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Nano Research 2022, 15(8): 7320-7328 https://doi.org/10.1007/s12274-022-4359-6
Research Article | Issue | Published: 24 May 2022

Biomimetic copper single-atom nanozyme system for self-enhanced nanocatalytic tumor therapy

Show Author's Information Daoming Zhu1,§,  Ruoyu Ling1,§,  Hao Chen1,§,  Meng Lyu4,  Haisheng Qian2,  Konglin Wu3( ),  Guoxin Li1( ),  Xianwen Wang2( )
Department of General Surgery & Guangdong Provincial Key Laboratory of Precision Medicine for Gastrointestinal Tumor, Nanfang Hospital, The First School of Clinical Medicine, Southern Medical University, Guangzhou 510515, China
School of Biomedical Engineering, Research and Engineering Center of Biomedical Materials, Anhui Medical University, Hefei 230032, China
Institute of Clean Energy and Advanced Nanocatalysis, School of Chemistry and Chemical Engineering, Anhui University of Technology, Maanshan 243002, China
Department of Radiation and Medical Oncology, Hubei Key Laboratory of Tumor Biological Behaviors, Hubei Cancer Clinical Study Center, Zhongnan Hospital of Wuhan University, Wuhan 430071, China

§ Daoming Zhu, Ruoyu Ling, and Hao Chen contributed equally to this work.

Keywords:
single-atom nanozymes biomimetic system, self-enhanced nanocatalytic tumor therapy, glutamine metabolism inhibition, glutathione (GSH) depletion
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Zhu D, Ling R, Chen H, et al. Biomimetic copper single-atom nanozyme system for self-enhanced nanocatalytic tumor therapy. Nano Research, 2022, 15(8): 7320-7328. https://doi.org/10.1007/s12274-022-4359-6
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Abstract Full text Electronic supplementary material About this article

Single-atom nanozymes (SAZs) with peroxidase (POD)-like activity have good nanocatalytic tumor therapy (NCT) capabilities. However, insufficient hydrogen peroxide (H2O2) and hydrogen ions in the cells limit their therapeutic effects. Herein, to overcome these limitations, a biomimetic single-atom nanozyme system was developed for self-enhanced NCT. We used a previously described approach to produce platelet membrane vesicles. Using a high-temperature carbonization approach, copper SAZs with excellent POD-like activity were successfully synthesized. Finally, through physical extrusion, a proton pump inhibitor (PPI; pantoprazole sodium) and the SAZs were combined with platelet membrane vesicles to create PPS. Both in vivo and in vitro, PPS displayed good tumor-targeting and accumulation abilities. PPIs were able to simultaneously regulate the hydrogen ion, glutathione (GSH), and H2O2 content in tumor cells, significantly improve the catalytic ability of SAZs, and achieve self-enhanced NCT. Our in vivo studies showed that PPS had a tumor suppression rate of > 90%. PPS also limited the synthesis of GSH in cells at the source; thus, glutamine metabolism therapy and NCT were integrated into an innovative method, which provides a novel strategy for multimodal tumor therapy.


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Electronic supplementary material
About this article

Biomimetic copper single-atom nanozyme system for self-enhanced nanocatalytic tumor therapy

Show Author's information Daoming Zhu1,§, Ruoyu Ling1,§, Hao Chen1,§, Meng Lyu4, Haisheng Qian2, Konglin Wu3( ), Guoxin Li1( ), Xianwen Wang2( )
Department of General Surgery & Guangdong Provincial Key Laboratory of Precision Medicine for Gastrointestinal Tumor, Nanfang Hospital, The First School of Clinical Medicine, Southern Medical University, Guangzhou 510515, China
School of Biomedical Engineering, Research and Engineering Center of Biomedical Materials, Anhui Medical University, Hefei 230032, China
Institute of Clean Energy and Advanced Nanocatalysis, School of Chemistry and Chemical Engineering, Anhui University of Technology, Maanshan 243002, China
Department of Radiation and Medical Oncology, Hubei Key Laboratory of Tumor Biological Behaviors, Hubei Cancer Clinical Study Center, Zhongnan Hospital of Wuhan University, Wuhan 430071, China

§ Daoming Zhu, Ruoyu Ling, and Hao Chen contributed equally to this work.

