Issue

Vol. 16 (2024)

Deep Insight of Design, Mechanism, and Cancer Theranostic Strategy of Nanozymes

https://doi.org/10.1007/s40820-023-01224-0
Lu Yang
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
Shuming Dong
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
Shili Gai
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
Dan Yang
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
He Ding
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
Lili Feng
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China
Guixin Yang
Key Laboratory of Green Chemical Engineering and Technology of Heilongjiang Province, College of Material Science and Chemical Engineering, Harbin University of Science and Technology, Harbin 150040, People’s Republic of China
Ziaur Rehman
Department of Chemistry, Quaid-i-Azam University, Islamabad 45320, Pakistan
Piaoping Yang
Key Laboratory of Superlight Materials and Surface Technology, Ministry of Education, College of Materials Science and Chemical Engineering, Harbin Engineering University, Harbin 150001, People’s Republic of China

Corresponding Author: Piaoping Yang

yangpiaoping@hrbeu.edu.cn

Nano-Micro Letters, Vol. 16 (2024), Article Number: 28

Abstract

Since the discovery of enzyme-like activity of Fe3O4 nanoparticles in 2007, nanozymes are becoming the promising substitutes for natural enzymes due to their advantages of high catalytic activity, low cost, mild reaction conditions, good stability, and suitable for large-scale production. Recently, with the cross fusion of nanomedicine and nanocatalysis, nanozyme-based theranostic strategies attract great attention, since the enzymatic reactions can be triggered in the tumor microenvironment to achieve good curative effect with substrate specificity and low side effects. Thus, various nanozymes have been developed and used for tumor therapy. In this review, more than 270 research articles are discussed systematically to present progress in the past five years. First, the discovery and development of nanozymes are summarized. Second, classification and catalytic mechanism of nanozymes are discussed. Third, activity prediction and rational design of nanozymes are focused by highlighting the methods of density functional theory, machine learning, biomimetic and chemical design. Then, synergistic theranostic strategy of nanozymes are introduced. Finally, current challenges and future prospects of nanozymes used for tumor theranostic are outlined, including selectivity, biosafety, repeatability and stability, in-depth catalytic mechanism, predicting and evaluating activities.


Highlights:
1 Classification and catalytic mechanism of nanozymes with different mimicking activities are dissertated.
2 Activity prediction and rational design methods of nanozymes are highlighted, including density functional theory, machine learning, biomimetic and chemical design.
3 The roles of nanozymes in different synergistic theranostic strategies for tumor are summarized and explained by representative examples in the past five years.

Keywords

Nanozymes Classification Prediction and design Catalytic mechanism Tumor theranostics
Yang, Lu, Shuming Dong, Shili Gai, Dan Yang, He Ding, Lili Feng, Guixin Yang, Ziaur Rehman, and Piaoping Yang. 2023. “Deep Insight of Design, Mechanism, and Cancer Theranostic Strategy of Nanozymes”. Nano-Micro Letters 16 (November):28. https://doi.org/10.1007/s40820-023-01224-0.
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References
  1. H. Sung, J. Ferlay, R.L. Siegel, M. Laversanne, I. Soerjomataram et al., Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA-Cancer J. Clin. 71(3), 209–249 (2021). https://doi.org/10.3322/caac.21660
  2. R.A. Sharma, R. Plummer, J.K. Stock, T.A. Greenhalgh, O. Ataman et al., Clinical development of new drug–radiotherapy combinations. Nat. Rev. Clin. Oncol. 13(10), 627–642 (2016). https://doi.org/10.1038/nrclinonc.2016.79
  3. H. Greenlee, M.J. DuPont-Reyes, L.G. Balneaves, L.E. Carlson, M.R. Cohen et al., Clinical practice guidelines on the evidence-based use of integrative therapies during and after breast cancer treatment. CA-Cancer J. Clin. 67(3), 195–232 (2017). https://doi.org/10.3322/caac.21397
  4. D.E. Citrin, Recent developments in radiotherapy. N. Engl. J. Med. 377(11), 1065–1075 (2017). https://doi.org/10.1056/NEJMra1608986
  5. J.L. Markman, A. Rekechenetskiy, E. Holler, J.Y. Ljubimova, Nanomedicine therapeutic approaches to overcome cancer drug resistance. Adv. Drug Deliv. Rev. 65(13–14), 1866–1879 (2013). https://doi.org/10.1016/j.addr.2013.09.019
  6. Y. Yang, Z.T. Zeng, E. Almatrafi, D.L. Huang, C. Zhang et al., Core-shell structured nanops for photodynamic therapy-based cancer treatment and related imaging. Coord. Chem. Rev. 458, 214427 (2022). https://doi.org/10.1016/j.ccr.2022.214427
  7. H.T. Sun, Q. Zhang, J.C. Li, S.J. Peng, X.L. Wang et al., Near-infrared photoactivated nanomedicines for photothermal synergistic cancer therapy. Nano Today 37, 101073 (2021). https://doi.org/10.1016/j.nantod.2020.101073
  8. S. Liu, X.T. Pan, H.Y. Liu, Two-dimensional nanomaterials for photothermal therapy. Angew. Chem. Int. Ed. 59(15), 5890–5900 (2020). https://doi.org/10.1002/anie.201911477
  9. Z.L. Ding, Y.H. Gu, C. Zheng, Y.Q. Gu, J. Yang et al., Organic small molecule-based photothermal agents for cancer therapy: design strategies from single-molecule optimization to synergistic enhancement. Coord. Chem. Rev. 464, 214564 (2022). https://doi.org/10.1016/j.ccr.2022.214564
  10. P.-C. Lo, M. Salome Rodriguez-Morgade, R.K. Pandey, D.K.P. Ng, T. Torres et al., The unique features and promises of phthalocyanines as advanced photosensitisers for photodynamic therapy of cancer. Chem. Soc. Rev. 49(4), 1041–1056 (2020). https://doi.org/10.1039/C9CS00129H
  11. X. Li, J.F. Lovell, J. Yoon, X. Chen, Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. 17(11), 657–674 (2020). https://doi.org/10.1038/s41571-020-0410-2
  12. U. Chilakamarthi, L. Giribabu, Photodynamic therapy: past, present and future. Chem. Rec. 17(8), 775–802 (2017). https://doi.org/10.1002/tcr.201600121
  13. Y. Liu, P. Bhattarai, Z.F. Dai, X.Y. Chen, Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 48(7), 2053–2108 (2019). https://doi.org/10.1039/C8CS00618K
  14. C. Xu, K.Y. Pu, Second near-infrared photothermal materials for combinational nanotheranostics. Chem. Soc. Rev. 50(2), 1111–1137 (2021). https://doi.org/10.1039/D0CS00664E
  15. X. Deng, Z. Shao, Y. Zhao, Solutions to the drawbacks of photothermal and photodynamic cancer therapy. Adv. Sci. 8(3), 2002504 (2021). https://doi.org/10.1002/advs.202002504
  16. Y. Huang, J. Ren, X. Qu, Nanozymes: classification, catalytic mechanisms, activity regulation, and applications. Chem. Rev. 119(6), 4357–4412 (2019). https://doi.org/10.1021/acs.chemrev.8b00672
  17. H. Wang, X. Zhang, Y. Xie, Recent progress in ultrathin two-dimensional semiconductors for photocatalysis. Mater. Sci. Eng. R. Rep. 130, 1–39 (2018). https://doi.org/10.1016/j.mser.2018.04.002
  18. M. Shao, Q. Chang, J.-P. Dodelet, R. Chenitz, Recent advances in electrocatalysts for oxygen reduction reaction. Chem. Rev. 116(6), 3594–3657 (2016). https://doi.org/10.1021/acs.chemrev.5b00462
  19. B. Yang, Y. Chen, J. Shi, Nanocatalytic medicine. Adv. Mater. 31(39), e1901778 (2019). https://doi.org/10.1002/adma.201901778
  20. Q. Bao, P. Hu, Y. Xu, T. Cheng, C. Wei et al., Simultaneous blood–brain barrier crossing and protection for stroke treatment based on edaravone-loaded ceria nanops. ACS Nano 12(7), 6794–6805 (2018). https://doi.org/10.1021/acsnano.8b01994
  21. B.W. Yang, Y. Chen, J.L. Shi, Exogenous/endogenous-triggered mesoporous silica cancer nanomedicine. Adv. Healthc. Mater. 7(20), e1800268 (2018). https://doi.org/10.1002/adhm.201800268
  22. K. Lu, T. Aung, N. Guo, R. Weichselbaum, W. Lin, Nanoscale metal–organic frameworks for therapeutic, imaging, and sensing applications. Adv. Mater. 30(37), 1707634 (2018). https://doi.org/10.1002/adma.201707634
  23. B.S. Pattni, V.V. Chupin, V.P. Torchilin, New developments in liposomal drug delivery. Chem. Rev. 115(19), 10938–10966 (2015). https://doi.org/10.1021/acs.chemrev.5b00046
