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化学进展 2023, Vol. 35 Issue (10): 1492-1504 DOI: 10.7536/PC230301 前一篇   后一篇

• 综述 •

金属组学和金属蛋白质组学技术于生物医药研究的应用

王宇传*()   

  1. 华北理工大学基础医学院 河北省慢性疾病重点实验室 唐山 063210
  • 收稿日期:2023-03-07 修回日期:2023-04-09 出版日期:2023-10-24 发布日期:2023-06-12
  • 作者简介:
    王宇传 香港大学博士,先后于中山大学化学学院和中国科学院深圳先进技术研究院任副研究员。在金属组学方法开发、细胞内金属蛋白鉴定、金属蛋白功能及金属药物作用机理研究等方面做出了系统的研究工作。以第一或共同通讯作者发表学术论文10余篇,主持或作为课题骨干参加多项国家级课题。研究方向为生物样品中金属元素的检测分析、生物金属机理探究等。
  • 基金资助:
    河北省高校基本科研业务费(JQN2022026)

Applications of Metallomics and Metalloproteomics Techniques in Biomedical Research

Yuchuan Wang*()   

  1. Heibei Key Laboratory for Chronic Diseases, School of Basic Medical Sciences, North China University of Science and Technology,Tangshan 063210, China
  • Received:2023-03-07 Revised:2023-04-09 Online:2023-10-24 Published:2023-06-12
  • Contact: *e-mail: wangych@ncst.edu.cn
  • Supported by:
    Fundamental Research Funds for the Central Universities(JQN2022026)

金属是生命过程中必不可少的辅助因子,是许多关键细胞进程中的必需元素。金属组学作为一门新兴的研究领域,旨在了解并揭示基于金属的生命过程的分子机制及金属的生物活性,相关研究在近年来得以蓬勃发展并受到广泛关注。本文详述了金属组学的概念及相关研究技术,重点介绍金属组学的一个重要研究分支——金属蛋白质组学,并对该领域应用于生物医药研究取得的进展进行综述,内容涵盖金属/金属药物在单细胞层面的摄取研究,组织和器官中的金属/金属药物分布研究、及其在细胞内结合靶点蛋白的鉴定及表征,金属蛋白的生物信息学分析等方面。基于以上研究现状,进一步探讨了金属组学技术在生物医药研究中所面临的挑战及发展前景。

Metals are recognized as essential cofactors in life processes and are fundamental elements in many key cellular processes. Metallomics, as an emerging research field, aims to understand and reveal the functions of bio-active metals and the molecular mechanisms of metal-based life processes, and the related studies have received growing attention due to its rapid development as a frontier science. In this review, we first introduce the concept of metallomics and the related research technologies, and focuses on an important research branch in this field, metalloproteomics, which aims to recognize the relationships between biometals and cellular proteins in a systematic manner. The development of this field has provided a number of practical research tools. We summarize and highlight the recent applications, major progress and important research findings of metallomics and metalloproteomics in biomedical research, which cover the studies of metals/metallodrugs uptake at the single-cell level, the distributions of metals/metallodrugs in cells, tissues and organs, the identification and characterization of intracellular metal-binding proteins, as well as the bioinformatics analysis of metalloproteins. Based on the current research status, the challenges and prospects of the applications of metallomics techniques in biomedical research are further discussed. Moreover, popularization of the metalloproteomics research would be an innovate and efficient way to obtain a complete understanding of the role of bioactive metals in cells. We believe that the development of new methodologies in metallomics and metalloproteomics, as well as the discovery of novel metal-related biological mechanisms will facilitate, support and expand the research perspectives in biomedicine and clinical research.

