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Phylogenetic Divergence of Fish and Mammalian Metallothionein: Relationships with Structural Diversification and Organismal Temperature

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Abstract

Metallothioneins (MTs) are nonenzymatic low molecular weight proteins, that play an important role in the homeostasis and detoxification of heavy metals in a large variety of organisms. These proteins are endowed with striking features, including an unusual amino acid composition characterized by the presence of 20 cysteines out of a total of 60 residues and absence of secondary structure elements. It is generally accepted that MTs underwent few modifications during evolution because of these structural and functional constraints. Such a conclusion is founded on the studies carried out mostly on MTs of mammalian origin. For such a reason, we have decided to compare the MTs of homeothermic and poikilothermic organisms, such as mammals and fish, with the specific aim to put in relation phylogenetic divergence and structural/functional adaptation to temperature. We have included in our analysis also Antarctic Notothenioids, a fish group characterized by genetic isolation and cold-adaptation to a particular harsh environment. We have determined the average hydropathic index of ancestral MT sequences and used them to infer the temperatures of the environment housing the hypothetical ancestor organisms. Finally, we have derived phylogenetic relationships of MT molecules from the pairwise comparison of their three-dimensional structures.

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References

  1. GK Andrews LP Fernando KL Moore TP Dalton RJ Sobieski (1996) ArticleTitleAvian metallothioneins: Structure, regulation and evolution. J Nutr 126 1317S–1323S Occurrence Handle1:CAS:528:DyaK28XhvFant7s%3D Occurrence Handle8642478

    CAS  PubMed  Google Scholar 

  2. L Bargelloni R Scudiero E Parisi V Carginale C Capasso T Patarnello (1999) ArticleTitleMetallothioneins in Antarctic fish: Evidence for independent duplication and gene conversion. Mol Biol Evol 16 885–897 Occurrence Handle1:CAS:528:DyaK1MXksFOls78%3D Occurrence Handle10406107

    CAS  PubMed  Google Scholar 

  3. PF Barker J Burrell (1977) ArticleTitleThe opening of the Drake Passage. Mar Geol 25 15–34 Occurrence Handle10.1016/0025-3227(77)90045-7

    Article  Google Scholar 

  4. PA Binz JHR Kagi (1999) Metallothionein: Molecular evolution and classification. CD Klaassen (Eds) . Birkhauser Verlag Basel 7–13

    Google Scholar 

  5. C Capasso O Abugo F Tanfani A Scire V Carginale R Scudiero E Parisi S D’Auria (2002) ArticleTitleStability and conformational dynamics of metallothioneins from the Antarctic fish Notothenia coriiceps and mouse. Proteins 46 259–267 Occurrence Handle10.1002/prot.10050 Occurrence Handle1:CAS:528:DC%2BD38Xht1Krt7g%3D Occurrence Handle11835501

    Article  CAS  PubMed  Google Scholar 

  6. C Capasso V Carginale O Crescenzi D Di Maro E Parisi R Spadaccini PA Temussi (2003) ArticleTitleSolution structure of MT_nc, a novel metallothionein from the Antarctic fish Notothenia coriiceps. Structure 11 435–443 Occurrence Handle10.1016/S0969-2126(03)00044-3 Occurrence Handle1:CAS:528:DC%2BD3sXislelu74%3D Occurrence Handle12679021

    Article  CAS  PubMed  Google Scholar 

  7. S D’Auria V Carginale R Scudiero O Crescenzi D Di Maro PA Temussi et al. (2001) ArticleTitleStructural characterization and thermal stability of Notothenia coriiceps metallothionein. Biochem J 354 291–299 Occurrence Handle10.1042/0264-6021:3540291 Occurrence Handle1:CAS:528:DC%2BD3MXitFWrsL4%3D Occurrence Handle11171106

    Article  CAS  PubMed  Google Scholar 

  8. MS Johnson MJ Sutcliffe TL Blundell (1990) ArticleTitleMolecular anatomy: Phyletic relationships derived from three-dimensional structures of proteins. J Mol Evol 30 43–59 Occurrence Handle2107323

    PubMed  Google Scholar 

  9. JH Kagi Y Kojima MM Kissling K Lerch (1979) ArticleTitleMetallothionein: An exceptional metal thiolate protein. Ciba Found Symp 72 223–237 Occurrence Handle162047