Abstract

Single-atom nanozymes (SAZs) with peroxidase (POD)-like activity have good nanocatalytic tumor therapy (NCT) capabilities. However, insufficient hydrogen peroxide (H2O2) and hydrogen ions in the cells limit their therapeutic effects. Herein, to overcome these limitations, a biomimetic single-atom nanozyme system was developed for self-enhanced NCT. We used a previously described approach to produce platelet membrane vesicles. Using a high-temperature carbonization approach, copper SAZs with excellent POD-like activity were successfully synthesized. Finally, through physical extrusion, a proton pump inhibitor (PPI; pantoprazole sodium) and the SAZs were combined with platelet membrane vesicles to create PPS. Both in vivo and in vitro, PPS displayed good tumor-targeting and accumulation abilities. PPIs were able to simultaneously regulate the hydrogen ion, glutathione (GSH), and H2O2 content in tumor cells, significantly improve the catalytic ability of SAZs, and achieve self-enhanced NCT. Our in vivo studies showed that PPS had a tumor suppression rate of > 90%. PPS also limited the synthesis of GSH in cells at the source; thus, glutamine metabolism therapy and NCT were integrated into an innovative method, which provides a novel strategy for multimodal tumor therapy.

Keywords: single-atom nanozymes biomimetic system, self-enhanced nanocatalytic tumor therapy, glutamine metabolism inhibition, glutathione (GSH) depletion

References(64)

1

Wang, Y.; Zheng, X. B.; Wang, D. S. Design concept for electrocatalysts. Nano Res. 2022, 15, 1730–1752.
DOI Google Scholar
2
Jing, H. Y. ; Zhu, P. ; Zheng, X. B. ; Zhang, Z. D. ; Wang, D. S. ; Li, Y. D. Theory-oriented screening and discovery of advanced energy transformation materials in electrocatalysis. Adv. Powder Mater. 2021, in press, https://doi.org/10.1016/j.apmate.2021.10.004.
DOI
3

Li, W. H.; Yang, J. R.; Jing, H. Y.; Zhang, J.; Wang, Y.; Li, J.; Zhao, J.; Wang, D. S.; Li, Y. D. Creating high regioselectivity by electronic metal–support interaction of a single-atomic-site catalyst. J. Am. Chem. Soc. 2021, 143, 15453–15461.
DOI Google Scholar
4

Yang, J. R.; Li, W. H.; Tan, S. D.; Xu, K. N.; Wang, Y.; Wang, D. S.; Li, Y. D. The electronic metal–support interaction directing the design of single atomic site catalysts: Achieving high efficiency towards hydrogen evolution. Angew. Chem. 2021, 133, 19233–19239.
DOI Google Scholar
5

Han, A. L.; Wang, X. J.; Tang, K.; Zhang, Z. D.; Ye, C. L.; Kong, K. J.; Hu, H. B.; Zheng, L. R.; Jiang, P.; Zhao, C. X. et al. An adjacent atomic platinum site enables single-atom iron with high oxygen reduction reaction performance. Angew. Chem., Int. Ed. 2021, 60, 19262–19271.
DOI Google Scholar
6

Liu, Z. H.; Du, Y.; Zhang, P. F.; Zhuang, Z. C.; Wang, D. S. Bringing catalytic order out of chaos with nitrogen-doped ordered mesoporous carbon. Matter 2021, 4, 3161–3194.
DOI Google Scholar
7

Xiong, Y.; Sun, W. M.; Han, Y. H.; Xin, P. Y.; Zheng, X. S.; Yan, W. S.; Dong, J. C.; Zhang, J.; Wang, D. S.; Li, Y. D. Cobalt single atom site catalysts with ultrahigh metal loading for enhanced aerobic oxidation of ethylbenzene. Nano Res. 2021, 14, 2418–2423.
DOI Google Scholar
8

