Copper in Helix pomatia (Gastropoda) is regulated by one single cell type: Differently responsive metal pools in rhogocytes

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 289, Issue 4 58-4, 2005, Pages

  Dallinger, Reinhard ^a   Chabicovsky, Monika ^b   Hödl, Elisabeth ^a   Prem, Caroline ^a   Hunziker, Peter ^c   Manzl, Claudia ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b Igeneon AG   (Austria)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Copper metallothionein; In situ hybridization; Pore cell; Subcellular compartmentalization

Indexed keywords

COPPER; ISOPROTEIN; MESSENGER RNA; METAL; METALLOTHIONEIN; TRACE ELEMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL TYPE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EXPOSURE; GASTROPOD; HELIX POMATIA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMEOSTASIS; IN SITU HYBRIDIZATION; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SNAIL; SURVIVAL;

ANIMALS; CELLS, CULTURED; COPPER; HELIX (SNAILS); METALS; ORGAN SPECIFICITY; TISSUE DISTRIBUTION;

EID: 25844448059     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00052.2005     Document Type: Article

References (64)

1. Albrecht U, Keller H, Gebauer W, and Markl J. Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata. Cell Tissue Res 304: 455-462, 2001.
2. Berger B and Dallinger R. Terrestrial snails as quantitative indicators of environmental metal pollution. Environ Monit Assess 25: 65-84, 1993.
3. Berger B, Dallinger R, Gehrig P, and Hunziker PE. Primary structure of a copper-binding metallothionein isoform from mantle tissue of the terrestrial gastropod Helix pomatia L. Biochem J 328: 219-224, 1997.
4. Blasco J, Arias AM, and Saenz V. Heavy metal concentrations in Squilla mantis (L.) (Crustacea, Stomatopoda) from the gulf of Cadiz - evaluation of the impact of the Aznalcollar mining spill. Environ Int 28: 111-116, 2002.
5. Boldrin F, Santovito G, Irato P, and Piccinni E. Metal interaction and regulation of Tetrahymenapigmentosa metallothionein genes. Protist 153: 283-291, 2002.
6. Bruissant O and Wahli W. A simplified in situ hybridisation protocol using non-radioactive labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1: 10-16, 1998.
7. Bremner I. Metallothionein and copper metabolism in liver. Methods Enzymol 205: 584-591, 1991.
8. Brouwer M, Syring R, and Brouwer TH. Role of a copper-specific metallothionein of the blue crab, Callinectes sapidus, in copper metabolism associated with degradation and synthesis of hemocyanin. J Inorg Biochem 88: 228-239, 2002.
9. Brown AC. Elimination of foreign particles by the snail, Helix aspersa. Nature 18: 1154-1155, 1967.
10. Bury NR, Walker PA, and Glover CN. Nutritive metal uptake in teleost fish. J Exp Biol 206: 11-23, 2003.
11. Chabicovsky M, Niederstaetter H, Thaler R, Hödl E, Parson W, Rossmanith W, and Dallinger R. Localisation and quantification of Cd- and Cu-specific metallothionein isoform mRNA in cells and organs of the terrestrial gastropod Helix pomatia. Toxicol Appl Pharmacol 190: 25-36, 2003.
12. Dallinger R and Wieser W. Patterns of accumulation, distribution and liberation of Zn, Cu, Cd and Pb in different organs of the land snail Helix pomatia L. Comp Biochem Physiol C 79: 117-124, 1984.
13. Dallinger R. Metallothionein research in terrestrial invertebrates: synopsis and perspectives. Comp Biochem Physiol C 113: 125-133, 1996.
14. Dallinger R, Berger B, Hunziker P, Birchler N, Hauer C, and Kägi JHR. Purification and primary structure of snail metallothionein: similarity of the N-terminal sequence with histones H4 and H2A. Eur J Biochem 216: 739-746, 1993.
15. Dallinger R, Berger B, Hunziker PE, and Kägi JHR. Metallothionein in snail Cd and Cu metabolism. Nature 388: 237-238, 1997.
16. Dallinger R, Berger B, Gruber C, and Stürzenbaum S. Metallothioneins in terrestrial invertebrates: structural aspects, biological significance, and implications for their use as biomarkers. Cell Mol Biol (Noisy-legrand) 46: 331-346, 2000.
17. Dallinger R, Wang Y, Berger B, Mackay E, and Kägi JHR. Spectroscopic characterization of metallothionein from the terrestrial snail, Helix pomatia. Eur J Biochem 268: 4126-4133, 2001.
