Aberrant expression of copper associated genes after copper accumulation in COMMD1-deficient dogs

Journal of Trace Elements in Medicine and Biology

Volumn 29, Issue , 2015, Pages 347-353

  Favier, Robert P ^a   Spee, Bart ^a   Fieten, Hille ^a   van den Ingh, Ted S G A M ^b   Schotanus, Baukje A ^a   Brinkhof, Bas ^a   Rothuizen, Jan ^a   Penning, Louis C ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b TCCI Consultancy BV   (Netherlands)

Author keywords

COMMD1 deficient dogs; Copper accumulation; Translational research

Indexed keywords

CATALASE; CERULOPLASMIN; COPPER; COPPER CHAPERONE FOR SUPEROXIDE DISMUTASE; COPPER METABOLISM DOMAIN CONTAINING PROTEIN1; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE ASSEMBLY HOMOLOG; GLUTATHIONE PEROXIDASE 1; MENKES PROTEIN; MESSENGER RNA; METALLOTHIONEIN 1 A; METALLOTHIONEIN I; PENICILLAMINE; PEPTIDES AND PROTEINS; PEROXIREDOXIN 3; UNCLASSIFIED DRUG; WILSON DISEASE PROTEIN; ALANINE AMINOTRANSFERASE; BILE ACID; CATION TRANSPORT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL TISSUE; ARTICLE; ATOX1 GENE; ATP7A GENE; ATP7B GENE; BLOOD ANALYSIS; CATALASE GENE; CCS GENE; CHRONIC HEPATITIS; COPPER INDUCED CHRONIC HEPATITIS; COPPER METABOLISM; COX17 GENE; CP GENE; DESCRIPTIVE RESEARCH; GENE; GENE EXPRESSION; GENE PRODUCT; GENETIC ASSOCIATION; GPX1 GENE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER BIOPSY; MT1A GENE; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; SOD1 GENE; SUDDEN DEATH; TREND STUDY; ANIMAL; BLOOD; DEFICIENCY; DOG; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEPATITIS; MALE; METABOLISM; PATHOLOGY;

ANIMALIA; CANIS FAMILIARIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALANINE TRANSAMINASE; ANIMALS; BILE ACIDS AND SALTS; CATION TRANSPORT PROTEINS; COPPER; DOGS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEPATITIS; MALE;

EID: 84919642153     PISSN: 0946672X     EISSN: 18783252     Source Type: Journal    
DOI: 10.1016/j.jtemb.2014.06.007     Document Type: Article

References (56)

1. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Curr Med Chem 2005, 12:1161-1208.
2. Kim B.E., Nevitt T., Thiele D.J. Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 2008, 4:176-185.
3. Kaplan J.H., Lutsenko S. Copper transport in mammalian cells: special care for a metal with special needs. J Biol Chem 2009, 284:25461-25465.
4. Valko M., Leibfritz D., Moncol J., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007, 39:44-84.
5. Coyle P., Philcox J.C., Carey L.C., Rofe A.M. Metallothionein the multipurpose protein. Cell Mol Life Sci 2002, 59:627-647.
6. Lutsenko S., Petris M.J. Function and regulation of the mammalian copper-transporting atpases: insights from biochemical and cell biological approaches. J Membr Biol 2003, 191:1-12.
7. Vulpe C., Levinson B., Whitney S., Packman S., Gitschier J. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 1993, 3:7-13.
8. Chelly, Tümer Z., Tønnesen T., Petterson A., Ishikawa-Brush Y., Tommerup N., et al. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 1993, 3:14-19.
9. Mercer J.F., Livingston J., Hall B., Paynter J.A., Begy C., Chandrasekharappa S., et al. Isolation of a partial candidate for Menkes disease by positional cloning. Nat Genet 1993, 3:20-25.
10. Schaefer M., Roelofsen H., Wolters H., Hofmann W.J., Mueller M., Kuipers F., et al. Localization of the Wilson's disease protein in human liver. Gastroenterology 1999, 117:1380-1385.
11. Roelofsen H., Wolters H., van Luyn M.J.A., Miura N., Kuipers F., Vonk R.J. Copper- induced apical trafficking of ATP7B in polarized hepatoma cells provided a mechanism for biliary copper excretion. Gastroenterology 2000, 119:782-793.
12. Mercer J.F. The molecular basis of copper-transport diseases. Trends Mol Med 2001, 7:64-69.
13. Van de Sluis B., Rothuizen J., Pearson P.L., van Oost B.A., Wijmenga C. Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum Mol Genet 2002, 11:165-173.
14. Klomp A.E., van de Sluis B., Klomp L.W., Wijmenga C. The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J Hepatol 2003, 39:703-709.
15. Ganesh L., Burstein E., Guha-Niyogi A., Louder M.K., Mascola J.R., Klomp L.W., et al. The gene product Murr1 restricts HIV-1 replication in resting CD4+ lymphocytes. Nature 2003, 426:853-857.
16. Spee B., Arends B., van Wees A.M., Bode P., Penning L.C., Rothuizen J. Functional consequences of RNA interference targeting COMMD1 in a canine hepatic cell line in relation to copper toxicosis. Anim Genet 2007, 38:168-170.
17. Vonk W.I., Bartuzi P., de Bie P., Kloosterhuis N., Wichers C.G., Berger R., et al. Liver-specific Commd1 knockout mice are susceptible to hepatic copper accumulation. PLoS One 2011, 6:e29183.
18. Favier R.P., Spee B., Schotanus B.A., van de Ingh T.S.G.A.M., Fieten H., Brinkhof B., et al. COMMD1-deficient dogs accumulate copper in hepatocytes and provide a good model for chronic hepatitis and fibrosis. PLoS One 2012, 7:e42158.
19. de Bie P., van de Sluis B., Burstein E., van de Berghe P.V., Muller Berger P.R., Gitlin J.D., et al. Distinct Wilson's disease mutations in ATP7B are associated with enhanced binding to COMMD1 and reduced stability of ATP7B. Gastroenterology 2007, 133:1316-1326.
20. La Fontaine S., Theophilos M.B., Firth S.D., Gould R., Parton R.G., Mercer J.F. Effect of the toxic milk mutation (tx) on the function and intracellular localization of Wnd the murine homologue of the Wilson copper ATPase. Hum Mol Genet 2001, 10:361-370.
21. Li Y., Togashi Y., Sato S., Emoto T., Kang J.H., Takeichi N., et al. Spontaneous hepatic copper accumulation in Long-Evans Cinnamon rats with hereditary hepatitis. A model of Wilson's disease. J Clin Invest 1991, 87:1858-1861.
22. Wu J., Forbes J.R., Chen H.S., Cox D.W. The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat Genet 1994, 7:541-547.
23. -/- (Wilson disease gene) knockout mice. Am J Pathol 2006, 168:423-434.
24. Gray L.W., Peng F., Molloy S.A., Pendyala V.S., Muchenditsi A., Muzik O., et al. Urinary copper elevation in a mouse model of Wilson's Disease is a regulated process to specifically decrease the hepatic copper load. PloS One 2012, 7:e38827.
25. Van de Sluis B., Muller P., Duran K., Chen A., Groot A.J., Klomp L.W., et al. Increased activity of hypoxia-inducible factor 1 is associated with early embryonic lethality in Commd1 null mice. Mol Cell Biol 2007, 27:4142-4156.
26. Brewer G.J., Terry C.A., Aisen A.M., Hill G.M. Worsening of neurologic syndrome in patients with Wilson's disease with metal penicillamine therapy. Arch Neurol 1987, 44:490-493.
27. Rolfe D., Twedt D.C. Copper associated hepatopathies in dogs. Vet Clin North Am Small Anim Pract 1995, 25:399-417.
28. Fieten H., Dirksen K., van den Ingh T.S., Winter E.A., Watson A.L., Leegwater P.A., et al. d-penicillamine treatment of copper-associated hepatitis in Labrador retrievers. Vet J 2013, 196:522-527.
29. Favier R.P., Spee B., Penning L.C., Brinkhof B., Rothuizen J. Quantitative PCR method to detect a 13-kb deletion in the MURR1 gene associated with copper toxicosis and HIV-1 replication. Mamm Genome 2005, 16:460-463.
