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Research Article

Engineering CeO2/CuO heterostructure anchored on upconversion nanoparticles with boosting ROS generation-primed apoptosis-ferroptosis for cancer dynamic therapy

Xuan Gao1,2, Jing Feng1,2( ), Kehong Lv1,2, Yifei Zhou1,2, Ruohao Zhang1,2, Shuyan Song1,2, Hongjie Zhang1,2,3( ), Daguang Wang4( )
State Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, China
School of Applied Chemistry and Engineering, University of Science and Technology of China, Hefei 230026, China
Department of Chemistry, Tsinghua University, Beijing 100084, China
Gastric and Intestinal Department, General Surgery Center, First Hospital of Jilin University, Changchun 130021, China
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Graphical Abstract

An intelligent nanocomposite with designed CeO2/CuO heterostructure anchored on upconversion nanoparticles and cancer cell membrane modification exhibits great cytotoxicity toward cancer cells to trigger combinative apoptosis and ferroptosis via synergistic synergistic photodynamic therapy (PDT)/chemodynamic therapy (CDT).

Abstract

Highly toxic reactive oxygen species (ROS) induced apoptosis and ferroptosis have been considered as significant cell death pathways for cancer therapy. However, insufficient amount of intracellular ROS extremely restricts the therapeutic effect. Toward this, we report a rationally designed nanocomposite (mUCC) with enhanced ROS generation ability, inducing the combination of apoptosis and ferroptosis through synergistic photodynamic therapy (PDT) and chemodynamic therapy (CDT). Under 808 nm near-infrared (NIR) light irradiation, photocatalytic reaction is triggered starting from the separation of electron–hole pairs on the surface of heterojunction (CeO2/CuO), realizing improved ROS production. Simultaneously, mUCC served as Fenton-like agent exhibits considerable ability to generate highly toxic ·OH under tumor microenvironment (TME). The boosted accumulation of ROS disrupts the redox balance within tumor cells and results in the integration of apoptosis and ferroptosis. In addition, mUCC shows satisfactory tumor targeting property benefiting from the cancer cell membrane functionalization under the guidance of magnetic resonance imaging (MRI) and NIR fluorescence imaging. The intelligent mUCC with good biocompatibility and excellent antitumor response achieves efficient tumor elimination under synergistic PDT and CDT. This work offers an elective approach for further development of ROS-based therapeutic nanoplatform in cancer therapy.

Keywords

upconversion nanoparticlesheterojunctionreactive oxygen speciesapoptosis-ferroptosissynergistic dynamic therapy

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References

[1]

Brown, S. B.; Brown, E. A.; Walker, I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 2004, 5, 497–508.
Crossref Google Scholar
[2]

Castano, A. P.; Mroz, P.; Hamblin, M. R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545.
Crossref Google Scholar
[3]

Agostinis, P.; Berg, K.; Cengel, K. A.; Foster, T. H.; Girotti, A. W.; Gollnick, S. O.; Hahn, S. M.; Hamblin, M. R.; Juzeniene, A.; Kessel, D. et al. Photodynamic therapy of cancer: An update. Ca Cancer J. Clin. 2011, 61, 250–281.
Crossref Google Scholar
[4]

DeRosa, M. C.; Crutchley, R. J. Photosensitized singlet oxygen and its applications. Coord. Chem. Rev. 2002, 233–234, 351–371.
Crossref Google Scholar
[5]

Choi, J.; Sun, I. C.; Hwang, H. S.; Yoon, H. Y.; Kim, K. Light-triggered photodynamic nanomedicines for overcoming localized therapeutic efficacy in cancer treatment. Adv. Drug Delivery Rev. 2022, 186, 114344.
Crossref Google Scholar
[6]

Chen, C.; Wu, C. S.; Yu, J. M.; Zhu, X. H.; Wu, Y. H.; Liu, J. L.; Zhang, Y. Photodynamic-based combinatorial cancer therapy strategies: Tuning the properties of nanoplatform according to oncotherapy needs. Coord. Chem. Rev. 2022, 461, 214495.
Crossref Google Scholar
[7]

