Toxic milk mice models of Wilson's disease.
Animal models
Hepatolenticular degeneration
Toxic milk mouse
WD
Wilson’s disease
Journal
Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
received:
23
10
2020
accepted:
28
01
2021
pubmed:
17
2
2021
medline:
8
6
2021
entrez:
16
2
2021
Statut:
ppublish
Résumé
Wilson's disease (WD) is a rare genetic disorder inherited as an autosomal recessive trait. The signs and symptoms of this disease are related to dysfunctional ATP7B protein which leads to copper accumulation and cellular damage. The organs that are most commonly affected by WD are the liver and brain. The dysfunctional ATP7B homolog has previously been identified in many different species, including two naturally occurring murine models called toxic milk mice. The aim of this paper was to compare the toxic milk mouse described by Rauch (tx) to that from Jackson Laboratory (txJ) through a review of studies on these two groups of mice. The two mice strains differ in the type of carried mutation and the phenotype of the disease. The data of the studies showed that the tx mice developed mild chronic hepatitis but suffered severe organ destruction with faster progression to full-liver cirrhosis. No changes were noted in the neurological and behavioral status of this strain despite the described toxic accumulation of copper and neuronal destruction in their brain. On the other hand, though the Jackson toxic milk mice (txJ) also presented chronic hepatitis, the condition was a bit milder with slower progression to end-stage disease. Moreover, hepatocyte suitable to perform neurobehavioral research as their phenotype characterized by tremors and locomotor disabilities better corresponds with the cliniconeurological picture of the humans.
Identifiants
pubmed: 33590415
doi: 10.1007/s11033-021-06192-5
pii: 10.1007/s11033-021-06192-5
pmc: PMC7925478
doi:
Substances chimiques
Copper
789U1901C5
Atp7b protein, mouse
EC 7.2.2.8
Copper-Transporting ATPases
EC 7.2.2.8
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1903-1914Références
Kinnier Wilson SA (1912) Progressive lenticular degeneration: a familial nervous disease associated with cirrhosis of the liver. Brain 34:295–209
doi: 10.1093/brain/34.4.295
Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY (2007) Function and regulation of human copper-transporting ATPases. Physiol Rev 87(3):1011–1046. https://doi.org/10.1152/physrev.00004.2006
doi: 10.1152/physrev.00004.2006
pubmed: 17615395
Terada K, Schilsky ML, Miura N, Sugiyama T (1998) ATP7B (WND) protein. Int J Biochem Cell Biol 30(10):1063–1067. https://doi.org/10.1016/s1357-2725(98)00073-9
doi: 10.1016/s1357-2725(98)00073-9
pubmed: 9785470
Lee J, Pena MM, Nose Y, Thiele DJ (2002) Biochemical characterization of the human copper transporter Ctr1. J Biol Chem 277(6):4380–4387. https://doi.org/10.1074/jbc.M104728200
doi: 10.1074/jbc.M104728200
pubmed: 11734551
Robinson NJ, Winge DR (2010) Copper metallochaperones. Annu Rev Biochem 79:537–562. https://doi.org/10.1146/annurev-biochem-030409-143539
doi: 10.1146/annurev-biochem-030409-143539
pubmed: 20205585
pmcid: 3986808
Sternlieb I (1968) Mitochondrial and fatty changes in hepatocytes of patients with Wilson’s disease. Gastroenterology 55(3):354–367
doi: 10.1016/S0016-5085(19)34045-4
Sternlieb I, Feldmann G (1976) Effects of anticopper therapy on hepatocellular mitochondria in patients with Wilson’s disease: an ultrastructural and stereological study. Gastroenterology 71(3):457–461
doi: 10.1016/S0016-5085(76)80455-6
Kalita J, Kumar V, Misra UK, Ranjan A, Khan H, Konwar R (2014) A study of oxidative stress, cytokines and glutamate in Wilson disease and their asymptomatic siblings. J Neuroimmunol 274(1–2):141–148. https://doi.org/10.1016/j.jneuroim.2014.06.013