Chen, Y. J.; Gao, R.; Ji, S. F.; Li, H. J.; Tang, K.; Jiang, P.; Hu, H. B.; Zhang, Z. D.; Hao, H. G.; Qu, Q. Y. et al. Atomic-level modulation of electronic density at cobalt single-atom sites derived from metal-organic frameworks: Enhanced oxygen reduction performance. Angew. Chem., Int. Ed. 2021, 60, 3212–3221.
DOI Google Scholar
9

Zhang, S. L.; Ao, X.; Huang, J.; Wei, B.; Zhai, Y. L.; Zhai, D.; Deng, W. Q.; Su, C. L.; Wang, D. S.; Li, Y. D. Isolated single-atom Ni-N5 catalytic site in hollow porous carbon capsules for efficient lithium-sulfur batteries. Nano Lett. 2021, 21, 9691–9698.
DOI Google Scholar
10

Zhang, N. Q.; Zhang, X. X.; Tao, L.; Jiang, P.; Ye, C. L.; Lin, R.; Huang, Z. W.; Li, A.; Pang, D. W.; Yan, H. et al. Silver single-atom catalyst for efficient electrochemical CO2 reduction synthesized from thermal transformation and surface reconstruction. Angew. Chem., Int. Ed. 2021, 60, 6170–6176.
DOI Google Scholar
11

Gao, G.; Jiang, Y. W.; Guo, Y. X.; Jia, H. R.; Cheng, X. T.; Deng, Y.; Yu, Y. X.; Zhu, Y. X.; Guo, H. Y.; Sun, W. et al. Enzyme-mediated tumor starvation and phototherapy enhance mild-temperature photothermal therapy. Adv. Funct. Mater. 2020, 30, 1909391.
DOI Google Scholar
12

Chang, M. Y.; Hou, Z. Y.; Wang, M.; Yang, C. Z.; Wang, R. F.; Li, F.; Liu, D. L.; Peng, T. L.; Li, C. X.; Lin, J. Single-atom Pd nanozyme for ferroptosis-boosted mild-temperature photothermal therapy. Angew. Chem., Int. Ed. 2021, 60, 12971–12979.
DOI Google Scholar
13

Zhu, Y.; Wang, W. Y.; Cheng, J. J.; Qu, Y. T.; Dai, Y.; Liu, M. M.; Yu, J. N.; Wang, C. M.; Wang, H. J.; Wang, S. C. et al. Stimuli-responsive manganese single-atom nanozyme for tumor therapy via integrated cascade reactions. Angew. Chem. 2021, 133, 9566–9574.
DOI Google Scholar
14

Zhang, R. F.; Yan, X. Y.; Fan, K. L. Nanozymes inspired by natural enzymes. Acc. Mater. Res. 2021, 2, 534–547.
DOI Google Scholar
15

Han, A. J.; Chen, W. X.; Zhang, S. L.; Zhang, M. L.; Han, Y. H.; Zhang, J.; Ji, S. F.; Zheng, L. R.; Wang, Y.; Gu, L. et al. A polymer encapsulation strategy to synthesize porous nitrogen-doped carbon-nanosphere-supported metal isolated-single-atomic-site catalysts. Adv. Mater. 2018, 30, 1706508.
DOI Google Scholar
16

Huang, L.; Chen, J. X.; Gan, L. F.; Wang, J.; Dong, S. J. Single-atom nanozymes. Sci. Adv. 2019, 5, eaav5490.
DOI Google Scholar
17

Huo, M. F.; Wang, L. Y.; Wang, Y. W.; Chen, Y.; Shi, J. L. Nanocatalytic tumor therapy by single-atom catalysts. ACS Nano 2019, 13, 2643–2653.
Google Scholar
18

Jiao, L.; Yan, H. Y.; Wu, Y.; Gu, W. L.; Zhu, C. Z.; Du, D.; Lin, Y. H. When nanozymes meet single-atom catalysis. Angew. Chem., Int. Ed. 2020, 59, 2565–2576.
DOI Google Scholar
19