Xie, J. L.; Wang, Y. W.; Choi, W.; Jangili, P.; Ge, Y. Q.; Xu, Y. J.; Kang, J. L.; Liu, L. P.; Zhang, B.; Xie, Z. J. et al. Overcoming barriers in photodynamic therapy harnessing nano-formulation strategies. Chem. Soc. Rev. 2021, 50, 9152–9201.
Crossref Google Scholar
[8]

Chen, H.; Wan, Y. P.; Cui, X.; Li, S. L.; Lee, C. S. Recent advances in hypoxia-overcoming strategy of aggregation-induced emission photosensitizers for efficient photodynamic therapy. Adv. Healthc. Mater. 2021, 10, 2101607.
Crossref Google Scholar
[9]

Wang, Y. Y.; Liu, Y. C.; Sun, H. W.; Guo, D. S. Type I photodynamic therapy by organic–inorganic hybrid materials: From strategies to applications. Coord. Chem. Rev. 2019, 395, 46–62.
Crossref Google Scholar
[10]

Ethirajan, M.; Chen, Y. H.; Joshi, P.; Pandey, R. K. The role of porphyrin chemistry in tumor imaging and photodynamic therapy. Chem. Soc. Rev. 2011, 40, 340–362.
Crossref Google Scholar
[11]

McKenzie, L. K.; Bryant, H. E.; Weinstein, J. A. Transition metal complexes as photosensitisers in one- and two-photon photodynamic therapy. Coord. Chem. Rev. 2019, 379, 2–29.
Crossref Google Scholar
[12]

Pham, T. C.; Nguyen, V. N.; Choi, Y.; Lee, S.; Yoon, J. Recent strategies to develop innovative photosensitizers for enhanced photodynamic therapy. Chem. Rev. 2021, 121, 13454–13619.
Crossref Google Scholar
[13]

Fan, J. X.; Liu, M. D.; Li, C. X.; Hong, S.; Zheng, D. W.; Liu, X. H.; Chen, S.; Cheng, H.; Zhang, X. Z. A metal-semiconductor nanocomposite as an efficient oxygen-independent photosensitizer for photodynamic tumor therapy. Nanoscale Horiz. 2017, 2, 349–355.
Crossref Google Scholar
[14]

Younis, M. R.; He, G.; Qu, J. L.; Lin, J.; Huang, P.; Xia, X. H. Inorganic nanomaterials with intrinsic singlet oxygen generation for photodynamic therapy. Adv. Sci. 2021, 8, 2102587.
Crossref Google Scholar
[15]

Rodríguez-Barajas, N.; Anaya-Esparza, L. M.; Villágran-De La Mora, Z.; Sánchez-Burgos, J. A.; Pérez-Larios, A. Review of therapies using TiO2 nanomaterials for increased anticancer capability. Anticancer Agents Med. Chem. 2022, 22, 2241–2254.
Crossref Google Scholar
[16]

Doane, T. L.; Burda, C. The unique role of nanoparticles in nanomedicine: Imaging, drug delivery and therapy. Chem. Soc. Rev. 2012, 41, 2885–2911.
Crossref Google Scholar
[17]

Zhen, W. Y.; Liu, Y.; Jia, X. D.; Wu, L.; Wang, C.; Jiang, X. E. Reductive surfactant-assisted one-step fabrication of a BiOI/BiOIO3 heterojunction biophotocatalyst for enhanced photodynamic theranostics overcoming tumor hypoxia. Nanoscale Horiz. 2019, 4, 720–726.
Crossref Google Scholar
[18]

Cheng, Y.; Kong, X. P.; Chang, Y.; Feng, Y. L.; Zheng, R. X.; Wu, X. Q.; Xu, K. Q.; Gao, X. F.; Zhang, H. Y. Spatiotemporally synchronous oxygen self-supply and reactive oxygen species production on Z-scheme heterostructures for hypoxic tumor therapy. Adv. Mater. 2020, 32, 1908109.
Crossref Google Scholar
[19]