    PubMed  Google Scholar 

  10. JHR Kagi (1993) Evolution, structure and chemical activity of class I metallothioneins: An overview. KT Suzuki N Imura M Kimura (Eds) Metallothionein III, biological roles and medical implications. Birkhauser Verlag Basel 29–55

    Google Scholar 

  11. JHR Kagi A Schaffer (1988) ArticleTitleBiochemistry of metallothionein. Biochemistry 27 8509 Occurrence Handle3064814

    PubMed  Google Scholar 

  12. JHR Kagi BL Vallee (1960) ArticleTitleMetallothionein: A cadmium and zinc containing protein from equine renal cortex. J Biol Chem 235 3460–3465 Occurrence Handle1:CAS:528:DyaF3MXjvVyhug%3D%3D Occurrence Handle13750713

    CAS  PubMed  Google Scholar 

  13. JP Kennett (1977) ArticleTitleCenozoic evolution of Antarctic glaciation, the circum-Antarctic ocean and their impact on global paleogeography. J Geophys Res 82 3843–3876 Occurrence Handle1:CAS:528:DyaE1cXisFKmsg%3D%3D

    CAS  Google Scholar 

  14. P Kille A Hemmings EA Lunney (1994) ArticleTitleMemories of metallothionein. Biochim Biophys Acta 1205 151–161 Occurrence Handle10.1016/0167-4838(94)90228-3 Occurrence Handle1:CAS:528:DyaK2cXksFantr4%3D Occurrence Handle8155693

    Article  CAS  PubMed  Google Scholar 

  15. S Kumar K Tamura M Nei (1994) ArticleTitleMEGA: Molecular evolutionary genetic analysis software for microcomputers. Comput Appl Biosci 10 189–191 Occurrence Handle1:CAS:528:DyaK2cXltVOmsb0%3D Occurrence Handle8019868

    CAS  PubMed  Google Scholar 

  16. J Kyte RF Doolittle (1982) ArticleTitleA simple method for displaying the hydropathic character of a protein. J Mol Biol 157 105–132 Occurrence Handle1:CAS:528:DyaL38Xks1yjtro%3D Occurrence Handle7108955

    CAS  PubMed  Google Scholar 

  17. W Maret (1994) ArticleTitleOxidative metal release from metallothionein via zinc-thiol/disulfide interchange. Proc Natl Acad Sci USA 91 237–241 Occurrence Handle1:CAS:528:DyaK2cXpvFyitg%3D%3D Occurrence Handle8278372

    CAS  PubMed  Google Scholar 

  18. CJ Marshall (1997) ArticleTitleCold-adapted enzymes. Trends Biotechnol 15 359–364 Occurrence Handle10.1016/S0167-7799(97)01086-X Occurrence Handle1:CAS:528:DyaK2sXlslWqsrY%3D Occurrence Handle9293034

    Article  CAS  PubMed  Google Scholar 

  19. G Oz K Zangger IM Armitage (2001) ArticleTitleThree-dimensional structure and dynamics of a brain specific growth inhibitory factor: Metallothionein-3. Biochemistry 40 11433–11441 Occurrence Handle10.1021/bi010827l Occurrence Handle1:STN:280:DC%2BD3Mrht1ymtQ%3D%3D Occurrence Handle11560491

    Article  CAS  PubMed  Google Scholar 

  20. PM Rees MT Gibbs AM Ziegler JE Kutzbach PJ Behling (1999) ArticleTitlePermian climates evaluating model predictions using global paleobotanical data. Geology 27 891–894 Occurrence Handle10.1130/0091-7613(1999)027<0891:PCEMPU>2.3.CO;2

    Article  Google Scholar 

  21. R Riek B Precheur Y Wang EA Mackay G Wider P Guntert et al. (1999) ArticleTitleNMR structure of the sea urchin (Strongylocentrotus purpuratus) metallothionein MTA. J Mol Biol 291 417–428 Occurrence Handle10.1006/jmbi.1999.2967 Occurrence Handle1:CAS:528:DyaK1MXkvFKju7g%3D Occurrence Handle10438629

    Article  CAS  PubMed  Google Scholar 

  22. AH Robbins CD Stout (1991) ArticleTitleX-ray structure of metallothionein. Methods Enzymol 205 485–502 Occurrence Handle1:CAS:528:DyaK38XitV2rtL8%3D Occurrence Handle1779813