Contents

1 Introduction

2 Metallomics and metalloproteomics

2.1 Definition

2.2 Research methods and techniques

3 Applications and progress in biomedical research

3.1 Metals/metallodrugs uptake studies at single cell levels

3.2 Distribution studies of metals/metallodrugs in cells and tissues

3.3 Identification of metallodrug-targeting proteins in cells

4 Conclusion and outlook

()
图1 金属蛋白质组学方法及应用。(A) 由ICP-MS和LC-MS/MS技术组成的传统整合分析方法;(B) 大肠杆菌胞浆中与Ag+相关的蛋白质图谱;(C)固定化金属亲和色谱法(IMAC);(D) 药物下拉实验的工作流程
Fig.1 Illustration of metalloproteomics approaches and the applications. (A) Conventional integrated analytical methods consisted of ICP-MS and LC-MS/MS; (B) Map of Ag+-associated proteins in the E. coli cytosol; (C) The workflow of immobilized metal affinity chromatography (IMAC); (D) The workflow of drug pull-down assay
图2 单剂量钌和锇化合物在CT-26肿瘤小鼠组织中的分布。图像为连续H&E染色组织切片图与LA-ICP-MS分析得到的图像
Fig.2 Metal distribution in tissues of mice bearing a CT-26 tumour treated with a single dose of ruthenium and osmium compounds. The images are obtained from consecutive H&E stained tissue sections and LA-ICP-MS analysis
图3 铋剂药物抑制幽门螺旋杆菌的多靶点作用模式示意图
Fig.3 A model for the multi-targeted mode of action of Bi drug in eradicating H. pylori
[1]
Valdez C E, Smith Q A, Nechay M R, Alexandrova A N. Acc. Chem. Res., 2014, 47(10): 3110.

doi: 10.1021/ar500227u     URL    
[2]
Foster A W, Young T R, Chivers P T, Robinson N J. Curr. Opin. Chem. Biol., 2022, 66: 102095.

doi: 10.1016/j.cbpa.2021.102095     URL    
[3]
Chandrangsu P, Rensing C, Helmann J D. Nat. Rev. Microbiol., 2017, 15(6): 338.

doi: 10.1038/nrmicro.2017.15     pmid: 28344348
[4]
Mounicou S, Szpunar J, Lobinski R. Chem. Soc. Rev., 2009, 38(4): 1119.

doi: 10.1039/b713633c     pmid: 19421584
[5]
Xiong X L, Liu L Y, Mao Z W, Zou T T. Coord. Chem. Rev., 2022, 453: 214311.

doi: 10.1016/j.ccr.2021.214311     URL    
[6]
Wang Y C, Li H Y, Sun H Z. Inorg. Chem., 2019, 58(20): 13673.

doi: 10.1021/acs.inorgchem.9b01199     URL    
[7]
Wang H, Zhou Y, Xu X, Li H, Sun H. Curr. Opin. Chem. Biol., 2020, 55: 171.

doi: 10.1016/j.cbpa.2020.02.006     URL    
[8]
Scalese G, Kostenkova K, Crans D C, Gambino D. Curr. Opin. Chem. Biol., 2022, 67: 102127.

doi: 10.1016/j.cbpa.2022.102127     URL    
[9]
Waldron K J, Rutherford J C, Ford D, Robinson N J. Nature, 2009, 460(7257): 823.

doi: 10.1038/nature08300    
[10]
Waldron K J, Robinson N J. Nat. Rev. Microbiol., 2009, 7(1): 25.

doi: 10.1038/nrmicro2057     pmid: 19079350
[11]
Xu X H, Wang H B, Li H Y, Sun H Z. Chem. Lett., 2020, 49(6): 697.

doi: 10.1246/cl.200155     URL    
[12]
She Y M, Narindrasorasak S, Yang S Y, Spitale N, Roberts E A, Sarkar B. Mol. Cell. Proteom., 2003, 2(12): 1306.

doi: 10.1074/mcp.M300080-MCP200     URL    
[13]
Babak M V, Meier S M, Huber K V M, Reynisson J, Legin A A, Jakupec M A, Roller A, Stukalov A, Gridling M, Bennett K L, Colinge J, Berger W, Dyson P J, Superti-Furga G, Keppler B K, Hartinger C G. Chem. Sci., 2015, 6(4): 2449.

doi: 10.1039/C4SC03905J     URL    
[14]
Williams R J P. Coord. Chem. Rev., 2001, 216/217: 583.

doi: 10.1016/S0010-8545(00)00398-2     URL    
[15]
Haraguchi H. J. Anal. At. Spectrom., 2004, 19(1): 5.