Zhao, C.; Xiong, C.; Liu, X. K.; Qiao, M.; Li, Z. J.; Yuan, T. W.; Wang, J.; Qu, Y. T.; Wang, X. Q.; Zhou, F. Y. et al. Unraveling the enzyme-like activity of heterogeneous single atom catalyst. Chem. Commun 2019, 55, 2285–2288.
DOI Google Scholar
20

Ji, S. F.; Jiang, B.; Hao, H. G.; Chen, Y. J.; Dong, J. C.; Mao, Y.; Zhang, Z. D.; Gao, R.; Chen, W. X.; Zhang, R. F. et al. Matching the kinetics of natural enzymes with a single-atom iron nanozyme. Nat. Catal. 2021, 4, 407–417.
DOI Google Scholar
21

Cao, F. F.; Zhang, L.; You, Y. W.; Zheng, L. R.; Ren, J. S.; Qu, X. G. An enzyme-mimicking single-atom catalyst as an efficient multiple reactive oxygen and nitrogen species scavenger for sepsis management. Angew. Chem., Int. Ed. 2020, 59, 5108–5115.
DOI Google Scholar
22

Wang, X.; Zhao, Y. B.; Shi, L.; Hu, Y.; Song, G. B.; Cai, K. Y.; Li, M. H.; Luo, Z. Tumor-targeted disruption of lactate transport with reactivity-reversible nanocatalysts to amplify oxidative damage. Small 2021, 17, 2100130.
DOI Google Scholar
23

Fu, L. H.; Hu, Y. R.; Qi, C.; He, T.; Jiang, S. S.; Jiang, C.; He, J.; Qu, J. L.; Lin, J.; Huang, P. Biodegradable manganese-doped calcium phosphate nanotheranostics for traceable cascade reaction-enhanced anti-tumor therapy. ACS Nano 2019, 13, 13985–13994.
DOI Google Scholar
24

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.
DOI Google Scholar
25

Meng, X. Q.; Li, D. D.; Chen, L.; He, H. L.; Wang, Q.; Hong, C. Y.; He, J. Y.; Gao, X. F.; Yang, Y. L.; Jiang, B. et al. High-performance self-cascade pyrite nanozymes for apoptosis-ferroptosis synergistic tumor therapy. ACS Nano 2021, 15, 5735–5751.
DOI Google Scholar
26

Altman, B. J.; Stine, Z. E.; Dang, C. V. From Krebs to clinic: Glutamine metabolism to cancer therapy. Nat. Rev. Cancer 2016, 16, 619–634.
DOI Google Scholar
27

Niu, B. Y.; Liao, K. X.; Zhou, Y. X.; Wen, T.; Quan, G. L.; Pan, X.; Wu, C. B. Application of glutathione depletion in cancer therapy: Enhanced ROS-based therapy, ferroptosis, and chemotherapy. Biomaterials 2021, 277, 121110.
DOI Google Scholar
28

Welbourne, T. C. Ammonia production and glutamine incorporation into glutathione in the functioning rat kidney. Can. J. Biochem. 1979, 57, 233–237.
Google Scholar
29

Wang, L.; Huang, X. J.; You, X. R.; Yi, T. Q.; Lu, B.; Liu, J. L.; Lu, G. H.; Ma, M. L.; Lu, G. H.; Ma, M. L. et al. Nanoparticle enhanced combination therapy for stem-like progenitors defined by single-cell transcriptomics in chemotherapy-resistant osteosarcoma. Sig. Trans. Target. Ther. 2020, 5, 196.
DOI Google Scholar
30

Yang, Y.; Liu, X.; Ma, W.; Xu, Q.; Chen, G.; Wang, Y. F.; Xiao, H. H.; Li, N.; Liang, X. J.; Yu, M. et al. Light-activatable liposomes for repetitive on-demand drug release and immunopotentiation in hypoxic tumor therapy. Biomaterials 2021, 265, 120456.
DOI Google Scholar
31

