Structural and bioinformatic analysis of the Roman snail Cd-Metallothionein gene uncovers molecular adaptation towards plasticity in coping with multifarious environmental stress

Molecular Ecology

Volumn 18, Issue 11, 2009, Pages 2426-2443

  Egg, Margit ^a   HÖckner, Martina ^a   BrandstÄtter, Anita ^b   Schuler, Dietmar ^a   Dallinger, Reinhard ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Environmental stress response; Helicid gastropod; Helix pomatia; Metal tolerance; Metallothionein induction; Molecular adaptation

Indexed keywords

CADMIUM; CADMIUM BINDING PROTEIN; CADMIUM-BINDING PROTEIN; METALLOTHIONEIN; TRANSCRIPTION FACTOR;

ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BINDING SITE; BIOLOGY; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; POLLUTANT; PROMOTER REGION; SNAIL;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CADMIUM; COMPUTATIONAL BIOLOGY; ENVIRONMENTAL POLLUTANTS; METALLOTHIONEIN; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RESPONSE ELEMENTS; SEQUENCE ANALYSIS, DNA; SNAILS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

GASTROPODA; HELICIDAE; HELIX POMATIA;

EID: 65949117238     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04191.x     Document Type: Article

References (90)

1. Abu-Bakar A, Lamsa V, Arpiainen S, Moore MR, Lang MA, Hakkola J (2007) Regulation of Cytochrome P450 2A5 gene by the transcription factor NRF2 (Nuclear Factor (Erythroid-Derived 2) -Like 2. Drug Metabolism and Disposition, 35, 787 794.
2. Andrews GK (2000) Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochemical Pharmacology, 59, 95 104.
3. Bai G, Stuebing EW, Parker HR, Harlow P, Nemer M (1993) Combinatorial regulation by promoter and intron 1 regions of the Metallothionein SpMTA gene in the sea urchin embryo. Molecular and Cellular Biology, 13, 993 1001.
4. Baird SK, Kurz T, Brunk UT (2006) Metallothionein protects against oxidative stress-induced lysosomal destabilization. Biochemical Journal, 394, 275 283.
5. Beattie JH, Owen HL, Wallace SM et al 2005) Metallothionein overexpression and resistance to toxic stress. Toxicology Letters, 157, 69 78.
6. Benham CJ (1981) A theoretical analysis of competing conformational transitions in torsionally stressed DNA. Journal of Molecular Biology, 150, 43 68.
7. Benham CJ (1992) The energetics of the strand separation transition in superhelical DNA. Journal of Molecular Biology, 225, 835 847.
8. Berger B, Hunziker PE, Hauer CR, Birchler N, Dallinger R (1995) Mass spectrometry and amino acid sequence of two cadmium-binding metallothionein isoforms from the terrestrial gastropod Arianta arbustorum. Biochemical Journal, 311, 951 957.
9. Bernot RJ (2003) Trematode infection alters the antipredator behaviour of a pulmonate snail. Journal of the North American Benthological Society, 22, 241 248.
10. Bi C, Benham CJ (2004) WebSIDD: server for predicting stress-induced duplex destabilized (SIDD) sites in superhelical DNA. Bioinformatics, 20, 1477 1479.
11. Binz PA, Kägi JHR (1999) Metallothionein: molecular evolution and classification. In : Metallothionein IV (ed. Klaassen C), pp. 7 13. Birkhäuser Verlag, Basel, Switzerland.
12. Bird CP, Stranger BE, Dermitzakis ET (2006) Functional variation and evolution of non-coding DNA. Current Opinion in Genetics and Development, 16, 559 564.
13. Bode J, Winkelmann S, Götze S et al 2006) Correlations between scaffold/matrix attachment region (S/MAR) binding activity and DANN Duplex Destabilization Energy. Journal of Molecular Biology, 358, 597 613.
14. Britten RJ (1996) DNA sequence insertion and evolutionary variation in gene regulation. Proceedings of the National Academy of Sciences, USA, 93, 9374 9377.
