Forgotten partners and function regulators of inducible metallothioneins

1. Vallee BL. Metallothionein: historical review and perspectives. In: Kägi JHR, Nordberg M, editors. Metallothionein. Experientia Supplementum. Vol. 34. Basel: Birkhäuser; 1979. p. 19-39. doi: 10.1007/978-3-0348-6493-0_110.1007/978-3-0348-6493-0_1Open DOISearch in Google Scholar

2. Capdevila M, Bofill R, Palacios Ò, Atrian S. State-of-the-art of metallothioneins at the beginning of the 21^st century. Coord Chem Rev 2012;256:46-62. doi: 10.1016/j.ccr.2011.07.00610.1016/j.ccr.2011.07.006Open DOISearch in Google Scholar

3. Hidalgo J, Chung R, Penkowa M, Vasak M. Structure and function of vertebrate metallothioneins. In: Sigel A, Sigel H, Sigel RKO, editors. Metallothioneins and related chelators: Metal ions in life sciences. Cambridge: RSC Publishing; 2009. p. 279-317. doi: 10.1039/9781847558992-0027910.1039/9781847558992-00279Open DOISearch in Google Scholar

4. Ziller A, Fraissinet-Tachet L. Metallothionein diversity and distribution in the tree of life: a multifunctional protein. Metallomics 2018;10:1549-59. doi: 10.1039/c8mt00165k10.1039/C8MT00165KSearch in Google Scholar

5. Jiang L-J, Maret W, Vallee BL. The glutathione redox couple modulates zinc transfer from metallothionein to zinc-depleted sorbitol dehydrogenase. Proc Natl Acad Sci U S A 1998;95:3483-8. doi: 10.1073/pnas.95.7.348310.1073/pnas.95.7.3483Search in Google Scholar

6. Chen Y, Maret W. Catalytic selenols couple the redox cycles of metallothionein and glutathione. Eur J Biochem 2001;268:3346-53. doi: 10.1046/j.1432-1327.2001.02250.x10.1046/j.1432-1327.2001.02250.xOpen DOISearch in Google Scholar

7. Jiang L-J, Maret W, Vallee BL. The ATP-metallothionein complex. Proc Natl Acad Sci U S A 1998;95:9146-9. doi: 10.1073/pnas.95.16.914610.1073/pnas.95.16.9146Open DOISearch in Google Scholar

8. Maret W, Heffron G, Hill HA, Djuricic D, Jiang L-J, Vallee BL. The ATP/metallothionein interaction: NMR and STM. Biochemistry 2002;41:1689-94. doi: 10.1021/bi01160831181436410.1021/bi0116083Search in Google Scholar

9. Romero-Isart N, Vasák M. Advances in the structure and chemistry of metallothioneins. J Inorg Biochem 2002;88:388-96. doi: 10.1016/S0162-0134(01)00347-610.1016/S0162-0134(01)00347-6Open DOISearch in Google Scholar

10. Sabolić I, Breljak D, Škarica M, Herak-Kramberger CM. Role of metallothionein in cadmium traffic and toxicity in kidneys and other mammalian organs. BioMetals 2010;23:897-926. doi: 10.1007/s10534-010-9351-z10.1007/s10534-010-9351-z20549307Search in Google Scholar

11. Wong DL, Merrifield-MacRae ME, Stillman MJ. Lead(II) binding in metallothioneins. In: Sigel A, Sigel H, Sigel R, editors. Lead - Its effects on environment and health. Berlin, Boston: De Gruyter; 2017. p. 241-70. doi: 10.1515/9783110434330-00910.1515/9783110434330-00928731302Open DOISearch in Google Scholar

12. Bell SG, Vallee BL. The metallothionein/thionein system: an oxidoreductive metabolic zinc link. Chembiochem 2009;10:55-62. doi: 10.1002/cbic.20080051110.1002/cbic.200800511Open DOISearch in Google Scholar

13. Cai L, Satoh M, Tohyama C, Cherian MG. Metallothionein in radiation exposure: its induction and protective role. Toxicology 1999;132:85-98. doi: 10.1016/s0300-483x(98)00150-410.1016/s0300-483x(98)00150-4Open DOISearch in Google Scholar