    CAS  PubMed  Google Scholar 

  23. R Scudiero C Capasso V Carginale M Riggio A Capasso M Ciaramella et al. (1997a) ArticleTitlePCR amplification and cloning of metallothionein complementary DNAs in temperate and Antarctic sea urchin characterized by a large difference in egg metallothionein content. Cell Mol Life Sci 53 472–477 Occurrence Handle1:CAS:528:DyaK2sXjs12nsbY%3D

    CAS  Google Scholar 

  24. R Scudiero V Carginale M Riggio C Capasso A Capasso P Kille et al. (1997b) ArticleTitleDifference in hepatic metallothionein content in Antarctic red-blooded and haemoglobinless fish: Undetectable metallothionein levels in haemoglobinless fish is accompanied by accumulation of untranslated metallothionein mRNA. Biochem J 322 207–211 Occurrence Handle1:CAS:528:DyaK2sXhslKrurc%3D

    CAS  Google Scholar 

  25. R Scudiero V Carginale C Capasso M Riggio S Filosa E Parisi (2001) ArticleTitleStructural and functional analysis of metal regulatory elements in the promoter region of genes encoding metallothionein isoforms in the Antarctic fish Chionodraco hamatus (icefish). Gene 274 199–208 Occurrence Handle10.1016/S0378-1119(01)00609-6 Occurrence Handle1:CAS:528:DC%2BD3MXms1Grsbg%3D Occurrence Handle11675012

    Article  CAS  PubMed  Google Scholar 

  26. R Scudiero C Verde V Carginale P Kille C Capasso G di Prisco E Parisi (2000) ArticleTitleTissue-specific regulation of metallothionein and metallothionein mRNA accumulation in the Antarctic notothenioid, Nototheinia coriiceps. Polar Biol 23 17–23 Occurrence Handle10.1007/s003000050003

    Article  Google Scholar 

  27. GN Somero (1995) ArticleTitleProteins and temperature. Annu Rev Physiol 57 43–68 Occurrence Handle1:CAS:528:DyaK2MXksVeqsrg%3D Occurrence Handle7778874

    CAS  PubMed  Google Scholar 

  28. MJ Stillman AY Law WH Cai AJ Zelazowski (1987) ArticleTitleInformation on metal binding properties of metallothioneins from optical spectroscopy. Exs 52 203–211 Occurrence Handle1:CAS:528:DyaL1cXovF2iug%3D%3D

    CAS  Google Scholar 

  29. K Strimmer A von Haeseler (1996) ArticleTitleQuartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13 964–969 Occurrence Handle1:CAS:528:DyaK28XltlSmsLk%3D

    CAS  Google Scholar 

  30. N Takezaki A Rzhetsky M Nei (1995) ArticleTitlePhylogenetic test of the molecular clock and linearized tree. Mol Biol Evol 12 823–833 Occurrence Handle1:CAS:528:DyaK2MXns1yqsbg%3D Occurrence Handle7476128

    CAS  PubMed  Google Scholar 

  31. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe Clustal_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25 4876–4882 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    Article  CAS  PubMed  Google Scholar 

  32. K Zangger G Oz JD Otvos IM Armitage (1999) ArticleTitleThree-dimensional solution structure of mouse [Cd7]-metallothionein-1 by homonuclear and heteronuclear NMR spectroscopy. Protein Sci 8 2630–2638 Occurrence Handle1:CAS:528:DC%2BD3cXhtFynug%3D%3D Occurrence Handle10631978

    CAS  PubMed  Google Scholar 

  33. J Zhang M Nei (1997) ArticleTitleAccuracies of ancestral amino acid sequences inferred by the parsimony, likelihood, and distance method. J Mol Evol 44 IssueIDSuppl 1 S139–S146 Occurrence Handle1:CAS:528:DyaK2sXhsFKjsLY%3D Occurrence Handle9071022

    CAS  PubMed  Google Scholar 

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Correspondence to Elio Parisi.

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Capasso, C., Carginale, V., Scudiero, R. et al. Phylogenetic Divergence of Fish and Mammalian Metallothionein: Relationships with Structural Diversification and Organismal Temperature . J Mol Evol 57 (Suppl 1), S250–S257 (2003). https://doi.org/10.1007/s00239-003-0034-z

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  • DOI: https://doi.org/10.1007/s00239-003-0034-z

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