15. Chabicovsky M, Niederstätter H, Thaler R et al 2003) Localization and quantification of Cd- and Cu-specific Metallothionein isoform mRNA in cells and organs of the terrestrial gastropod Helix pomatia. Toxicology and Applied Pharmacology, 190, 25 36.
16. Chabicovsky M, Klepal W, Dallinger R (2004) Mechanisms of cadmium toxicity in terrestrial pulmonates: programmed cell death and metallothionein overload. Environmental Toxicology and Chemistry, 23, 648 655.
17. Dallinger R, Berger B, Hunziker PE, Kägi JHR (1997) Metallothionein in snail Cd and Cu metabolism. Nature (London), 388, 237 238.
18. Dallinger R, Berger B, Gruber C, Hunziker PE, Stürzenbaum S (2000) Metallothioneins in terrestrial invertebrates: structural aspects, biological significance, and implications for their use as biomarkers. Cellular and Molecular Biology (Noisy-le-Grand), 46, 331 346.
19. Dallinger R, Berger B, Triebskorn R, Köhler HR (2001) Soil biology and ecotoxicology. In : Biology of Terrestrial Molluscs (ed. Baker G), pp. 489 525. CAB International, Wallingford, England.
20. Dallinger R, Chabicovsky M, Berger B (2004a) Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia L. I. Molecular, biochemical and methodical background. Environmental Toxicology and Chemistry, 23, 890 901.
21. Dallinger R, Chabicovsky M, Lagg B, Schipflinger R, Weirich HG, Berger B (2004b) Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia L. II. A differential biomarker approach under laboratory and field conditions. Environmental Toxicology and Chemistry, 23, 902 910.
22. Dallinger R, Lagg B, Egg M, Schipflinger R, Chabicovsky M (2004c) Cd accumulation and Cd-Metallothionein as a biomarker in Cepaea hortensis (Helicidae, Pulmonata) from laboratory exposure and metal-polluted habitats. Ecotoxicology, 13, 757 772.
23. David E, Tanguy A, Pichavant K, Moraga D (2005) Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS Journal, 272, 5635 56652.
24. Davis SR, Cousins RJ (2000) Metallothionein expression in animals: a physiological perspective on function. Journal of Nutrition, 130, 1085 1088.
25. De Zoysa M, Kang HS, Song YB, Jee Y, Lee YD, Lee J (2007) First report of invertebrate Mx: cloning, characterization and expression analysis of Mx cDNA in disk abalone (Haliotis discus discus). Fish and Shellfish Immunology, 23, 86 96.
26. Egli D, Yepiskoposyan H, Selvaraj A et al 2006) A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Molecular and Cellular Biology, 26, 2286 2296.
27. English TE, Storey KB (2003) Freezing and anoxia stresses induce expression of metallothionein in the foot muscle and hepatopancreas of the marine gastropod Littorina littorea. Journal of Experimental Biology, 206, 2517 2524.
28. Escriva H, Safi R, Hänni C et al 1997) Ligand binding was acquired during evolution of nuclear receptors. Proc. Natl. Acad. Sci. USA, 94, 6803 6808.
29. Fedorova L, Fedorov A (2003) Introns in gene evolution. Genetica, 118, 123 131.
30. Filmus J, Remani J, Klein MH (1992) Synergistic induction of promoters containing metal- and glucocorticoid-responsive elements. Nucleic Acids Research, 20, 2755 2760.
31. Fritsche TR (1986) Studies on the coccidian parasites (Apicomplexa: Eimeriidae and Pfeifferinellidae) of pulmonate gastropods. Journal of Eukaryotic Microbiology, 34, 75 78.
32. Georgel P, Kappler C, Langley E et al 1995) Drosophila immunity. A sequence homologous to mammalian interferon consensus response element enhances the activity of the diptericin promoter. Nucleic Acids Research, 23, 1140 1145.