14. Mocchegiani E, Costarelli L, Basso A, Giacconi R, Piacenza F, Malavolta M. Metallothioneins, ageing and cellular senescence: a future therapeutic target. Curr Pharm Des 2013;19:1753-64. doi: 10.2174/138161281131909002210.2174/1381612811319090022Open DOISearch in Google Scholar

15. Malavolta M, Orlando F, Piacenza F, Giacconi R, Costarelli L, Basso A, Lucarini G, Pierpaoli E, Provinciali M. Metallothioneins, longevity and cancer: Comment on “Deficiency of metallothionein-1 and -2 genes shortens the lifespan of the 129/Sv mouse strain”. Exp Gerontol 2016;73:28-30. doi: 10.1016/j.exger.2015.11.01410.1016/j.exger.2015.11.01426615880Open DOISearch in Google Scholar

16. Jarosz M, Olbert M, Wyszogrodzka G, Młyniec K, Librowski T. Antioxidant and anti-inflammatory effects of zinc. Zinc-dependent NF-κB signaling. Inflammopharmacology 2017;25:11-24. doi: 10.1007/s10787-017-0309-410.1007/s10787-017-0309-4530617928083748Open DOISearch in Google Scholar

17. Muckenthaler MU, Rivella S, Hentze MW, Galy B. A red carpet for iron metabolism. Cell 2017;168:344-61. https://doi.org/10.1016/j.cell.2016.12.03410.1016/j.cell.2016.12.034570645528129536Open DOISearch in Google Scholar

18. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J 2012;5:9-19. doi: 10.1097/WOX.0b013e318243961310.1097/WOX.0b013e3182439613348892323268465Open DOISearch in Google Scholar

19. Maret W. The redox biology of redox-inert zinc ions. Free Radic Biol Med 2019;134:311-26. doi: 10.1016/j.freeradbiomed.2019.01.00610.1016/j.freeradbiomed.2019.01.00630625394Open DOISearch in Google Scholar

20. Maret W. The metals in the biological periodic system of the elements: concepts and conjectures. Int J Mol Sci 2016;17:pii: E66. doi: 10.3390/ijms1701006610.3390/ijms17010066473031126742035Open DOISearch in Google Scholar

21. Nishito Y, Kambe T. Absorption mechanisms of iron, copper, and zinc: an overview. J Nutr Sci Vitaminol (Tokyo) 2018;64:1-7. doi: 10.3177/jnsv.64.110.3177/jnsv.64.129491267Open DOISearch in Google Scholar

22. Zhang CC, Volkmann M, Tuma S, Stremmel W, Merle U. Metallothionein is elevated in liver and duodenum of Atp7b^(−/−) mice. BioMetals 2018;31:617-25. doi: 10.1007/s10534-018-0110-x10.1007/s10534-018-0110-x29732486Open DOISearch in Google Scholar

23. Kimura T, Kambe T. The functions of metallothionein and ZIP and ZnT transporters: an overview and perspective. Int J Mol Sci 2016;17:336. doi: 10.3390/ijms1703033610.3390/ijms17030336481319826959009Open DOISearch in Google Scholar

24. Hara T, Takeda TA, Takagishi T, Fukue K, Kambe T, Fukada T. Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. J Physiol Sci 2017;67:283-301. doi: 10.1007/s12576-017-0521-410.1007/s12576-017-0521-428130681Open DOISearch in Google Scholar

25. Baltaci AK, Yuce K. Zinc transporter proteins. Neurochem Res 2018;43:517-30. doi: 10.1007/s11064-017-2454-y10.1007/s11064-017-2454-y29243032Open DOISearch in Google Scholar

26. Baltaci AK, Yuce K, Mogulkoc R. Zinc metabolism and metallothioneins. Biol Trace Elem Res 2018;183:22-31. doi: 10.1007/s12011-017-1119-710.1007/s12011-017-1119-728812260Open DOISearch in Google Scholar

27. Casey JR, Grinstein S, Orlowski J. Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 2010;11:50-61. doi: 10.1038/nrm282010.1038/nrm282019997129Open DOISearch in Google Scholar

28. Stockwell BR, Friedmann A J, Bayir H, Bush AI, Conrad M, Dixon SJ, Fulda S, Gascón S, Hatzios SK, Kagan VE, Noel K, Jiang X, Linkermann A, Murphy ME, Overholtzer M, Oyagi A,Pagnussat GC, Park J, Ran Q, Rosenfeld CS, Salnikow K, Tang D, Torti FM, Torti SV, Toyokuni S, Woerpel KA, Zhang DD. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell 2017; 171:273-85. doi: 10.1016/j.cell.2017.09.02110.1016/j.cell.2017.09.021568518028985560Open DOISearch in Google Scholar

