Multiple Cu-ATPase genes are differentially expressed and transcriptionally regulated by Cu exposure in sea bream, Sparus aurata

Aquatic Toxicology

Volumn 97, Issue 1, 2010, Pages 23-33

  Minghetti, Matteo ^a   Leaver, Michael J ^a   George, Stephen G ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

ATOX1; ATP7A; ATP7B; Copper; Cu ATPases; Fish; Homeostasis

Indexed keywords

CARRIER PROTEIN; COPPER; MENKES PROTEIN; MESSENGER RNA; PROTEIN ATOX1; UNCLASSIFIED DRUG; WILSON DISEASE PROTEIN;

COPPER; GENE EXPRESSION; HOMEOSTASIS; PERCIFORM; POLLUTION EXPOSURE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; DIETARY INTAKE; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; ENZYME ANALYSIS; ENZYME STRUCTURE; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; INTESTINE; LIVER PARENCHYMA; METAL BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA BREAM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES COMPARISON; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; WATER CONTAMINATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; CATION TRANSPORT PROTEINS; COPPER; DIET; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE; HUMANS; METALLOTHIONEIN; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEA BREAM; SEQUENCE HOMOLOGY; WATER POLLUTANTS, CHEMICAL;

ARCHOSARGUS RHOMBOIDALIS; MAMMALIA; SPARUS AURATA; VERTEBRATA;

EID: 77549083085     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.11.017     Document Type: Article

References (74)