33. Ghoshal K, Wang Y, Sheridan JF, Jacob ST (1998) Metallothionein induction in response to restraint stress - transcriptional control, adaptation to stress, and role of glucocorticoid. Journal of Biological Chemistry, 273, 27904 27910.
34. Girod PA, Nguyen DQ, Calabrese D et al 2007) Genome-wide prediction of matrix attachment regions that increase gene expression in mammalian cells. Nature Medicine, 4, 747 753.
35. Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annual Review of Physiology, 58, 539 563.
36. Hispard F, Schuler D, de Vaufleury A, Scheifler R, Badot PM, Dallinger R (2008) Metal distribution and metallothionein induction after cadmium exposure in the terrestrial snail Helix aspersa (Gastropoda, Pulmonata). Environmental Toxicology and Chemistry, 27, 1533 1542.
37. Iglesias J, Santos M, Castillejo J (1996) Annual activity cycles of the land snail Helix aspersa Müller in natural populations in North-Western Spain. Journal of Molluscan Studies, 62, 495 505.
38. Janssens TKS, Mariën J, Cenijn P, Legler J, van Straalen NM, Roelofs D (2007) Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta. BMC Evolutionary Biology, 2007, 88.
39. Janssens TK, del Rio Lopéz R, Mariën J et al 2008) Comparative population analysis of metallothionein promoter alleles suggests stress-induced microevolution in the field. Environmental Science and Technology, 42, 3873 3878.
40. Kägi JHR (1993) Evolution, structure and chemical activity of class I metallothioneins: an overview. In : Metallothionein III (eds Suzuki KT, Imura N, Kimura M), pp. 29 55. Birkhäuser Verlag, Basel, Switzerland.
41. Karin M, Haslinger A, Holtgreve H et al 1984) Characterization of DNA sequences through which cadmium and glucocorticoid hormones induce the human metallothionein-IIA gene. Nature, 308, 513 519.
42. Karin M, Haslinger A, Heguy A, Dietlin T, Cooke T (1987) Metal-responsive elements act as positive modulators of human metallothionein-IIA enhancer activity. Molecular and Cellular Biology, 7, 606 613.
43. Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annual Reviews of Pharmacology and Toxicology, 39, 267 294.
44. Kyo S, Takakura M, Taira T, Itoh H, Yutsudo M, Ariga H, Inoue M (2000) Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Research, 28, 669 677.
45. Larkin MA, Blackshields G, Brown NP et al 2007) ClustalW and Clustal-X, version 2.0. Bioinformatics, 23, 2947 2948.
46. LaRochelle O, Labbé S, Harrisson JF et al 2008) Nuclear factor-1 and metal transcription factor-1 synergistically activate the mouse metallothionein-1 gene in response to metal ions. Journal of Biological Chemistry, 283, 8190 8201.
47. Liebich I, Bode J, Reuter I, Wingender E (2002) Evaluation of sequence motifs found in scaffold/matrix-attachment regions (S/MARs). Nucleic Acids Research, 30, 3433 3442.
48. Lin CH, Chung MY, Chen WB, Chien CH (2007) Growth inhibitory effect of the human NIT2 gene and its allelic imbalance in cancers. FEBS Journal, 274, 2946 2956.
49. 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.
50. Moilanen LH, Fukushige T, Freedman JH (1999) Regulation of metallothionein gene transcription - identification of upstream regulatory elements and transcription factors responsible for cell-specific expression of the metallothionein genes from Caenorhabditis elegans. Journal of Biological Chemistry, 274, 29655 26665.
51. Montazer-Torbati MB, Hue-Beauvais C, Droineau S et al 2008) Epigenetic modifications and chromatin loop organization explain the different expression profiles of the Tbrg4, WAP and Ramp3 genes. Experimental Cell Research, 314, 975 987.
52. Morgan AJ, Kille P, Stürzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environmental Science and Technology, 41, 1085 1096.
