Wilson Disease: Epigenetic effects of choline supplementation on phenotype and clinical course in a mouse model

References

• Riordan SM, Williams R. The Wilson's disease gene and phenotypic diversity. J Hepatol 2001; 34:165-71; PMID:11211896; http://dx.doi.org/10.1016/S0168-8278(00)00028-3
   PubMed Web of Science ®Google Scholar
• Lutsenko S. Modifying factors and phenotypic diversity in Wilson's disease. Ann N Y Acad Sci 2014; 1315:56-63; PMID:24702697; http://dx.doi.org/10.1111/nyas.12420
   PubMed Web of Science ®Google Scholar
• Medici V, Shibata NM, Kharbanda KK, LaSalle JM, Woods R, Liu S, Engelberg JA, Devaraj S, Torok NJ, Jiang JX, et al. Wilson's disease: changes in methionine metabolism and inflammation affect global DNA methylation in early liver disease. Hepatology 2013; 57:555-65; PMID:22945834; http://dx.doi.org/10.1002/hep.26047
   PubMed Web of Science ®Google Scholar
• Medici V, Shibata NM, Kharbanda KK, Islam MS, Keen CL, Kim K, Tillman B, French SW, Halsted CH, LaSalle JM. Maternal choline modifies fetal liver copper, gene expression, DNA methylation, and neonatal growth in the tx-j mouse model of Wilson disease. Epigenetics 2014; 9:286-96; PMID:24220304; http://dx.doi.org/10.4161/epi.27110
   PubMed Web of Science ®Google Scholar
• Huster D, Kuhne A, Bhattacharjee A, Raines L, Jantsch V, Noe J, Schirrmeister W, Sommerer I, Sabri O, Berr F, et al. Diverse functional properties of Wilson disease ATP7B variants. Gastroenterology 2012; 142:947-56. e5; PMID:22240481; http://dx.doi.org/10.1053/j.gastro.2011.12.048
   PubMed Web of Science ®Google Scholar
• Bethin KE, Petrovic N, Ettinger MJ. Identification of a major hepatic copper binding protein as S-adenosylhomocysteine hydrolase. J Biol Chem 1995; 270:20698-702; PMID:7657650; http://dx.doi.org/10.1074/jbc.270.35.20698
   PubMed Web of Science ®Google Scholar
• Li M, Li Y, Chen J, Wei W, Pan X, Liu J, Liu Q, Leu W, Zhang L, Yang X, et al. Copper ions inhibit S-adenosylhomocysteine hydrolase by causing dissociation of NAD+ cofactor. Biochemistry 2007; 46:11451-8; PMID:17892301; http://dx.doi.org/10.1021/bi700395d
   PubMed Web of Science ®Google Scholar
• Halsted CH, Medici V. Vitamin-dependent methionine metabolism and alcoholic liver disease. Adv Nutr 2011; 2:421-7; PMID:22332083; http://dx.doi.org/10.3945/an.111.000661
   PubMed Web of Science ®Google Scholar
• Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293:1089-93; PMID:11498579; http://dx.doi.org/10.1126/science.1063443
   PubMed Web of Science ®Google Scholar
• Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet 2005; 14(Spec No 1):R47-58; PMID:15809273; http://dx.doi.org/10.1093/hmg/ddi114
   PubMedGoogle Scholar
• Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 2008; 105:17046-9; PMID:18955703; http://dx.doi.org/10.1073/pnas.0806560105
   PubMed Web of Science ®Google Scholar
• Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet (London, England) 1986; 1:1077-81; PMID:2871345; http://dx.doi.org/10.1016/S0140-6736(86)91340-1
   PubMed Web of Science ®Google Scholar
• Huster D, Purnat TD, Burkhead JL, Ralle M, Fiehn O, Stuckert F, Olson NE, Teupser D, Lutsenko S. High copper selectively alters lipid metabolism and cell cycle machinery in the mouse model of Wilson disease. J Biol Chem 2007; 282:8343-55; PMID:17205981; http://dx.doi.org/10.1074/jbc.M607496200
   PubMed Web of Science ®Google Scholar