1. Achila D., Banci L., Bertini I., Bunce J., Ciofi-Baffoni S., and Huffman D.L. Structure of human Wilson protein domains 5 and 6 and their interplay with domain 4 and the copper chaperone HAH1 in copper uptake. Proceedings of the National Academy of Sciences 103 15 (2006) 5729-5734
2. 1+ transporter of intestinal cells. American Journal of Physiology-Cell Physiology 284 6 (2003) C1525-C1530
3. Arredondo M., Uauy R., and Gonzalez M. Regulation of copper uptake and transport in intestinal cell monolayers by acute and chronic copper exposure. Biochimica et Biophysica Acta-General Subjects 1474 2 (2000) 169-176
4. Banci L., Bertine I., Chasapis C.T., Rosato A., and Tenori L. Interaction of two soluble metal-binding domains of yeast Cc2 with copper (I))-Atx1. Biochemical and Biophysical Research Communications 364 (2007) 645-649
5. Barnes N., Tsivkovskii R., Tsivkovskaia N., and Lutsenko S. The copper-transporting ATPases, Menkes and Wilson disease proteins, have distinct roles in adult and developing cerebellum. Journal of Biological Chemistry 280 10 (2005) 9640-9645
6. Bauerly K.A., Kelleher S.L., and Lonnerdal B. Functional and molecular responses of suckling rat pups and human intestinal Caco-2 cells to copper treatment. The Journal of Nutritional Biochemistry 15 3 (2004) 155-162
7. Braiterman L., Nyasae L., Guo Y., Bustos R., Lutsenko S., and Hubbard A. Apical targeting and Golgi retention signals reside within a 9-amino acid sequence in the copper-ATPase, ATP7B. American Journal of Physiology-Gastrointestinal and Liver Physiology 296 2 (2009) G433-G444
8. Brunet F.G., Crollius H.R., Paris M., Aury J.M., Gibert P., Jaillon O., Laudet V., and Robinson-Rechavi M. Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Molecular Biology and Evolution 23 9 (2006) 1808-1816
9. Burke R., Commons E., and Camakaris J. Expression and localization of the essential copper transporter DmATP7 in Drosophila neuronal and intestinal tissues. The International Journal of Biochemistry & Cell Biology 40 9 (2008) 1850-1860
10. Bury N.R., Grosell M., Grover A.K., and Wood C.M. ATP-dependent silver transport across the basolateral membrane of rainbow trout gills. Toxicology and Applied Pharmacology 159 1 (1999) 1-8
11. Bury N.R., Walker P.A., and Glover C.N. Nutritive metal uptake in teleost fish. Journal of Experimental Biology 206 1 (2003) 11-23
12. Campbell H.A., Handy R.D., and Nimmo M. Copper uptake kinetics across the gills of rainbow trout (Oncorhynchus mykiss) measured using an improved isolated perfused head technique. Aquatic Toxicology 46 (1999) 177-190
13. Cater M.A., Forbes J., La Fontaine S., Cox D., and Mercer J.F.B. Intracellular trafficking of the human Wilson protein: the role of the six N-terminal metal-binding sites. Biochemical Journal 380 3 (2004) 805-813
14. Clearwater S.J., Baskin S.J., Wood C.M., and McDonald D.G. Gastrointestinal uptake and distribution of copper in rainbow trout. Journal of Experimental Biology 203 16 (2000) 2455-2466
15. Craig P.M., Galus M., Wood C.M., and McClelland G.B. Dietary iron alters waterborne copper-induced gene expression in soft water acclimated zebrafish (Danio rerio). American Journal of Physiology-Regulatory Integrative and Comparative Physiology 296 2 (2009) R362-R373
16. Dehal P., and Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology 3 10 (2005) e314
17. DiDonato M., Hsu H.F., Narindrasorasak S., Que L., and Sarkar B. Copper-induced conformational changes in the N-terminal domain of the Wilson disease copper-transporting ATPase. Biochemistry 39 7 (2000) 1890-1896
18. El Meskini R., Culotta V.C., Mains R.E., and Eipper B.A. Supplying copper to the cuproenzyme peptidylglycine alpha-Amidating Monooxygenase. Journal of Biological Chemistry 278 14 (2003) 12278-12284
19. Forbes J.R., and Cox D.W. Functional characterization of Missense mutations in ATP7B: Wilson disease mutation or normal variant?. The American Journal of Human Genetics 63 6 (1998) 1663-1674
20. George S.G., and Viarengo A. A model for heavy metal homeostasis and detoxification. In: Vernberg W., et al. (Ed). Marine Pollution and Physiology: Recent Advances (1985), University of South Carolina Press, Columbia 125-143
21. Grosell M., Hogstrand C., and Wood C.M. Renal Cu and Na excretion and hepatic Cu metabolism in both Cu acclimated and non acclimated rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 40 (1998) 275-291
22. Grosell M., Hogstrand C., and Wood C.M. Cu uptake and turnover in both Cu-acclimated and non-acclimated rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 38 (1997) 257-276
23. Grosell M., Wood C.M., and Walsh P.J. Copper homeostasis and toxicity in the elasmobranch Raja erinacea and the teleost Myoxocephalus octodecemspinosus during exposure to elevated water-borne copper, comparative biochemistry and physiology. Toxicology & Pharmacology: Comparative Biochemistry and Physiology 135 (2003) 179-190
