Tetrahymena metallothioneins fall into two discrete subfamilies

PLoS ONE

Volumn 2, Issue 3, 2007, Pages

  Diaz, Silvia ^a   Amaro, Francisco ^a   Rico, Daniel ^a   Campos, Virginia ^a   Benitez, Laura ^a   Martín González, Ana ^a   Hamilton, Eileen P ^b   Orias, Eduardo ^b   Gutiérrez, Juan C ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; COPPER; CYSTEINE; METALLOTHIONEIN; METALLOTHIONEIN 5; METALLOTHIONEIN I; METALLOTHIONEIN III; UNCLASSIFIED DRUG; MESSENGER RNA; PROTOZOAL PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; DNA BINDING MOTIF; DNA FLANKING REGION; DNA SEQUENCE; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CONSERVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PH; PHYLOGENY; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; START CODON; TEMPERATURE STRESS; TETRAHYMENA THERMOPHILA; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG EFFECT; GENETICS; MOLECULAR GENETICS; SEQUENCE HOMOLOGY; TETRAHYMENA;

CILIOPHORA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

3' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CADMIUM; COPPER; METALLOTHIONEIN; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 35548946697     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000291     Document Type: Article

References (83)

1. Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multipurpose protein. Cell Mol Life Sci 59: 627-647.
2. Robinson NJ, Whitehall SK, Cavet JS (2001) Microbial metallothioneins. In: Poole RK, ed. Advances in Microbial Physiology. New York: Academic. pp. 183-213.
3. Cousins RJ (1985) Absorption, transport and hepatic metabolism of copper and Zn: special reference to metallothionein and caeruloplasmin. Physiol Rev 65: 238-309.
4. Liu J, Klaassen CD (1996) Absorption and distribution of cadmium in metallothionein-I transgenic mice. Fundam Appl Toxicol 29: 294-300.
5. Viarengo A, Burlando B, Ceratto N, Panfoli I (2000) Antioxidant role of metallothioneins: a comparative overview. Cell. Mol Biol 46: 407-417.
6. Klaassen CD, Liu J (1998) Induction of metallothionein as an adaptive mechanism affecting the magnitude and progression of toxicological injury. Environ Health Perspect 106: 297-300.
7. Penkowa M, Carrasco J, Giralt M, Molinero A, Hernandez J, et al. (2000) Altered central nervous system cytokine-growth factor expression profiles and angiogenesis in metallothionein-I+II deficient mice. J Cereb Blood Flow Metab 20: 1174-1189.
8. Vidal F, Hidalgo J (1993) Effect of zinc and copper on preimplantation mouse embryo development in vitro and metallothionein levels. Zygote 1: 225-229.
9. Masters BA, Kelly EJ, Quaife CJ, Brinster RL, Palmiter RD (1994) Targeted distruption of metallothionein I and II genes increases sensitivity to cadmium. Proc. Natl. Acad. Sci. USA 91: 548-588.
10. Egli D, Yepiskoposyan H, Selvaraj A, Balamurugan K, Rajaram R, et al. (2006) A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol. Cell. Biol. 26: 2286-2296.
11. Hughes S, Sturzenbaum SR (2007) Single and double metallothionein knockout in the nematode C. elegans reveals cadmium dependent and independent toxic effects on life history traits. Environ. Pollution 145: 395-400.
12. Nilsson JR (1989) Tetrahymena in cytotoxicology: with special reference to effects of heavy metals and selected drugs. Eur J Protistol 25: 2-25.
13. Gutiérrez JC, Martín-González A, Díaz S, Ortega R (2003) Ciliates as a potential source of cellular and molecular biomarkers/ biosensors for heavy metal pollution. Eur J Protistol 39: 461-467.
14. Martín-González A, Díaz S, Jareño C, Gutiérrez JC (1999) The use of protists in ecotoxicology: applications and perspectives. In: Pandalai SG, ed. Recent Research Developments in Microbiology. India: Research Signpost: 93-111.
15. Martín-González A, Borniquel S, Díaz S, Gallego A, Gutiérrez JC (2006) Cytotoxicity and Bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Research Microbiol 157: 108-118.
16. Turkewitz AP, Orias E, Kapler G (2002) Functional genomics: the coming of age for Tetrahymena thermophila. Trends Genet 18: 35-40.
17. Piccinni E, Staudenmann W, Albergoni V, De Gabrieli R, James P (1994) Purification and primary structure of metallothioneins induced by cadmium in the protists Tetrahymena pigmenlosa and Tetrahymena pyriformis. Europ J Biochem 226: 853-859.
18. Piccinni E, Bertaggia D, Santovito G, Miceli C, Kraen A (1999) Cadmium metallothionein gene of Tetrahymena pyriformis. Gene 234: 51-59.
19. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, et al. (2002) A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci USA 97: 3734-3739.