53. Murphy BJ, Kimura T, Sato BG, Shi Y, Andrews GK (2008) Metallothionein induction by hypoxia involves cooperative interactions between metal-responsive transcription factor-1 and hypoxia-inducible transcription factor-1α. Molecular Cancer Research, 6, 483 490.
54. Nemer M, Bai G, Stuebing EW (1993) Highly identical cassettes of gene regulatory elements, genomically repetitive and present in RNA. Proceedings of the National Academy of Sciences, USA, 90, 10851 10855.
55. Nevitt T, Pereira J, Azevedo D, Guerreiro P, Rodrigues-Pousada C (2004) Expression of YAP4 in Saccharomyces cerevisiae under osmotic stress. Biochemical Journal, 379, 367 374.
56. Nguyen T, Sherratt PJ, Pickett CB (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annual Reviews of Pharmacology and Toxicology, 43, 233 260.
57. Nittler MP, Hocking-Murray D, Foo CK, Sil A (2005) Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Molecular Biology of the Cell, 16, 4792 4813.
58. Oh S, Park S, Han KH (2003) Transcriptional regulation of secondary growth in Arabidopsis thaliana. Journal of Experimental Botany, 54 (393 2709 2722.
59. Pakay JL, Withers PC, Hobbs AA, Guppy M (2002) In vivo downregulation of protein synthesis in the snail Helix aspersa during estivation. American Journal of Physiology Regulatory, Integrative and Comparative Physiology, 283, R197 R204.
60. Palenik B, Ren Q, Dupont CL et al 2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proceedings of the National Academy of Sciences, USA, 103, 13555 13559.
61. Palenik B, Grimwood J, Aerts A et al 2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proceedings of the National Academy of Sciences, USA, 104, 7705 7710.
62. Pichtel J, Kuroiwa K, Sawyerr HT (2000) Distribution of Pb, Cd and Ba in soils and plants of two contaminated sites. Evironmental Pollution, 110, 171 178.
63. Platts AE, Quayle AK, Krawetz SA (2006) In-silico prediction and observations of nuclear matrix attachment. Cellular and Molecular Biology Letters, 11, 191 213.
64. Prick T (2007) Osmosensitivität der Autophagie in der Hefe Saccharomyces cerevisiae - parallelen und Unterschiede zur Säugerleber. PhD Dissertation, Mathematisch-Naturwissenschaftliche Fakultät, University of Düsseldorf, Düsseldorf Germany. (URL. http://docserv.uni-duesseldorf. de/servlets/DocumentServlet?id=3603).
65. +-ATPase activity during estivation in the land snail Otala lactea L. Journal of Experimental Biology, 209, 677 688.
66. Remondelli P, Leone A (1997) Interactions of the zinc-regulated factor (ZiRF1) with the mouse metallothionein Ia promoter. Biochemical Journal, 323, 79 85.
67. Řezáč P, Palkovič L, Holasová E, Bušta J (1994) Modes of entry of the first-stage larvae of Elaphostrongylus cervi (Nematoda: Protostrongylidae) into pulmonate snails Arianta arbustorum and Helix pomatia. Folia Parasitologica, 41, 209 214.
68. Roelofs D, Aarts MGM, Schat H, van Straalen NM (2008) Functional ecological genomics to demonstrate general and specific responses to abiotic stress. Functional Ecology, 22, 8 18.
69. Samson SLA, Gedamu L (1995) Metal-responsive elements of the rainbow trout metallothionein-b gene function for basal and metal-induced activity. Journal of Biological Chemistry, 270, 6884 6871.
70. Satish Kumar K, Dayananda S, Subramanyam C (2005) Copper alone, but not oxidative stress, induces copper-metallothionein gene in Neurospora crassa. FEMS Microbiology Letters, 242, 45 50.
