Abstract
Metallothioneins (MTs) are a family of ubiquitous, low-molecular-mass, cysteine-rich proteins that play a significant role in maintaining intracellular metal homeostasis, eliminating metal toxification, and protecting cells against oxidative damages. Research activity on plant MTs, although known for 30 years, has only moderately increased in the past few years. In this study, a type 1 MT from maize (Zea mays) (ZmMT1) was successfully expressed in Escherichia coli strain BL21 (DE3). The UV absorption spectra recorded after the reconstitution of apo-ZmMT1 with different metals demonstrated that ZmMT1 can coordinate up to six Zn(II) ions, six Cd(II) ions, and even higher amounts of Pb(II). In addition, the general metal ion coordination abilities of ZmMT1 characterized by pH-dependent zinc-, lead- and cadmium-binding stability and by the competitive reaction with 5,5′-dithiobis-(2-nitrobenzoic acid) (DTNB) were evaluated. Results showed that the affinity of metal ions for the recombinant form of ZmMT1 can be arranged as follows: Cd(II) > Pb(II) > Zn(II). The observation revealed that chelating agents, such as ethylene diamine tetraacetic acid (EDTA) and ATP, accelerate the oxidation of ZmMT1 in the following order: EDTA ≫ l-histidine > ATP ≈ citrate. Meanwhile, commonly used buffers increase the reactivity of ZmMT1 with DTNB in the following order: PBS > Tris–HCl > HEPES.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76(2):160–202. https://doi.org/10.1016/j.aquatox.2005.08.015
Banerjea D, Kaden TA, Sigel H (1981) Enhanced stability of ternary complexes in solution through the participation of heteroaromatic N bases. Comparison of the coordination tendency of pyridine, imidazole, ammonia, acetate, and hydrogen phosphate toward metal ion nitrilotriacetate complexes. Inorg Chem 20:2586–2590. https://doi.org/10.1021/ic50222a040
Capdevila M, Bofill R, Palacios Ò, Atrian S (2012) State-of-the-art of metallothioneins at the beginning of the 21st century. Coord Chem Rev 256:46–62. https://doi.org/10.1016/j.ccr.2011.07.006
Chevalier C, Bourgeois E, Pradet A, Raymond P (1995) Molecular cloning and characterization of six cDNAs as expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Mol Biol 28:473–485. https://doi.org/10.1007/BF00020395
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev Plant Biol 53:159–182. https://doi.org/10.1146/annurev.arplant.53.100301.135154
Damodaran S (1985) Estimation of disulfide bonds using 2-nitro-5-thiosulfobenzoic acid: limitations. Anal Biochem 145:200–204. https://doi.org/10.1016/0003-2697(85)90348-3
de Framond AJ (1991) A metallothionein-like gene from maize (Zea mays) cloning and characterization. FEBS Lett 290:103–106. https://doi.org/10.1016/0014-5793(91)81236-2
Evans IM, Gatehouse LN, Gatehouse JA, Robinson NJ, Croy RR (1990) A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Lett 262:29–32
Feng W, Benz FW, Cai J, Pierce WM, Kang YJ (2006) Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J Biol Chem 281:681–687. https://doi.org/10.1074/jbc.M506956200
Fischer BE, Häring UK, Tribolet R, Sigel H (1979) Metal ion/buffer interactions, stability of binary and ternary complexes containing 2-amino-2(hydroxymethyl)-l, 3-propanediol (tris) and adenosine 5′-triphosphate (ATP). Eur J Biochem 94:523–530. https://doi.org/10.1111/j.1432-1033.1979.tb12921.x
Freisinger E (2007) Spectroscopic characterization of a fruit-specific metallothionein: M. acuminata MT3. Inorg Chim Acta 360:369–380. https://doi.org/10.1016/j.ica.2006.07.059
Freisinger E (2008) Plant MTs-long neglected members of the metallothionein superfamily. Dalton Trans 47:6663–6675. https://doi.org/10.1039/b809789e
Jiang LJ, Maret W, Vallee BL (1998) The ATP-metallothionein complex. Proc Natl Acad Sci USA 95(16):9146–9149
Jiang LJ, Vašák M, Vallee BL, Maret W (2000) Zinc transfer potentials of the α- and β-clusters of metallothionein are affected by domain interactions in the whole molecule. Proc Natl Acad Sci USA 97:2503–2508. https://doi.org/10.1073/pnas.97.6.2503
Kăgi J, Vallee BL (1960) Metallothionein: a cadmium and zinc-containing protein from equine renal cortex. J Biol Chem 235:3460–3465
Kreźel A, Maret W (2007) Dual nanomolar and picomolar Zn(II) binding properties of metallothionein. J Am Chem Soc 129:10911–10921. https://doi.org/10.1021/ja071979s
Leszczyszyn OI, Imam HT, Blindauer CA (2013) Diversity and distribution of plant metallothioneins: a review of structure, properties and functions. Metallomics 9(5):1146–1169. https://doi.org/10.1039/c3mt00072a
Li Y, Chen YY, Yang SG, Tian WM (2015) Cloning and characterization of HbMT2a, a metallothionein gene from Hevea brasiliensis Muell. Arg differently responds to abiotic stress and heavy metals. Biochem Biophys Res Commun 461:95–101. https://doi.org/10.1016/j.bbrc.2015.03.175