20. Boldrin F, Santovito G, Gaertig J, Wloga D, Cassidy-Hanley D, et al. (2006) Metallothionein gene from Tetrahymena thermophila with a copper-inducible-repressible promoter. Eukaryot Cell 5: 422-425.
21. Fu C, Miao W (2006) Cloning and Characterization of a New Multi-Stress Inducible Metallothionein Gene in Tetrahymena pyriformis. Protist 157: 193-203.
22. Boldrin F, Santovito G, Irato P, Piccinni E (2002) Metal interaction and regulation of Tetrahymena pigmenlosa metallothionein genes. Protist 153: 283-291.
23. Dondero F, Cavaletto M, Ghezzi AR, La Terza A, Banni M, et al. (2004) Biochemical characterization and quantitative gene expression analysis of the multi-stress inducible metallothionein from Tetrahymena thermophila. Protist 155: 157-168.
24. Santovito G, Irato P, Piccinni E (2000) Regulation of metallothionein in Tetrahymena: induction of MT-mRNA and protein by cadmium exposure. Europ J Protistol 36: 417-422.
25. Wong L, Klionsky L, Wickert S, Merrian V, Orias E, et al. (2000) Autonomously replicating macronuclear DNA pieces are the physical basis of coassortment groups in Tetrahymena thermophila. Genetics 155: 1119-1125.
26. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, et al. (2006) Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model Eukaryote. PLoS Biol 4: e286.
27. Wuitschick JD, Karrer KM (1999) Analysis of genomic G+C content, codon usage, initiator codon context and translation termination sites in Tetrahymena thermophila. J Eukaryot Microbiol 46: 239-247.
28. Kojima Y, Berger C, Vallee BL, Kagi JH (1976) Amino-acid sequence of equine renal metallothionein-1B. Proc Natl Acad Sci U S A 73: 3413-7.
29. Pan KP, Hou F, Cody CW, Huang PC (1994) Substitution of glutamic acids for the conserved lysies in the α domain affects metal binding in both α and β domains of mammalian metallothionein. Biochem Biophys Res Commun 202: 621-628.
30. Cody CW, Huang PC (1994) Replacement of all α-domain lysines with glutamate reduces metallothionein detoxification function. Biochem Biophys Res Commun 202: 954-959.
31. Emoto T, Kurasaki M, Oikawa S, Suzuki-Kurasaki M, Okabe M, et al. (1996) Roles of the Conserved Serines of Metallothionein in Cadmium Binding. Biochem Genetics 34: 239-251.
32. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
33. Binz P-A, Kägi JHR (1999) Metallothionein: Molecular evolution and classification. In: Klaassen C, ed. Metallothionein IV. Basel: Birkhäuser Verlag. pp. 7-13.
34. Tanguy A, Moraga D (2001) Cloning and characterization of a gene coding for a novel metallothionein in the Pacific oyster Crassostrea gigas (CgMT2): a case of adaptive response to metal-induced stress. Gene 273: 123-130.
35. Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Ann Rev Pharmacol Toxicol 39: 267-294.
36. Henkel G, Krebs B (2004) Metallothioneins: Zinc, Cadmium, Mercury, and Copper Thiolates and Selenolates Mimicking Protein Active Site Features - Structural Aspects and Biological Implications. Chem Rev 104: 801-824.
37. Kagi JHR (1991) Overview of Metallothionein. Methods in Enzymology 205: 613-626.
38. Olafson RW, McCubbin WD, Kay CM (1988) Primary- and secondary-structural analysis of a unique prokaryotic metallothionein from a Synechococcus sp. cyanobacterium. Biochem J 251: 691-699.
39. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxifications and homeostasis. Annu Rev Plant Biol 53: 159-182.
40. Valls M, Bofill R, Gonzalez-Duarte R, Gonzalez-Duarte P, Capdevila M, et al. (2001) A new insight into metallothionein (MT) classification and evolution. The in vivo and in vitro metal binding features of Homarus americanus recombinant MT. J Biol Chem 276: 32835-32843.
41. Tio L, Villarreal L, Atrian S, Capdevila M (2004) Functional differentiation in the mammalian Metallothionein gene family. J Biol Chem 279: 24403-24413.
42. Villarreal L, Tio L, Capdevila M, Atrian S (2006) Comparative metal binding and genomic analysis of the avian (chicken) and mammalian metallothionein. FEBS J 273: 523-535.
43. 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.
44. Dondero F, Piacentinia L, Bannia M, Rebeloa M, Burlandoa B, et al. (2005) Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345: 259-270.
45. Santovito G, Irato P, Palermo S, Boldrin F, Sack R, et al. (2001) Identification, cloning and characterization of a novel copper-metallothionein in Tetrahymena pigmenlosa. Sequencing of cDNA and expression. Protist 152: 219-29.
46. Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-90.
47. Ohno S (1970) Evolution by gene duplication. New York: Springer-Verlag.
48. Taylor JS, Raes J (2004) Duplication and Divergence: The Evolution of New Genes and Old Ideas. Annu Rev Genet 38: 615-643.