doi: 10.1016/j.jneuroim.2014.06.013
pubmed: 25002079
Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A, Koka S, Eisele K, Klarl BA, Rubben H, Schmid KW, Mann K, Hildenbrand S, Hefter H, Huber SM, Wieder T, Erhardt A, Haussinger D, Gulbins E, Lang F (2007) Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 13(2):164–170. https://doi.org/10.1038/nm1539
doi: 10.1038/nm1539
pubmed: 17259995
Sternlieb I, Scheinberg IH (1968) Prevention of Wilson’s disease in asymptomatic patients. N Engl J Med 278(7):352–359. https://doi.org/10.1056/nejm196802152780702
doi: 10.1056/nejm196802152780702
pubmed: 5635646
Cocos R, Sendroiu A, Schipor S, Bohiltea LC, Sendroiu I, Raicu F (2014) Genotype-phenotype correlations in a mountain population community with high prevalence of Wilson’s disease: genetic and clinical homogeneity. PLoS ONE 9(6):e98520. https://doi.org/10.1371/journal.pone.0098520
doi: 10.1371/journal.pone.0098520
pubmed: 24897373
pmcid: 4045667
Gao J, Brackley S, Mann JP (2019) The global prevalence of Wilson disease from next-generation sequencing data. Genet Med 21(5):1155–1163. https://doi.org/10.1038/s41436-018-0309-9
doi: 10.1038/s41436-018-0309-9
pubmed: 30254379
Petrukhin K, Fischer SG, Pirastu M, Tanzi RE, Chernov I, Devoto M, Brzustowicz LM, Cayanis E, Vitale E, Russo JJ, Matseoane D, Boukhgalter B, Wasco W, Figus AL, Loudianos J, Cao A, Sternlieb I, Evgrafov O, Parano E, Pavone L, Warburton D, Ott J, Penchaszadeh GK, Scheinberg IH, Gilliam TC (1993) Mapping, cloning and genetic characterization of the region containing the Wilson disease gene. Nat Genet 5(4):338–343. https://doi.org/10.1038/ng1293-338
doi: 10.1038/ng1293-338
pubmed: 8298640
Tanzi RE, Petrukhin K, Chernov I, Pellequer JL, Wasco W, Ross B, Romano DM, Parano E, Pavone L, Brzustowicz LM et al (1993) The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat Genet 5(4):344–350. https://doi.org/10.1038/ng1293-344
doi: 10.1038/ng1293-344
pubmed: 8298641
Bull PC, Thomas GR, Rommens JM, Forbes JR, Cox DW (1993) The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 5(4):327–337. https://doi.org/10.1038/ng1293-327
doi: 10.1038/ng1293-327
pubmed: 8298639
Thomas GR, Forbes JR, Roberts EA, Walshe JM, Cox DW (1995) The Wilson disease gene: spectrum of mutations and their consequences. Nat Genet 9(2):210–217. https://doi.org/10.1038/ng0295-210
doi: 10.1038/ng0295-210
pubmed: 7626145
Das SK, Ray K (2006) Wilson’s disease: an update. Nature clinical practice Neurology 2(9):482–493. https://doi.org/10.1038/ncpneuro0291
doi: 10.1038/ncpneuro0291
pubmed: 16932613
Brackley S, Gao J, Mann JP (2018) Wilson disease mutation database. http://www.wilsondisease.tk/ . 2019
Chang IJ, Hahn SH (2017) The genetics of Wilson disease. Handb Clin Neurol 142:19–34. https://doi.org/10.1016/b978-0-444-63625-6.00003-3
doi: 10.1016/b978-0-444-63625-6.00003-3
pubmed: 28433102
pmcid: 5648646
Czlonkowska A, Gromadzka G, Chabik G (2009) Monozygotic female twins discordant for phenotype of Wilson’s disease. Mov Disord 24(7):1066–1069. https://doi.org/10.1002/mds.22474
doi: 10.1002/mds.22474
pubmed: 19306278
Gheorghe L, Popescu I, Iacob S, Gheorghe C, Vaidan R, Constantinescu A, Iacob R, Becheanu G, Angelescu C, Diculescu M (2004) Wilson’s disease: a challenge of diagnosis. The 5-year experience of a tertiary centre. Rom J Gastroenterol 13(3):179–185
pubmed: 15470529
Svetel M, Potrebic A, Pekmezovic T, Tomic A, Kresojevic N, Jesic R, Dragasevic N, Kostic VS (2009) Neuropsychiatric aspects of treated Wilson’s disease. Parkinsonism Relat Disord 15(10):772–775. https://doi.org/10.1016/j.parkreldis.2009.01.010
