Applications of Metallomics and Metalloproteomics Techniques in Biomedical Research

Yuchuan Wang

doi:10.7536/PC230301

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Prog Chem ›› 2023, Vol. 35 ›› Issue (10) : 1492-1504. DOI: 10.7536/PC230301

Review

Applications of Metallomics and Metalloproteomics Techniques in Biomedical Research

Yuchuan Wang ^*

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Abstract

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

Key words

metallomics / metalloproteomics / metallodrugs / drug-targeting proteins

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Yuchuan Wang. Applications of Metallomics and Metalloproteomics Techniques in Biomedical Research[J]. Progress in Chemistry. 2023, 35(10): 1492-1504 https://doi.org/10.7536/PC230301

References

List( Publishing order | Descend order by publishing year | Descend order by cited within ) Chart analysis

[1]	Valdez C E, Smith Q A, Nechay M R, Alexandrova A N. Acc. Chem. Res., 2014, 47(10): 3110. Cited in this article [1]

[2]	Foster A W, Young T R, Chivers P T, Robinson N J. Curr. Opin. Chem. Biol., 2022, 66: 102095. Cited in this article [1]

[3]	Chandrangsu P, Rensing C, Helmann J D. Nat. Rev. Microbiol., 2017, 15(6): 338. Cited in this article [1]

[4]	Mounicou S, Szpunar J, Lobinski R. Chem. Soc. Rev., 2009, 38(4): 1119. Cited in this article [1]

[5]	Xiong X L, Liu L Y, Mao Z W, Zou T T. Coord. Chem. Rev., 2022, 453: 214311. Cited in this article [2]

[6]	Wang Y C, Li H Y, Sun H Z. Inorg. Chem., 2019, 58(20): 13673. Cited in this article [2]

[7]	Wang H, Zhou Y, Xu X, Li H, Sun H. Curr. Opin. Chem. Biol., 2020, 55: 171. Cited in this article [1]

[8]	Scalese G, Kostenkova K, Crans D C, Gambino D. Curr. Opin. Chem. Biol., 2022, 67: 102127. Cited in this article [1]

[9]	Waldron K J, Rutherford J C, Ford D, Robinson N J. Nature, 2009, 460(7257): 823. Cited in this article [1]

[10]	Waldron K J, Robinson N J. Nat. Rev. Microbiol., 2009, 7(1): 25. Cited in this article [1]

[11]	Xu X H, Wang H B, Li H Y, Sun H Z. Chem. Lett., 2020, 49(6): 697. Cited in this article [1]

[12]	She Y M, Narindrasorasak S, Yang S Y, Spitale N, Roberts E A, Sarkar B. Mol. Cell. Proteom., 2003, 2(12): 1306. Cited in this article [1]

[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. Cited in this article [3]

[14]	Williams R J P. Coord. Chem. Rev., 2001, 216/217: 583. Cited in this article [1]

[15]	Haraguchi H. J. Anal. At. Spectrom., 2004, 19(1): 5. Cited in this article [1]

[16]	Maret W. Metallomics: the Science of Biometals and Biometalloids, 2018. Cited in this article [1]

[17]	Maret W. Metallomics, 2022, 14 (8): mfac051. Cited in this article [1]

[18]	da Silva M A, Sussulini A, Arruda M A. Expert Rev. Proteom., 2010, 7(3): 387. Cited in this article [1]

[19]	Yannone S M, Hartung S, Menon A L, Adams M W, Tainer J A. Curr. Opin. Biotechnol., 2012, 23(1): 89. Cited in this article [2]

[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. Cited in this article [5]

[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. Cited in this article [2]

[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. Cited in this article [1]

[23]	Shi W X, Chance M R. Curr. Opin. Chem. Biol., 2011, 15(1): 144. Cited in this article [1]

[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. Cited in this article [1]

[25]	JimÉnez-Lamana J, Szpunar J. Metallomics, 2017, 9(8): 1014. Cited in this article [1]

[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. Cited in this article [3]

[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. Cited in this article [1]

[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. Cited in this article [2]

[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. Cited in this article [2]

[30]	Prange A, Pröfrock D. Anal. Bioanal. Chem., 2005, 383(3): 372. Cited in this article [1]

[31]	Holtkamp H U, Movassaghi S, Morrow S J, Kubanik M, Hartinger C G. Metallomics, 2018, 10(3): 455. Cited in this article [1]

[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. Cited in this article [3]

[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. Cited in this article [2]