• Cordero P, Gomez-Uriz AM, Campion J, Milagro FI, Martinez JA. Dietary supplementation with methyl donors reduces fatty liver and modifies the fatty acid synthase DNA methylation profile in rats fed an obesogenic diet. Genes Nutr 2013; 8:105-13; PMID:22648174; http://dx.doi.org/10.1007/s12263-012-0300-z
   PubMed Web of Science ®Google Scholar
• Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 2002; 132:2393S-400S; PMID:12163699
   PubMed Web of Science ®Google Scholar
• Ala A, Schilsky M. Genetic modifiers of liver injury in hereditary liver disease. Semin Liver Dis 2011; 31:208-14; PMID:21538285; http://dx.doi.org/10.1055/s-0031-1276648
   PubMed Web of Science ®Google Scholar
• Steindl P, Ferenci P, Dienes HP, Grimm G, Pabinger I, Madl C, Maier-Dobersberger T, Herneth A, Dragosics B, Meryn S, et al. Wilson's disease in patients presenting with liver disease: a diagnostic challenge. Gastroenterology 1997; 113:212-8; PMID:9207280; http://dx.doi.org/10.1016/S0016-5085(97)70097-0
   PubMed Web of Science ®Google Scholar
• Weiss KH, Gotthardt DN, Klemm D, Merle U, Ferenci-Foerster D, Schaefer M, Ferenci P, Stremmel W. Zinc monotherapy is not as effective as chelating agents in treatment of Wilson disease. Gastroenterology 2011; 140:1189-98. ne1; PMID:21185835; http://dx.doi.org/10.1053/j.gastro.2010.12.034
   PubMed Web of Science ®Google Scholar
• Sternlieb I. Mitochondrial and fatty changes in hepatocytes of patients with Wilson's disease. Gastroenterology 1968; 55:354-67; PMID:5675366
   PubMed Web of Science ®Google Scholar
• Sternlieb I, Quintana N, Volenberg I, Schilsky ML. An array of mitochondrial alterations in the hepatocytes of Long-Evans Cinnamon rats. Hepatology (Baltimore, Md) 1995; 22:1782-7; PMID:7489989; http://dx.doi.org/10.1002/hep.1840220626
   PubMed Web of Science ®Google Scholar
• Schapira AHV. Mitochondrial involvement in Parkinson's disease, Huntington's disease, hereditary spastic paraplegia and Friedreich's ataxia. Biochim Biophys Acta 1999; 1410:159-70; PMID:10076024; http://dx.doi.org/10.1016/S0005-2728(98)00164-9
   PubMed Web of Science ®Google Scholar
• Wang X, Wang W, Li L, Perry G, Lee H-g, Zhu X. Oxidative stress and mitochondrial dysfunction in Alzheimer's disease. Biochim Biophys Acta 2014; 1842:1240-7; PMID:24189435; http://dx.doi.org/10.1016/j.bbadis.2013.10.015
   PubMed Web of Science ®Google Scholar
• Benchoua A, Trioulier Y, Zala D, Gaillard M-C, Lefort N, Dufour N, Saudou F, Elalouf J-M, Hirsch E, Hantraye P, et al. Involvement of mitochondrial complex II defects in neuronal death produced by N-terminus fragment of mutated huntingtin. Mol Biol Cell 2006; 17:1652-63; PMID:16452635; http://dx.doi.org/10.1091/mbc.E05-07-0607
   PubMed Web of Science ®Google Scholar
• Aspuria PJ, Lunt SY, Varemo L, Vergnes L, Gozo M, Beach JA, Salumbides B, Reue K, Wiedemeyer WR, Nielsen J, et al. Succinate dehydrogenase inhibition leads to epithelial-mesenchymal transition and reprogrammed carbon metabolism. Cancer Metab 2014; 2:21; PMID:25671108; http://dx.doi.org/10.1186/2049-3002-2-21
   PubMedGoogle Scholar
• Bourgeron T, Rustin P, Chretien D, Birch-Machin M, Bourgeois M, Viegas-Pequignot E, Munnich A, Rotig A. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat Genet 1995; 11:144-9; PMID:7550341; http://dx.doi.org/10.1038/ng1095-144
   PubMed Web of Science ®Google Scholar