  24. L. Liu, A. Corma, Metal catalysts for heterogeneous catalysis: from single atoms to nanoclusters and nanops. Chem. Rev. 118(10), 4981–5079 (2018). https://doi.org/10.1021/acs.chemrev.7b00776
  25. M. Stubbs, P.M.J. McSheehy, J.R. Griffiths, C.L. Bashford, Causes and consequences of tumour acidity and implications for treatment. Mol. Med. Today 6(1), 15–19 (2000). https://doi.org/10.1016/S1357-4310(99)01615-9
  26. J. Zou, F. Zhang, S. Zhang, S.F. Pollack, M. Elsabahy et al., Poly(ethylene oxide)-block-polyphosphoester-graft-paclitaxel conjugates with acid-labile linkages as a pH-sensitive and functional nanoscopic platform for paclitaxel delivery. Adv. Healthc. Mater. 3(3), 441–448 (2014). https://doi.org/10.1002/adhm.201300235
  27. J. Liu, Q. Chen, L. Feng, Z. Liu, Nanomedicine for tumor microenvironment modulation and cancer treatment enhancement. Nano Today 21, 55–73 (2018). https://doi.org/10.1016/j.nantod.2018.06.008
  28. A.V.V.V. Ravi Kiran, G. Kusuma Kumari, P.T. Krishnamurthy, R.R. Khaydarov, Tumor microenvironment and nanotherapeutics: intruding the tumor fort. Biomater. Sci. 9(23), 7667–7704 (2021). https://doi.org/10.1039/D1BM01127H
  29. M. Upreti, A. Jyoti, P. Sethi, Tumor microenvironment and nanotherapeutics. Transl. Cancer Res. 2(4), 309–319 (2013)
  30. L.Z. Feng, Z.L. Dong, D.L. Tao, Y.C. Zhang, Z. Liu, The acidic tumor microenvironment: a target for smart cancer nano-theranostics. Natl. Sci. Rev. 5(2), 269–286 (2018). https://doi.org/10.1093/nsr/nwx062
  31. W. Zhang, J. Lu, X. Gao, P. Li, W. Zhang et al., Enhanced photodynamic therapy by reduced levels of intracellular glutathione obtained by employing a nano-MOF with CuII as the active center. Angew. Chem. Int. Ed. 57(18), 4891–4896 (2018). https://doi.org/10.1002/anie.201710800
  32. L. Yu, Y. Chen, H. Chen, H2O2-responsive theranostic nanomedicine. Chin. Chem. Lett. 28(9), 1841–1850 (2017). https://doi.org/10.1016/j.cclet.2017.05.023
  33. N.E. Sounni, A. Noel, Targeting the tumor microenvironment for cancer therapy. Clin. Chem. 59(1), 85–93 (2013). https://doi.org/10.1373/clinchem.2012.185363
  34. Y. Xiao, D. Yu, Tumor microenvironment as a therapeutic target in cancer. Pharmacol. Ther. 221, 107753 (2021). https://doi.org/10.1016/j.pharmthera.2020.107753
  35. H.-J. Li, J.-Z. Du, J. Liu, X.-J. Du, S. Shen et al., Smart superstructures with ultrahigh pH-sensitivity for targeting acidic tumor microenvironment: Instantaneous size switching and improved tumor penetration. ACS Nano 10(7), 6753–6761 (2016). https://doi.org/10.1021/acsnano.6b02326
  36. J.-X. Fan, M.-Y. Peng, H. Wang, H.-R. Zheng, Z.-L. Liu et al., Engineered bacterial bioreactor for tumor therapy via Fenton-like reaction with localized H2O2 generation. Adv. Mater. 31(16), 1808278 (2019). https://doi.org/10.1002/adma.201808278
  37. B. Ma, S. Wang, F. Liu, S. Zhang, J. Duan et al., Self-assembled copper–amino acid nanops for in situ glutathione “AND” H2O2 sequentially triggered chemodynamic therapy. J. Am. Chem. Soc. 141(2), 849–857 (2019). https://doi.org/10.1021/jacs.8b08714
  38. Z. He, Y. Dai, X. Li, D. Guo, Y. Liu et al., Hybrid nanomedicine fabricated from photosensitizer-terminated metal–organic framework nanops for photodynamic therapy and hypoxia-activated cascade chemotherapy. Small 15(4), 1804131 (2019). https://doi.org/10.1002/smll.201804131
  39. T. Hao, J. Li, F. Yao, D. Dong, Y. Wang et al., Injectable fullerenol/alginate hydrogel for suppression of oxidative stress damage in brown adipose-derived stem cells and cardiac repair. ACS Nano 11(6), 5474–5488 (2017). https://doi.org/10.1021/acsnano.7b00221
  40. D. Furtado, M. Björnmalm, S. Ayton, A.I. Bush, K. Kempe et al., Overcoming the blood–brain barrier: the role of nanomaterials in treating neurological diseases. Adv. Mater. 30(46), 1801362 (2018). https://doi.org/10.1002/adma.201801362
  41. H. Lin, Y. Chen, J. Shi, Nanop-triggered in situ catalytic chemical reactions for tumour-specific therapy. Chem. Soc. Rev. 47(6), 1938–1958 (2018). https://doi.org/10.1039/C7CS00471K
  42. L. Gao, H. Koo, Do catalytic nanops offer an improved therapeutic strategy to combat dental biofilms? Nanomedicine 12(4), 275–279 (2017). https://doi.org/10.2217/nnm-2016-0400
  43. Z.A. Zhang, K.L. Fan, Bioorthogonal nanozymes: an emerging strategy for disease therapy. Nanoscale 15(1), 41–62 (2022). https://doi.org/10.1039/D2NR05920G
  44. Y.C. Li, R.F. Zhang, X.Y. Yan, K.L. Fan, Machine learning facilitating the rational design of nanozymes. J. Mater. Chem. B 11(28), 6466–6477 (2023). https://doi.org/10.1039/D3TB00842H
  45. Q. Li, T.T. Wu, X.W. Fan, X.B. Guo, W. Jiang et al., Multifaceted nanozymes for synergistic antitumor therapy: a review. Mater. Des. 224, 111430 (2022). https://doi.org/10.1016/j.matdes.2022.111430
  46. X. Zhang, X. Chen, Y. Zhao, Nanozymes: versatile platforms for cancer diagnosis and therapy. Nano-Micro Lett. 14(1), 95 (2022). https://doi.org/10.1007/s40820-022-00828-2
  47. X. Ding, Z. Zhao, Y. Zhang, M. Duan, C. Liu et al., Activity regulating strategies of nanozymes for biomedical applications. Small 19(11), 2207142 (2023). https://doi.org/10.1002/smll.202207142
  48. W. Yang, X. Yang, L. Zhu, H. Chu, X. Li et al., Nanozymes: activity origin, catalytic mechanism, and biological application. Coord. Chem. Rev. 448, 214170 (2021). https://doi.org/10.1016/j.ccr.2021.214170
  49. R. Wolfenden, M.J. Snider, The depth of chemical time and the power of enzymes as catalysts. Acc. Chem. Res. 34(12), 938–945 (2001). https://doi.org/10.1021/ar000058i
  50. U.T. Bornscheuer, G.W. Huisman, R.J. Kazlauskas, S. Lutz, J.C. Moore et al., Engineering the third wave of biocatalysis. Nature 485(7397), 185–194 (2012). https://doi.org/10.1038/nature11117
  51. R.R. Breaker, DNA enzymes. Nat. Biotechnol. 15(5), 427–431 (1997). https://doi.org/10.1038/nbt0597-427
  52. A.J. Kirby, Efficiency of proton transfer catalysis in models and enzymes. Acc. Chem. Res. 30(7), 290–296 (1997). https://doi.org/10.1021/ar960056r
  53. I. Hubatsch, M. Ridderström, B. Mannervik, Human glutathione transferase A4–4: an Alpha class enzyme with high catalytic efficiency in the conjugation of 4-hydroxynonenal and other genotoxic products of lipid peroxidation. Biochem. J. 330(1), 175–179 (1998). https://doi.org/10.1042/bj3300175
  54. J. Haseloff, W.L. Gerlach, Simple RNA enzymes with new and highly specific endoribonuclease activities. Nature 334(6183), 585–591 (1988). https://doi.org/10.1038/334585a0
  55. M. Liang, X. Yan, Nanozymes: from new concepts, mechanisms, and standards to applications. Acc. Chem. Res. 52(8), 2190–2200 (2019). https://doi.org/10.1021/acs.accounts.9b00140
  56. Y. Lin, J. Ren, X. Qu, Catalytically active nanomaterials: a promising candidate for artificial enzymes. Acc. Chem. Res. 47(4), 1097–1105 (2014). https://doi.org/10.1021/ar400250z
  57. H. Wei, E. Wang, Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes. Chem. Soc. Rev. 42(14), 6060–6093 (2013). https://doi.org/10.1039/C3CS35486E
  58. J. Wu, X. Wang, Q. Wang, Z. Lou, S. Li et al., Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes (II). Chem. Soc. Rev. 48(4), 1004–1076 (2019). https://doi.org/10.1039/C8CS00457A
  59. F. Manea, F.B. Houillon, L. Pasquato, P. Scrimin, Nanozymes: gold-nanop-based transphosphorylation catalysts. Angew. Chem. Int. Ed. 43(45), 6165–6169 (2004). https://doi.org/10.1002/anie.200460649
  60. L. Gao, J. Zhuang, L. Nie, J. Zhang, Y. Zhang et al., Intrinsic peroxidase-like activity of ferromagnetic nanops. Nat. Nanotechnol. 2(9), 577–583 (2007). https://doi.org/10.1038/nnano.2007.260
  61. B. Xu, H. Wang, W. Wang, L. Gao, S. Li et al., A single-atom nanozyme for wound disinfection applications. Angew. Chem. Int. Ed. 58(15), 4911–4916 (2019). https://doi.org/10.1002/anie.201813994
  62. Y. Sang, F. Cao, W. Li, L. Zhang, Y. You et al., Bioinspired construction of a nanozyme-based H2O2 homeostasis disruptor for intensive chemodynamic therapy. J. Am. Chem. Soc. 142(11), 5177–5183 (2020). https://doi.org/10.1021/jacs.9b12873