24. Grosell M., and Wood C.M. Copper uptake across rainbow trout gills: mechanisms of apical entry. Journal of Experimental Biology 205 8 (2002) 1179-1188
25. Guo Y., Nyasae L., Braiterman L.T., and Hubbard A.L. NH2-terminal signals in ATP7B Cu-ATPase mediate its Cu-dependent anterograde traffic in polarized hepatic cells. American Journal of Physiology-Gastrointestinal and Liver Physiology 289 5 (2005) G904-G916
26. Halliwell B., and Gutteridge J.M. Free radicals, lipid peroxidation and cell damage. Lancet 2 8411 (1984) 1095
27. Hamza I., Prohaska J., and Gitlin J.D. Essential role for Atox1 in the copper-mediated intracellular trafficking of the Menkes ATPase. Proceedings of the National Academy of Sciences 100 3 (2003) 1215-1220
28. Handy R.D., Eddy F.B., and Baines H. Sodium-dependent copper uptake across epithelia: a review of rationale with experimental evidence from gill and intestine. Biochimica et Biophysica Acta 1566 1-2 (2002) 104-115
29. Handy R.D., Musonda M.M., Phillips C., and Falla S.J. Mechanisms of gastrointestinal copper absorption in the African walking catfish: copper dose-effects and a novel anion-dependent pathway in the intestine. Journal of Experimental Biology 203 15 (2000) 2365-2377
30. Hoyle I., Shaw B.J., and Handy R.D. Dietary copper exposure in the African walking catfish, Clarias gariepinus: transient osmoregulatory disturbances and oxidative stress. Aquatic Toxicology 83 1 (2007) 62-72
31. Hung I.H., Casareno R.L., Labesse G., Mathews F.S., and Gitlin J.D. HAH1 is a copper-binding protein with distinct amino acid residues mediating copper homeostasis and antioxidant defense. Journal of Biological Chemistry 273 3 (1998) 1749-1754
32. Huster D., and Lutsenko S. The distinct roles of the N-terminal copper-binding sites in regulation of catalytic activity of the Wilson's disease protein. Journal of Biological Chemistry 278 34 (2003) 32212-32218
33. Itoh S., Kim H.W., Nakagawa O., Ozumi K., Lessner S.M., Aoki H., Akram K., McKinney R.D., Ushio-Fukai M., and Fukai T. Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation. Journal of Biological Chemistry 283 14 (2008) 9157-9167
34. Kamunde C., Clayton C., and Wood C.M. Waterborne vs. dietary copper uptake in rainbow trout and the effects of previous waterborne copper exposure. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 283 1 (2002) R69-R78
35. Kaplan J.H., and Lutsenko S. Copper transport in mammalian cells: special care for a metal with special needs. Journal of Biological Chemistry (2009) R109
36. Kim B.E., Nevitt T., and Thiele D.J. Mechanisms for copper acquisition, distribution and regulation. Nature Chemical Biology 4 3 (2008) 176-185
37. Kuo Y.M., Gitschier J., and Packman S. Developmental expression of the mouse mottled and toxic milk genes suggests distinct functions for the Menkes and Wilson disease copper transporters. Human Molecular Genetics 6 7 (1997) 1043-1049
38. Lauren D.J., and McDonald D.G. Effects of copper on branchial ionregulationin the rainbow trout, Salmo gairdnei Richardson-modulation by water hardness and pH. Journal of Comparative Physiology 155 (1985) 635-644
39. La Fontaine S., and Mercer J.F.B. Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Archives of Biochemistry and Biophysics 463 2 (2007) 149-167
40. +-ATPase activities in Mozambique tilapia (Oreochromis mossambicus). Aquatic Toxicology 43 1 (1998) 1-11
41. Linder M.C. Biochemistry of Copper New York (1991)
42. Linder M.C., Wooten L., Cerveza P., Cotton S., Shulze R., and Lomeli N. Copper transport. American Journal of Clinical Nutrition 67 Suppl. (5) (1998) 965S-971S
43. Linz R., and Lutsenko S. Copper-transporting ATPases ATP7A and ATP7B: cousins, not twins. Journal of Bioenergetics and Biomembranes 39 5-6 (2007) 403-407
44. Liu N., Lo L.S., Askary S.H., Jones L., Kidane T.Z., Trang T., Nguyen M., Goforth J., Chu Y.H., Vivas E., Tsai M., Westbrook T., and Linder M.C. Transcuprein is a macroglobulin regulated by copper and iron availability. Journal of Nutritional Biochemistry 18 9 (2007) 597-608
45. Lutsenko S., Barnes N.L., Bartee M.Y., and Dmitriev O.Y. Function and regulation of human copper-transporting ATPases. Physiological Reviews 87 3 (2007) 1011-1046
46. Lutsenko S., Gupta A., Burkhead J.L., and Zuzel V. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance. Archives of Biochemistry and Biophysics 476 1 (2008) 22-32
47. Lutsenko S., LeShane E.S., and Shinde U. Biochemical basis of regulation of human copper-transporting ATPases. Archives of Biochemistry and Biophysics 463 2 (2007) 134-148
48. Mendelsohn B.A., Yin C., Johnson S.L., Wilm T.P., Solnica-Krezel L., and Gitlin J.D. Atp7a determines a hierarchy of copper metabolism essential for notochord development. Cell Metabolism 4 2 (2006) 155-162
49. Mercer J.F. The molecular basis of copper-transport diseases. Trends in Molecular Medicine 7 2 (2001) 64-69