doi: 10.1016/j.parkreldis.2009.01.010
pubmed: 19559640
Kayser B (1902) Uber einen Fall von angeborener Grunlicherverfarbung der Cornea. Kiln Mbl Augenheilk 40:22–25
Fleming CR, Dickson ER, Wahner HW, Hollenhorst RW, McCall JT (1977) Pigmented corneal rings in non-Wilsonian liver disease. Ann Intern Med 86(3):285–288
doi: 10.7326/0003-4819-86-3-285
Holmberg CG, Laurell CB (1948) Investigations on serum copper II. Isolation of the copper containing protein and a description of properties. Acta Chem Scand 2(10):950–956. https://doi.org/10.3891/acta.chem.scand.02-0550
doi: 10.3891/acta.chem.scand.02-0550
Frieden E, Hsieh HS (1976) Ceruloplasmin: the copper transport protein with essential oxidase activity. Adv Enzymol Relat Areas Mol Biol 44:187–236
pubmed: 775938
Tu JB, Blackwell RQ (1967) Studies on levels of penicillamine-induced cupriuresis in heterozygotes of Wilson’s disease. Metabolism 16(6):507–513
doi: 10.1016/0026-0495(67)90079-0
Nicastro E, Ranucci G, Vajro P, Vegnente A, Iorio R (2010) Re-evaluation of the diagnostic criteria for Wilson disease in children with mild liver disease. Hepatology (Baltimore, MD) 52(6):1948–1956. https://doi.org/10.1002/hep.23910
doi: 10.1002/hep.23910
Dhawan A, Taylor RM, Cheeseman P, De Silva P, Katsiyiannakis L, Mieli-Vergani G (2005) Wilson’s disease in children: 37-year experience and revised King’s score for liver transplantation. Liver Transpl 11(4):441–448. https://doi.org/10.1002/lt.20352
doi: 10.1002/lt.20352
pubmed: 15776453
pmcid: 15776453
Wu J, Forbes JR, Chen HS, Cox DW (1994) The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat Genet 7(4):541–545. https://doi.org/10.1038/ng0894-541
doi: 10.1038/ng0894-541
pubmed: 7951327
Jia G, Tohyama C, Sone H (2002) DNA damage triggers imbalance of proliferation and apoptosis during development of preneoplastic foci in the liver of Long-Evans Cinnamon rats. Int J Oncol 21(4):755–761
pubmed: 12239613
Fujiwara N, Iso H, Kitanaka N, Kitanaka J, Eguchi H, Ookawara T, Ozawa K, Shimoda S, Yoshihara D, Takemura M, Suzuki K (2006) Effects of copper metabolism on neurological functions in Wistar and Wilson’s disease model rats. Biochem Biophys Res Commun 349(3):1079–1086. https://doi.org/10.1016/j.bbrc.2006.08.139
doi: 10.1016/j.bbrc.2006.08.139
pubmed: 16970921
Rauch H (1983) Toxic milk, a new mutation affecting cooper metabolism in the mouse. J Hered 74(3):141–144
doi: 10.1093/oxfordjournals.jhered.a109751
Rauch H, Wells AJ (1995) The toxic milk mutation, tx, which results in a condition resembling Wilson disease in humans, is linked to mouse chromosome 8. Genomics 29(2):551–552. https://doi.org/10.1006/geno.1995.9968
doi: 10.1006/geno.1995.9968
pubmed: 8666408
Reed V, Williamson P, Bull PC, Cox DW, Boyd Y (1995) Mapping of the mouse homologue of the Wilson disease gene to mouse chromosome 8. Genomics 28(3):573–575. https://doi.org/10.1006/geno.1995.1191
doi: 10.1006/geno.1995.1191
pubmed: 7490097
Theophilos MB, Cox DW, Mercer JF (1996) The toxic milk mouse is a murine model of Wilson disease. Hum Mol Genet 5(10):1619–1624
doi: 10.1093/hmg/5.10.1619
Michalczyk AA, Rieger J, Allen KJ, Mercer JF, Ackland ML (2000) Defective localization of the Wilson disease protein (ATP7B) in the mammary gland of the toxic milk mouse and the effects of copper supplementation. Biochem J 352(Pt 2):565–571
doi: 10.1042/bj3520565
Wadwa J, Chu YH, Nguyen N, Henson T, Figueroa A, Llanos R, Ackland ML, Michalczyk A, Fullriede H, Brennan G, Mercer JF, Linder MC (2014) Effects of ATP7A overexpression in mice on copper transport and metabolism in lactation and gestation. Physiol Rep 2(1):e00195. https://doi.org/10.1002/phy2.195
