Gains, losses and changes of function after gene duplication: Study of the metallothionein family

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Moleirinho, Ana ^a   Carneiro, João ^a   Matthiesen, Rune ^a   Silva, Raquel M ^a   Amorim, António ^a   Azevedo, Luísa ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

METALLOTHIONEIN;

ARTICLE; CONTROLLED STUDY; GENE; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE LOSS; GENE MUTATION; GENE SEQUENCE; GENETIC GAIN; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; MT1 GENE; MT2 GENE; MT3 GENE; MT4 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PSEUDOGENE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ANIMAL; BAYES THEOREM; CHEMISTRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; HAPLOTYPE; MAMMAL; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOUSE; MULTIGENE FAMILY;

MAMMALIA; PRIMATES;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BAYES THEOREM; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FREQUENCY; HAPLOTYPES; HUMANS; MAMMALS; METALLOTHIONEIN; MICE; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPEN READING FRAMES; PHYLOGENY; POLYMORPHISM, GENETIC; PSEUDOGENES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 79955562969     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018487     Document Type: Article

References (59)

1. Hughes AL, (2002) Adaptive evolution after gene duplication. Trends Genet 18: 433-434.
2. Lynch M, Katju V, (2004) The altered evolutionary trajectories of gene duplicates. Trends Genet 20: 544-549.
3. Lynch M, (2007) The origins of genome architecture Sunderland Sinauer Associates.
4. Ohno S, (1970) Evolution by gene duplication Heidelberg Springer-Verlag.
5. Ohta T, (1990) How gene families evolve. Theor Popul Biol 37: 213-219.
6. Lynch M, Conery JS, (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
7. Ohta T, (1987) Simulating evolution by gene duplication. Genetics 115: 207-213.
8. Prince VE, Pickett FB, (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3: 827-837.
9. Force A, Lynch M, Pickett FB, Amores A, Yan YL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
10. Lynch M, Force A, (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
11. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, et al. (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421: 63-66.
12. Ihmels J, Collins SR, Schuldiner M, Krogan NJ, Weissman JS, (2007) Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss. Mol Syst Biol 3: 86.
13. Maroni G, Wise J, Young JE, Otto E, (1987) Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117: 739-744.
14. Egli D, Domenech J, Selvaraj A, Balamurugan K, Hua H, et al. (2006) The four members of the Drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification. Genes to Cells 11: 647-658.
15. Chung RS, West AK, (2004) A role for extracellular metallothioneins in CNS injury and repair. Neuroscience 123: 595-599.
16. Hozumi I, Inuzuka T, Hiraiwa M, Uchida Y, Anezaki T, et al. (1995) Changes of growth inhibitory factor after stab wounds in rat brain. Brain Res 688: 143-148.
17. Quaife CJ, Findley SD, Erickson JC, Froelick GJ, Kelly EJ, et al. (1994) Induction of a New Metallothionein Isoform (MT-IV) Occurs during Differentiation of Stratified Squamous Epithelia. Biochemistry 33: 7250-7259.
18. Villarreal L, Tío L, Capdevila M, Atrian S, (2006) Comparative metal binding and genomic analysis of the avian (chicken) and mammalian metallothionein. FEBS Journal 273: 523-535.
19. Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, et al. (2009) Ensembl 2009. Nucleic Acids Res 37: D690-697.
20. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
21. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
22. Posada D, (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
23. Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
24. Rambaut A, Drummond AJ, (2007) Tracer v1.4 [http://beast.bio.ed.ac.uk/Tracer].
25. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
26. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, et al. (2007) Database resources of the National Center for Biotechnology Information. Nucl Acids Res 35: D5-12.
27. Kasprzyk A, Keefe D, Smedley D, London D, Spooner W, et al. (2004) EnsMart: a generic system for fast and flexible access to biological data. Genome Res 14: 160-169.
28. Braun W, Vasak M, Robbins AH, Stout CD, Wagner G, et al. (1992) Comparison of the NMR solution structure and the x-ray crystal structure of rat metallothionein-2. Proc Natl Acad Sci U S A 89: 10124-10128.
29. Sali A, Blundell TL, (1993) Comparative Protein Modelling by Satisfaction of Spatial Restraints. Journal of Molecular Biology 234: 779-815.