  63. W. Feng, X. Han, H. Hu, M. Chang, L. Ding et al., 2D vanadium carbide MXenzyme to alleviate ROS-mediated inflammatory and neurodegenerative diseases. Nat. Commun. 12(1), 2203 (2021). https://doi.org/10.1038/s41467-021-22278-x
  64. Z. Zhou, Y. Wang, F. Peng, F. Meng, J. Zha et al., Intercalation-activated layered MoO3 nanobelts as biodegradable nanozymes for tumor-specific photo-enhanced catalytic therapy. Angew. Chem. Int. Ed. 61(16), e202115939 (2022). https://doi.org/10.1002/anie.202115939
  65. W. Gao, J. He, L. Chen, X. Meng, Y. Ma et al., Deciphering the catalytic mechanism of superoxide dismutase activity of carbon dot nanozyme. Nat. Commun. 14(1), 160 (2023). https://doi.org/10.1038/s41467-023-35828-2
  66. H. Ding, Y. Cai, L. Gao, M. Liang, B. Miao et al., Exosome-like nanozyme vesicles for H2O2-responsive catalytic photoacoustic imaging of xenograft nasopharyngeal carcinoma. Nano Lett. 19(1), 203–209 (2019). https://doi.org/10.1021/acs.nanolett.8b03709
  67. H. Wang, K. Wan, X. Shi, Recent advances in nanozyme research. Adv. Mater. 31(45), 1805368 (2019). https://doi.org/10.1002/adma.201805368
  68. Q. Liu, A. Zhang, R. Wang, Q. Zhang, D. Cui, A review on metal- and metal oxide-based nanozymes: properties, mechanisms, and applications. Nano-Micro Lett. 13(1), 154 (2021). https://doi.org/10.1007/s40820-021-00674-8
  69. H. Sun, Y. Zhou, J. Ren, X. Qu, Carbon nanozymes: enzymatic properties, catalytic mechanism, and applications. Angew. Chem. Int. Ed. 57(30), 9224–9237 (2018). https://doi.org/10.1002/anie.201712469
  70. D.M. He, M.M. Yan, P.J. Sun, Y.Q. Sun, L.B. Qu et al., Recent progress in carbon-dots-based nanozymes for chemosensing and biomedical applications. Chin. Chem. Lett. 32(10), 2994–3006 (2021). https://doi.org/10.1016/j.cclet.2021.03.078
  71. L.-F. Javier, D. Bhaskar, E. Christopher, C. Cuong, Gold nanozymes: from concept to biomedical applications. Nano-Micro Lett. 13(1), 10 (2020). https://doi.org/10.1007/s40820-020-00532-z
  72. M. Lang, J. Fuben, F. Xin, W. Liyun, H. Chao et al., Metal-organic-framework-engineered enzyme-mimetic catalysts. Adv. Mater. 32(49), e2003065 (2020). https://doi.org/10.1002/adma.202003065
  73. X. Niu, X. Li, Z. Lyu, J. Pan, S. Ding et al., Metal–organic framework based nanozymes: promising materials for biochemical analysis. Chem. Commun. 56(77), 11338–11353 (2020). https://doi.org/10.1039/D0CC04890A
  74. O.L.-C. Diana, G.-G. Reyna Berenice, S. Ashutosh, B. Muhammad, P.-S. Roberto et al., Bioactive material-based nanozymes with multifunctional attributes for biomedicine: expanding antioxidant therapeutics for neuroprotection, cancer, and anti-inflammatory pathologies. Coord. Chem. Rev. 469, 214685 (2022). https://doi.org/10.1016/j.ccr.2022.214685
  75. X. Fan, F. Yang, C.X. Nie, L. Ma, C. Cheng et al., Biocatalytic nanomaterials: a new pathway for bacterial disinfection. Adv. Mater. 33(33), e2100637 (2021). https://doi.org/10.1002/adma.202100637
  76. Y.X. Shang, F.S. Liu, Y.N. Wang, N. Li, B.Q. Ding, Enzyme mimic nanomaterials and their biomedical applications. ChemBioChem 21(17), 2408–2418 (2020). https://doi.org/10.1002/cbic.202000123
  77. Y. Ai, Z.-N. Hu, X. Liang, H.-B. Sun, H. Xin et al., Recent advances in nanozymes: from matters to bioapplications. Adv. Funct. Mater. 32(14), 2110432 (2022). https://doi.org/10.1002/adfm.202110432
  78. K. Fan, H. Wang, J. Xi, Q. Liu, X. Meng et al., Optimization of Fe3O4 nanozyme activity via single amino acid modification mimicking an enzyme active site. Chem. Commun. 53(2), 424–427 (2017). https://doi.org/10.1039/C6CC08542C
  79. Q. Wang, C.Y. Li, X.Y. Wang, J. Pu, S. Zhang et al., eg occupancy as a predictive descriptor for spinel oxide nanozymes. Nano Lett. 22(24), 10003–10009 (2022). https://doi.org/10.1021/acs.nanolett.2c03598
  80. A.P. Nagvenkar, A. Gedanken, Cu0.89Zn0.11O, a new peroxidase-mimicking nanozyme with high sensitivity for glucose and antioxidant detection. ACS Appl. Mater. Interfaces 8(34), 22301–22308 (2016). https://doi.org/10.1021/acsami.6b05354
  81. F. Gong, N. Yang, Y. Wang, M. Zhuo, Q. Zhao et al., Oxygen-deficient bimetallic oxide FeWOX nanosheets as peroxidase-like nanozyme for sensing cancer via photoacoustic imaging. Small 16(46), 2003496 (2020). https://doi.org/10.1002/smll.202003496
  82. S. Li, L. Shang, B. Xu, S. Wang, K. Gu et al., A nanozyme with photo-enhanced dual enzyme-like activities for deep pancreatic cancer therapy. Angew. Chem. Int. Ed. 58(36), 12624–12631 (2019). https://doi.org/10.1002/anie.201904751
  83. H. Su, D.-D. Liu, M. Zhao, W.-L. Hu, S.-S. Xue et al., Dual-enzyme characteristics of polyvinylpyrrolidone-capped iridium nanops and their cellular protective effect against H2O2-induced oxidative damage. ACS Appl. Mater. Interfaces 7(15), 8233–8242 (2015). https://doi.org/10.1021/acsami.5b01271
  84. G. Jin, J. Liu, C. Wang, W. Gu, G. Ran et al., Ir nanops with multi-enzyme activities and its application in the selective oxidation of aromatic alcohols. Appl. Catal. B 267, 118725 (2020). https://doi.org/10.1016/j.apcatb.2020.118725
  85. J.-M. Park, H.-W. Jung, Y.W. Chang, H.-S. Kim, M.-J. Kang et al., Chemiluminescence lateral flow immunoassay based on Pt nanop with peroxidase activity. Anal. Chim. Acta 853, 360–367 (2015). https://doi.org/10.1016/j.aca.2014.10.011
  86. J. Wang, J. Sun, W. Hu, Y. Wang, T. Chou et al., A porous Au@Rh bimetallic core–shell nanostructure as an H2O2-driven oxygenerator to alleviate tumor hypoxia for simultaneous bimodal imaging and enhanced photodynamic therapy. Adv. Mater. 32(22), 2001862 (2020). https://doi.org/10.1002/adma.202001862
  87. Y. Zhang, J. Zhao, L. Zhang, Y. Zhao, Y. Zhang et al., A cascade nanoreactor for enhancing sonodynamic therapy on colorectal cancer via synergistic ROS augment and autophagy blockage. Nano Today 49, 101798 (2023). https://doi.org/10.1016/j.nantod.2023.101798
  88. B. Hu, X. Xiao, P. Chen, J. Qian, G. Yuan et al., Enhancing anti-tumor effect of ultrasensitive bimetallic RuCu nanops as radiosensitizers with dual enzyme-like activities. Biomaterials 290, 121811 (2022). https://doi.org/10.1016/j.biomaterials.2022.121811
  89. M. Hou, H. Su, Q. Wu, W. Sun, P. Zhang et al., A self-enhancing nanoreactor reinforces radioimmunotherapy by reprogramming nutrients and redox metabolisms. Adv. Funct. Mater. 33(16), 2212510 (2023). https://doi.org/10.1002/adfm.202212510
  90. J. Xi, R. Zhang, L. Wang, W. Xu, Q. Liang et al., A nanozyme-based artificial peroxisome ameliorates hyperuricemia and ischemic stroke. Adv. Funct. Mater. 31(9), 2007130 (2021). https://doi.org/10.1002/adfm.202007130
  91. K. Fan, J. Xi, L. Fan, P. Wang, C. Zhu et al., In vivo guiding nitrogen-doped carbon nanozyme for tumor catalytic therapy. Nat. Commun. 9(1), 1440 (2018). https://doi.org/10.1038/s41467-018-03903-8
  92. S. Ji, B. Jiang, H. Hao, Y. Chen, J. Dong et al., Matching the kinetics of natural enzymes with a single-atom iron nanozyme. Nat. Catal. 4(5), 407–417 (2021). https://doi.org/10.1038/s41929-021-00609-x
  93. M. Wen, J. Ouyang, C. Wei, H. Li, W. Chen et al., Artificial enzyme catalyzed cascade reactions: antitumor immunotherapy reinforced by NIR-II light. Angew. Chem. Int. Ed. 58(48), 17425–17432 (2019). https://doi.org/10.1002/anie.201909729
  94. X. Wei, J. Chen, M.C. Ali, J.C. Munyemana, H. Qiu, Cadmium cobaltite nanosheets synthesized in basic deep eutectic solvents with oxidase-like, peroxidase-like, and catalase-like activities and application in the colorimetric assay of glucose. Microchim. Acta 187(6), 314 (2020). https://doi.org/10.1007/s00604-020-04298-4
  95. J. Wu, Y. Yu, Y. Cheng, C. Cheng, Y. Zhang et al., Ligand-dependent activity engineering of glutathione peroxidase-mimicking MIL-47(V) metal-organic framework nanozyme for therapy. Angew. Chem. Int. Ed. 60(3), 1227–1234 (2021). https://doi.org/10.1002/anie.202010714
  96. M. Jiao, Z. Li, X. Li, Z. Zhang, Q. Yuan et al., Solving the H2O2 by-product problem using a catalase-mimicking nanozyme cascade to enhance glycolic acid oxidase. Chem. Eng. J. 388, 124249 (2020). https://doi.org/10.1016/j.cej.2020.124249
  97. F. Attar, M.G. Shahpar, B. Rasti, M. Sharifi, A.A. Saboury et al., Nanozymes with intrinsic peroxidase-like activities. J. Mol. Liq. 278, 130–144 (2019). https://doi.org/10.1016/j.molliq.2018.12.011