Wang, K.; Zhang, Z.; Lin, L.; Chen, J.; Hao, K.; Tian, H. Y.; Chen, X. S. Covalent organic nanosheets integrated heterojunction with two strategies to overcome hypoxic-tumor photodynamic therapy. Chem. Mater. 2019, 31, 3313–3323.
Crossref Google Scholar
[20]

Wang, Y.; Zhao, J. X.; Chen, Z.; Zhang, F.; Wang, Q.; Guo, W.; Wang, K.; Lin, H. M.; Qu, F. Y. Construct of MoSe2/Bi2Se3 nanoheterostructure: Multimodal CT/PT imaging-guided PTT/PDT/chemotherapy for cancer treating. Biomaterials 2019, 217, 119282.
Crossref Google Scholar
[21]

Li, S. L.; Jiang, P.; Jiang, F. L.; Liu, Y. Recent advances in nanomaterial-based nanoplatforms for chemodynamic cancer therapy. Adv. Funct. Mater. 2021, 31, 2100243.
Crossref Google Scholar
[22]

Liu, Y.; Zhen, W. Y.; Jin, L. H.; Zhang, S. T.; Sun, G. Y.; Zhang, T. Q.; Xu, X.; Song, S. Y.; Wang, Y. H.; Liu, J. H. et al. All-in-one theranostic nanoagent with enhanced reactive oxygen species generation and modulating tumor microenvironment ability for effective tumor eradication. ACS Nano 2018, 12, 4886–4893.
Crossref Google Scholar
[23]

Tian, Q. W.; Xue, F. F.; Wang, Y. R.; Cheng, Y. Y.; An, L.; Yang, S. P.; Chen, X. Y.; Huang, G. Recent advances in enhanced chemodynamic therapy strategies. Nano Today 2021, 39, 101162.
Crossref Google Scholar
[24]

Zhou, Y. F.; Fan, S. Y.; Feng, L. L.; Huang, X. L.; Chen, X. Y. Manipulating intratumoral Fenton chemistry for enhanced chemodynamic and chemodynamic-synergized multimodal therapy. Adv. Mater. 2021, 33, 2104223.
Crossref Google Scholar
[25]

Jia, C. Y.; Guo, Y. X.; Wu, F. G. Chemodynamic therapy via Fenton and Fenton-like nanomaterials: Strategies and recent advances. Small 2022, 18, 2103868.
Crossref Google Scholar
[26]

Cao, C. Y.; Wang, X. R.; Yang, N.; Song, X. J.; Dong, X. C. Recent advances of cancer chemodynamic therapy based on Fenton/Fenton-like chemistry. Chem. Sci. 2022, 13, 863–889.
Crossref Google Scholar
[27]

Chen, J.; Chen, F.; Zhang, L.; Yang, Z. Y.; Deng, T.; Zhao, Y. F.; Zheng, T. Y.; Gan, X. L.; Zhong, H. T.; Geng, Y. Q. et al. Self-assembling porphyrins as a single therapeutic agent for synergistic cancer therapy: A one stone three birds strategy. ACS Appl. Mater. Interfaces 2021, 13, 27856–27867.
Crossref Google Scholar
[28]

Zhang, L.; Li, C. X.; Wan, S. S.; Zhang, X. Z. Nanocatalyst-mediated chemodynamic tumor therapy. Adv. Healthc. Mater. 2022, 11, 2101971.
Crossref Google Scholar
[29]
Fu, J. T.; Zhou, Y. X.; Liu, T.; Wang, W. H.; Zhao, Y. T.; Sun, Y.; Zhang, Y. M.; Qin, W. X.; Chen, Z. W.; Lu, C. et al. A triple-enhanced chemodynamic approach based on glucose-powered hybrid nanoreactors for effective bacteria killing. Nano Res., in press, https://doi.org/10.1007/s12274-022-4854-9.
[30]

Liang, L.; Duan, Y.; Xiong, Y.; Zuo, W.; Ye, F.; Zhao, S. Synergistic cocatalytic effect of MoO3 and creatinine on Cu-Fenton reactions for efficient decomposition of H2O2. Mater. Today Chem. 2022, 24, 100805.
Crossref Google Scholar
[31]

