wu1Xuanjie Xia1Jian Dong2Yu Xin4Ruiyang Xie5Jianzhong Shou5Wei Sun6Yuan Pang3( )Yuan Lu1( )
Key Laboratory of Industrial Biocatalysis, Ministry of Education, Department of Chemical Engineering, Tsinghua University, Beijing 100084, China
Tianjin Industrial Microbiology Key Laboratory, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, China
Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, China
Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100070, China
National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
Biomanufacturing Center, Dept. of Mechanical Engineering, Tsinghua University, Beijing 100084, China

§ Dong Liu, Ruirui Guo, and Shuangshuang Mao contributed equally to this work.

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Graphical Abstract

A sunflower-like nanocatalytic active swarm (SNCAS) controlled by three-dimensional (3D) magnetic field was proposed for synergistic tumor-selective nanocatalysis and magnetic-actively tumor-targeting therapeutics. SNCAS presented significant lethality toward 3D organoid structure after magnetic targeting propulsion. Patient-derived 3D cancer organoid was proved as a powerful tool for the effectiveness verification of tumor therapeutic outcomes.

Abstract

Nanocatalytic medicine triggering in situ catalytic reactions has been considered as a promising strategy for tumor-selective therapeutics. However, the targeted distribution of nanocatalysts was still low, considering the absence of targeting propulsion capability. Here, encouraged by the fast-developing controllable microrobotics for targeting delivery, a sunflower-like nanocatalytic active swarm (SNCAS) controlled by a three-dimensional (3D) magnetic field was proposed for synergistic tumor-selective and magnetic-actively tumor-targeting therapeutics. Furthermore, a patient-derived renal cancer cell 3D organoid was utilized for the verification of the effective tumor therapeutic outcomes. Under the targeted control of 3D magnetic field, the multiple cascade catalytic efficiency of SNCAS based on Fenton reaction was evaluated, resulting in efficient tumor cell apoptosis and death. For the patient-derived organoid treatment, the SNCAS presented significant lethality toward 3D organoid structure to induce cell apoptosis with the collapse of organoid morphology. The targeting efficiency was further enhanced under the magnetic-controllable of SNCAS. Overall, empowered by the magnetic control technology, the synergistic therapeutic strategy based on controllable swarm combined active targeting and tumor-specific catalytic nanomedicine has provided a novel way for advanced cancer therapy. Meanwhile, 3D patient-derived organoids were proved as a powerful tool for the effectiveness verification of nanocatalytic medicine.

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References

[1]

Lin, H.; Chen, Y.; Shi, J. L. Nanoparticle-triggered in situ catalytic chemical reactions for tumour-specific therapy. Chem. Soc. Rev. 2018, 47, 1938–1958.

[2]

Yang, B. W.; Chen, Y.; Shi, J. L. Nanocatalytic medicine. Adv. Mater. 2019, 31, 1901778.

[3]

Huo, M. F.; Wang, L. Y.; Chen, Y.; Shi, J. L. Tumor-selective catalytic nanomedicine by nanocatalyst delivery. Nat. Commun. 2017, 8, 357.

[4]

Zhang, C.; Zhao, K. L.; Bu, W. B.; Ni, D. L.; Liu, Y. Y.; Feng, J. W.; Shi, J. L. Marriage of scintillator and semiconductor for synchronous radiotherapy and deep photodynamic therapy with diminished oxygen dependence. Angew. Chem., Int. Ed. 2015, 54, 1770–1774.

[5]

Zhang, C.; Ni, D. L.; Liu, Y. Y.; Yao, H. L.; Bu, W. B.; Shi, J. L. Magnesium silicide nanoparticles as a deoxygenation agent for cancer starvation therapy. Nat. Nanotechnol. 2017, 12, 378–386.

[6]

Huang, P.; Qian, X. Q.; Chen, Y.; Yu, L. D.; Lin, H.; Wang, L. Y.; Zhu, Y. F.; Shi, J. L. Metalloporphyrin-encapsulated biodegradable nanosystems for highly efficient magnetic resonance imaging-guided sonodynamic cancer therapy. J. Am. Chem. Soc. 2017, 139, 1275–1284.

[7]

Gu, T. X.; Wang, Y.; Lu, Y. H.; Cheng, L.; Feng, L. Z.; Zhang, H.; Li, X.; Han, G. R.; Liu, Z. Platinum nanoparticles to enable electrodynamic therapy for effective cancer treatment. Adv. Mater. 2019, 31, 1806803.

[8]

Ding, B. B.; Shao, S.; Yu, C.; Teng, B.; Wang, M. F.; Cheng, Z. Y.; Wong, K. L.; Ma, P. A.; Lin, J. Large-pore mesoporous-silica-coated upconversion nanoparticles as multifunctional immunoadjuvants with ultrahigh photosensitizer and antigen loading efficiency for improved cancer photodynamic immunotherapy. Adv. Mater. 2018, 30, 1802479.