29. Klaassen CD, Choudhuri S, McKim JM Jr, Lehman-McKeeman LD, Kershaw WC. In vitro and in vivo studies on the degradation of metallothionein. Environ Health Perspect 1994;102(Suppl 3):141-6. doi: 10.1289/ehp.94102s314110.1289/ehp.94102s314115674347843089Open DOISearch in Google Scholar

30. Arosio P, Elia L, Poli M. Ferritin, cellular iron storage and regulation. IUBMB Life 2017;69:414-22. doi: 10.1002/iub.162110.1002/iub.162128349628Open DOISearch in Google Scholar

31. Baird SK, Kurz T, Brunk UT. Metallothionein protects against oxidative stress-induced lysosomal destabilization. Biochem J 2006;394:275-83. doi: 10.1042/BJ2005114310.1042/BJ20051143138602616236025Open DOISearch in Google Scholar

32. Kurz T, Terman A, Brunk UT. Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch Biochem Biophys 2007;462:220-30. doi: 10.1016/j.abb.2007.01.01310.1016/j.abb.2007.01.013Open DOISearch in Google Scholar

33. Terman A, Kurz T. Lysosomal iron, iron chelation, and cell death. Antioxid Redox Signal 2013;18:888-98. doi: 10.1089/ars.2012.488510.1089/ars.2012.4885Open DOISearch in Google Scholar

34. Kojima N, Young CR, Bates GW. Failure of metallothionein to bind iron or act as an iron mobilizing agent. Biochim Biophys Acta 1982;716:273-5. doi: 10.1016/0304-4165(82)90278-110.1016/0304-4165(82)90278-1Open DOISearch in Google Scholar

35. Good M, Vasak M. Iron(II)-substituted metallothionein: evidence for the existence of iron-thiolate clusters. Biochemistry 1986;25:8353-6. doi: 10.1021/bi00374a00310.1021/bi00374a00338282843828284Open DOISearch in Google Scholar

36. Ding X, Bill E, Good M, Trautwein A X, Vašák M. Mössbauer studies on the metal-thiolate cluster formation in Fe(II)-metallothionein. Eur J Biochem 1988;171:711-4. doi: 10.1111/j.1432-1033.1988.tb13843.x10.1111/j.1432-1033.1988.tb13843.x3345754Open DOISearch in Google Scholar

37. Werth MT, Johnson MK. Magnetic circular dichroism and electron paramagnetic resonance studies of iron(II)-metallothionein. Biochemistry 1989;28:3982-8. doi: 10.1021/bi00435a05310.1021/bi00435a0532546588Search in Google Scholar

38. Fleet JC, Andrews GK, McCormick CC. Iron-induced metallothionein in chick liver: a rapid, route-dependent effect independent of zinc status. J Nutr 1990;120:1214-22. doi: 10.1093/jn/120.10.121410.1093/jn/120.10.12142213249Open DOISearch in Google Scholar

39. Kennedy MC, Gan T, Antholine WE, Petering DH. Metallothionein reacts with Fe²⁺ and NO to form products with a g=2.039 ESR signal. Biochem Biophys Res Commun 1993;196:632-5. doi: 10.1006/bbrc.1993.229610.1006/bbrc.1993.22968240338Open DOISearch in Google Scholar

40. Ding XQ, Bill E, Trautwein AX, Hartmann HJ, Weser U. Mössbauer studies on iron(II)-substituted yeast metallothionein. Eur J Biochem 1994;223:841-5. doi: 10.1111/j.1432-1033.1994.tb19060.x10.1111/j.1432-1033.1994.tb19060.x8055961Open DOISearch in Google Scholar

41. Sano Y, Onoda A, Sakurai R, Kitagishi H, Hayashi T. Preparation and reactivity of a tetranuclear Fe(II) core in the metallothionein α-domain. J Inorg Biochem 2011;105:702-8. doi: 10.1016/j.jinorgbio.2011.01.01110.1016/j.jinorgbio.2011.01.01121450274Search in Google Scholar