doi: 10.1039/b308213j     URL    
[16]
Maret W. Metallomics: the Science of Biometals and Biometalloids, 2018.
[17]
Maret W. Metallomics, 2022, 14 (8): mfac051.

doi: 10.1093/mtomcs/mfac051     URL    
[18]
da Silva M A, Sussulini A, Arruda M A. Expert Rev. Proteom., 2010, 7(3): 387.

doi: 10.1586/epr.10.16     URL    
[19]
Yannone S M, Hartung S, Menon A L, Adams M W, Tainer J A. Curr. Opin. Biotechnol., 2012, 23(1): 89.

doi: 10.1016/j.copbio.2011.11.005     URL    
[20]
Hu L G, Cheng T F, He B, Li L, Wang Y C, Lai Y T, Jiang G B, Sun H Z. Angew. Chem. Int. Ed., 2013, 52(18): 4916.

doi: 10.1002/anie.v52.18     URL    
[21]
Wang H B, Wang M J, Xu X H, Gao P, Xu Z L, Zhang Q, Li H Y, Yan A X, Kao R Y T, Sun H Z. Nat. Commun., 2021, 12: 3331.

doi: 10.1038/s41467-021-23659-y    
[22]
de Jonge M D, Holzner C, Baines S B, Twining B S, Ignatyev K, Diaz J, Howard D L, Legnini D, Miceli A, McNulty I, Jacobsen C J, Vogt S. Proc. Natl. Acad. Sci. U. S. A., 2010, 107(36): 15676.

doi: 10.1073/pnas.1001469107     URL    
[23]
Shi W X, Chance M R. Curr. Opin. Chem. Biol., 2011, 15(1): 144.

doi: 10.1016/j.cbpa.2010.11.004     URL    
[24]
Cvetkovic A, Lal Menon A, Thorgersen M P, Scott J W, Poole F L, Jenney F E, Lancaster W A, Praissman J L, Shanmukh S, Vaccaro B J, Trauger S A, Kalisiak E, Apon J V, Siuzdak G, Yannone S M, Tainer J A, Adams M W W. Nature, 2010, 466(7307): 779.

doi: 10.1038/nature09265    
[25]
JimÉnez-Lamana J, Szpunar J. Metallomics, 2017, 9(8): 1014.

doi: 10.1039/C7MT00054E     URL    
[26]
Wang D Y, He B, Yan X T, Nong Q Y, Wang C, Jiang J, Hu L G, Jiang G B. Talanta, 2019, 197: 145.

doi: 10.1016/j.talanta.2019.01.025     URL    
[27]
Yan X T, He B, Wang D Y, Hu L G, Liu L H, Liao C Y, Jiang G B. Talanta, 2018, 184: 404.

doi: 10.1016/j.talanta.2018.03.037     URL    
[28]
Xu M, Yang Q Y, Xu L N, Rao Z Y, Cao D, Gao M, Liu S J. Part. Fibre Toxicol., 2019, 16(1): 46.

doi: 10.1186/s12989-019-0322-4    
[29]
Nong Q Y, Chen X, Hu L G, Huang Y S, Luan T G, Liu H T, Chen B W. Talanta, 2020, 219: 121281.

doi: 10.1016/j.talanta.2020.121281     URL    
[30]
Prange A, Pröfrock D. Anal. Bioanal. Chem., 2005, 383(3): 372.

doi: 10.1007/s00216-005-3420-0     URL    
[31]
Holtkamp H U, Movassaghi S, Morrow S J, Kubanik M, Hartinger C G. Metallomics, 2018, 10(3): 455.

doi: 10.1039/c8mt00024g     pmid: 29484339
[32]
Wang H B, Yan A X, Liu Z G, Yang X M, Xu Z L, Wang Y C, Wang R M, Koohi-Moghadam M, Hu L G, Xia W, Tang H R, Wang Y L, Li H Y, Sun H Z. PLoS Biol., 2019, 17(6): e3000292.

doi: 10.1371/journal.pbio.3000292     URL    
[33]
Wang Y C, Hu L G, Yang X M, Chang Y Y, Hu X Q, Li H Y, Sun H Z. Metallomics, 2015, 7(10): 1399.