• Hardman B, Michalczyk A, Greenough M, Camakaris J, Mercer J, Ackland L. Distinct Functional Roles for the Menkes and Wilson Copper Translocating P-type ATPases in Human Placental Cells. Cell Physiol Biochem 2007; 20:1073-84; PMID:17975309; http://dx.doi.org/10.1159/000110718
   PubMed Web of Science ®Google Scholar
• Roberts EA, Robinson BH, Yang S. Mitochondrial structure and function in the untreated Jackson toxic milk (tx-j) mouse, a model for Wilson disease. Mol Genet Metab 2008; 93:54-65; PMID:17981064; http://dx.doi.org/10.1016/j.ymgme.2007.08.127
   PubMed Web of Science ®Google Scholar
• Huster D, Purnat TD, Burkhead JL, Ralle M, Fiehn O, Stuckert F, Olson NE, Teupser D, Lutsenko S. High Copper Selectively Alters Lipid Metabolism and Cell Cycle Machinery in the Mouse Model of Wilson Disease. J Biol Chem 2007; 282:8343-55; PMID:17205981; http://dx.doi.org/10.1074/jbc.M607496200
   PubMed Web of Science ®Google Scholar
• Litwin T, Gromadzka G, Czlonkowska A. Gender differences in Wilson's disease. J Neurol Sci 2012; 312:31-5; PMID:21917273; http://dx.doi.org/10.1016/j.jns.2011.08.028
   PubMed Web of Science ®Google Scholar
• Litwin T, Gromadzka G, Członkowska A. Gender differences in Wilson's disease. J Neurol Sci 2012; 312:31-5; PMID:21917273; http://dx.doi.org/10.1016/j.jns.2011.08.028
   PubMed Web of Science ®Google Scholar
• Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 2009; 18:4046-53; PMID:19656776; http://dx.doi.org/10.1093/hmg/ddp353
   PubMed Web of Science ®Google Scholar
• Wang X, Sato R, Brown MS, Hua X, Goldstein JL. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 1994; 77:53-62; PMID:8156598; http://dx.doi.org/10.1016/0092-8674(94)90234-8
   PubMed Web of Science ®Google Scholar
• Wilmarth P, Short K, Fiehn O, Lutsenko S, David L, Burkhead JL. A systems approach implicates nuclear receptor targeting in the Atp7b(−/−) mouse model of Wilson's Disease. Metallomics 2012; 4:660-8; PMID:22565294; http://dx.doi.org/10.1039/c2mt20017a
   PubMed Web of Science ®Google Scholar
• Wooton-Kee CR, Jain AK, Wagner M, Grusak MA, Finegold MJ, Lutsenko S, Moore DD. Elevated copper impairs hepatic nuclear receptor function in Wilson's disease. J Clin Invest 2015; 125:3449-60; PMID:26241054; http://dx.doi.org/10.1172/JCI78991
   PubMed Web of Science ®Google Scholar
• Hamilton JP, Koganti L, Muchenditsi A, Pendyala VS, Huso D, Hankin J, Murphy RC, Huster D, Merle U, Mangels C, et al. Activation of liver X receptor/retinoid X receptor pathway ameliorates liver disease in Atp7B−/− (Wilson disease) mice. Hepatology 2016; 63:1828-41; PMID:26679751; http://dx.doi.org/10.1002/hep.28406
   PubMed Web of Science ®Google Scholar
• Lei KY. Alterations in plasma lipid, lipoprotein and apolipoprotein concentrations in copper-deficient rats. J Nutr 1983; 113:2178-83; PMID:6631537
   PubMed Web of Science ®Google Scholar
• Kaya A, Altıner A, ÖZpınar A. Effect of copper deficiency on blood lipid profile and haematological parameters in broilers. J Vet Med Series A 2006; 53:399-404; PMID:16970628; http://dx.doi.org/10.1111/j.1439-0442.2006.00835.x
   PubMed Web of Science ®Google Scholar
• Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G. Associations of Dietary and Serum Copper with Inflammation, Oxidative Stress, and Metabolic Variables in Adults. J Nutr 2008; 138:305-10; PMID:18203896
   PubMed Web of Science ®Google Scholar