Rubio, I.; Suva, L. J.; Todorova, V.; Bhattacharyya, S.; Kaufmann, Y.; Maners, A.; Smith, M.; Klimberg, V. S. Oral glutamine reduces radiation morbidity in breast conservation surgery. J. Parenter. Enteral Nutr. 2013, 37, 623–630.
DOI Google Scholar
32

Cao, Y. H.; Kennedy, R.; Klimberg, V. S. Glutamine protects against doxorubicin-induced cardiotoxicity. J. Surg. Res. 1999, 85, 178–182.
DOI Google Scholar
33

Reinfeld, B. I.; Madden, M. Z.; Wolf, M. M.; Chytil, A.; Bader, J. E.; Patterson, A. R.; Sugiura, A.; Cohen, A. S.; Ali, A.; Do, B. T. et al. Cell-programmed nutrient partitioning in the tumour microenvironment. Nature 2021, 593, 282–288.
DOI Google Scholar
34

Xiao, Y. T.; Xiang, L. X.; Shao, J. Z. Vacuolar H+-ATPase. Int. J. Biochem. Cell Biol. 2008, 40, 2002–2006.
DOI Google Scholar
35

Luciani, F.; Spada, M.; De Milito, A.; Molinari, A.; Rivoltini, L.; Montinaro, A.; Marra, M.; Lugini, L.; Logozzi, M.; Lozupone, F. et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J. Natl. Cancer Inst. 2004, 96, 1702–1713.
DOI Google Scholar
36

Huang, Q.; Du, J.; Cheng, S. Q.; Gong, Z. C. Progress of proton pump inhibitors using in cancer patients. Chin. J. Clin. Pharmacol. Ther. 2018, 23, 1179–1187.
DOI Google Scholar
37

Xu, H. X.; Ren, D. J. Lysosomal physiology. Annu. Rev. Physiol. 2015, 77, 57–80.
DOI Google Scholar
38

Mayers, J. R.; Heiden, M. G. V. Famine versus feast: Understanding the metabolism of tumors in vivo. Trends Biochem. Sci. 2015, 40, 130–140.
DOI Google Scholar
39

Ye, H.; Wang, K. Y.; Wang, M. L.; Liu, R. Z.; Song, H.; Li, N.; Lu, Q.; Zhang, W. J.; Du, Y. Q.; Yang, W. Q. et al. Bioinspired nanoplatelets for chemo-photothermal therapy of breast cancer metastasis inhibition. Biomaterials 2019, 206, 1–12.
DOI Google Scholar
40

Duo, Y. H.; Liu, Q.; Zhu, D. M.; Zhang, B.; Luo, G. H.; Wang, F. B.; Chen, J. H.; Cao, Y. H. Proof of concept for dual anticancer effects by a novel nanomaterial-mediated cancer cell killing and nano-radiosensitization. Chem. Eng. J. 2022, 429, 132328.
DOI Google Scholar
41

Fang, R. H.; Kroll, A. V.; Gao, W. W.; Zhang, L. F. Cell membrane coating nanotechnology. Adv. Mater. 2018, 30, 1706759.
DOI Google Scholar
42

Zhu, D. M.; Duo, Y. H.; Suo, M.; Zhao, Y. H.; Xia, L. G.; Zheng, Z.; Li, Y.; Tang, B. Z. Tumor-exocytosed exosome/aggregation-induced emission luminogen hybrid nanovesicles facilitate efficient tumor penetration and photodynamic therapy. Angew. Chem. 2020, 132, 13940–13947.
DOI Google Scholar
43

Ma, W. J.; Zhu, D. M.; Li, J. H.; Chen, X.; Xie, W.; Jiang, X.; Wu, L.; Wang, G. G.; Xiao, Y. S.; Liu, Z. S. et al. Coating biomimetic nanoparticles with chimeric antigen receptor T cell-membrane provides high specificity for hepatocellular carcinoma photothermal therapy treatment. Theranostics 2020, 10, 1281–1295.
DOI Google Scholar
44