doi: 10.1039/C5MT00054H     URL    
[34]
Timerbaev A R, Pawlak K, Aleksenko S S, Foteeva L S, Matczuk M, Jarosz M. Talanta, 2012, 102: 164.

doi: 10.1016/j.talanta.2012.07.031     pmid: 23182589
[35]
Yan X T, He B, Liu L H, Qu G B, Shi J B, Hu L G, Jiang G B. Metallomics, 2018, 10(4): 557.

doi: 10.1039/C7MT00328E     URL    
[36]
Yang L C, McRae R, Henary M M, Patel R, Lai B, Vogt S, Fahrni C J. Proc. Natl. Acad. Sci. U. S. A., 2005, 102(32): 11179.

doi: 10.1073/pnas.0406547102     URL    
[37]
Fahrni C J. Curr. Opin. Chem. Biol., 2007, 11(2): 121.

doi: 10.1016/j.cbpa.2007.02.039     URL    
[38]
Doble P A, de Vega R G, Bishop D P, Hare D J, Clases D. Chem. Rev., 2021, 121(19): 11769.

doi: 10.1021/acs.chemrev.0c01219     URL    
[39]
Van Malderen S J M, Managh A J, Sharp B L, Vanhaecke F. J. Anal. At. Spectrom., 2016, 31(2): 423.

doi: 10.1039/C5JA00430F     URL    
[40]
Sun X S, Chiu J F, He Q Y. Methods in Molecular Biology?. Totowa, NJ: Humana Press, 2008. 205.
[41]
Sun X S, Chiu J F, He Q Y. Expert Rev. Proteom., 2005, 2(5): 649.

doi: 10.1586/14789450.2.5.649     URL    
[42]
Block H, Maertens B, Spriestersbach A, Brinker N, Kubicek J, Fabis R, Labahn J, Schäfer F. Methods in Enzymology. Amsterdam: Elsevier, 2009. 439.
[43]
Sun X S, Yu G C, Xu Q, Li N, Xiao C L, Yin X F, Cao K, Han J L, He Q Y. Metallomics, 2013, 5(7): 928.

doi: 10.1039/c3mt00126a     URL    
[44]
Wang Y C, Tsang C N, Xu F, Kong P W, Hu L G, Wang J W, Chu I K, Li H Y, Sun H Z. Chem. Commun., 2015, 51(92): 16479.

doi: 10.1039/C5CC04958J     URL    
[45]
Meier S M, Kreutz D, Winter L, Klose M H M, Cseh K, Weiss T, Bileck A, Alte B, Mader J C, Jana S, Chatterjee A, Bhattacharyya A, Hejl M, Jakupec M A, Heffeter P, Berger W, Hartinger C G, Keppler B K, Wiche G, Gerner C. Angew. Chem. Int. Ed., 2017, 56(28): 8267.

doi: 10.1002/anie.v56.28     URL    
[46]
Shi J B, Ji X M, Wu Q, Liu H W, Qu G B, Yin Y G, Hu L G, Jiang G B. Anal. Chem., 2020, 92(1): 622.

doi: 10.1021/acs.analchem.9b03719     URL    
[47]
Sun Y Z, Liu N, Wang Y Y, Yin Y G, Qu G B, Shi J B, Song M Y, Hu L G, He B, Liu G L, Cai Y, Liang Y, Jiang G B. Anal. Chem., 2020, 92(22): 14872.

doi: 10.1021/acs.analchem.0c02285     URL    
[48]
Wu Q, Shi J B, Ji X M, Xia T, Zeng L, Li G T, Wang Y Y, Gao J, Yao L L, Ma J J, Liu X L, Liu N, Hu L G, He B, Liang Y, Qu G B, Jiang G B. ACS Nano, 2020, 14(10): 12828.

doi: 10.1021/acsnano.0c03587     URL    
[49]
Bendall S C, Simonds E F, Qiu P, Amir E A D, Krutzik P O, Finck R, Bruggner R V, Melamed R, Trejo A, Ornatsky O I, Balderas R S, Plevritis S K, Sachs K, Pe’er D, Tanner S D, Nolan G P. Science, 2011, 332(6030): 687.