• Relling DP, Esberg LB, Johnson WT, Murphy EJ, Carlson EC, Lukaski HC, Saari JT, Ren J. Dietary Interaction of High Fat and Marginal Copper Deficiency on Cardiac Contractile Function. Obesity 2007; 15:1242-57; PMID:17495201; http://dx.doi.org/10.1038/oby.2007.146
   PubMed Web of Science ®Google Scholar
• Koupparis AJ, Jeremy J, Angelini G, Persad RAJ, Shukla N. Penicillamine administration reverses the inhibitory effect of hyperhomocysteinaemia on endothelium-dependent relaxation in the corpus cavernosum in the rabbit. BJU Int 2006; 98:440-4; PMID:16879692; http://dx.doi.org/10.1111/j.1464-410X.2006.06212.x
   PubMed Web of Science ®Google Scholar
• Jungalwala F, Dawson R. The origin of mitochondrial phosphatidylcholine within the liver cell. Eur J Biochem 1970; 12:399-402; PMID:5459578; http://dx.doi.org/10.1111/j.1432-1033.1970.tb00865.x
   PubMedGoogle Scholar
• Sachan DS, Hongu N, Johnsen M. Decreasing Oxidative Stress with Choline and Carnitine in Women. J Am Coll Nutr 2005; 24:172-6; PMID:15930482; http://dx.doi.org/10.1080/07315724.2005.10719462
   PubMed Web of Science ®Google Scholar
• Castegna A, Iacobazzi V, Infantino V. The mitochondrial side of epigenetics. Physiol Genomics 2015; 47:299-307; PMID:26038395; http://dx.doi.org/10.1152/physiolgenomics.00096.2014
   PubMed Web of Science ®Google Scholar
• Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621-8; PMID:18516045; http://dx.doi.org/10.1038/nmeth.1226
   PubMed Web of Science ®Google Scholar
• Wickramasinghe S, Rincon G, Islas-Trejo A, Medrano JF. Transcriptional profiling of bovine milk using RNA sequencing. BMC Genomics 2012; 13:1471-2164; http://dx.doi.org/10.1186/1471-2164-13-45
   Web of Science ®Google Scholar
• Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 2005; 33:W741-W8; PMID:15980575; http://dx.doi.org/10.1093/nar/gki475
   PubMed Web of Science ®Google Scholar
• Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 2013; 41:W77-83; PMID:23703215; http://dx.doi.org/10.1093/nar/gkt439
   PubMed Web of Science ®Google Scholar
• Cope-Yokoyama S, Finegold MJ, Sturniolo GC, Kim K, Mescoli C, Rugge M, Medici V. Wilson disease: Histopathological correlations with treatment on follow-up liver biopsies. World J Gastroenterol 2010; 16:1487-94; PMID:20333789; http://dx.doi.org/10.3748/wjg.v16.i12.1487
   PubMed Web of Science ®Google Scholar
• Clegg MS, Keen CL, Lönnerdal B, Hurley LS. Influence of ashing techniques on the analysis of trace elements in animal tissue. Biol Trace Elem Res 1981; 3:107-15; PMID:24271640; http://dx.doi.org/10.1007/BF02990451
   PubMed Web of Science ®Google Scholar
• Giulidori P, Stramentinoli G. A radioenzymatic method for S-adenosyl-l-methionine determination in biological fluids. Anal Biochem 1984; 137:217-20; PMID:6731799; http://dx.doi.org/10.1016/0003-2697(84)90373-7
   PubMed Web of Science ®Google Scholar
• Aguer C, Fiehn O, Seifert EL, Bézaire V, Meissen JK, Daniels A, Scott K, Renaud J-M, Padilla M, Bickel DR, et al. Muscle uncoupling protein 3 overexpression mimics endurance training and reduces circulating biomarkers of incomplete β-oxidation. FASEB J 2013; 27:4213-25; PMID:23825224; http://dx.doi.org/10.1096/fj.13-234302
   PubMed Web of Science ®Google Scholar
• Woods R, Vallero RO, Golub MS, Suarez JK, Ta TA, Yasui DH, Chi LH, Kostyniak PJ, Pessah IN, Berman RF, et al. Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Hum Mol Genet 2012; 21:2399-411; PMID:22343140; http://dx.doi.org/10.1093/hmg/dds046
   PubMed Web of Science ®Google Scholar