Shang, H. S.; Zhou, X. Y.; Dong, J. C.; Li, A.; Zhao, X.; Liu, Q. H.; Lin, Y.; Pei, J. J.; Li, Z.; Jiang, Z. L. et al. Engineering unsymmetrically coordinated Cu-S1N3 single atom sites with enhanced oxygen reduction activity. Nat. Commun. 2020, 11, 3049.
DOI Google Scholar
45

Jiang, Z. L.; Sun, W. M.; Shang, H. S.; Chen, W. X.; Sun, T. T.; Li, H. J.; Dong, J. C.; Zhou, J.; Li, Z.; Wang, Y. et al. Atomic interface effect of a single atom copper catalyst for enhanced oxygen reduction reactions. Energy Environ. Sci. 2019, 12, 3508–3514.
DOI Google Scholar
46

Chen, S. H.; Wang, B. Q.; Zhu, J. X.; Wang, L. Q.; Ou, H. H.; Zhang, Z. D.; Liang, X.; Zheng, L. R.; Zhou, L.; Su, Y. Q. et al. Lewis acid site-promoted single-atomic Cu catalyzes electrochemical CO2 methanation. Nano Lett. 2021, 21, 7325–7331.
DOI Google Scholar
47

Chen, S. H.; Li, W. H.; Jiang, W. J.; Yang, J. R.; Zhu, J. X.; Wang, L. Q.; Ou, H. H.; Zhuang, Z. C.; Chen, M. Z.; Sun, X. H. et al. MOF encapsulating N-heterocyclic carbene-ligated copper single-atom site catalyst towards efficient methane electrosynthesis. Angew. Chem., Int. Ed. 2022, 61, e202114450.
DOI Google Scholar
48

Ma, Q. L.; Fan, Q.; Xu, J. L.; Bai, J. Y.; Han, X.; Dong, Z. L.; Zhou, X. Z.; Liu, Z.; Gu, Z.; Wang, C. Calming cytokine storm in pneumonia by targeted delivery of TPCA-1 using platelet-derived extracellular vesicles. Matter 2020, 3, 287–301.
DOI Google Scholar
49

Ng, S. K.; Wood, J. P. M.; Chidlow, G.; Han, G. G.; Kittipassorn, T.; Peet, D. J.; Casson, R. J. Cancer-like metabolism of the mammalian retina. Clin. Exp. Ophthalmol. 2015, 43, 367–376.
DOI Google Scholar
50

Fu, Y. J.; Liu, S. S.; Yin, S. H. L.; Niu, W. H.; Xiong, W.; Tan, M.; Li, G. Y.; Zhou, M. The reverse Warburg effect is likely to be an Achilles’ heel of cancer that can be exploited for cancer therapy. Oncotarget 2017, 8, 57813–57825.
DOI Google Scholar
51

Upadhyay, M.; Samal, J.; Kandpal, M.; Singh, O. V.; Vivekanandan, P. The Warburg effect: Insights from the past decade. Pharmacol. Ther. 2013, 137, 318–330.
DOI Google Scholar
52

Lu, R. J.; Zhang, X. S.; Li, X. J.; Wan, X. F. Circ_0016418 promotes melanoma development and glutamine catabolism by regulating the miR-605–5p/GLS axis. Int. J. Clin. Exp. Pathol. 2020, 13, 1791–1801.
Google Scholar
53

Wang, R. J.; Xiang, W. Q.; Xu, Y.; Han, L. Y.; Li, Q. G.; Dai, W. X.; Cai, G. X. Enhanced glutamine utilization mediated by SLC1A5 and GPT2 is an essential metabolic feature of colorectal signet ring cell carcinoma with therapeutic potential. Ann Transl. Med. 2020, 8, 302.
DOI Google Scholar
54