50. Mercer J.F.B., Barnes N., Stevenson J., Strausak D., and Llanos R.M. Copper-induced trafficking of the Cu-ATPases: a key mechanism for copper homeostasis. BioMetals 16 1 (2003) 175-184
51. Minghetti M., Leaver M.J., Carpenè E., and George S.G. Copper transporter 1, metallothionein and glutathione reductase genes are differentially expressed in tissues of sea bream (Sparus aurata) after exposure to dietary or waterborne copper. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 147 4 (2008) 450-459
52. Morillo J., Usero J., and Gracia I. Biomonitoring of trace metals in a mine-polluted estuarine system (Spain). Chemosphere 58 10 (2005) 1421-1430
53. Norgate M., Lee E., Southon A., Farlow A., Batterham P., Camakaris J., and Burke R. Essential roles in development and pigmentation for the Drosophila copper transporter DmATP7. Molecular Biology of the Cell 17 1 (2006) 475-484
54. Nyasae L., Bustos R., Braiterman L., Eipper B., and Hubbard A. Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells: copper-dependent redistribution between two intracellular sites. American Journal of Physiology-Gastrointestinal and Liver Physiology 292 4 (2007) G1181-G1194
55. Petris M.J., and Mercer J.F. The Menkes protein (ATP7A; MNK) cycles via the plasma membrane both in basal and elevated extracellular copper using a C-terminal di-leucine endocytic signal. Human Molecular Genetics 8 11 (1999) 2107-2115
56. Petris M.J., Strausak D., and Mercer J.F.B. The Menkes copper transporter is required for the activation of tyrosinase. Human Molecular Genetics 9 19 (2000) 2845-2851
57. Portnoy M.E., Schmidt P.J., Rogers R.S., and Culotta V.C. Metal transporters that contribute copper to metallochaperones in Saccharomyces cerevisiae. Molecular Genetics and Genomics 265 5 (2001) 873-882
58. Predki P.F., and Sarkar B. Effect of replacement of "zinc finger" zinc on estrogen receptor DNA interactions. Journal of Biological Chemistry 267 9 (1992) 5842-5846
59. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4 4 (1987) 406-425
60. Schaefer M., Hopkins R.G., Failla M.L., and Gitlin J.D. Hepatocyte-specific localization and copper-dependent trafficking of the Wilson's disease protein in the liver. American Journal of Physiology-Gastrointestinal and Liver Physiology 276 3 (1999) G639-G646
61. Schofield R.M., Postlethwait J.H., and Lefevre H.W. MeV-ion microprobe analyses of whole Drosophila suggest that zinc and copper accumulation is regulated storage not deposit excretion. Journal of Experimental Biology 200 24 (1997) 3235-3243
62. Shaw B.J., and Handy R.D. Dietary copper exposure and recovery in Nile tilapia, Oreochromis niloticus. Aquatic Toxicology 76 2 (2006) 111-121
63. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software, Version 4.0. Molecular Biology and Evolution 24 8 (2007) 1596-1599
64. Tchaparian E.H., Uriu-Adams J.Y., Keen C.L., Mitchell A.E., and Rucker R.B. Lysyl Oxidase and P-ATPase-7A expression during embryonic development in the rat. Archives of Biochemistry and Biophysics 379 1 (2000) 71-77
65. Tennant J., Stansfield M., Yamaji S., Srai S.K., and Sharp P. Effects of copper on the expression of metal transporters in human intestinal Caco-2 cells. FEBS Letters 527 (2002) 239-244
66. Terada K., Nakako T., Yang X.L., Iida M., Aiba N., Minamiya Y., Nakai M., Sakaki T., Miura N., and Sugiyama T. Restoration of Holoceruloplasmin synthesis in LEC rat after infusion of recombinant adenovirus bearing WND cDNA. Journal of Biological Chemistry 273 3 (1998) 1815-1820
67. Thompson J.D., Plewniak F., Thierry J.C., and Poch O. DbClustal: rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acids Research 28 15 (2000) 2919-2926
68. Turnlund J.R. Human whole-body copper metabolism. American Journal of Clinical Nutrition 67 5 (1998) 960S-9964S
69. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., and Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 7 (2002) presearch0034
70. Voskoboinik I., and Camakaris J. Menkes copper-translocating P-type ATPase (ATP7A): biochemical and cell biology properties, and role in Menkes disease. Journal of Bioenergetics and Biomembranes 34 5 (2002) 363-371
71. Wernimont A.K., Huffman D.L., Lamb A.L., O'Halloran T.V., and Rosenzweig A.C. Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nature Structural & Molecular Biology 7 9 (2000) 766-771
72. Wessling-Resnick M. Iron Imports. III. Transfer of iron from the mucosa into circulation. American Journal of Physiology-Gastrointestinal and Liver Physiology 290 1 (2006) G1-G6
73. Zar J.H. Biostatistical Analysis. 4th edn (1999), Prentice-Hall International, New Jersey p. 663
74. Zimnicka A.M., Maryon E.B., and Kaplan J.H. Human copper transporter hCTR1 mediates basolateral uptake of copper into enterocytes: implications for copper homeostasis. Journal of Biological Chemistry 282 36 (2007) 26471-26480