doi: 10.1126/science.1198704     pmid: 21551058
[50]
Zeng X, Cheng Y, Wang C. Biochemistry, 2021, 60(46): 3507.

doi: 10.1021/acs.biochem.1c00404     pmid: 34406001
[51]
Passerini A, Andreini C, Menchetti S, Rosato A, Frasconi P. BMC Bioinform., 2007, 8(1): 39.

doi: 10.1186/1471-2105-8-39    
[52]
Passerini A, Lippi M, Frasconi P. Nucleic Acids Res., 2011, 39(2): W288.

doi: 10.1093/nar/gkr365     URL    
[53]
Zhang Y, Zheng J G. Molecules, 2020, 25(15): 3366.

doi: 10.3390/molecules25153366     URL    
[54]
Hasty J, Pradines J, Dolnik M, Collins J J. Proc. Natl. Acad. Sci. U. S. A., 2000, 97(5): 2075.

doi: 10.1073/pnas.040411297     URL    
[55]
Tsang C N, Ho K S, Sun H Z, Chan W T. J. Am. Chem. Soc., 2011, 133(19): 7355.

doi: 10.1021/ja2013278     URL    
[56]
Zhou Y, Wang H B, Tse E, Li H Y, Sun H Z. Anal. Chem., 2018, 90(17): 10465.

doi: 10.1021/acs.analchem.8b02444     URL    
[57]
Liu N, Huang Y S, Zhang H Z, Wang T, Tao C, Zhang A Q, Chen B W, Yin Y G, Song M Y, Qu G B, Liang Y, Shi J B, He B, Hu L G, Jiang G B. Environ. Sci. Technol., 2021, 55(6): 3819.

doi: 10.1021/acs.est.0c05989     URL    
[58]
Fan Z X, Rong Y, Sadhukhan T, Liang S X, Li W Q, Yuan Z X, Zhu Z L, Guo S W, Ji S M, Wang J Q, Kushwaha R, Banerjee S, Raghavachari K, Huang H Y. Angew. Chem. Int. Ed., 2022, 61(23): e202202098.
[59]
Tomik B, Chwiej J, Szczerbowska-Boruchowska M, Lankosz M, WÓjcik S, Adamek D, Falkenberg G, Bohic S, Simionovici A, Stegowski Z, Szczudlik A. Neurochem. Res., 2006, 31(3): 321.

pmid: 16733809
[60]
Yoshida S, Ide-Ektessabi A, Fujisawa S. Struct. Chem., 2003, 14(1): 85.

doi: 10.1023/A:1021673127598     URL    
[61]
Ide-Ektessabi A, Fujisawa S, Yoshida S. J. Appl. Phys., 2002, 91(3): 1613.

doi: 10.1063/1.1426244     URL    
[62]
Matusch A, Fenn L S, Depboylu C, Klietz M, Strohmer S, McLean J A, Becker J S. Anal. Chem., 2012, 84(7): 3170.

doi: 10.1021/ac203112c     URL    
[63]
Theiner S, Schweikert A, Haberler C, Peyrl A, Koellensperger G. Metallomics, 2020, 12(8): 1246.

doi: 10.1039/d0mt00080a     pmid: 32525499
[64]
Theiner S, Schweikert A, Van Malderen S J M, Schoeberl A, Neumayer S, Jilma P, Peyrl A, Koellensperger G. Anal. Chem., 2019, 91(13): 8207.

doi: 10.1021/acs.analchem.9b00698     pmid: 31121096
[65]
van Acker T, van Malderen S J M, van Heerden M, McDuffie J E, Cuyckens F, Vanhaecke F. Anal. Chim. Acta, 2016, 945: 23.

doi: 10.1016/j.aca.2016.10.014     URL    
[66]
Theiner S, Kornauth C, Varbanov H P, Galanski M S, Van Schoonhoven S, Heffeter P, Berger W, Egger A E, Keppler B K. Metallomics, 2015, 7(8): 1256.

doi: 10.1039/c5mt00028a     pmid: 25856224
[67]
Klose M H M, Theiner S, Kornauth C, Meier-Menches S M, Heffeter P, Berger W, Koellensperger G, Keppler B K. Metallomics, 2018, 10(3): 388.