71. Schmitt-Wrede HP, Koewius H, Tschuschke S, Greven H, Wunderlich F (2004) Genomic organization of the cadmium-inducible tandem repeat 25-kDa metallothionein of the oligochaete worm Enchytraeus buchholzi. Biochimica et Biophysica Acta-Gene Structure and Expression, 1680, 24 33.
72. Schug J (2003) Using TESS to predict transcription factor binding sites in DNA sequence. Curr. Protoc. Bioinform., 21, 2.6.1 2.6.15.
73. Schug J, Overton GC (1997) TESS: Transcription Element Search Software on the www. Technical Report. Computational Biology and Informatics Laboratory School of Medicine, University of Pennsylvania, Philadelphia, PA.
74. Schüpbach HU, Baur B (2008) Parasitic mites influence fitness components of their host, the land snail Arianta arbustroum. Invertebrate Biology, 127, 350 356.
75. Singh GB (2000) Discovering matrix attachment regions (MARs) in genomic databases. SIGKDD Explorations, 1, 39 45.
76. Singh GB, Kramer JA, Krawetz SA (1997) Mathematical model to predict regions of chromatin attachment to the nuclear matrix. Nucleic Acids Research, 25, 1419 1425.
77. Sogawa N, Sogawa CA, Fukuoka H et al 2003) The changes of hepatic metallothionein synthesis and the hepatic damage induced by starvation in mice. Methods and Findings in Experimental and Clinical Pharmacology, 25, 601 606.
78. Sugiura T, Kuroda E, Yamashita U (2004) Dysfunction of macrophages in metallothionein-knock out mice. Journal of UOEH, 26, 193 205.
79. Tamai KT, Liu X, Silar P, Sosinowski T, Thiele DJ (1994) Heat shock transcription factor activates yeast metallothionein gene expression in response to heat and glucose starvation via distinct signalling pathways. Molecular and Cellular Biology, 14, 8155 8165.
80. Tanaka N, Kawakami T, Taniguchi T (1993) Recognition DNA sequences of interferon regulatory factor 1 (IRF-1) and IRF-2, regulators of cell growth and the interferon system. Molecular and Cellular Biology, 13, 4531 4538.
81. Tetko IV, Haberer G, Rudd S, Meyers B, Mewes HW, Mayer KFX (2006) Spatiotemporal expression control correlates with intragenic. scaffold matrix attachment regions (S/MARs) in Arabidopsis thaliana. PLoS Computational Biology, 2, 0136 0145. Available from URL: (http://www.ploscompbiol.org)
82. Thornton JW (2003) Topic 1.14. Nonmammalian nuclear receptors: evolution and endocrine disruption. Pure and Applied Chemistry, 75, 1827 1839.
83. Timmermans MJTN, Ellers J, Van Straalen NM (2007) Allelic diversity of metallothionein in Orchesella cincta (L.): traces of natural selection by environmental pollution. Heredity, 98, 311 319.
84. Treger JM, Magee TR, McEntee K (1998) Functional analysis of the stress response element and its role in the multistress response of Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications, 243, 13 19.
85. Wang H, Benham CJ (2008) Superhelical destabilization in regulatory regions of stress response genes. PLoS Computational Biology, 4, 0062 0076. Available from URL: (http://www.ploscompbiol.org)
86. Westin G, Schaffner W (1988) A zinc-responsive factor interacts with a metal-regulated enhancer element (MRE) of the mouse metallothionein-I gene. EMBO Journal, 7, 3763 3770.
87. Wittkopp PJ (2006) Evolution of cis-regulatory sequence and function in Diptera. Heredity, 97, 139 147.
88. Xian X (1989) Effect of chemical forms of cadmium, zinc, and lead in polluted soils on their uptake by cabbage plants. Plant and Soil, 113, 257 264.
89. Yan CHM, Chan KM (2004) Cloning of zebrafish metallothionein gene and characterization of its gene promoter region in HepG2 cell line. Biochimica et Biophysica Acta-Gene Structure and Expression, 1679, 47 58.
90. Yukilevich R, Lachance J, Aoki F, True JR (2008) Long-term adaptation of epistatic genetic networks. Evolution, 62, 2215 2235.