30. Hoffmann G., van den Ingh T.S., Bode P., Rothuizen J. Copper-associated chronic hepatitis in Labrador Retrievers. J Vet Intern Med 2006, 20:856-861.
31. Hoffmann G., IJzer J., Brinkhof B., van den Ingh T.S.G.A.M., Penning L.C., Rothuizen J. Comparison of different methods to obtain and store liver biopsies for molecular and histological research. Comp Hepatol 2009, 8:3.
32. Van den Ingh T.S.G.A.M., Rothuizen J., Cupery R. Chronic active hepatitis with cirrhosis in the Doberman pinscher. Vet Quart 1988, 10:84-89.
33. Teske E., Brinkhuis B.G., Bode P., van den Ingh T.S., Rothuizen J. Cytological detection of copper for the diagnosis of inherited copper toxicosis in Bedlington terriers. Vet Rec 1992, 131:30-32.
34. Van den Ingh T.S.G.A.M., Van Winkle T.J., Cullen J.M., Charles J.A., Desmet V.J. Morphological classification of parenchymal disorders of the canine and feline liver. WSAVA Standards for Clinical and Histological Diagnosis of Canine and Feline Liver Diseases 2006, 85-101. Saunders Elsevier, PPhiladelphia PA, USA. 1st ed. J. Rothuizen, S.E. Bunch, J.A. Charles, M.E. Cullen, V.J. Desmet, V. Szatmári, D.C. Twedt, T.S.G.A.M. van den Ingh, T. Van Winkle, R.J. Washabau (Eds.).
35. Bode P. Automation and quality assurance in the neutron activation facilities in Delft. J Radioanal Nucl Chem 2000, 245:127-132.
36. Schultheiss P.C., Bedwell C.L., Hamar D.W., Fettman M.J. Canine liver iron, copper, and zinc concentrations and association with histologic lesions. J Vet Diagn Invest 2002, 14:396-402.
37. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415.
38. Spee B., Arends B., van den Ingh T.S.G.A.M., Penning L.C., Rothuizen J. Copper metabolism and oxidative stress in chronic inflammatory and cholestatic liver diseases in dogs. J Vet Intern Med 2006, 20:1085-1092.
39. Brinkhof B., Spee B., Rothuizen J., Penning L.C. Development and evaluation of canine reference genes for accurate quantification of gene expression. Anal Biochem 2006, 356:36-43.
40. Van de Sompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 18. RESEARCH0034.
41. R Development Core Team R: A Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0. http://www.R-project.org.
42. Johnson G.F., Morell A.G., Stockert R.J. Sternlieb. Hepatic lysosomol copper protein in dogs with an inherited copper toxicosis. Hepatology 1981, 1:243-248.
43. Sternlieb I. Hepatic lysosomal copper-thionein. Experientia Suppl 1987, 52:647-653.
44. Huster D., Purnat T.D., Burkhead J.L., Ralle M., Fiehn O., Stuckert F., et al. High copper selectively alters lipid metabolism and cell cycle machinery in the mouse model of Wilson disease. J Biol Chem 2007, 282:8343-8355.
45. Spee B., Mandigers P.J., Arends B., Bode P., van den Ingh T.S.G.A.M., Hoffmann G., et al. Differential expression of copper-associated and oxidative stress related proteins in a new variant of copper toxicosis in Doberman pinschers. Comp Hepatol 2005, 4:3.
46. Packman S., Palmiter R.D., Karin M., O'Toole C. Metallothionein messenger RNA regulation in the mottled mouse and Menkes kinky hair syndrome. J Clin Invest 1987, 79:1338-1342.
47. Manzl C., Enrich J., Ebner H., Dallinger R., Krumschnabel G. Copper-induced formation of reactive oxygen species causes cell death and disruption of calcium homeostasis in trout hepatocytes. Toxicology 2004, 196:57-64.
48. Samuele A., Mangiagalli A., Armentero M.T., Fancellu R., Bazzini E., Vairetti M., et al. Oxidative stress and pro-apoptotic conditions in a rodent model of Wilson's disease. Biochim Biophys Acta 1741, 2005:325-330.
49. Yamamoto H., Watanabe T., Mizuno H., Endo K., Fukushige J., Hosokawa T., et al. In vivo evidence for accelerated generation of hydroxyl radicals in liver of long- evens cinnamon (LEC) rats with acute hepatitis. Free Radic BiolMed 2001, 30:547-554.
50. Sokol R.J., Twedt D., McKim J.M., Devereaux M.W., Karrer F.M., Kam I., et al. Oxidant injury to hepatic mitochondria in patients with Wilson's disease and Bedlington terriers with Cu toxicosis. Gastroenterology 1994, 107:1788-1798.
51. Koopman W.J., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecci F., Smeitink J.A., et al. Mammalian mitochondrial complex I: biogenesis, regulation and reactive oxygen species generation. Antioxid Redox Signal 2010, 12:1431-1470.
52. Zischka H., Lichtmannegger J., Schmitt S., Jägemann N., Schulz S., Wartini D., et al. Liver mitochondrial membrane cross linking and destruction in a rat model of Wilson disease. J Clin Invest 2011, 121:1508-1518.
53. Yamamoto H., Hirose K., Hayasaki Y., Masuda M., Kazusaka A., Fujita S. Mechanisms of enhanced lipid peroxidation in the liver of Long-Evans cinnamon (LEC) rats. Arch Toxicol 1999, 73:457-464.
54. Fuentealba I.C., Aburto E.M. Animal models of copper-associated liver disease. Comp Hepatol 2003, 2:5.
55. Coronado V.A., O'Neill B., Nanji M., Cox D.W. Polymorphisms in canine ATP7B: candidate modifier of copper toxicosis in the Bedlington terrier. Vet J 2008, 177:293-296.
56. Fieten H., Hugen S., van den Ingh T.S., Hendriks W.H., Vernooij J.C., Bode P., et al. Urinary excretion of copper, zinc and iron with and without d-penicillamine administration in relation to hepatic copper concentration in dogs. Vet J 2013, 2:468-473.