[34]	Timerbaev A R, Pawlak K, Aleksenko S S, Foteeva L S, Matczuk M, Jarosz M. Talanta, 2012, 102: 164. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[37]	Fahrni C J. Curr. Opin. Chem. Biol., 2007, 11(2): 121. Cited in this article [1]

[38]	Doble P A, de Vega R G, Bishop D P, Hare D J, Clases D. Chem. Rev., 2021, 121(19): 11769. Cited in this article [2]

[39]	Van Malderen S J M, Managh A J, Sharp B L, Vanhaecke F. J. Anal. At. Spectrom., 2016, 31(2): 423. Cited in this article [1]

[40]	Sun X S, Chiu J F, He Q Y. Methods in Molecular Biology?. Totowa, NJ: Humana Press, 2008. 205. Cited in this article [1]

[41]	Sun X S, Chiu J F, He Q Y. Expert Rev. Proteom., 2005, 2(5): 649. Cited in this article [2]

[42]	Block H, Maertens B, Spriestersbach A, Brinker N, Kubicek J, Fabis R, Labahn J, Schäfer F. Methods in Enzymology. Amsterdam: Elsevier, 2009. 439. Cited in this article [2]

[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. Cited in this article [1]

[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. Cited in this article [3]

[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. Cited in this article [4]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [2]

[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. Cited in this article [1]

[50]	Zeng X, Cheng Y, Wang C. Biochemistry, 2021, 60(46): 3507. Cited in this article [2]

[51]	Passerini A, Andreini C, Menchetti S, Rosato A, Frasconi P. BMC Bioinform., 2007, 8(1): 39. Cited in this article [1]

[52]	Passerini A, Lippi M, Frasconi P. Nucleic Acids Res., 2011, 39(2): W288. Cited in this article [1]

[53]	Zhang Y, Zheng J G. Molecules, 2020, 25(15): 3366. Cited in this article [1]

[54]	Hasty J, Pradines J, Dolnik M, Collins J J. Proc. Natl. Acad. Sci. U. S. A., 2000, 97(5): 2075. Cited in this article [1]

[55]	Tsang C N, Ho K S, Sun H Z, Chan W T. J. Am. Chem. Soc., 2011, 133(19): 7355. Cited in this article [1]

[56]	Zhou Y, Wang H B, Tse E, Li H Y, Sun H Z. Anal. Chem., 2018, 90(17): 10465. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[60]	Yoshida S, Ide-Ektessabi A, Fujisawa S. Struct. Chem., 2003, 14(1): 85. Cited in this article [1]

[61]	Ide-Ektessabi A, Fujisawa S, Yoshida S. J. Appl. Phys., 2002, 91(3): 1613. Cited in this article [1]

[62]	Matusch A, Fenn L S, Depboylu C, Klietz M, Strohmer S, McLean J A, Becker J S. Anal. Chem., 2012, 84(7): 3170. Cited in this article [1]

[63]	Theiner S, Schweikert A, Haberler C, Peyrl A, Koellensperger G. Metallomics, 2020, 12(8): 1246. Cited in this article [2]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[69]	Wang Y C, Wang H B, Li H Y, Sun H Z. Dalton Trans., 2015, 44(2): 437. Cited in this article [1]

[70]	Holtkamp H U, Hartinger C G. Trac Trends Anal. Chem., 2018, 104: 110. Cited in this article [1]

[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. Cited in this article [2]

[72]	Wehner K A, Schütz S, Sarnow P. Mol. Cell. Biol., 2010, 30(8): 2006. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [2]

[75]	Satelli A, Li S L. Cell. Mol. Life Sci., 2011, 68(18): 3033. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [2]

[78]	Henikoff S, Smith M M. Cold Spring Harb. Perspect. Biol., 2015, 7(1): a019364. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [2]

[82]	Wiche G, Osmanagic-Myers S, CastañÓn M J. Curr. Opin. Cell Biol., 2015, 32: 21. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[85]	McInroy L, Määttä A. Exp. Cell Res., 2011, 317(17): 2468. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [2]

[88]	Wang X X, Zhang J Y, Zhao X Y, Wei W, Zhao J. Metallomics, 2019, 11(8): 1344. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[91]	Lemire J A, Harrison J J, Turner R J. Nat. Rev. Microbiol., 2013, 11(6): 371. Cited in this article [1]

[92]	Turner R J. Microb. Biotechnol., 2017, 10(5): 1062. Cited in this article [1]

[93]	Gaberc-Porekar V, Menart V. J. Biochem. Biophys. Methods, 2001, 49(1/3): 335. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]

[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. Cited in this article [1]