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Metallothionein protein evolution: a miniassay

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Abstract

Metallothionein (MT) evolution is one of the most obscure yet fascinating aspects of the study of these atypical metal-binding peptides. The different members of the extremely heterogeneous MT protein superfamily probably evolved through a web of duplication, functional differentiation, and/or convergence events leading to the current scenario, which is particularly hard to interpret in terms of molecular evolution. Difficulties in drawing straight evolutionary relationships are reflected in the lack of definite MT classification criteria. Presently, MTs are categorized either according to a pure taxonomic clustering or depending on their metal binding preferences and specificities. Extremely well documented MT revisions were recently published. But beyond classic approaches, this review of MT protein evolution will bring together new aspects that have seldom been discussed before. Hence, the emergence of life on our planet, since metal ion utilization is accepted to be at the root of the emergence of living organisms, and global trends that underlie structural and functional MT diversification, will be presented. Major efforts are currently being devoted to identifying rules for function-constrained MT evolution that may be applied to different groups of organisms.

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Abbreviations

GYA:

Billion years ago

hlMT:

Horse liver metallothionein

MT:

Metallothionein

References

  1. Sigel A, Sigel H, Sigel RKO (eds) (2009) Metal ions in life sciences 5: metallothioneins and related chelators. Royal Society of Chemistry, Cambridge

    Google Scholar 

  2. Williams RJP (2010) J Biol Inorg Chem 15:1175–1176

    Article  CAS  Google Scholar 

  3. Palmiter RD (1998) Proc Natl Acad Sci USA 95:8428–8430

    Article  PubMed  CAS  Google Scholar 

  4. Margoshes M, Vallee BL (1957) J Am Chem Soc 79:4813

    Article  CAS  Google Scholar 

  5. Wolfe KH, Shields DC (1997) Nature 387:708–713

    Article  PubMed  CAS  Google Scholar 

  6. Lundin LG (1999) Semin Cell Dev Biol 10:523–530

    Article  PubMed  CAS  Google Scholar 

  7. Holland PW, Garcia-Fernandez J, Williams NA, Sidow A (1994) Dev Suppl 43:125–133

    Google Scholar 

  8. Gonzalez-Duarte P (2003) Compr Coord Chem II 8:213–228

    Google Scholar 

  9. Blindauer CA, Leszczyszyn OI (2010) Nat Prod Rep 27:720–741

    Article  PubMed  CAS  Google Scholar 

  10. Palacios O, Pagani A, Perez-Rafael S, Egg M, Höckner M, Brandstätter A, Capdevila M, Atrian S, Dallinger R (2011) BMC Biol 9:4

    Article  PubMed  CAS  Google Scholar 

  11. Valls M, Bofill R, Gonzalez-Duarte R, Gonzalez-Duarte P, Capdevila M, Atrian S (2001) J Biol Chem 276:32835–32843

    Article  PubMed  CAS  Google Scholar 

  12. Bofill R, Capdevila M, Atrian S (2009) Metallomics 1:229–234

    Article  PubMed  CAS  Google Scholar 

  13. Williams RJP (2002) J Inorg Biochem 88:241–250

    Article  PubMed  CAS  Google Scholar 

  14. Mulkidjanian AY, Galperin MY (2010) Proc Natl Acad Sci USA 107:E138

    Article  Google Scholar 

  15. Dupont C, Butcher A, Valas RE, Bourne PE, Caetano-Anolles G (2010) Proc Natl Acad Sci USA 107:10567–10572

    Article  PubMed  CAS  Google Scholar 

  16. Mulkidjanian AY (2009) Biol Direct 4:26

    Article  PubMed  Google Scholar 

  17. Mulkidjanian AY, Galperin MY (2009) Biol Direct 4:27

    Article  PubMed  Google Scholar 

  18. Abolmaali B, Taylor HV, Weser U (1998) Struct Bond 91:91–190

    Article  CAS  Google Scholar 

  19. Bertini I, Rosato A (2003) Proc Natl Acad Sci USA 100:3601–3604

    Article  PubMed  CAS  Google Scholar 

  20. Decaria L, Bertini I, Williams RJP (2010) Metallomics 2:706–709

    Article  PubMed  CAS  Google Scholar 

  21. Decaria L, Bertini I, Williams RJP (2011) Metallomics 3:56–60

    Article  PubMed  CAS  Google Scholar 

  22. Blair Hedges S (2002) Nat Rev Genet 3:838–849

    Article  PubMed  Google Scholar 

  23. Olafson RW, McCubbin WD, Kay CM (1988) Biochem J 251:691–699

    PubMed  CAS  Google Scholar 

  24. Cook WJ, Kar SR, Taylor KB, Hall LM (1998) J Mol Biol 275:337–346

    Article  PubMed  CAS  Google Scholar 

  25. Blindauer CA, Harrison MD, Parkinson JA, Robinson AK, Cavet JS, Robinson NJ, Sadler PJ (2001) Proc Natl Acad Sci USA 98:9593–9598

    Article  PubMed  CAS  Google Scholar 

  26. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Mol Microbiol 45:1421–1432