Zhang, R. Y.; Liu, T.; Li, W. Z.; Ma, Z. Y.; Pei, P.; Zhang, W. W.; Yang, K.; Tao, Y. G. Tumor microenvironment-responsive BSA nanocarriers for combined chemo/chemodynamic cancer therapy. J. Nanobiotechnol. 2022, 20, 223.
Crossref Google Scholar
[32]

Zhu, H. J.; Huang, S. Y.; Ding, M. B.; Li, Z. B.; Li, J. C.; Wang, S. H.; Leong, D. T. Sulfur defect-engineered biodegradable cobalt sulfide quantum dot-driven photothermal and chemodynamic anticancer therapy. ACS Appl. Mater. Interfaces 2022, 14, 25183–25196.
Crossref Google Scholar
[33]

Qian, Y.; Zhang, J. H.; Zou, J. L.; Wang, X. Y.; Meng, X. F.; Liu, H. J.; Lin, Y. F.; Chen, Q. W.; Sun, L.; Lin, W. C. et al. NIR-II responsive PEGylated nickel nanoclusters for photothermal enhanced chemodynamic synergistic oncotherapy. Theranostics 2022, 12, 3690–3702.
Crossref Google Scholar
[34]

Yang, N.; Zhang, T.; Cao, C. Y.; Mao, G. X.; Shao, J. J.; Song, X. J.; Wang, W. J.; Mou, X. Z.; Dong, X. C. BSA stabilized photothermal-Fenton reactor with cisplatin for chemo/chemodynamic cascade oncotherapy. Nano Res. 2022, 15, 2235–2243.
Crossref Google Scholar
[35]

Liu, C. H.; Wang, D. D.; Zhang, S. Y.; Cheng, Y. R.; Yang, F.; Xing, Y.; Xu, T. L.; Dong, H. F.; Zhang, X. J. Biodegradable biomimic copper/manganese silicate nanospheres for chemodynamic/photodynamic synergistic therapy with simultaneous glutathione depletion and hypoxia relief. ACS Nano 2019, 13, 4267–4277.
Crossref Google Scholar
[36]

Cui, Y. Y.; Chen, X.; Cheng, Y.; Lu, X. Y.; Meng, J. J.; Chen, Z. W.; Li, M. K.; Lin, C. C.; Wang, Y. L.; Yang, J. CuWO4 nanodots for NIR-induced photodynamic and chemodynamic synergistic therapy. ACS Appl. Mater. Interfaces 2021, 13, 22150–22158.
Crossref Google Scholar
[37]

Chen, M. Y.; Yang, J. X.; Zhou, L. L.; Hu, X. C.; Wang, C. H.; Chai, K. K.; Li, R. H.; Feng, L.; Sun, Y. T.; Dong, C. Y. et al. Dual-responsive and ROS-augmented nanoplatform for chemo/photodynamic/chemodynamic combination therapy of triple negative breast cancer. ACS Appl. Mater. Interfaces 2022, 14, 57–68.
Crossref Google Scholar
[38]

Yang, H. Y.; Liu, R. F.; Xu, Y. X.; Qian, L. X.; Dai, Z. F. Photosensitizer nanoparticles boost photodynamic therapy for pancreatic cancer treatment. Nano-Micro Lett. 2021, 13, 35.
Crossref Google Scholar
[39]

Wang, L.; Xu, Y. T.; Liu, C.; Si, W. L.; Wang, W. J.; Zhang, Y. W.; Zhong, L. P.; Dong, X. C.; Zhao, Y. X. Copper-doped MOF-based nanocomposite for GSH depleted chemo/photothermal/chemodynamic combination therapy. Chem. Eng. J. 2022, 438, 135567.
Crossref Google Scholar
[40]

Lv, H. H.; Zhen, C. X.; Liu, J. Y.; Yang, P. F.; Hu, L. J.; Shang, P. Unraveling the potential role of glutathione in multiple forms of cell death in cancer therapy. Oxid. Med. Cell. Longev. 2019, 2019, 3150145.
Crossref Google Scholar
[41]