Loebus J, Peroza EA, Blüthgen N, Fox T, Meyer-Klaucke W, Zerbe O, Freisinger E (2011) Protein and metal cluster structure of the wheat metallothionein domain γ-Ec-1: the second part of the puzzle. J Biol Inorg Chem 16:683–694. https://doi.org/10.1007/s00775-011-0770-2
Meloni G, Knipp M, Vašák M (2005) Detection of neuronal growth inhibitory factor (metallothionein-3) in polyacrylamide gels and by Western blot analysis. J Biochem Biophys Method 64:76–81. https://doi.org/10.1016/j.jbbm.2005.05.005
Morgoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79:4813–4814. https://doi.org/10.1021/ja01574a064
Mudalkar S, Golla R, Sengupta D, Ghatty S, Reddy AR (2014) Molecular cloning and characterisation of metallothionein type 2a gene from Jatropha curcas L., a promising biofuel plant. Mol Biol Rep 41:113–124. https://doi.org/10.1007/s11033-013-2843-5
Palacios Ò, Espart A, Espín J, Ding C, Thiele DJ, Atrian S, Capdevila M (2014) Full characterization of the Cu-, Zn-, and Cd-binding properties of CnMT1 and CnMT2, two metallothioneins of the pathogenic fungus Cryptococcus neoformans acting as virulence factors. Metallomics 6:279–291. https://doi.org/10.1039/c3mt00266g
Pan PKY, Zheng ZF, Lyu PC, Huang PC (1999) Why reversing the sequence of the α domain of human metallothionein-2 does not change its metal-binding and folding characteristics. Eur J Biochem 266:33–39. https://doi.org/10.1046/j.1432-1327.1999.00811.x
Peroza EA, Freisinger E (2007) Metal ion binding properties of Tricium aestivum Ec-1 metallothionein: evidence supporting two separate metal thiolate clusters. J Biol Inorg Chem 12:377–391. https://doi.org/10.1007/s00775-006-0195-5
Pirzadeh S, Shahpiri A (2016) Functional characterization of a type 2 metallothionein isoform (OsMTI-2b) from rice. Int J Biol Macromol 88:491–496. https://doi.org/10.1016/j.ijbiomac.2016.04.021
Reinecke F, Levanets O, Olivier Y, Louw R, Semete B, Grobler A, Hidalgo J, Smeitink J, Olckers A, Van der Westhuizen FH (2006) Metallothionein isoform 2A expression is inducible and protects against ROS-mediated cell death in rotenone-treated HeLa cells. Biochem J 395:405–415. https://doi.org/10.1042/bj20051253
Savas MM, Shaw CF III, Petering DH (1993) The oxidation of rabbit liver metallothionein-II by 5,5′-dithiobis (2-nitrobenzoic acid) and glutathione disulfide. J Inorg Biochem 52:235–249. https://doi.org/10.1016/0162-0134(93)80028-8
Schicht O, Freisinger E (2009) Spectroscopic characterization of Cicer arietinum metallothionein 1. Inorg Chim Acta 362:714–724. https://doi.org/10.1016/j.ica.2008.03.097
Shahpiri A, Soleimanifard I, Asadollahi MA (2015) Functional characterization of a type 3 metallolthionein isoform (OsMTI-3a) from rice. Int J Biol Macromol 73:154–159. https://doi.org/10.1016/j.ijbiomac.2014.10.067
Thannhauser TW, Konishi Y, Scheraga HA (1984) Sensitive quantitative analysis of disulfide bonds in polypeptides and proteins. Anal Biochem 138:181–188. https://doi.org/10.1016/0003-2697(84)90786-3
Tommey AM, Shi JG, Lindsay WP, Urwin PE, Robinson NJ (1991) Expression of the pea genePsMTA in E. coli metal-binding properties of the expressed protein. FEBS Lett 292:48–52. https://doi.org/10.1016/0014-5793(91)80831-m
Vašák M, Kăgi JHR (1983) Spectroscopic properties of metallothionein. In: Metal ions in biological systems, vol 15. Marcel Dekker Inc, New York, pp 213–273
Vašák M, Kăgi JHR, Hill HAO (1981) Zinc(II), cadmium(II), and mercury(II) thiolate transitions in metallothionein. Biochemistry 20:2852–2856. https://doi.org/10.1021/bi00513a022
Wan XQ, Freisinger E (2009) The plant metallothionein 2 from Cicer arietinum forms a single metal–thiolate cluster. Metallomics 1:489–500. https://doi.org/10.1039/b906428a
Winge DR, Miklossy KA (1982) Domain nature of metallothionein. J Biol Chem 257:3471–3476
Xing BG, Shi YB, Tang WX (2000) Kinetic studies of the reactions of some metal reconstituted metallothioneins with the electrophilic disulfide 5,5′-dithiobis(2-nitrobenzoic acid) (DTNB). Biometals 13(4):295–300. https://doi.org/10.1023/A:1009201325771
Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58:839–855. https://doi.org/10.1007/s11103-005-8268-3
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 21301126), the Natural Science Foundation of Shanxi Province (Grant Nos. 2013021009-3, 201701D221038) and Scientific and Technological Innovation Programs of Higher Education and Institutions in Shanxi (STIP) (Grant No. 2017128).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Duan, L., Kong, JJ., Wang, TQ. et al. Binding of Cd(II), Pb(II), and Zn(II) to a type 1 metallothionein from maize (Zea mays). Biometals 31, 539–550 (2018). https://doi.org/10.1007/s10534-018-0100-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-018-0100-z