  98. X. Liu, D. Huang, C. Lai, L. Qin, G. Zeng et al., Peroxidase-like activity of smart nanomaterials and their advanced application in colorimetric glucose biosensors. Small 15(17), e1900133 (2019). https://doi.org/10.1002/smll.201900133
  99. B. Yuan, H.L. Chou, Y.K. Peng, Disclosing the origin of transition metal oxides as peroxidase (and catalase) mimetics. ACS Appl. Mater. Interfaces 14(20), 22728–22736 (2022). https://doi.org/10.1021/acsami.1c13429
  100. Y. Qiu, B. Yuan, H. Mi, J.-H. Lee, S.-W. Chou et al., An atomic insight into the confusion on the activity of Fe3O4 nanops as peroxidase mimetics and their comparison with horseradish peroxidase. J. Phys. Chem. Lett. 13(38), 8872–8878 (2022). https://doi.org/10.1021/acs.jpclett.2c02331
  101. X.M. Shen, Z.Z. Wang, X.J.J. Gao, X.F. Gao, Reaction mechanisms and kinetics of nanozymes: insights from theory and computation. Adv. Mater. (2023). https://doi.org/10.1002/adma.202211151
  102. W. Zhang, S.L. Hu, J.-J. Yin, W. He, W. Lu et al., Prussian blue nanops as multienzyme mimetics and reactive oxygen species scavengers. J. Am. Chem. Soc. 138(18), 5860–5865 (2016). https://doi.org/10.1021/jacs.5b12070
  103. H. Dong, W. Du, J. Dong, R. Che, F. Kong et al., Depletable peroxidase-like activity of Fe3O4 nanozymes accompanied with separate migration of electrons and iron ions. Nat. Commun. 13(1), 5365 (2022). https://doi.org/10.1038/s41467-022-33098-y
  104. Y.F. Lai, J.Y. Wang, N. Yue, Q.C. Zhang, J.J.X. Wu et al., Glutathione peroxidase-like nanozymes: mechanism, classification, and bioapplication. Biomater. Sci. 11(7), 2292–2316 (2023). https://doi.org/10.1039/D2BM01915A
  105. S. Wang, R. Cazelles, W.-C. Liao, M. Vázquez-González, A. Zoabi et al., Mimicking horseradish peroxidase and NADH peroxidase by heterogeneous Cu2+-modified graphene oxide nanops. Nano Lett. 17(3), 2043–2048 (2017). https://doi.org/10.1021/acs.nanolett.7b00093
  106. Z. Wang, R. Yu, Hollow micro/nanostructured ceria-based materials: synthetic strategies and versatile applications. Adv. Mater. 31(38), 1800592 (2019). https://doi.org/10.1002/adma.201800592
  107. X. Jiao, H. Song, H. Zhao, W. Bai, L. Zhang et al., Well-redispersed ceria nanops: promising peroxidase mimetics for H2O2 and glucose detection. Anal. Methods 4(10), 3261–3267 (2012). https://doi.org/10.1039/C2AY25511A
  108. Z. Yang, Z. Shuna, F. Jing, S. Shuyan, S. Weidong et al., Unraveling the physical chemistry and materials science of CeO2-based nanostructures. Chem 7(8), 2022–2059 (2021). https://doi.org/10.1016/j.chempr.2021.02.015
  109. V. Baldim, F. Bedioui, N. Mignet, I. Margaill, J.F. Berret, The enzyme-like catalytic activity of cerium oxide nanops and its dependency on Ce3+ surface area concentration. Nanoscale 10(15), 6971–6980 (2018). https://doi.org/10.1039/C8NR00325D
  110. E.G. Heckert, S. Seal, W.T. Self, Fenton-like reaction catalyzed by the rare earth inner transition metal cerium. Environ. Sci. Technol. 42(13), 5014–5019 (2008). https://doi.org/10.1021/es8001508
  111. X. Jiao, W. Liu, D. Wu, W. Liu, H. Song, Enhanced peroxidase-like activity of Mo-doped ceria nanops for sensitive colorimetric detection of glucose. Anal. Methods 10(1), 76–83 (2018). https://doi.org/10.1039/C7AY02459B
  112. T. Pirmohamed, J.M. Dowding, S. Singh, B. Wasserman, E. Heckert et al., Nanoceria exhibit redox state-dependent catalase mimetic activity. Chem. Commun. 46(16), 2736–2738 (2010). https://doi.org/10.1039/B922024K
  113. S. Dong, Y. Dong, T. Jia, S. Liu, J. Liu et al., GSH-depleted nanozymes with hyperthermia-enhanced dual enzyme-mimic activities for tumor nanocatalytic therapy. Adv. Mater. 32(42), 2002439 (2020). https://doi.org/10.1002/adma.202002439
  114. M.M. Pereira, M. Santana, M. Teixeira, A novel scenario for the evolution of haem–copper oxygen reductases. Biochim. Biophys. Acta-Bioenerg. 1505(2), 185–208 (2001). https://doi.org/10.1016/S0005-2728(01)00169-4
  115. X. Liu, Q. Wang, H. Zhao, L. Zhang, Y. Su et al., BSA-templated MnO2 nanops as both peroxidase and oxidase mimics. Analyst 137(19), 4552–4558 (2012). https://doi.org/10.1039/C2AN35700C
  116. S. Cai, C. Qi, Y. Li, Q. Han, R. Yang et al., PtCo bimetallic nanops with high oxidase-like catalytic activity and their applications for magnetic-enhanced colorimetric biosensing. J. Mater. Chem. B 4(10), 1869–1877 (2016). https://doi.org/10.1039/C5TB02052B
  117. H. Cheng, S. Lin, F. Muhammad, Y.-W. Lin, H. Wei, Rationally modulate the oxidase-like activity of nanoceria for self-regulated bioassays. ACS Sens. 1(11), 1336–1343 (2016). https://doi.org/10.1021/acssensors.6b00500
  118. Y. Xiong, S. Chen, F. Ye, L. Su, C. Zhang et al., Synthesis of a mixed valence state Ce–MOF as an oxidase mimetic for the colorimetric detection of biothiols. Chem. Commun. 51(22), 4635–4638 (2015). https://doi.org/10.1039/C4CC10346G
  119. Y. Chong, Q. Liu, C. Ge, Advances in oxidase-mimicking nanozymes: classification, activity regulation and biomedical applications. Nano Today 37, 101076 (2021). https://doi.org/10.1016/j.nantod.2021.101076
  120. Y. Wang, Z. Zhang, G. Jia, L. Zheng, J. Zhao et al., Elucidating the mechanism of the structure-dependent enzymatic activity of Fe–N/C oxidase mimics. Chem. Commun. 55(36), 5271–5274 (2019). https://doi.org/10.1039/C9CC01503E
  121. J. Liu, X. Jiang, L. Wang, Z. Hu, T. Wen et al., Ferroxidase-like activity of Au nanorod/Pt nanodot structures and implications for cellular oxidative stress. Nano Res. 8(12), 4024–4037 (2015). https://doi.org/10.1007/s12274-015-0904-x
  122. J. Chen, Q. Ma, M. Li, D. Chao, L. Huang et al., Glucose-oxidase like catalytic mechanism of noble metal nanozymes. Nat. Commun. 12(1), 3375 (2021). https://doi.org/10.1038/s41467-021-23737-1
  123. Y. Chen, T. Chen, X. Wu, G. Yang, Oxygen vacancy-engineered PEGylated MoO3−x nanops with superior sulfite oxidase mimetic activity for vitamin B1 detection. Small 15(46), 1903153 (2019). https://doi.org/10.1002/smll.201903153
  124. S. Biella, L. Prati, M. Rossi, Selective oxidation of D-glucose on gold catalyst. J. Catal. 206(2), 242–247 (2002). https://doi.org/10.1006/jcat.2001.3497
  125. M. Comotti, C. Della Pina, R. Matarrese, M. Rossi, The catalytic activity of “Naked” gold ps. Angew. Chem. Int. Ed. 43(43), 5812–5815 (2004). https://doi.org/10.1002/anie.200460446
  126. R. Ragg, F. Natalio, M.N. Tahir, H. Janssen, A. Kashyap et al., Molybdenum trioxide nanops with intrinsic sulfite oxidase activity. ACS Nano 8(5), 5182–5189 (2014). https://doi.org/10.1021/nn501235j
  127. Y. Chen, X. Wu, T. Chen, G. Yang, Hot carriers and photothermal effects of monolayer MoOx for promoting sulfite oxidase mimetic activity. ACS Appl. Mater. Interfaces 12(17), 19357–19368 (2020). https://doi.org/10.1021/acsami.0c04987
  128. C. Glorieux, P.B. Calderon, Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biol. Chem. 398(10), 1095–1108 (2017). https://doi.org/10.1515/hsz-2017-0131
  129. D. Xu, L. Wu, H. Yao, L. Zhao, Catalase-like nanozymes: classification, catalytic mechanisms, and their applications. Small 18(37), 2203400 (2022). https://doi.org/10.1002/smll.202203400
  130. Z. Wang, W. Wang, J. Wang, D. Wang, M. Liu et al., Single-atom catalysts with ultrahigh catalase-like activity through electron filling and orbital energy regulation. Adv. Funct. Mater. 33(2), 2209560 (2023). https://doi.org/10.1002/adfm.202209560
  131. B.T. Qiao, A.Q. Wang, X.F. Yang, L.F. Allard, Z. Jiang et al., Single-atom catalysis of CO oxidation using Pt-1/FeOx. Nat. Chem. 3(8), 634–641 (2011). https://doi.org/10.1038/nchem.1095
  132. I. Fridovich, Superoxide radicals, superoxide dismutases and the aerobic lifestyle. Photochem. Photobiol. 28(4–5), 733–741 (1978). https://doi.org/10.1111/j.1751-1097.1978.tb07009.x
  133. H. Zhao, R. Zhang, X. Yan, K. Fan, Superoxide dismutase nanozymes: an emerging star for anti-oxidation. J. Mater. Chem. B 9(35), 6939–6957 (2021). https://doi.org/10.1039/D1TB00720C
  134. C. Korsvik, S. Patil, S. Seal, W.T. Self, Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanops. Chem. Commun. 10, 1056–1058 (2007). https://doi.org/10.1039/B615134E