49. Kondrashov FA, Kondrashov AS (2006) Role of selection in fixation of gene duplications. J Theoretical Biology 239: 141-151.
50. Li W-H, Yang J, Gu X (2005) Expression divergence between duplicated genes. TIG 21: 602-607.
51. Haq F, Mahoney M, Koropatnick J (2003) Signalling events for metallothionein induction. Mutation Res 533: 211-226.
52. Bustin SA (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25: 169-193.
53. Ikebuchi H, Teshima R, Suzuki T, Terao T, Yamane Y (1986) Simultaneous induction of Pb-metallothionein-like protein and Zn-thionein in the liver of rats given lead acetate. Biochem J 233: 541-546.
54. Church HJ, Day JP, Braithwaite RA, Brown SS (1993) Binding of lead to a metallothionein-like protein in human erythrocytes. J Inorg Biochem 49: 55-68.
55. Cheung A, Pok L, Vincent KLL, King MC (2005) Tilapia metallothionein genes: PCR-cloning and gene expression studies. Biochim Biophys Acta 1731: 191-201.
56. Waalkes MP, Harvey MJ, Klaassen CD (1984) Relative in vitro affinity of hepatic metallothionein for metals. Toxicol Lett 20: 33-39.
57. Erk M, Raspor B (2001) Interference of Pb leaching from the pH electrode on Cd-metallothionein complex. Analytic Chim Acta 442: 165-170.
58. Kovalchuk I, Titov V, Hohn B, Kovalchuck O (2005) Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutation Res 570: 149-161.
59. Park JD, Liu Y, Klaassen CD (2001) Protective effect of metallothionein against the toxicity of cadmium and other metals. Toxicology 163: 93-100.
60. Gaertig J, Gao Y, Tishgarten T, Clark TG, Dickerson HW (1999) Surface display of a parasite antigen in the ciliate Tetrahymena thermophila. Nat Biotechnol 17: 462-465.
61. Peterson DS, Gao Y, Asokan K, Gaertig J (2002) The circumsporozoite protein of Plasmodium falciparum is expressed and localized to the cell surface in the free-living ciliate Tetrahymena thermophila. Mol Biochem Parasitol 122: 119-26.
62. Zhang B, Egli D, Georgiev O, Schaffner W (2001) The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Mol Cell Biol 21: 4505-4514.
63. Furst P, Hu S, Hackett R, Hamer D (1988) Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell 55: 705-717.
64. Smith JJ, Cole ES, Romero DP (2004) Transcriptional control of RAD51 expression in the ciliate Tetrahymena thermophila. Nucl Acids Res 32: 4313-4321.
65. Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4E: 131-136.
66. Wu A, Wemmie JA, Edgington NP, Goebl M, Guevara JL, et al. (1993) Yeast bZip proteins mediate pleiotropic drug and metal resistance. J Biol Chem 268: 18850-18858.
67. Miceli C, La Terza A, Bradshaw RA, Luporini P (1992) Identification and structural characterization of a cDNA clone encoding a membrane-bound form of the polypeptide pheromone Er-1 in the ciliate protozoan Euplotes raikovi. Proc Natl Acad Sci USA 89: 1988-1992.
68. Luporini P, Alimenti C, Ortenzi C, Vallesi A (2005) Ciliate Mating Types and Their Specific Protein Pheromones. Acta Protozool 44: 89-101.
69. Nury D, Chabanon H, Levadoux-Martin M, Hesketh J (2005) An eleven nucleotide section of the 3′-untranslated region is required for perinuclear localization of rat metallothionein-1 mRNA. Biochem J 387: 419-428.
70. Jansen RP (2001) mRNA localization: message on the move. Nature Reviews 2: 247-256.
71. Chabanon H, Mickleburgh I, Hesketh J (2004) Zipcodes and postage stamps: mRNA localization signals and their trans-acting binding proteins. Briefings in Functional Genomics and Proteomics 3: 240-256.
72. Kaney AR, Speare VJ (1983) An amicronucleate mutant of Tetrahymena thermophila. Exp Cell Res 143: 461-467.
73. Hamilton EP, Orias E (2000) Genetically mapping new mutants and cloned genes. Methods Cell Biol 62: 265-280.
74. Hamilton EP, Orias E (2000) Genetic crosses: setting up crosses, testing progeny, and isolating phenotypic assortants. Methods Cell Biol 62: 219-228.
75. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
76. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
77. Neuwald AF, Liu JS, Lawrence CE (1995) Gibbs motif sampling. Prot Science 4: 1618-1632.
78. Notredame C, Higgins D, Heringa J (2000) T-Coffee: A novel method for multiple sequence alignments. J Mol Biol 302: 205-217.
79. Schneider TD, Stephens RM (1990) Sequence logos: A new way to display consensus sequences. Nucleic Acids Res 18: 6097-6100.
80. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
81. Shannon CE (1948) A mathematical theory of communication. Bell Systems Tech J 27: 379-423 and 623-656.
82. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
83. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa NJ: Humana Press. pp. 365-386. Source code available at http://fokker.wi.mit.edu/ primer3/.