42. Orihuela R, Fernández B, Palacios O, Valero E, Atrian S, Watt RK, Dominguez-Vera JM, Capdevila M. Ferritin and metallothionein: dangerous liaisons. Chem Commun 2011;47:12155-7. doi: 10.1039/c1cc14819b10.1039/c1cc14819b21991581Open DOISearch in Google Scholar

43. Carmona F, Mendoza D, Kord S, Asperti M, Arosio P, Atrian S, Capdevila M, Dominguez-Vera JM. Chemically and biologically harmless versus harmful ferritin/copper-metallothionein couples. Chemistry 2015;21:808-13. doi: 10.1002/chem.20140466010.1002/chem.20140466025370199Open DOISearch in Google Scholar

44. Raghunath A, Sundarraj K, Nagarajan R, Arfuso F, Bian J, Kumar AP, Sethi G, Perumal E. Antioxidant response elements: Discovery, classes, regulation and potential applications. Redox Biol 2018;17:297-314. doi: 10.1016/j.redox.2018.05.00210.1016/j.redox.2018.05.002600781529775961Open DOISearch in Google Scholar

45. Song Y, Yang H, Lin R, Jiang K, Wang BM. The role of ferroptosis in digestive system cancer. Oncol Lett 2019; 18:2159-64. doi: 10.3892/ol.2019.1056810.3892/ol.2019.1056831402933667671031402933Open DOISearch in Google Scholar

46. Slater EP, Cato AC, Karin M, Baxter JD, Beato M. Progesterone induction of metallothionein-II_A gene expression. Mol Endocrinol 1988;2:485-91. doi: 10.1210/mend-2-6-48510.1210/mend-2-6-48528437582843758Open DOISearch in Google Scholar

47. Orct T, Jurasović J, Micek V, Karaica D, Sabolić I. Macro-and microelements in the rat liver, kidneys, and brain tissues; sex differences and effect of blood removal by perfusion in vivo. J Trace Elem Med Biol 2017;40:104-11. doi: 10.1016/j.jtemb.2016.12.01510.1016/j.jtemb.2016.12.01528159217Open DOISearch in Google Scholar

48. Ljubojević M, Orct T, Micek V, Karaica D, Jurasović J, Breljak D, Vrhovac Madunić I, Rašić D, Novak Jovanović I, Peraica M, Gerić M, Gajski G, Kralik Oguić S, Rogić D, Nanić L, Rubelj I, Sabolić I. Sex-dependent expression of metallothioneins MT1 and MT2 and concentrations of trace elements in rat liver and kidney tissues: Effect of gonadectomy. J Trace Elem Med Biol 2019;53:98-108. doi: 10.1016/j.jtemb.2019.02.01010.1016/j.jtemb.2019.02.01030910215Open DOISearch in Google Scholar

49. Shimada H, Hashiguchi T, Yasutake A, Waalkes MP. Imamura Y. Sexual dimorphism of cadmium-induced toxicity in rats: involvement of sex hormones. Arch Toxicol 2012;86:1475-80. doi: 10.1007/s00204-012-0844-010.1007/s00204-012-0844-022466070Open DOISearch in Google Scholar

50. Hahn P, Song Y, Ying GS, He X, Beard J, Dunaief JL. Age-dependent and gender-specific changes in mouse tissue iron by strain. Exp Gerontol 2009;44:594-600. doi: 10.1016/j.exger.2009.06.0061956387710.1016/j.exger.2009.06.006455218819563877Search in Google Scholar

51. Thévenod F, Wolff NA. Iron transport in the kidney: implications for physiology and cadmium nephrotoxicity. Metallomics 2016;8:17-42. doi: 10.1039/c5mt00215j10.1039/C5MT00215JOpen DOISearch in Google Scholar

52. Kong WN, Niu QM, Ge L, Zhang N, Yan SF, Chen WB, Chang YZ, Zhao SE. Sex differences in iron status and hepcidin expression in rats. Biol Trace Elem Res 2014;160:258-67. doi: 10.1007/s12011-014-0051-310.1007/s12011-014-0051-3Open DOISearch in Google Scholar

53. Sangkhae V, Nemeth E. Regulation of the iron homeostatic hormone hepcidin. Adv Nutr 2017;8:126-36. doi: 10.3945/an.116.01396110.3945/an.116.013961Search in Google Scholar