  135. H.W. Kroto, J.R. Heath, S.C. O’Brien, R.F. Curl, R.E. Smalley, C60: buckminsterfullerene. Nature 318(6042), 162–163 (1985). https://doi.org/10.1038/318162a0
  136. S.S. Ali, J.I. Hardt, K.L. Quick, J. Sook Kim-Han, B.F. Erlanger et al., A biologically effective fullerene (C60) derivative with superoxide dismutase mimetic properties. Free Radic. Biol. Med. 37(8), 1191–1202 (2004). https://doi.org/10.1016/j.freeradbiomed.2004.07.002
  137. X. Shen, W. Liu, X. Gao, Z. Lu, X. Wu et al., Mechanisms of oxidase and superoxide dismutation-like activities of gold, silver, platinum, and palladium, and their alloys: a general way to the activation of molecular oxygen. J. Am. Chem. Soc. 137(50), 15882–15891 (2015). https://doi.org/10.1021/jacs.5b10346
  138. S. Guo, L. Guo, Unraveling the multi-enzyme-like activities of iron oxide nanozyme via a first-principles microkinetic study. J. Phys. Chem. C 123(50), 30318–30334 (2019). https://doi.org/10.1021/acs.jpcc.9b07802
  139. B. Yang, H. Yao, J. Yang, C. Chen, Y. Guo et al., In situ synthesis of natural antioxidase mimics for catalytic anti-inflammatory treatments: rheumatoid arthritis as an example. J. Am. Chem. Soc. 144(1), 314–330 (2022). https://doi.org/10.1021/jacs.1c09993
  140. I. Celardo, J.Z. Pedersen, E. Traversa, L. Ghibelli, Pharmacological potential of cerium oxide nanops. Nanoscale 3(4), 1411–1420 (2011). https://doi.org/10.1039/C0NR00875C
  141. L. Gabrielli, L.J. Prins, F. Rastrelli, F. Mancin, P. Scrimin, Hydrolytic nanozymes. Eur. J. Org. Chem. 2020(32), 5044–5055 (2020). https://doi.org/10.1002/ejoc.202000356
  142. Q. Hou, X. Zhang, M. Lin, Y. Dai, F. Xia, Organic monolayer on gold nanops as hydrolytic nanozymes. Giant 12, 100122 (2022). https://doi.org/10.1016/j.giant.2022.100122
  143. Y. Ding, N.H. Williams, C.A. Hunter, A synthetic vesicle-to-vesicle communication system. J. Am. Chem. Soc. 141(44), 17847–17853 (2019). https://doi.org/10.1021/jacs.9b09102
  144. L. Pasquato, F. Rancan, P. Scrimin, F. Mancin, C. Frigeri, N-Methylimidazole-functionalized gold nanops as catalysts for cleavage of a carboxylic acid ester. Chem. Commun. 22, 2253–2254 (2000). https://doi.org/10.1039/B005244M
  145. I. Fernández, J. Pérez-Juste, P. Hervés, Cationic mixed micelles as reaction medium for hydrolysis reactions. J. Solut. Chem. 44(9), 1866–1874 (2015). https://doi.org/10.1007/s10953-015-0383-4
  146. L.J. Prins, Emergence of complex chemistry on an organic monolayer. Acc. Chem. Res. 48(7), 1920–1928 (2015). https://doi.org/10.1021/acs.accounts.5b00173
  147. G. Pieters, L.J. Prins, Catalytic self-assembled monolayers on gold nanops. New J. Chem. 36(10), 1931–1939 (2012). https://doi.org/10.1039/C2NJ40424A
  148. P. Pengo, S. Polizzi, L. Pasquato, P. Scrimin, Carboxylate−imidazole cooperativity in dipeptide-functionalized gold nanops with esterase-like activity. J. Am. Chem. Soc. 127(6), 1616–1617 (2005). https://doi.org/10.1021/ja043547c
  149. T. Serizawa, Y. Hirai, M. Aizawa, Novel synthetic route to peptide-capped gold nanops. Langmuir 25(20), 12229–12234 (2009). https://doi.org/10.1021/la9021799
  150. D.J. Mikolajczak, J.L. Heier, B. Schade, B. Koksch, Catalytic activity of peptide–nanop conjugates regulated by a conformational change. Biomacromol 18(11), 3557–3562 (2017). https://doi.org/10.1021/acs.biomac.7b00887
  151. S. Liang, X.-L. Wu, M.-H. Zong, W.-Y. Lou, Construction of Zn-heptapeptide bionanozymes with intrinsic hydrolase-like activity for degradation of di(2-ethylhexyl) phthalate. J. Colloid Interface Sci. 622, 860–870 (2022). https://doi.org/10.1016/j.jcis.2022.04.122
  152. P. Lin, M. Cao, F. Xia, H. Liao, H. Sun et al., A phosphatase-mimetic nano-stabilizer of mast cells for long-term prevention of allergic disease. Adv. Sci. 8(8), 2004115 (2021). https://doi.org/10.1002/advs.202004115
  153. D.J. Mikolajczak, J. Scholz, B. Koksch, Tuning the catalytic activity and substrate specificity of peptide-nanop conjugates. ChemCatChem 10(24), 5665–5668 (2018). https://doi.org/10.1002/cctc.201801521
  154. D.J. Mikolajczak, B. Koksch, Peptide-gold nanop conjugates as sequential cascade catalysts. ChemCatChem 10(19), 4324–4328 (2018). https://doi.org/10.1002/cctc.201800961
  155. S. Li, Z. Zhou, Z. Tie, B. Wang, M. Ye et al., Data-informed discovery of hydrolytic nanozymes. Nat. Commun. 13(1), 827 (2022). https://doi.org/10.1038/s41467-022-28344-2
  156. X. Shen, Z. Wang, X. Gao, Y. Zhao, Density functional theory-based method to predict the activities of nanomaterials as peroxidase mimics. ACS Catal. 10(21), 12657–12665 (2020). https://doi.org/10.1021/acscatal.0c03426
  157. Z. Wang, J. Wu, J.-J. Zheng, X. Shen, L. Yan et al., Accelerated discovery of superoxide-dismutase nanozymes via high-throughput computational screening. Nat. Commun. 12(1), 6866 (2021). https://doi.org/10.1038/s41467-021-27194-8
  158. X. Wang, X.J. Gao, L. Qin, C. Wang, L. Song et al., eg occupancy as an effective descriptor for the catalytic activity of perovskite oxide-based peroxidase mimics. Nat. Commun. 10(1), 704 (2019). https://doi.org/10.1038/s41467-019-08657-5
  159. Y.H. Wei, J. Wu, Y.X. Wu, H.J. Liu, F.Q. Meng et al., Prediction and design of nanozymes using explainable machine learning. Adv. Mater. 34(27), 2201736 (2022). https://doi.org/10.1002/adma.202201736
  160. C.H. Zhang, Y.X. Yu, S.G. Shi, M.M. Liang, D.Q. Yang et al., Machine learning guided discovery of superoxide dismutase nanozymes for androgenetic alopecia. Nano Lett. 22(21), 8592–8600 (2022). https://doi.org/10.1021/acs.nanolett.2c03119
  161. J. Razlivina, N. Serov, O. Shapovalova, V. Vinogradov, DiZyme: open-access expandable resource for quantitative prediction of nanozyme catalytic activity. Small 18(12), 2105673 (2022). https://doi.org/10.1002/smll.202105673
  162. J. Zhuang, A.C. Midgley, Y. Wei, Q. Liu, D. Kong et al., Machine-learning-assisted nanozyme design: lessons from materials and engineered enzymes. Adv. Mater. 885, 848 (2023). https://doi.org/10.1002/adma.202210848
  163. R. Zhang, X. Yan, K. Fan, Nanozymes inspired by natural enzymes. Acc. Mater. Res. 2(7), 534–547 (2021). https://doi.org/10.1021/accountsmr.1c00074
  164. J.Y. Liang, W.N. Lipscomb, Binding of substrate CO2 to the active site of human carbonic anhydrase II: a molecular dynamics study. Proc. Natl. Acad. Sci. 87(10), 3675–3679 (1990). https://doi.org/10.1073/pnas.87.10.3675
  165. L. Gráf, A. Jancsó, L. Szilágyi, G. Hegyi, K. Pintér et al., Electrostatic complementarity within the substrate-binding pocket of trypsin. Proc. Natl. Acad. Sci. 85(14), 4961–4965 (1988). https://doi.org/10.1073/pnas.85.14.4961
  166. B.L. Vallee, D.S. Auld, Active-site zinc ligands and activated H2O of zinc enzymes. Proc. Natl. Acad. Sci. 87(1), 220–224 (1990). https://doi.org/10.1073/pnas.87.1.220
  167. B.L. Vallee, R.J. Williams, Metalloenzymes: the entatic nature of their active sites. Proc. Natl. Acad. Sci. 59(2), 498–505 (1968). https://doi.org/10.1073/pnas.59.2.498
  168. M. Zhao, H.-B. Wang, L.-N. Ji, Z.-W. Mao, Insights into metalloenzyme microenvironments: biomimetic metal complexes with a functional second coordination sphere. Chem. Soc. Rev. 42(21), 8360–8375 (2013). https://doi.org/10.1039/C3CS60162E
  169. W. Nam, High-valent iron(IV)–oxo complexes of heme and non-heme ligands in oxygenation reactions. Acc. Chem. Res. 40(7), 522–531 (2007). https://doi.org/10.1021/ar700027f
  170. Q. Liang, J. Xi, X.J. Gao, R. Zhang, Y. Yang et al., A metal-free nanozyme-activated prodrug strategy for targeted tumor catalytic therapy. Nano Today 35, 100935 (2020). https://doi.org/10.1016/j.nantod.2020.100935
  171. L. Zhang, H. Wang, X. Qu, Biosystem-inspired engineering of nanozymes for biomedical applications. Adv. Mater. (2023). https://doi.org/10.1002/adma.202211147
  172. M. Wei, J. Lee, F. Xia, P. Lin, X. Hu et al., Chemical design of nanozymes for biomedical applications. Acta Biomater. 126, 15–30 (2021). https://doi.org/10.1016/j.actbio.2021.02.036
  173. Z. Qin, B. Chen, Y. Mao, C. Shi, Y. Li et al., Achieving ultrasmall prussian blue nanops as high-performance biomedical agents with multifunctions. ACS Appl. Mater. Interfaces 12(51), 57382–57390 (2020). https://doi.org/10.1021/acsami.0c18357