[9]

Gao, S. S.; Lin, H.; Zhang, H. X.; Yao, H. L.; Chen, Y.; Shi, J. L. Nanocatalytic tumor therapy by biomimetic dual inorganic nanozyme-catalyzed cascade reaction. Adv. Sci. 2019, 6, 1801733.

[10]

Yang, B. W.; Chen, Y.; Shi, J. L. Reactive oxygen species (ROS)-based nanomedicine. Chem. Rev. 2019, 119, 4881–4985.

[11]

Wang, B.; Kostarelos, K.; Nelson, B. J.; Zhang, L. Trends in micro-/nanorobotics: Materials development, actuation, localization, and system integration for biomedical applications. Adv. Mater. 2021, 33, 2002047.

[12]

Yan, X. H.; Zhou, Q.; Vincent, M.; Deng, Y.; Yu, J. F.; Xu, J. B.; Xu, T. T.; Tang, T.; Bian, L. M.; Wang, Y. X. J. et al. Multifunctional biohybrid magnetite microrobots for imaging-guided therapy. Sci. Robot. 2017, 2, eaaq1155.

[13]

Hu, W. Q.; Lum, G. Z.; Mastrangeli, M.; Sitti, M. Small-scale soft-bodied robot with multimodal locomotion. Nature 2018, 554, 81–85.

[14]

Alapan, Y.; Bozuyuk, U.; Erkoc, P.; Karacakol, A. C.; Sitti, M. Multifunctional surface microrollers for targeted cargo delivery in physiological blood flow. Sci. Robot. 2020, 5, eaba5726.

[15]

Yu, J. F.; Wang, B.; Du, X. Z.; Wang, Q. Q.; Zhang, L. Ultra-extensible ribbon-like magnetic microswarm. Nat. Commun. 2018, 9, 3260.

[16]

Yu, J. F.; Jin, D. D.; Chan, K. F.; Wang, Q. Q.; Yuan, K.; Zhang, L. Active generation and magnetic actuation of microrobotic swarms in bio-fluids. Nat. Commun. 2019, 10, 5631.

[17]

Xie, H.; Sun, M. M.; Fan, X. J.; Lin, Z. H.; Chen, W. N.; Wang, L.; Dong, L. X.; He, Q. Reconfigurable magnetic microrobot swarm: Multimode transformation, locomotion, and manipulation. Sci. Robot. 2019, 4, eaav8006.

[18]

Jin, D. D.; Yuan, K.; Du, X. Z.; Wang, Q. Q.; Wang, S. J.; Zhang, L. Domino reaction encoded heterogeneous colloidal microswarm with on-demand morphological adaptability. Adv. Mater. 2021, 33, 2100070.

[19]

Xu, H. X.; Lyu, X. D.; Yi, M.; Zhao, W. H.; Song, Y. P.; Wu, K. M. Organoid technology and applications in cancer research. J. Hematol. Oncol. 2018, 11, 116.

[20]

Pampaloni, F.; Reynaud, E. G.; Stelzer, E. H. K. The third dimension bridges the gap between cell culture and live tissue. Nat. Rev. Mol. Cell Biol. 2007, 8, 839–845.

[21]

Invrea, F.; Rovito, R.; Torchiaro, E.; Petti, C.; Isella, C.; Medico, E. Patient-derived xenografts (PDXs) as model systems for human cancer. Curr. Opin. Biotechnol. 2020, 63, 151–156.

[22]

Di Renzo, M. F.; Corso, S. Patient-derived cancer models. Cancers, 2020, 12, 3779.

[23]

Li, M.; Belmonte, J. C. I. Organoids—Preclinical models of human disease. N. Engl. J. Med. 2019, 380, 569–579.

[24]

Lee, S. H.; Hu, W. H.; Matulay, J. T.; Silva, M. V.; Owczarek, T. B.; Kim, K.; Chua, C. W.; Barlow, L. J.; Kandoth, C.; Williams, A. B. et al. Tumor evolution and drug response in patient-derived organoid models of bladder cancer. Cell 2018, 173, 515–528.e17.

[25]

Van De Wetering, M.; Francies, H. E.; Francis, J. M.; Bounova, G.; Iorio, F.; Pronk, A.; Van Houdt, W.; Van Gorp, J.; Taylor-Weiner, A.; Kester, L. et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 2015, 161, 933–945.

[26]

Kim, M.; Mun, H.; Sung, C. O.; Cho, E. J.; Jeon, H. J.; Chun, S. M.; Jung, D. J.; Shin, T. H.; Jeong, G. S.; Kim, D. K. et al. Patient-derived lung cancer organoids as in vitro cancer models for therapeutic screening. Nat. Commun. 2019, 10, 3991.