18. Dallinger R, Chabicovsky M, and Berger B. Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia L. I. Molecular, biochemical and methodical background. Environ Toxicol Chem 23: 890-901, 2004.
19. Dallinger R, Chabicovsky M, Lagg B, Schipflinger R, Weirich HG, and Berger B. Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia L. II. A differential biomarker approach under laboratory and field conditions. Environ Toxicol Chem 23: 902-910, 2004.
20. Dallinger R, Lagg B, Egg M, Schipflinger R, and Chabicovsky M. Cd accumulation and Cd-Metallothionein as a biomarker in Cepaea hortensis (Helicidae, Pulmonata) from laboratory exposure and metal-polluted habitats. Ecotoxicology 13: 757-772, 2004.
21. De Boeck G, Ngo TTH, Van Campenhout K, and Blust R. Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquat Toxicol 65: 413-424, 2003.
22. Dietrich HF and Fontane AR. A decalcification method for ultrastructure of echinoderm tissues. Stain Technol 50: 351-353, 1975.
23. Engel DW, Brouwer M, and Mercaldo-Allen R. Effects of molting and environmental factors on trace metal body-burdens and hemocyanin concentrations in the American lobster, Homarus americanus. Mar Environ Res 52: 257-269, 2001.
24. Geffard A, Geffard O, His E, and Amiard JC. Relationships between metal bioaccumulation and metallothionein levels in larvae of Mytilus galloprovincialis exposed to contaminated estuarine sediment elutriate. Mar Ecol Prog Ser 233: 131-142, 2002.
25. Gehrig P, You C, Dallinger R, Gruber C, Brouwer M, Kägi JHR, and Hunziker PE. Electrospray ionization mass spectrometry of. zinc, cadmium and copper metallothioneins: evidence for metal binding cooperativity. Protein Sci 9: 395-402, 2000.
26. Godan D. Schadschnecken und ihre Bekämpfung. Stuttgart, Germany. Eugen Ulmer, 1979, p. 467.
27. Gomot A and Pihan F. Comparison of the bioaccumulation capacities of copper and zinc in two snail subspecies (Helix). Ecotoxicol Environ Saf 38: 85-94, 1997.
28. Grosell M, Wood CM, and Walsh PJ. Copper homeostasis and toxicity in the elasmobranch Raja erinacea and the teleost Myoxocephalus octodecemspinosus during exposure to elevated water-borne copper. Camp Biochem Physiol C Toxicol Pharmacol 135: 179-190, 2003.
29. Haszprunar G. The molluscan rhogocyte (pore-cell, Blasenzelle, cellule nucale), and its significance for ideas on nephridial evolution. J Molluscan Stud 62: 185-211, 1996.
30. Howell JS. Histochemical demonstration of copper in copper-fed rats and in hepatolenticular degeneration. J Pathol Bacteriol 11: 473-483, 1959.
31. Kägi JHR and Schäffer A. Biochemistry of metallothionein. Biochemistry 27: 8509-8515, 1988.
32. Klein D, Bartsch R, and Summer KH. Quantification of Cu-containing metallothionein by a Cd-saturation method. Anal Biochem 189: 35-39, 1990.
33. Konings WN, van Driel R, van Bruggen EF, and Gruber M. Structure and properties of hemocyanins. V. Binding of oxygen and copper in Helix pomatia hemocyanin. Biochim Biophys Acta 194: 55-66, 1969.
34. Lemoine S, Bigot Y, Sellos D, Cosson RP, and Laulier M. Metallothionein isoforms in Mytilus edulis (Mollusca, Bivalvia): complementary DNA characterization and quantification of expression in different organs after exposure to cadmium, zinc, and copper. Mar Biotechnol 2: 195-203, 2000.
35. Lerch K. Copper metallothionein, a copper-binding protein from Neurospora crassa. Nature 284: 368-370, 1980.
36. Luchtel DL and Deyrup-Olsen I. Body wall: form and function. In: The Biology of Terrestrial Molluscs, edited by Barker GM. Wallingford, UK: CAB International, 2001, p. 147-178.
37. Marigomez I, Soto M, Cajaraville MP, Angulo E, and Giamberini L. Cellular and subcellular distribution of metals in molluscs. Microsc Res Tech 56: 358-392, 2002.
38. Marjorette M, Peña O, Koch KA, and Thiele DJ. Dynamic regulation of copper uptake arid detoxification genes in Saccharomyces cerevisiae. Mol Cell Biol 18: 2514-2523, 1998.
39. Martell AE and Smith RM. Critical Stability Constants. New York: Plenum, 1989, vol. 1-6, p. 349.
40. Mason AZ and Borja MR. A study of Cu turnover in proteins of the visceral complex of Littorina littorea by stable isotopic analysis using coupled HPLC-ICP-MS. Mar Environ Res 54: 351-355, 2002.
41. Martoja M, Tue VT, and Elkaim B. Bioaccumulation de cuivre chez Littorina littorea (L.) (Gasteropode Prosobranch): signification physi-ologique et ecologique. J Exp Mar Biol Ecol 43: 251-270, 1980.