  174. Y. Wang, Z. Tan, Z. Zhang, P. Zhu, S.W. Tam et al., Facet-dependent activity of CeO2 nanozymes regulate the fate of human neural cell via redox homeostasis. ACS Appl. Mater. Interfaces 14(31), 35423–35433 (2022). https://doi.org/10.1021/acsami.2c09304
  175. Y. Wu, W. Xu, L. Jiao, Y. Tang, Y. Chen et al., Defect engineering in nanozymes. Mater. Today 52, 327–347 (2022). https://doi.org/10.1016/j.mattod.2021.10.032
  176. S. Dong, Y. Dong, Z. Zhao, J. Liu, S. Liu et al., “Electron transport chain interference” strategy of amplified mild-photothermal therapy and defect-engineered multi-enzymatic activities for synergistic tumor-personalized suppression. J. Am. Chem. Soc. 145(17), 9488–9507 (2023). https://doi.org/10.1021/jacs.2c09608
  177. H. Fan, J. Zheng, J. Xie, J. Liu, X. Gao et al., Surface ligand engineering ruthenium nanozyme superior to horseradish peroxidase for enhanced immunoassay. Adv. Mater. 23, 387 (2023). https://doi.org/10.1002/adma.202300387
  178. G. Tang, J. He, J. Liu, X. Yan, K. Fan, Nanozyme for tumor therapy: surface modification matters. Exploration 1(1), 75–89 (2021). https://doi.org/10.1002/EXP.20210005
  179. W. Xia, P. Zhang, W. Fu, L. Hu, Y. Wang, Aggregation/dispersion-mediated peroxidase-like activity of MoS2 quantum dots for colorimetric pyrophosphate detection. Chem. Commun. 55(14), 2039–2042 (2019). https://doi.org/10.1039/C8CC09799B
  180. X. Zhang, G. Li, G. Chen, D. Wu, Y. Wu et al., Enzyme mimics for engineered biomimetic cascade nanoreactors: mechanism, applications, and prospects. Adv. Funct. Mater. 31(50), 2106139 (2021). https://doi.org/10.1002/adfm.202106139
  181. M. Tang, Z. Zhang, T. Sun, B. Li, Z. Wu, Manganese-based nanozymes: preparation, catalytic mechanisms, and biomedical applications. Adv. Healthc. Mater. 11(21), e2201733 (2022). https://doi.org/10.1002/adhm.202201733
  182. H. Dong, Y. Fan, W. Zhang, N. Gu, Y. Zhang, Catalytic mechanisms of nanozymes and their applications in biomedicine. Bioconjug. Chem. 30(5), 1273–1296 (2019). https://doi.org/10.1021/acs.bioconjchem.9b00171
  183. M. Fanchi, Z. Pengbo, Y. Lini, X. Lixin, L. Hongyang, Nanozymes with atomically dispersed metal centers: structure-activity relationships and biomedical applications. Chem. Eng. J. 452(2), 139411 (2022). https://doi.org/10.1016/j.cej.2022.139411
  184. X. Cai, L. Jiao, H. Yan, Y. Wu, W. Gu et al., Nanozyme-involved biomimetic cascade catalysis for biomedical applications. Mater. Today 44, 211–228 (2021). https://doi.org/10.1016/j.mattod.2020.12.005
  185. S.-Y. Yin, G. Song, Y. Yang, Y. Zhao, P. Wang et al., Persistent regulation of tumor microenvironment via circulating catalysis of MnFe2O4@metal–organic frameworks for enhanced photodynamic therapy. Adv. Funct. Mater. 29(25), 1901417 (2019). https://doi.org/10.1002/adfm.201901417
  186. D. Jiang, D. Ni, Z.T. Rosenkrans, P. Huang, X. Yan et al., Nanozyme: new horizons for responsive biomedical applications. Chem. Soc. Rev. 48(14), 3683–3704 (2019). https://doi.org/10.1039/C8CS00718G
  187. Y. Chen, Z.-H. Li, J.-J. Hu, S.-Y. Peng, L. Rong et al., Remote-controlled multi-enzyme system for enhanced tumor therapy via dark/light relay catalysis. Nanoscale Horiz. 5(2), 283–293 (2020). https://doi.org/10.1039/C9NH00583H
  188. Z. Ma, L. Wu, K. Han, H. Han, Pt nanozyme for O2 self-sufficient, tumor-specific oxidative damage and drug resistance reversal. Nanoscale Horiz. 4(5), 1124–1131 (2019). https://doi.org/10.1039/C9NH00088G
  189. R. Zhao, Y. Zhu, J. Zhou, B. Liu, Y. Du et al., Dual glutathione depletion enhanced enzyme catalytic activity for hyperthermia assisted tumor therapy on semi-metallic VSe2/Mn-CS. ACS Nano 16(7), 10904–10917 (2022). https://doi.org/10.1021/acsnano.2c03222
  190. Y. Wang, G.R. Jia, X.Q. Cui, X. Zhao, Q.H. Zhang et al., Coordination number regulation of molybdenum single-atom nanozyme peroxidase-like specificity. Chem 7(2), 436–449 (2021). https://doi.org/10.1016/j.chempr.2020.10.023
  191. J. Zhou, D. Xu, G. Tian, Q. He, X. Zhang et al., Coordination-driven self-assembly strategy-activated Cu single-atom nanozymes for catalytic tumor-specific therapy. J. Am. Chem. Soc. 145(7), 4279–4293 (2023). https://doi.org/10.1021/jacs.2c13597
  192. G. Liu, J. Zhu, H. Guo, A. Sun, P. Chen et al., Mo2C-derived polyoxometalate for NIR-II photoacoustic imaging-guided chemodynamic/photothermal synergistic therapy. Angew. Chem. Int. Ed. 58(51), 18641–18646 (2019). https://doi.org/10.1002/anie.201910815
  193. Y. Yang, M. Chen, B. Wang, P. Wang, Y. Liu et al., NIR-II driven plasmon-enhanced catalysis for a timely supply of oxygen to overcome hypoxia-induced radiotherapy tolerance. Angew. Chem. Int. Ed. 58(42), 15069–15075 (2019). https://doi.org/10.1002/anie.201906758
  194. J. Xu, W. Han, P. Yang, T. Jia, S. Dong et al., Tumor microenvironment-responsive mesoporous MnO2-coated upconversion nanoplatform for self-enhanced tumor theranostics. Adv. Funct. Mater. 28(36), 1803804 (2018). https://doi.org/10.1002/adfm.201803804
  195. F. Liu, L. Lin, Y. Zhang, Y. Wang, S. Sheng et al., A tumor-microenvironment-activated nanozyme-mediated theranostic nanoreactor for imaging-guided combined tumor therapy. Adv. Mater. 31(40), 1902885 (2019). https://doi.org/10.1002/adma.201902885
  196. Z. Wang, Z. Li, Z. Sun, S. Wang, Z. Ali et al., Visualization nanozyme based on tumor microenvironment “unlocking” for intensive combination therapy of breast cancer. Sci. Adv. 6(48), eabc8733 (2020). https://doi.org/10.1126/sciadv.abc8733
  197. Z. Ma, M.F. Foda, H. Liang, Y. Zhao, H. Han, In situ nanozyme-amplified NIR-II phototheranostics for tumor-specific imaging and therapy. Adv. Funct. Mater. 31(37), 2103765 (2021). https://doi.org/10.1002/adfm.202103765
  198. M. Wang, M. Chang, Q. Chen, D. Wang, C. Li et al., Au2Pt-PEG-Ce6 nanoformulation with dual nanozyme activities for synergistic chemodynamic therapy / phototherapy. Biomaterials 252, 120093 (2020). https://doi.org/10.1016/j.biomaterials.2020.120093
  199. F. Yang, S. Hu, Y. Zhang, X. Cai, Y. Huang et al., A hydrogen peroxide-responsive O2 nanogenerator for ultrasound and magnetic-resonance dual modality imaging. Adv. Mater. 24(38), 5205–5211 (2012). https://doi.org/10.1002/adma.201202367
  200. C. Cao, H. Zou, N. Yang, H. Li, Y. Cai et al., Fe3O4/Ag/Bi2MoO6 photoactivatable nanozyme for self-replenishing and sustainable cascaded nanocatalytic cancer therapy. Adv. Mater. 33(52), 2106996 (2021). https://doi.org/10.1002/adma.202106996
  201. X. Zhong, X. Wang, L. Cheng, Y.A. Tang, G. Zhan et al., GSH-depleted PtCu3 nanocages for chemodynamic- enhanced sonodynamic cancer therapy. Adv. Funct. Mater. 30(4), 1907954 (2020). https://doi.org/10.1002/adfm.201907954
  202. L. Feng, B. Liu, R. Xie, D. Wang, C. Qian et al., An ultrasmall SnFe2O4 nanozyme with endogenous oxygen generation and glutathione depletion for synergistic cancer therapy. Adv. Funct. Mater. 31(5), 2006216 (2021). https://doi.org/10.1002/adfm.202006216
  203. D. Wang, H. Wu, S.Z.F. Phua, G. Yang, W. Qi Lim et al., Self-assembled single-atom nanozyme for enhanced photodynamic therapy treatment of tumor. Nat. Commun. 11(1), 357 (2020). https://doi.org/10.1038/s41467-019-14199-7
  204. R. Yue, C. Zhang, L. Xu, Y. Wang, G. Guan et al., Dual key co-activated nanoplatform for switchable MRI monitoring accurate ferroptosis-based synergistic therapy. Chem 8(7), 1956–1981 (2022). https://doi.org/10.1016/j.chempr.2022.03.009
  205. G.Q. Guan, C. Zhang, H.Y. Liu, Y.J. Wang, Z. Dong et al., Ternary alloy PtWMn as a Mn nanoreservoir for high-field MRI monitoring and highly selective ferroptosis therapy. Angew. Chem. Int. Ed. 61(31), e202117229 (2022). https://doi.org/10.1002/anie.202117229
  206. Z. Dong, P. Liang, G.Q. Guan, B.L. Yin, Y.J. Wang et al., Overcoming hypoxia-induced ferroptosis resistance via a F19/H1-MRI traceable core-shell nanostructure. Angew. Chem. Int. Ed. 61(48), e202206074 (2022). https://doi.org/10.1002/anie.202206074