doi: 10.1039/C8MT00012C     URL    
[68]
Xie H X, Tian X, He L N, Li J C, Cui L W, Cong X, Tang B C, Zhang Y, Guo Z Y, Zhou A Y, Chen D L, Wang L M, Zhao J T, Yu Y L, Li B, Li Y F. J. Agric. Food Chem., 2023, 71(5): 2658.

doi: 10.1021/acs.jafc.2c08112     URL    
[69]
Wang Y C, Wang H B, Li H Y, Sun H Z. Dalton Trans., 2015, 44(2): 437.

doi: 10.1039/C4DT02814G     URL    
[70]
Holtkamp H U, Hartinger C G. Trac Trends Anal. Chem., 2018, 104: 110.

doi: 10.1016/j.trac.2017.09.023     URL    
[71]
Fung S K, Zou T T, Cao B, Lee P Y, Fung Y M E, Hu D, Lok C N, Che C M. Angew. Chem. Int. Ed., 2017, 56(14): 3892.

doi: 10.1002/anie.201612583     pmid: 28247451
[72]
Wehner K A, Schütz S, Sarnow P. Mol. Cell. Biol., 2010, 30(8): 2006.

doi: 10.1128/MCB.01350-09     pmid: 20154146
[73]
Chen T, Ozel D, Qiao Y, Harbinski F, Chen L M, Denoyelle S, He X Y, Zvereva N, Supko J G, Chorev M, Halperin J A, Aktas B H. Nat. Chem. Biol., 2011, 7(9): 610.

doi: 10.1038/nchembio.613    
[74]
Wan P K, Tong K C, Lok C N, Zhang C L, Chang X Y, Sze K H, Wong A S T, Che C M. Proc. Natl. Acad. Sci. U. S. A., 2021, 118(17), e2025806118.
[75]
Satelli A, Li S L. Cell. Mol. Life Sci., 2011, 68(18): 3033.

doi: 10.1007/s00018-011-0735-1     pmid: 21637948
[76]
Hu X Q, Li H Y, Ip T K Y, Cheung Y F, Koohi-Moghadam M, Wang H B, Yang X M, Tritton D N, Wang Y C, Wang Y, Wang R M, Ng K M, Naranmandura H, Tse E W C, Sun H Z. Chem. Sci., 2021, 12(32): 10893.

doi: 10.1039/D1SC03119H     URL    
[77]
Xu X H, Wang H B, Li H Y, Hu X Q, Zhang Y, Guan X Y, Toy P H, Sun H Z. Chem. Commun., 2019, 55(87): 13120.

doi: 10.1039/C9CC07605K     URL    
[78]
Henikoff S, Smith M M. Cold Spring Harb. Perspect. Biol., 2015, 7(1): a019364.
[79]
Wang X X, Hu Y, Mo J B, Zhang J Y, Wang Z Z, Wei W, Li H L, Xu Y, Ma J, Zhao J, Jin Z, Guo Z J. Angew. Chem. Int. Ed., 2020, 59(13): 5151.

doi: 10.1002/anie.v59.13     URL    
[80]
Wang X, Zhang J, Hu Y, Zhao X, Wang Z, Zhang W, Liang J, Yu W, Tian T, Zhou H, Li J, Liu S, Zhao J, Jin Z, Wei W, Guo Z. ACS Appl. Mater. Interfaces., 2022, 14(40): 45137.

doi: 10.1021/acsami.2c10743     URL    
[81]
Neuditschko B, Legin A A, Baier D N, Schintlmeister A, Reipert S, Wagner M, Keppler B K, Berger W, Meier-Menches S M, Gerner C. Angewandte Chemie Int. Ed., 2021, 60(10): 4954.

doi: 10.1002/anie.v60.10     URL    
[82]
Wiche G, Osmanagic-Myers S, CastañÓn M J. Curr. Opin. Cell Biol., 2015, 32: 21.