Zhang, A. M.; Zhang, Q.; Alfranca, G.; Pan, S. J.; Huang, Z. C.; Cheng, J.; Ma, Q.; Song, J.; Pan, Y. X.; Ni, J. et al. GSH-triggered sequential catalysis for tumor imaging and eradication based on star-like Au/Pt enzyme carrier system. Nano Res. 2020, 13, 160–172.
Crossref Google Scholar
[42]

Maiorino, M.; Conrad, M.; Ursini, F. GPX4, lipid peroxidation, and cell death: Discoveries, rediscoveries, and open issues. Antioxid. Redox Signal. 2018, 29, 61–74.
Crossref Google Scholar
[43]

Proneth, B.; Conrad, M. Ferroptosis and necroinflammation, a yet poorly explored link. Cell Death Differ. 2019, 26, 14–24.
Crossref Google Scholar
[44]

Chen, X.; Li, J. B.; Kang, R.; Klionsky, D. J.; Tang, D. L. Ferroptosis: Machinery and regulation. Autophagy 2021, 17, 2054–2081.
Crossref Google Scholar
[45]

Wang, S. F.; Li, F. Y.; Qiao, R. R.; Hu, X.; Liao, H. W.; Chen, L. M.; Wu, J. H.; Wu, H. B.; Zhao, M.; Liu, J. N. et al. Arginine-rich manganese silicate nanobubbles as a ferroptosis-inducing agent for tumor-targeted theranostics. ACS Nano 2018, 12, 12380–12392.
Crossref Google Scholar
[46]

Dixon, S. J.; Lemberg, K. M.; Lamprecht, M. R.; Skouta, R.; Zaitsev, E. M.; Gleason, C. E.; Patel, D. N.; Bauer, A. J.; Cantley, A. M.; Yang, W. S. et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012, 149, 1060–1072.
Crossref Google Scholar
[47]

Yang, W. S.; SriRamaratnam, R.; Welsch, M. E.; Shimada, K.; Skouta, R.; Viswanathan, V. S.; Cheah, J. H.; Clemons, P. A.; Shamji, A. F.; Clish, C. B. et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 2014, 156, 317–331.
Crossref Google Scholar
[48]

He, H. Z.; Du, L. H.; Guo, H. L.; An, Y. C.; Lu, L. J.; Chen, Y. L.; Wang, Y.; Zhong, H. H.; Shen, J.; Wu, J. et al. Redox responsive metal organic framework nanoparticles induces ferroptosis for cancer therapy. Small 2020, 16, 2001251.
Crossref Google Scholar
[49]

Wu, T. S.; Liang, X.; Liu, X.; Li, Y. M.; Wang, Y. T.; Kong, L.; Tang, M. Induction of ferroptosis in response to graphene quantum dots through mitochondrial oxidative stress in microglia. Part. Fibre Toxicol. 2020, 17, 30.
Crossref Google Scholar
[50]

Luo, S. W.; Ma, D.; Wei, R. L.; Yao, W.; Pang, X. R.; Wang, Y.; Xu, X. D.; Wei, X. H.; Guo, Y.; Jiang, X. Q. et al. A tumor microenvironment responsive nanoplatform with oxidative stress amplification for effective MRI-based visual tumor ferroptosis. Acta Biomater. 2022, 138, 518–527.
Crossref Google Scholar
[51]

Jasim, K. A.; Waheed, I. F.; Topps, M.; Gesquiere, A. J. Multifunctional system for combined chemodynamic-photodynamic therapy employing the endothelin axis based on conjugated polymer nanoparticles. Polym. Chem. 2021, 12, 5449–5466.
Crossref Google Scholar
[52]

Song, W. L.; Jia, P. F.; Zhang, T.; Dou, K. K.; Liu, L. B.; Ren, Y. P.; Liu, F. J.; Xue, J. M.; Hasanin, M. S.; Qi, H. Z. et al. Cell membrane-camouflaged inorganic nanoparticles for cancer therapy. J. Nanobiotechnol. 2022, 20, 289.
Crossref Google Scholar
[53]