  207. L. Shi, Y. Wang, C. Zhang, Y. Zhao, C. Lu et al., An acidity-unlocked magnetic nanoplatform enables self-boosting ROS generation through upregulation of lactate for imaging-guided highly specific chemodynamic therapy. Angew. Chem. Int. Ed. 60(17), 9562–9572 (2021). https://doi.org/10.1002/anie.202014415
  208. R. Yue, M. Zhou, X. Li, L. Xu, C. Lu et al., GSH/APE1 cascade-activated nanoplatform for imaging therapy resistance dynamics and enzyme-mediated adaptive ferroptosis. ACS Nano 17(14), 13792–13810 (2023). https://doi.org/10.1021/acsnano.3c03443
  209. C. Lu, C. Zhang, P. Wang, Y. Zhao, Y. Yang et al., Light-free generation of singlet oxygen through manganese-thiophene nanosystems for pH-responsive chemiluminescence imaging and tumor therapy. Chem 6(9), 2314–2334 (2020). https://doi.org/10.1016/j.chempr.2020.06.024
  210. L. Teng, X. Han, Y. Liu, C. Lu, B. Yin et al., Smart nanozyme platform with activity-correlated ratiometric molecular imaging for predicting therapeutic effects. Angew. Chem. Int. Ed. 60(50), 26142–26150 (2021). https://doi.org/10.1002/anie.202110427
  211. X. Huang, J. Song, B.C. Yung, X. Huang, Y. Xiong et al., Ratiometric optical nanoprobes enable accurate molecular detection and imaging. Chem. Soc. Rev. 47(8), 2873–2920 (2018). https://doi.org/10.1039/C7CS00612H
  212. Y. Deng, W. Zhan, G. Liang, Intracellular self-assembly of peptide conjugates for tumor imaging and therapy. Adv. Healthc. Mater. 10(1), 2001211 (2021). https://doi.org/10.1002/adhm.202001211
  213. Y. Fan, S. Wang, F. Zhang, Optical multiplexed bioassays for improved biomedical diagnostics. Angew. Chem. Int. Ed. 58(38), 13208–13219 (2019). https://doi.org/10.1002/anie.201901964
  214. Z. Yang, Y. Dai, C. Yin, Q. Fan, W. Zhang et al., Activatable semiconducting theranostics: Simultaneous generation and ratiometric photoacoustic imaging of reactive oxygen species in vivo. Adv. Mater. 30(23), 1707509 (2018). https://doi.org/10.1002/adma.201707509
  215. K.C. Nicolaou, J.S. Chen, The art of total synthesis through cascade reactions. Chem. Soc. Rev. 38(11), 2993–3009 (2009). https://doi.org/10.1039/B903290H
  216. S. Gao, H. Lin, H. Zhang, H. Yao, Y. Chen et al., Nanocatalytic tumor therapy by biomimetic dual inorganic nanozyme-catalyzed cascade reaction. Adv. Sci. 6(3), 1801733 (2019). https://doi.org/10.1002/advs.201801733
  217. L. Wang, X. Zhang, Z. You, Z. Yang, M. Guo et al., A molybdenum disulfide nanozyme with charge-enhanced activity for ultrasound-mediated cascade-catalytic tumor ferroptosis. Angew. Chem. Int. Ed. 62(11), e202217448 (2023). https://doi.org/10.1002/anie.202217448
  218. M. Chang, Z. Wang, C. Dong, R. Zhou, L. Chen et al., Ultrasound-amplified enzyodynamic tumor therapy by perovskite nanoenzyme-enabled cell pyroptosis and cascade catalysis. Adv. Mater. 35(7), 2208817 (2023). https://doi.org/10.1002/adma.202208817
  219. Y. Zhao, W.H. Kong, P. Wang, G.S. Song, Z.L. Song et al., Tumor-specific multipath nucleic acid damages strategy by symbiosed nanozyme@enzyme with synergistic self-cyclic catalysis. Small 17(28), 2100766 (2021). https://doi.org/10.1002/smll.202100766
  220. X. Meng, D. Li, L. Chen, H. He, Q. Wang et al., High-performance self-cascade pyrite nanozymes for apoptosis–ferroptosis synergistic tumor therapy. ACS Nano 15(3), 5735–5751 (2021). https://doi.org/10.1021/acsnano.1c01248
  221. S.M. Dong, Y.S. Dong, T. Jia, F.M. Zhang, Z. Wang et al., Sequential catalytic, magnetic targeting nanoplatform for synergistic photothermal and NIR-enhanced chemodynamic therapy. Chem. Mater. 32(23), 9868–9881 (2020). https://doi.org/10.1021/acs.chemmater.9b05170
  222. M. Huo, L. Wang, Y. Chen, J. Shi, Tumor-selective catalytic nanomedicine by nanocatalyst delivery. Nat. Commun. 8(1), 357 (2017). https://doi.org/10.1038/s41467-017-00424-8
  223. R. André, F. Natálio, M. Humanes, J. Leppin, K. Heinze et al., V2O5 nanowires with an intrinsic peroxidase-like activity. Adv. Funct. Mater. 21(3), 501–509 (2011). https://doi.org/10.1002/adfm.201001302
  224. L. Han, L. Zeng, M. Wei, C.M. Li, A. Liu, A V2O3-ordered mesoporous carbon composite with novel peroxidase-like activity towards the glucose colorimetric assay. Nanoscale 7(27), 11678–11685 (2015). https://doi.org/10.1039/C5NR02694F
  225. L. Tian, J. Qi, K. Qian, O. Oderinde, Q. Liu et al., Copper (II) oxide nanozyme based electrochemical cytosensor for high sensitive detection of circulating tumor cells in breast cancer. J. Electroanal. Chem. 812, 1–9 (2018). https://doi.org/10.1016/j.jelechem.2017.12.012
  226. A. Jiao, L. Xu, Y. Tian, Q. Cui, X. Liu et al., Cu2O nanocubes–grafted highly dense Au nanops with modulated electronic structures for improving peroxidase catalytic performances. Talanta 225, 121990 (2021). https://doi.org/10.1016/j.talanta.2020.121990
  227. C. Liu, M. Zhang, H. Geng, P. Zhang, Z. Zheng et al., NIR enhanced peroxidase-like activity of Au@CeO2 hybrid nanozyme by plasmon-induced hot electrons and photothermal effect for bacteria killing. Appl. Catal. B 295, 120317 (2021). https://doi.org/10.1016/j.apcatb.2021.120317
  228. L. Huang, S. Zhao, J. Wu, L. Yu, N. Singh et al., Photodynamic therapy for hypoxic tumors: advances and perspectives. Coord. Chem. Rev. 438, 213888 (2021). https://doi.org/10.1016/j.ccr.2021.213888
  229. J.D. Lambeth, NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4(3), 181–189 (2004). https://doi.org/10.1038/nri1312
  230. S. Son, J.H. Kim, X. Wang, C. Zhang, S.A. Yoon et al., Multifunctional sonosensitizers in sonodynamic cancer therapy. Chem. Soc. Rev. 49(11), 3244–3261 (2020). https://doi.org/10.1039/C9CS00648F
  231. S. Liang, X. Deng, P.A. Ma, Z. Cheng, J. Lin, Recent advances in nanomaterial-assisted combinational sonodynamic cancer therapy. Adv. Mater. 32(47), e2003214 (2020). https://doi.org/10.1002/adma.202003214
  232. N.R. Patel, B.S. Pattni, A.H. Abouzeid, V.P. Torchilin, Nanopreparations to overcome multidrug resistance in cancer. Adv. Drug Deliv. Rev. 65(13–14), 1748–1762 (2013). https://doi.org/10.1016/j.addr.2013.08.004
  233. H. Liu, D. Chen, L. Li, T. Liu, L. Tan et al., Multifunctional gold nanoshells on silica nanorattles: a platform for the combination of photothermal therapy and chemotherapy with low systemic toxicity. Angew. Chem. Int. Ed. 50(4), 891–895 (2011). https://doi.org/10.1002/anie.201002820
  234. X. Zhu, Y. Gong, Y. Liu, C. Yang, S. Wu et al., Ru@CeO2 yolk shell nanozymes: Oxygen supply in situ enhanced dual chemotherapy combined with photothermal therapy for orthotopic/subcutaneous colorectal cancer. Biomaterials 242, 119923 (2020). https://doi.org/10.1016/j.biomaterials.2020.119923
  235. F. Li, H. Sun, J. Ren, B. Zhang, X. Hu et al., A nuclease-mimetic platinum nanozyme induces concurrent DNA platination and oxidative cleavage to overcome cancer drug resistance. Nat. Commun. 13(1), 7361 (2022). https://doi.org/10.1038/s41467-022-35022-w
  236. X. Zeng, J. Sun, S. Li, J. Shi, H. Gao et al., Blood-triggered generation of platinum nanop functions as an anti-cancer agent. Nat. Commun. 11(1), 567 (2020). https://doi.org/10.1038/s41467-019-14131-z
  237. J. Chen, X. Wang, Y. Yuan, H. Chen, L. Zhang et al., Exploiting the acquired vulnerability of cisplatin-resistant tumors with a hypoxia-amplifying DNA repair–inhibiting (HYDRI) nanomedicine. Sci. Adv. 7(13), eabc5267 (2021). https://doi.org/10.1126/sciadv.abc5267
  238. A. Yimit, O. Adebali, A. Sancar, Y. Jiang, Differential damage and repair of DNA-adducts induced by anti-cancer drug cisplatin across mouse organs. Nat. Commun. 10(1), 309 (2019). https://doi.org/10.1038/s41467-019-08290-2
  239. S. Rottenberg, C. Disler, P. Perego, The rediscovery of platinum-based cancer therapy. Nat. Rev. Cancer 21(1), 37–50 (2021). https://doi.org/10.1038/s41568-020-00308-y
  240. C.J. Lord, A. Ashworth, The DNA damage response and cancer therapy. Nature 481(7381), 287–294 (2012). https://doi.org/10.1038/nature10760
  241. P. Bouwman, J. Jonkers, The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nat. Rev. Cancer 12(9), 587–598 (2012). https://doi.org/10.1038/nrc3342
  242. S.P. Jackson, J. Bartek, The DNA-damage response in human biology and disease. Nature 461(7267), 1071–1078 (2009). https://doi.org/10.1038/nature08467