doi: 10.1016/j.ceb.2014.10.002     URL    
[83]
Shin S J, Smith J A, Rezniczek G A, Pan S, Chen R, Brentnall T A, Wiche G, Kelly K A. Proc. Natl. Acad. Sci. U. S. A., 2013, 110(48): 19414.

doi: 10.1073/pnas.1309720110     URL    
[84]
Sutoh Yoneyama M, Hatakeyama S, Habuchi T, Inoue T, Nakamura T, Funyu T, Wiche G, Ohyama C, Tsuboi S. Eur. J. Cell Biol., 2014, 93(4): 157.

doi: 10.1016/j.ejcb.2014.03.002     pmid: 24810881
[85]
McInroy L, Määttä A. Exp. Cell Res., 2011, 317(17): 2468.

doi: 10.1016/j.yexcr.2011.07.013     pmid: 21821021
[86]
Li J B, Cai W X, Yu J, Zhou S, Li X L, He Z G, Ouyang D F, Liu H Z, Wang Y J. Biomaterials, 2022, 287: 121651.

doi: 10.1016/j.biomaterials.2022.121651     URL    
[87]
Xiong X L, Huang K B, Wang Y, Cao B, Luo Y L, Chen H W, Yang Y, Long Y, Liu M Y, Chan A S C, Liang H, Zou T T. J. Am. Chem. Soc., 2022, 144(23): 10407.

doi: 10.1021/jacs.2c02435     URL    
[88]
Wang X X, Zhang J Y, Zhao X Y, Wei W, Zhao J. Metallomics, 2019, 11(8): 1344.

doi: 10.1039/c9mt00134d     URL    
[89]
Wang X X, Chen F, Zhang J Y, Sun J X, Zhao X Y, Zhu Y L, Wei W, Zhao J, Guo Z J. Sci. China Chem., 2020, 63(1): 65.

doi: 10.1007/s11426-019-9577-3    
[90]
Zhao X Y, Zhang J Y, Zhang W, Guo Z J, Wei W, Wang X X, Zhao J. Chem. Sci., 2023, 14(5): 1114.

doi: 10.1039/D2SC06171F     URL    
[91]
Lemire J A, Harrison J J, Turner R J. Nat. Rev. Microbiol., 2013, 11(6): 371.

doi: 10.1038/nrmicro3028    
[92]
Turner R J. Microb. Biotechnol., 2017, 10(5): 1062.

doi: 10.1111/mbt2.2017.10.issue-5     URL    
[93]
Gaberc-Porekar V, Menart V. J. Biochem. Biophys. Methods, 2001, 49(1/3): 335.

doi: 10.1016/S0165-022X(01)00207-X     URL    
[94]
Ge R G, Sun X S, Gu Q, Watt R M, Tanner J A, Wong B C Y, Xia H H, Huang J D, He Q Y, Sun H Z. JBIC J. Biol. Inorg. Chem., 2007, 12(6): 831.

doi: 10.1007/s00775-007-0237-7     URL    
[95]
Wang Y C, Han B J, Xie Y X, Wang H B, Wang R M, Xia W, Li H Y, Sun H Z. Chem. Sci., 2019, 10(24): 6099.

doi: 10.1039/C9SC01480B     URL    
[96]
Wang Y C, Hu L G, Xu F, Quan Q, Lai Y T, Xia W, Yang Y, Chang Y Y, Yang X M, Chai Z F, Wang J W, Chu I K, Li H Y, Sun H Z. Chem. Sci., 2017, 8(6): 4626.

doi: 10.1039/C7SC00766C     URL    
[97]
Wang R M, Lai T P, Gao P, Zhang H M, Ho P L, Woo P C Y, Ma G X, Kao R Y T, Li H Y, Sun H Z. Nat. Commun., 2018, 9: 439.

doi: 10.1038/s41467-018-02828-6    
[98]
Sun H Z, Zhang Q, Wang R M, Wang H B, Wong Y T, Wang M J, Hao Q, Yan A X, Kao R Y T, Ho P L, Li H Y. Nat. Commun., 2020, 11: 5263.

doi: 10.1038/s41467-020-18939-y    
[1] 施鹏飞,姜琴. 三价金配合物抗肿瘤活性研究*[J]. 化学进展, 2009, 21(04): 644-653.