42. Mercer JFB, Names N, Stevenson J, Strausak D, and Llanos RM. Copper-induced trafficking of the Cu-ATPase: a key mechanism for copper homeostasis. Biometals 16: 175-184, 2003.
43. Norum U, Bondgaard M, and Bjerregaard P. Copper and zinc handling during moult cycle of male and female shore crabs Carcinus maenas. Mar Biol 142: 757-769, 2003.
44. Okamoto K and Utamura M. Biologische Untersuchungen des Kupfers. I. Über die histochemische Kupfernachweismethode. Acata Scholae Med Univ Imp In Kioto 20: 573-580, 1937-1938.
45. Okuyama M, Kobayashi Y, Inouhe M, Tohoyama H, and Joho M. Effect of some heavy metal ions on copper-induced metallothionein synthesis in the yeast Saccharomyces cerevisiae. Biometals 12: 307-314, 1999.
46. Pase L, Voskoboinik I, Greenough M, and Camarkaris J. Copper stimulates trafficking of a distinct pool of the Menkes copper ATPase (ATP7A) to the plasma membrane and diverts it into a rapid recycling pool. Biochem J 378: 1031-1037, 2003.
47. Rabitsch W. Metal accumulation in terrestrial pulmonates at a lead/zinc smelter site with a long history of pollution in Arnoldstein, Austria. Bull Environ Contain Toxicol 56: 734-741, 1996.
48. Reynolds E. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17: 208-212, 1963.
49. Riggio M, Lee J, Scudiero R, Parisi E, Thiele DJ, and Filosa S. High affinity copper transport protein in the lizard Podarcis sicula: molecular cloning, functional characterization and expression in somatic tissues, follicular oocytes and eggs. Biochim Biophys Acta 1576: 127-135, 2002.
50. Romeis BR. Mikroskopische Technik. Munich, Germany: Oldenburch, 1968, p. 316-317.
51. Santovito G, Irato P, Palermo S, Boldrin F, Hunziker P, and Piccinni E. Identification, cloning and characterisation of a novel copper-metallothionein in Tetrahymena pigmentosa, sequencing of cDNA and expression. Protist 152: 219-229, 2001.
52. Schumann K, Classen HG, Dieter HH, Konig J, Multhaup G, Rukgauer M, Summer KH, Bernhardt J, and Biesalski HK. Hohenheim consensus workshop: copper. Eur J Clin Nutr 56: 469-483, 2002.
53. Simkiss K, and Mason AZ. Metal ions: metabolic and toxic effects. In: The Mollusca. Environmental Biochemistry and Physiology, edited by Hochachka PW. New York: Academic, 1983, vol. 2, p. 102-164.
54. Sminia T and Boer HH. Hemocyanin production in pore cells of the freshwater snail Lymnaea stagnalis. Z Zellforsch Mikrosk Anat 145: 443-445, 1973.
55. Sminia T and Vlugt van Daalen JE. Haemocyanin synthesis in pore cells of the terrestrial snail Helix aspersa. Cell Tissue Res 183: 299-301, 1977.
56. Sone T, Yamaoka K, Minami Y, and Tsunoo H. Induction of metallothionein synthesis in Menkes' and normal lymphoblastoid cells is controlled by the level of intracellular copper. J Biol Chem 262: 5878-5885, 1987.
57. Swaileh K, Hussein R, and Halaweh N. Metal accumulation from contaminated food and its effect on growth of juvenile land snails Helix engaddensis. J Environ Sci Health B 37: 151-159, 2002.
58. Syring RA, Brouwer TH, and Brouwer M. Cloning and sequencing of cDNAs encoding for a novel copper-specific metallothionein and two cadmium-inducible metallothioneins from the blue crab Callinectes sapidus. Comp Biochem Physiol C 125: 325-332, 2001.
59. Tapia L, Gonzalez-Aguero M, Cisternas MF, Suazo M, Cambiazo V, Uauy R, and Gonzalez M. Metallothionein is key for safe intracellular copper storage and cell survival at normal and supra-physiological exposure levels. Biochem J 378: 617-624, 2003.
60. Tapiero H, Townsend DM, and Tew KD. Trace elements in human physiology and pathology. Copper. Biomed Pharmacother 57: 386-398, 2003.
61. Thiele DJ. Integrating trace element metabolism from the cell to the whole organism. J Nutr 133, Suppl 1: 1579S-1580S, 2003.
62. Triebskorn R and Köhler HR. The impact of heavy metals on the grey garden slug, Deroceras reticulatutn (Müller): metal storage, cellular effects and semi-quantitative evaluation of metal toxicity. Environ Pollut 93: 327-343, 1996.
63. Wieser W. Über die Häutung von Procellio scaber Latr. Verh Dtsch Zool Ges Kiel: 178-195, 1965.
64. Wieser W and Klima J. Compartmentalization of copper in the hepatopancreas of isopods. Mikroskopie 24: 1-9, 1969.