30. Azevedo L, Carneiro J, van Asch B, Moleirinho A, Pereira F, et al. (2009) Epistatic interactions modulate the evolution of mammalian mitochondrial respiratory complex components. BMC Genomics 10: 266.
31. Laukens D, Waeytens A, De Bleser P, Cuvelier C, De Vos M, (2009) Human metallothionein expression under normal and pathological conditions: mechanisms of gene regulation based on in silico promoter analysis. Crit Rev Eukaryot Gene Expr 19: 301-317.
32. Waalkes MP, Goering PL, (1990) Metallothionein and other cadmium-binding proteins: recent developments. Chem Res in Toxicol 3: 281-288.
33. Boulanger Y, Goodman CM, Forte CP, Fesik SW, Armitage IM, (1983) Model for mammalian metallothionein structure. Proc Natl Acad Sci U S A 80: 1501-1505.
34. Duncan KER, Ngu TT, Chan J, Salgado MT, Merrifield ME, et al. (2006) Peptide Folding, Metal-Binding Mechanisms, and Binding Site Structures in Metallothioneins. Exp Biol Med 231: 1488-1499.
35. Cai B, Zheng Q, Teng X-C, Chen D, Wang Y, et al. (2006) The role of Thr5 in human neuron growth inhibitory factor. J Biol Inorg Chem 11: 476-482.
36. Romero-Isart N, Jensen LT, Zerbe O, Winge DR, Vasak M, (2002) Engineering of Metallothionein-3 Neuroinhibitory Activity into the Inactive Isoform Metallothionein-1. J Biol Chem 277: 37023-37028.
37. Tio L, Villarreal L, Atrian S, Capdevila M, (2004) Functional differentiation in the mammalian metallothionein gene family: metal binding features of mouse MT4 and comparison with its paralog MT1. J Biol Chem 279: 24403-24413.
38. Greer JM, Puetz J, Thomas KR, Capecchi MR, (2000) Maintenance of functional equivalence during paralogous Hox gene evolution. Nature 403: 661-665.
39. Gu Z, Rifkin SA, White KP, Li W-H, (2004) Duplicate genes increase gene expression diversity within and between species. Nat Genet 36: 577-579.
40. Hamilton AT, Huntley S, Tran-Gyamfi M, Baggott DM, Gordon L, et al. (2006) Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes. Genome Res 16: 584-594.
41. Byrne KP, Wolfe KH, (2007) Consistent patterns of rate asymmetry and gene loss indicate widespread neofunctionalization of yeast genes after whole-genome duplication. Genetics 175: 1341-1350.
42. Zou S, Kamei H, Modi Z, Duan C, (2009) Zebrafish IGF genes: gene duplication, conservation and divergence, and novel roles in midline and notochord development. PLoS One 4: e7026.
43. Masters BA, Quaife CJ, Erickson JC, Kelly EJ, Froelick GJ, et al. (1994) Metallothionein III is expressed in neurons that sequester zinc in synaptic vesicles. J Neurosci 14: 5844-5857.
44. Schmidt CJ, Hamer DH, (1986) Cell specificity and an effect of ras on human metallothionein gene expression. Proc Natl Acad Sci U S A 83: 3346-3350.
45. Stennard (1994) Biochim Biophys Acta.
46. Cherian MG, Jayasurya A, Bay BH, (2003) Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat Res 533: 201-209.
47. Haq F, Mahoney M, Koropatnick J, (2003) Signaling events for metallothionein induction. Mutat Res 533: 211-226.
48. Vasak M, Hasler DW, (2000) Metallothioneins: new functional and structural insights. Curr Opin Chem Biol 4: 177-183.
49. Karin M, Eddy RL, Henry WM, Haley LL, Byers MG, et al. (1984) Human metallothionein genes are clustered on chromosome 16. Proc Natl Acad Sci U S A 81: 5494-5498.
50. Rodewald HR, Paul S, Haller C, Bluethmann H, Blum C, (2001) Thymus medulla consisting of epithelial islets each derived from a single progenitor. Nature 414: 763-768.
51. Beach LR, Palmiter RD, (1981) Amplification of the metallothionein-I gene in cadmium-resistant mouse cells. Proc Natl Acad Sci U S A 78: 2110-2114.
52. Hager LJ, Palmiter RD, (1981) Transcriptional regulation of mouse liver metallothionein-I gene by glucocorticoids. Nature 291: 340-342.
53. Hahn Y, Lee B, (2006) Human-specific nonsense mutations identified by genome sequence comparisons. Human Genetics 119: 169-178.
54. Palmiter RD, Findley SD, Whitmore TE, Durnam DM, (1992) MT-III, a brain-specific member of the metallothionein gene family. Proceedings of the National Academy of Sciences of the United States of America 89: 6333-6337.
55. Lahti DW, Hoekman JD, Tokheim AM, Martin BL, Armitage IM, (2005) Identification of mouse brain proteins associated with isoform 3 of metallothionein. Protein Sci 14: 1151-1157.
56. Meloni G, Zovo K, Kazantseva J, Palumaa P, Vasak M, (2006) Organization and assembly of metal-thiolate clusters in epithelium-specific metallothionein-4. J Biol Chem 281: 14588-14595.
57. Cai B, Zheng Q, Huang Z-X, (2005) The properties of the metal-thiolate clusters in recombinant mouse metallothionein-4. Protein J 24: 327-336.
58. Otto E, Young JE, Maroni G, (1986) Structure and expression of a tandem duplication of the Drosophila metallothionein gene. Proc Natl Acad Sci U S A 83: 6025-6029.
59. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.