Li, Q. C.; Tian, Y.; Liang, Y.; Li, C. CircHIPK3/miR-876–5p/PIK3R1 axis regulates regulation proliferation, migration, invasion, and glutaminolysis in gastric cancer cells. Cancer Cell Int. 2020, 20, 391.
DOI Google Scholar
55

Moreadith, R. W.; Lehninger, A. L. The pathways of glutamate and glutamine oxidation by tumor cell mitochondria. Role of mitochondrial NAD(P)+-dependent malic enzyme. J. Biol. Chem. 1984, 259, 6215–6221.
Google Scholar
56

Sodi, V. L.; Khaku, S.; Krutilina, R.; Schwab, L. P.; Vocadlo, D. J.; Seagroves, T. N.; Reginato, M. J. mTOR/MYC axis regulates O-GlcNAc transferase expression and O-GlcNAcylation in breast cancer. Mol. Cancer Res. 2015, 13, 923–933.
DOI Google Scholar
57

Zhu, P.; Chen, Y.; Shi, J. L. Nanoenzyme-augmented cancer sonodynamic therapy by catalytic tumor oxygenation. ACS Nano 2018, 12, 3780–3795.
DOI Google Scholar
58

Huang, C. Y.; Ding, S. J.; Jiang, W.; Wang, F. B. Glutathione-depleting nanoplatelets for enhanced sonodynamic cancer therapy. Nanoscale 2021, 13, 4512–4518.
DOI Google Scholar
59

Song, G. S.; Cheng, L.; Chao, Y.; Yang, K.; Liu, Z. Emerging nanotechnology and advanced materials for cancer radiation therapy. Adv. Mater. 2017, 29, 1700996.
DOI Google Scholar
60

Gay, L. J.; Felding-Habermann, B. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer. 2011, 11, 123–134.
DOI Google Scholar
61

Alves, C. S.; Burdick, M. M.; Thomas, S. N.; Pawar, P.; Konstantopoulos, K. The dual role of CD44 as a functional P-selectin ligand and fibrin receptor in colon carcinoma cell adhesion. Am. J. Physiol. -Cell Physiol. 2008, 294, C907–C916.
DOI Google Scholar
62

Xu, L. L.; Gao, F.; Fan, F.; Yang, L. H. Platelet membrane coating coupled with solar irradiation endows a photodynamic nanosystem with both improved antitumor efficacy and undetectable skin damage. Biomaterials 2018, 159, 59–67.
DOI Google Scholar
63

Thiery, J. P.; Acloque, H.; Huang, R. Y. J.; Nieto, M. A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139, 871–890.
DOI Google Scholar
64

Xu, M.; Gong, A. H.; Yang, H. Q.; George, S. K.; Jiao, Z. J.; Huang, H. M.; Jiang, X. M.; Zhang, Y. L. Sonic hedgehog-glioma associated oncogene homolog 1 signaling enhances drug resistance in CD44+/Musashi-1+ gastric cancer stem cells. Cancer Lett. 2015, 369, 124–133.
DOI Google Scholar
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Publication history
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Acknowledgements

Publication history

Received: 31 December 2021
Revised: 07 March 2022
Accepted: 24 March 2022
Published: 24 May 2022
Issue date: August 2022

Copyright

© Tsinghua University Press 2022

Acknowledgements

Acknowledgements

We are grateful for the financial support from the financial support from the Guangdong Provincial Key Laboratory of Precision Medicine for Gastrointestinal Cancer (No. 2020B121201004), the Guangdong Provincial Major Talents Project (No. 2019JC05Y361), the Outstanding Youths Development Scheme of Nanfang Hospital, Southern Medical University (No. 2021J008), the Basic and Clinical Cooperative Research and Promotion Program of Anhui Medical University (No. 2021xkjT028), the Open Fund of Key Laboratory of Antiinflammatory and Immune Medicine (No. KFJJ-2021-11), and Grants for Scientific Research of BSKY from Anhui Medical University (No. 1406012201). The authors would like to thank Dr. Yufei Chen from Shiyanjia Lab (www.shiyanjia.com) for drawing schematic diagrams.

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