[27]

Tan, Q.; Choi, K. M.; Sicard, D.; Tschumperlin, D. J. Human airway organoid engineering as a step toward lung regeneration and disease modeling. Biomaterials 2017, 113, 118–132.

[28]

Liu, J.; Sun, Z. K.; Deng, Y. H.; Zou, Y.; Li, C. Y.; Guo, X. H.; Xiong, L. Q.; Gao, Y.; Li, F. Y.; Zhao, D. Y. Highly water-dispersible biocompatible magnetite particles with low cytotoxicity stabilized by citrate groups. Angew. Chem., Int. Ed. 2009, 48, 5875–5879.

[29]

Deng, H.; Li, X. L.; Peng, Q.; Wang, X.; Chen, J. P.; Li, Y. D. Monodisperse magnetic single-crystal ferrite microspheres. Angew. Chem. 2005, 117, 2842–2845.

[30]

Jana, D.; Zhao, Y. L. Strategies for enhancing cancer chemodynamic therapy performance. Exploration 2022, 2, 20210238.

[31]

Huang, H.; Dong, C. H.; Chang, M. Q.; Ding, L.; Chen, L.; Feng, W.; Chen, Y. Mitochondria-specific nanocatalysts for chemotherapy-augmented sequential chemoreactive tumor therapy. Exploration 2021, 1, 50–60.

[32]

Liu, Y. L.; Zhao, X. J.; Yang, X. X.; Li, Y. F. A nanosized metal-organic framework of Fe-MIL-88NH2 as a novel peroxidase mimic used for colorimetric detection of glucose. Analyst 2013, 138, 4526–4531.

[33]

Dai, Y. L.; Xu, C.; Sun, X. L.; Chen, X. Y. Nanoparticle design strategies for enhanced anticancer therapy by exploiting the tumour microenvironment. Chem. Soc. Rev. 2017, 46, 3830–3852.

[34]

Luo, W. J.; Zhu, C. F.; Su, S.; Li, D.; He, Y.; Huang, Q.; Fan, C. H. Self-catalyzed, self-limiting growth of glucose oxidase-mimicking gold nanoparticles. ACS Nano 2010, 4, 7451–7458.

[35]

Dong, Y.; Wang, L.; Yuan, K.; Ji, F. T.; Gao, J. H.; Zhang, Z. F.; Du, X. Z.; Tian, Y.; Wang, Q. Q.; Zhang, L. Magnetic microswarm composed of porous nanocatalysts for targeted elimination of biofilm occlusion. ACS Nano 2021, 15, 5056–5067.

[36]

Tuveson, D.; Clevers, H. Cancer modeling meets human organoid technology. Science 2019, 364, 952–955.

[37]

Keller, L.; Pantel, K. Unravelling tumour heterogeneity by single-cell profiling of circulating tumour cells. Nat. Rev. Cancer 2019, 19, 553–567.

[38]

Jiang, S. W.; Zhao, H. R.; Zhang, W. J.; Wang, J. Q.; Liu, Y. H.; Cao, Y. X.; Zheng, H. H.; Hu, Z. W.; Wang, S. B.; Zhu, Y. et al. An automated organoid platform with inter-organoid homogeneity and inter-patient heterogeneity. Cell Rep. Med. 2020, 1, 100161.

[39]

Vlachogiannis, G.; Hedayat, S.; Vatsiou, A.; Jamin, Y.; Fernández-Mateos, J.; Khan, K.; Lampis, A.; Eason, K.; Huntingford, I.; Burke, R. et al. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science 2018, 359, 920–926.

[40]

Nayman, A. H.; Siginc, H.; Zemheri, E.; Yencilek, F.; Yildirim, A.; Telci, D. Dual-inhibition of mTOR and Bcl-2 enhances the anti-tumor effect of everolimus against renal cell carcinoma in vitro and in vivo. J. Cancer 2019, 10, 1466–1478.

[41]

Zhang, Y. P.; Narayanan, S. P.; Mannan, R.; Raskind, G.; Wang, X. M.; Vats, P.; Su, F. Y.; Hosseini, N.; Cao, X. H.; Kumar-Sinha, C. et al. Single-cell analyses of renal cell cancers reveal insights into tumor microenvironment, cell of origin, and therapy response. Proc. Natl. Acad. Sci. USA 2021, 118, e2103240118.

Nano Research
Pages 1021-1032
Cite this article:
Liu D, Guo R, Mao S, et al. 3D magnetic field guided sunflower-like nanocatalytic active swarm targeting patients-derived organoids. Nano Research, 2023, 16(1): 1021-1032. https://doi.org/10.1007/s12274-022-4851-z
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Received: 03 June 2022
Revised: 31 July 2022
Accepted: 01 August 2022
Published: 12 September 2022
© Tsinghua University Press 2022
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