Fang, H. Y.; Li, M. T.; Liu, Q. Y.; Gai, Y. K.; Yuan, L. J.; Wang, S.; Zhang, X.; Ye, M.; Zhang, Y. X.; Gao, M. Y. et al. Ultra-sensitive nanoprobe modified with tumor cell membrane for UCL/MRI/PET multimodality precise imaging of triple-negative breast cancer. Nano-Micro Lett. 2020, 12, 62.
Crossref Google Scholar
[54]

Guller, A. E.; Generalova, A. N.; Petersen, E. V.; Nechaev, A. V.; Trusova, I. A.; Landyshev, N. N.; Nadort, A.; Grebenik, E. A.; Deyev, S. M.; Shekhter, A. B. et al. Cytotoxicity and non-specific cellular uptake of bare and surface-modified upconversion nanoparticles in human skin cells. Nano Res. 2015, 8, 1546–1562.
Crossref Google Scholar
[55]

Meng, A. Y.; Zhang, L. Y.; Cheng, B.; Yu, J. G. Dual cocatalysts in TiO2 photocatalysis. Adv. Mater. 2019, 31, 1807660.
Crossref Google Scholar
[56]

Dong, F.; Zhao, Z. W.; Xiong, T.; Ni, Z. L.; Zhang, W. D.; Sun, Y. J.; Ho, W. K. In situ construction of g-C3N4/g-C3N4 metal-free heterojunction for enhanced visible-light photocatalysis. ACS Appl. Mater. Interfaces 2013, 5, 11392–11401.
Crossref Google Scholar
[57]

Pan, C. S.; Xu, J.; Wang, Y. J.; Li, D.; Zhu, Y. F. Dramatic activity of C3N4/BiPO4 photocatalyst with core/shell structure formed by self-assembly. Adv. Funct. Mater. 2012, 22, 1518–1524.
Crossref Google Scholar
[58]

Wang, N.; Pan, Y.; Lu, T.; Li, X. Z.; Wu, S. K.; Wu, J. L. A new ribbon-ignition method for fabricating p-CuO/n-CeO2 heterojunction with enhanced photocatalytic activity. Appl. Surf. Sci. 2017, 403, 699–706.
Crossref Google Scholar
[59]

Cheng, G.; Li, W. Q.; Ha, L.; Han, X. H.; Hao, S. J.; Wan, Y.; Wang, Z. G.; Dong, F. P.; Zou, X.; Mao, Y. W. et al. Self-assembly of extracellular vesicle-like metal-organic framework nanoparticles for protection and intracellular delivery of biofunctional proteins. J. Am. Chem. Soc. 2018, 140, 7282–7291.
Crossref Google Scholar
[60]

Liu, Y.; Luo, J. S.; Chen, X. J.; Liu, W.; Chen, T. K. Cell membrane coating technology: A promising strategy for biomedical applications. Nano-Micro Lett. 2019, 11, 100.
Crossref Google Scholar
[61]

Yang, H.; Ding, Y.; Tong, Z. R.; Qian, X. H.; Xu, H.; Lin, F. H.; Sheng, G. P.; Hong, L. J.; Wang, W. L.; Mao, Z. W. pH-responsive hybrid platelet membrane-coated nanobomb with deep tumor penetration ability and enhanced cancer thermal/chemodynamic therapy. Theranostics 2022, 12, 4250–4268.
Crossref Google Scholar
Nano Research
Volume 16 Issue 4,
April 2023
Pages 5322-5334
DOI: 10.1007/s12274-022-5223-4
Cite this article:
Gao X, Feng J, Lv K, et al. Engineering CeO2/CuO heterostructure anchored on upconversion nanoparticles with boosting ROS generation-primed apoptosis-ferroptosis for cancer dynamic therapy. Nano Research, 2023, 16(4): 5322-5334. https://doi.org/10.1007/s12274-022-5223-4
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Received: 28 September 2022
Revised: 18 October 2022
Accepted: 19 October 2022
Published: 10 January 2023
© Tsinghua University Press 2022
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