    Article  PubMed  CAS  Google Scholar 

  27. Blindauer CA (2009) Met Ions Life Sci 5:51–81

    Article  CAS  Google Scholar 

  28. Leszczyszyn OI, White CRJ, Blindauer CA (2010) Mol Biosyst 6:1592–1603

    Article  PubMed  CAS  Google Scholar 

  29. Robinson NJ (2008) Nat Chem Biol 4:582–583

    Article  PubMed  CAS  Google Scholar 

  30. Schmidt A, Hagen M, Schütze E, Schmidt A, Kothe E (2010) J Basic Microbiol 50:1–8

    Article  Google Scholar 

  31. Gold B, Deng H, Bryk R, Vargas D, Eliezer D, Roberts J, Jiang X, Nathan C (2008) Nat Chem Biol 4:609–616

    Article  PubMed  CAS  Google Scholar 

  32. Blindauer CA, Leszczyszyn OI (2010) Nat Prod Rep 27:720–741

    Article  PubMed  CAS  Google Scholar 

  33. Morris CA, Nicolaus B, Harwood JL, Kille P, Sampson V (1999) Biochem J 338:553–560

    Article  PubMed  CAS  Google Scholar 

  34. Diaz S, Amaro F, Rico D, Campos V, Benitez L et al (2007) PLoS ONE 2(3):e291

    Article  PubMed  Google Scholar 

  35. Dolderer B, Hartmann H-J, Weser U (2009) Met Ions Life Sci 5:83–102

    Article  CAS  Google Scholar 

  36. Nemer M, Wilkinson DG, Travaglini EC, Sternberg EJ, Butt TR (1985) Proc Natl Acad Sci USA 82:4992–4994

    Article  PubMed  CAS  Google Scholar 

  37. Pagani A, Villarreal L, Capdevila M, Atrian S (2007) Mol Microbiol 63:256–269

    Article  PubMed  CAS  Google Scholar 

  38. Borrelly GPM, Harrison MD, Robinson AK, Cox SG, Robinson NJ, Whitehall SK (2002) J Biol Chem 277:30394–30400

    Article  PubMed  CAS  Google Scholar 

  39. Blindauer CA (2008) J Inorg Biochem 102:507–521

    Article  PubMed  CAS  Google Scholar 

  40. Villarreal L, Tio L, Capdevila M, Atrian S (2006) FEBS J 273:523–535

    Article  PubMed  CAS  Google Scholar 

  41. Cobbett C, Goldsbrough PB (2002) Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

  42. Devez A, Achterberg E, Gledhill M (2009) Met Ions Life Sci 5:441–481

    Article  CAS  Google Scholar 

  43. Freisinger E (2009) Met Ions Life Sci 5:107–154

    Article  CAS  Google Scholar 

  44. Freisinger E (2010) Chimia 64:217–224

    Article  PubMed  CAS  Google Scholar 

  45. Stürzenbaum SR (2009) Met Ions Life Sci 5:183–197

    Article  Google Scholar 

  46. Vergani L (2009) Met Ions Life Sci 5:199–238

    Article  CAS  Google Scholar 

  47. Bofill R, Orihuela R, Romagosa M, Domenech J, Atrian S, Capdevila M (2009) FEBS J 276:7040–7056

    Article  PubMed  CAS  Google Scholar 

  48. Valls M, Bofill R, Gonzalez-Duarte R, Gonzalez-Duarte P, Capdevila M, Atrian S (2001) J Biol Chem 276:32835–32843

    Article  PubMed  CAS  Google Scholar 

  49. Atrian S (2009) Met Ions Life Sci 5:155–182

    Article  CAS  Google Scholar 

  50. Domenech J, Palacios O, Villarreal L, Gonzalez-Duarte P, Capdevila M, Atrian S (2003) FEBS Lett 533:72–78

    Article  PubMed  CAS  Google Scholar 

  51. Hensbergen PJ, Donker MH, van Velzen MJ, Roelofs D, van der Schors RC, Hunziker PE, van Straalen NM (1999) Eur J Biochem 259:197–203

    Article  PubMed  CAS  Google Scholar 

  52. Riek R, Precheur B, Wang YY, Mackay EA, Wider G, Güntert P, Liu AZ, Kägi JHR, Wüthrich K (1999) J Mol Biol 291:417–428

    Article  PubMed  CAS  Google Scholar 

  53. Franchi N, Boldrin F, Ballarin L, Piccinni E (2010) J Exp Zool A 315:90–100

    Google Scholar 

  54. Hidalgo J, Chung R, Penkowa M, Vasak M (2009) Met Ions Life Sci 5:279–318

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Spanish Ministerio de Ciencia e Innovación for its financial support, precisely for the current projects BIO2009-12513-C02-01 to S.A. and BIO2009-12513-C02-02 to M.C.. The authors are members of the Grup de Recerca de la Generalitat de Catalunya reference 2009SGR-1457 and the COST Action (EU) CM0603 on Free Radicals in Chemical Biology.

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Correspondence to Sílvia Atrian.

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This article is part of a JBIC special issue on metallothioneins.

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Capdevila, M., Atrian, S. Metallothionein protein evolution: a miniassay. J Biol Inorg Chem 16, 977–989 (2011). https://doi.org/10.1007/s00775-011-0798-3

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