54. Liu Y, Liu J, Habeebu SM, Waalkes MP, Klaassen CD. Metallothionein-I/II null mice are sensitive to chronic oral cadmium-induced nephrotoxicity. Toxicol Sci 2000;57:167-76. doi: 10.1093/toxsci/57.1.16710.1093/toxsci/57.1.16710966523Open DOISearch in Google Scholar

55. Iszard RD, Liu Y, Dalton T, Andrews GK, Palmiter RD, Klaassen CD. Characterization of metallothionein-I-transgenic mice. Toxicol Appl Pharmacol 1995;133:305-12. doi: 10.1006/taap.1995.115510.1006/taap.1995.1155Open DOISearch in Google Scholar

56. Miura N, Koizumi S. Gene expression profiles in the liver and kidney of metallothionein-null mice. Biochem Biophys Res Commun 2005;332:949-55. doi: 10.1016/j.bbrc.2005.05.04310.1016/j.bbrc.2005.05.043Open DOISearch in Google Scholar

57. Kumar C, Igbaria A, D’Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, Toledano MB. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 2011;30:2044-56. doi: 10.1038/emboj.2011.10510.1038/emboj.2011.105Open DOISearch in Google Scholar

58. Zalewska M, Trefon J, Milnerowicz H. The role of metallothionein interactions with other proteins. Proteomics 2014;14:1343-56. doi: 10.1002/pmic.2013004962461628610.1002/pmic.201300496Search in Google Scholar

59. Oliván S, Calvo AC, Manzano R, Zaragoza P, Osta R. Sex differences in constitutive autophagy. BioMed Res Int 2014;2014:ID652817. doi: 10.1155/2014/65281710.1155/2014/652817Search in Google Scholar

60. Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 2014;509:105-9. doi: 10.1038/nature1314810.1038/13148Open DOISearch in Google Scholar

61. Fleming JT, Joshi JG. Ferritin: the role of aluminium in ferritin function. Neurobiol Aging 1991;12:413-8. doi: 10.1016/0197-4580(91)90066-S10.1016/0197-4580(91)90066-SSearch in Google Scholar

62. Rutherford JC, Bird AJ. Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 2004;3:1-13. doi: 10.1128/EC.3.1.1-13.20041487193210.1128/EC.3.1.1-13.2004Search in Google Scholar

63. Robertson A, Morrison JN, Wood AM, Bremner I. Effects of iron deficiency on metallothionein-I concentrations in blood and tissues of rats. J Nutr 1989;119:439-45. doi: 10.1093/jn/119.3.43910.1093/jn/119.3.439Open DOISearch in Google Scholar

64. Philpott CC, Ryu MS. Special delivery: distributing iron in the cytosol of mammalian cells. Front Pharmacol 2014;5:173. doi: 10.3389/fphar.2014.0017310.3389/fphar.2014.00173Open DOISearch in Google Scholar

65. Linder MC, Munro HN. Metabolic and chemical features of ferritins, a series of iron-inducible tissue proteins. Am J Pathol 1973;72:263-82. PMCID: PMC1903991Search in Google Scholar

66. Atrian S, Capdevila M. Metallothionein-protein interactions. Biomol Concepts 2013;4:143-60. doi: 10.1515/bmc-2012-004910.1515/bmc-2012-004925436572Open DOISearch in Google Scholar

67. Zangger K, Öz G, Armitage IM. Re-evaluation of the binding of ATP to metallothionein. J Biol Chem 2000;275:7534-8. Erratum in: J Biol Chem 2001;276:30570. doi: 10.1074/jbc.275.11.753410.1074/jbc.275.11.7534Search in Google Scholar

68. Zangger K, Armitage IM. Dynamics of interdomain and intermolecular interactions in mammalian metallothioneins. J Inorg Biochem 2002;88:135-43. doi: 10.1016/S0162-0134(01)00379-810.1016/S0162-0134(01)00379-8Open DOISearch in Google Scholar

69. Kuro-o M. A potential link between phosphate and aging-lessons from Klotho-deficient mice. Mech Ageing Dev 2010;131:270-5. doi: 10.1016/j.mad.2010.02.00810.1016/j.mad.2010.02.008Open DOISearch in Google Scholar

70. Ala A, Walker AP, Ashkan K, Dooley JS, Schilsky ML. Wilson’s disease. Lancet 2007;369:397-408. doi: 10.1016/S0140-6736(07)60196-210.1016/S0140-6736(07)60196-2Open DOISearch in Google Scholar