  243. D.M. Zhu, H. Chen, C.Y. Huang, G.X. Li, X. Wang et al., H2O2 self-producing single-atom nanozyme hydrogels as light-controlled oxidative stress amplifier for enhanced synergistic therapy by transforming “cold” tumors. Adv. Funct. Mater. 32(16), 2110268 (2022). https://doi.org/10.1002/adfm.202110268
  244. J.N. Xie, L.J. Gong, S. Zhu, Y. Yong, Z.J. Gu et al., Emerging strategies of nanomaterial-mediated tumor radiosensitization. Adv. Mater. 31(3), 25 (2019). https://doi.org/10.1002/adma.201802244
  245. C. Zhang, L. Yan, Z. Gu, Y. Zhao, Strategies based on metal-based nanops for hypoxic-tumor radiotherapy. Chem. Sci. 10(29), 6932–6943 (2019). https://doi.org/10.1039/C9SC02107H
  246. X. Yang, L. Gao, Q. Guo, Y. Li, Y. Ma et al., Nanomaterials for radiotherapeutics-based multimodal synergistic cancer therapy. Nano Res. 13(10), 2579–2594 (2020). https://doi.org/10.1007/s12274-020-2722-z
  247. C. Sandhya, M.C. Jared, D. Wei, G. Anna, N. Saadia et al., Mechanisms for tuning engineered nanomaterials to enhance radiation therapy of cancer. Adv. Sci. 7(24), 2003584 (2020). https://doi.org/10.1002/advs.202003584
  248. R.F. Zhang, L. Chen, Q. Liang, J.Q. Xi, H.Q. Zhao et al., Unveiling the active sites on ferrihydrite with apparent catalase-like activity for potentiating radiotherapy. Nano Today 41, 101317 (2021). https://doi.org/10.1016/j.nantod.2021.101317
  249. I. Martínez-Reyes, N.S. Chandel, Cancer metabolism: looking forward. Nat. Rev. Cancer 21(10), 669–680 (2021). https://doi.org/10.1038/s41568-021-00378-6
  250. C.A. Lyssiotis, A.C. Kimmelman, Metabolic interactions in the tumor microenvironment. Trends Cell Biol. 27(11), 863–875 (2017). https://doi.org/10.1016/j.tcb.2017.06.003
  251. W. Xie, W.-W. Deng, M. Zan, L. Rao, G.-T. Yu et al., Cancer cell membrane camouflaged nanops to realize starvation therapy together with checkpoint blockades for enhancing cancer therapy. ACS Nano 13(3), 2849–2857 (2019). https://doi.org/10.1021/acsnano.8b03788
  252. Z. Yu, P. Zhou, W. Pan, N. Li, B. Tang, A biomimetic nanoreactor for synergistic chemiexcited photodynamic therapy and starvation therapy against tumor metastasis. Nat. Commun. 9(1), 5044 (2018). https://doi.org/10.1038/s41467-018-07197-8
  253. L.K. Boroughs, R.J. DeBerardinis, Metabolic pathways promoting cancer cell survival and growth. Nat. Cell Biol. 17(4), 351–359 (2015). https://doi.org/10.1038/ncb3124
  254. J. Wu, Y. Zhang, K. Jiang, X. Wang, N.T. Blum et al., Enzyme-engineered conjugated polymer nanoplatform for activatable companion diagnostics and multistage augmented synergistic therapy. Adv. Mater. 34(18), 2200062 (2022). https://doi.org/10.1002/adma.202200062
  255. X. Li, C. Jiang, Q. Wang, S. Yang, Y. Cao et al., A “valve-closing” starvation strategy for amplification of tumor-specific chemotherapy. Adv. Sci. 9(8), 2104671 (2022). https://doi.org/10.1002/advs.202104671
  256. C. Zhang, D. Ni, Y. Liu, H. Yao, W. Bu et al., Magnesium silicide nanops as a deoxygenation agent for cancer starvation therapy. Nat. Nanotechnol. 12, 378 (2017). https://doi.org/10.1038/nnano.2016.280
  257. Z. Zhou, J. Huang, Z. Zhang, L. Zhang, Y. Cao et al., Bimetallic PdPt-based nanocatalysts for photothermal-augmented tumor starvation and sonodynamic therapy in NIR-II biowindow assisted by an oxygen self-supply strategy. Chem. Eng. J. 435, 135085 (2022). https://doi.org/10.1016/j.cej.2022.135085
  258. Y. Zou, W. Liu, W. Sun, J. Du, J. Fan et al., Highly inoxidizable heptamethine cyanine–glucose oxidase conjugate nanoagent for combination of enhanced photothermal therapy and tumor starvation. Adv. Funct. Mater. 32(17), 2111853 (2022). https://doi.org/10.1002/adfm.202111853
  259. D. Zhu, T. Zhang, Y. Li, C. Huang, M. Suo et al., Tumor-derived exosomes co-delivering aggregation-induced emission luminogens and proton pump inhibitors for tumor glutamine starvation therapy and enhanced type-I photodynamic therapy. Biomaterials 283, 121462 (2022). https://doi.org/10.1016/j.biomaterials.2022.121462
  260. M. Wang, M. Chang, C. Li, Q. Chen, Z. Hou et al., Tumor-microenvironment-activated reactive oxygen species amplifier for enzymatic cascade cancer starvation/chemodynamic /immunotherapy. Adv. Mater. 34(4), 2106010 (2022). https://doi.org/10.1002/adma.202106010
  261. K. Li, C. Lin, M. Li, K. Xu, Y. He et al., Multienzyme-like reactivity cooperatively impairs glutathione peroxidase 4 and ferroptosis suppressor protein 1 pathways in triple-negative breast cancer for sensitized ferroptosis therapy. ACS Nano 16(2), 2381–2398 (2022). https://doi.org/10.1021/acsnano.1c08664
  262. Z.H. Lei, C.X. Sun, P. Pei, S.F. Wang, D.D. Li et al., Stable, wavelength-tunable fluorescent dyes in the NIR-II region for in vivo high-contrast bioimaging and multiplexed biosensing. Angew. Chem. Int. Ed. 58(24), 8166–8171 (2019). https://doi.org/10.1002/anie.201904182
  263. Z. Liu, Q. Liu, H. Zhang, X. Zhang, J. Wu et al., Genetically engineered protein corona-based cascade nanozymes for enhanced tumor therapy. Adv. Funct. Mater. 32(51), 2208513 (2022). https://doi.org/10.1002/adfm.202208513
  264. Y.J. Li, Y. Zhang, Y. Dong, O.U. Akakuru, X.H. Yao et al., Ablation of gap junction protein improves the efficiency of nanozyme-mediated catalytic/starvation/mild-temperature photothermal therapy. Adv. Mater. 35(22), 2210464 (2023). https://doi.org/10.1002/adma.202210464
  265. G. Ningqiang, C.S. Neil, M.B. Margaret, H.J. Carl, J.M. Michael, Nanomaterials for T-cell cancer immunotherapy. Nat. Nanotechnol. 16(1), 25–36 (2021). https://doi.org/10.1038/s41565-020-00822-y
  266. M. Yarchoan, A. Hopkins, E.M. Jaffee, Tumor mutational burden and response rate to PD-1 inhibition. N. Engl. J. Med. 377(25), 2500–2501 (2017). https://doi.org/10.1056/NEJMc1713444
  267. J. Nam, S. Son, K.S. Park, W. Zou, L.D. Shea et al., Cancer nanomedicine for combination cancer immunotherapy. Nat. Rev. Mater. 4(6), 398–414 (2019). https://doi.org/10.1038/s41578-019-0108-1
  268. C.H. Patel, R.D. Leone, M.R. Horton, J.D. Powell, Targeting metabolism to regulate immune responses in autoimmunity and cancer. Nat. Rev. Drug Discov. 18(9), 669–688 (2019). https://doi.org/10.1038/s41573-019-0032-5
  269. X. Zhang, Y. Kang, J. Wang, J. Yan, Q. Chen et al., Engineered PD-L1-expressing platelets reverse new-onset type 1 diabetes. Adv. Mater. 32(26), 1907692 (2020). https://doi.org/10.1002/adma.201907692
  270. Z. Jiang, Z. Liu, M. Li, C. Chen, X. Wang, Increased glycolysis correlates with elevated immune activity in tumor immune microenvironment. EBioMed 42, 431–442 (2019). https://doi.org/10.1016/j.ebiom.2019.03.068
  271. C.-H. Chang, J. Qiu, D. O’Sullivan, M.D. Buck, T. Noguchi et al., Metabolic competition in the tumor microenvironment is a driver of cancer progression. Cell 162(6), 1229–1241 (2015). https://doi.org/10.1016/j.cell.2015.08.016
  272. S. Zhang, Y. Zhang, Y. Feng, J. Wu, Y. Hu et al., Biomineralized two-enzyme nanops regulate tumor glycometabolism inducing tumor cell pyroptosis and robust antitumor immunotherapy. Adv. Mater. 34(50), 2206851 (2022). https://doi.org/10.1002/adma.202206851
  273. Z. Zhao, S. Dong, Y. Liu, J. Wang, L. Ba et al., Tumor microenvironment-activable manganese-boosted catalytic immunotherapy combined with PD-1 checkpoint blockade. ACS Nano 16(12), 20400–20418 (2022). https://doi.org/10.1021/acsnano.2c06646
  274. M. de Miguel, E. Calvo, Clinical challenges of immune checkpoint inhibitors. Cancer Cell 38(3), 326–333 (2020). https://doi.org/10.1016/j.ccell.2020.07.004
  275. C. Zhang, K. Pu, Molecular and nanoengineering approaches towards activatable cancer immunotherapy. Chem. Soc. Rev. 49(13), 4234–4253 (2020). https://doi.org/10.1039/C9CS00773C
  276. L. Liu, Y. Pan, C. Zhao, P. Huang, X. Chen et al., Boosting checkpoint immunotherapy with biomaterials. ACS Nano 17(4), 3225–3258 (2023). https://doi.org/10.1021/acsnano.2c11691
  277. Q. Chen, Y. He, Y. Wang, C. Li, Y. Zhang et al., Penetrable nanoplatform for “cold” tumor immune microenvironment reeducation. Adv. Sci. 7(17), 2000411 (2020). https://doi.org/10.1002/advs.202000411
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