doi: 10.1002/phy2.195
pubmed: 24744874
pmcid: 3967678
Dorea JG (2000) Iron and copper in human milk. Nutrition 16(3):209–220. https://doi.org/10.1016/s0899-9007(99)00287-7
doi: 10.1016/s0899-9007(99)00287-7
pubmed: 10705077
Howell JM, Mercer JF (1994) The pathology and trace element status of the toxic milk mutant mouse. J Comp Pathol 110(1):37–47
doi: 10.1016/S0021-9975(08)80268-X
Allen KJ, Buck NE, Cheah DM, Gazeas S, Bhathal P, Mercer JF (2006) Chronological changes in tissue copper, zinc and iron in the toxic milk mouse and effects of copper loading. Biometals 19(5):555–564. https://doi.org/10.1007/s10534-005-5918-5
doi: 10.1007/s10534-005-5918-5
pubmed: 16937262
Deng DX, Ono S, Koropatnick J, Cherian MG (1998) Metallothionein and apoptosis in the toxic milk mutant mouse. Lab Invest 78(2):175–183
pubmed: 9484715
Voskoboinik I, Greenough M, La Fontaine S, Mercer JF, Camakaris J (2001) Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochem Biophys Res Commun 281(4):966–970. https://doi.org/10.1006/bbrc.2001.4445
doi: 10.1006/bbrc.2001.4445
pubmed: 11237756
La Fontaine S, Theophilos MB, Firth SD, Gould R, Parton RG, Mercer JF (2001) 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 10(4):361–370
doi: 10.1093/hmg/10.4.361
Biempica L, Rauch H, Quintana N, Sternlieb I (1988) Morphologic and chemical studies on a murine mutation (toxic milk mice) resulting in hepatic copper toxicosis. Lab Invest 59(4):500–508
pubmed: 2845190
Zischka H, Lichtmannegger J (2014) Pathological mitochondrial copper overload in livers of Wilson’s disease patients and related animal models. Ann N Y Acad Sci 1315:6–15. https://doi.org/10.1111/nyas.12347
doi: 10.1111/nyas.12347
pubmed: 24517326
Koropatnick J, Cherian MG (1993) A mutant mouse (tx) with increased hepatic metallothionein stability and accumulation. Biochem J 296(Pt 2):443–449
doi: 10.1042/bj2960443
Zhang J, Tang LL, Li LY, Cui SW, Jin S, Chen HZ, Yang WM, Xie DJ, Yu GR (2020) gandouling tablets inhibit excessive mitophagy in toxic milk (tx) model Mouse of Wilson disease via Pink1/Parkin pathway. Evid Based Complementary Altern Med 2020:3183714. https://doi.org/10.1155/2020/3183714
doi: 10.1155/2020/3183714
Chen DB, Feng L, Lin XP, Zhang W, Li FR, Liang XL, Li XH (2012) Penicillamine increases free copper and enhances oxidative stress in the brain of toxic milk mice. PLoS ONE 7(5):e37709. https://doi.org/10.1371/journal.pone.0037709
doi: 10.1371/journal.pone.0037709
pubmed: 22629446
pmcid: 3357430
Chen Y, Zhang B, Cao S, Huang W, Liu N, Yang W (2018) GanDouLing combined with Penicillamine improves cerebrovascular injury via PERK/eIF2α/CHOP endoplasmic reticulum stress pathway in the mouse model of Wilson’s disease. Biosci Rep. https://doi.org/10.1042/bsr20180800
doi: 10.1042/bsr20180800
pubmed: 30487161
pmcid: 6435564
Allen KJ, Cheah DM, Wright PF, Gazeas S, Pettigrew-Buck NE, Deal YH, Mercer JF, Williamson R (2004) Liver cell transplantation leads to repopulation and functional correction in a mouse model of Wilson’s disease. J Gastroenterol Hepatol 19(11):1283–1290. https://doi.org/10.1111/j.1440-1746.2004.03451.x
doi: 10.1111/j.1440-1746.2004.03451.x
pubmed: 15482536
Buck NE, Cheah DM, Elwood NJ, Wright PF, Allen KJ (2008) Correction of copper metabolism is not sustained long term in Wilson’s disease mice post bone marrow transplantation. Hep Intl 2(1):72–79. https://doi.org/10.1007/s12072-007-9039-9
doi: 10.1007/s12072-007-9039-9
Roberts EA, Robinson BH, Yang S (2008) Mitochondrial structure and function in the untreated Jackson toxic milk (tx-j) mouse, a model for Wilson disease. Mol Genet Metab 93(1):54–65. https://doi.org/10.1016/j.ymgme.2007.08.127
doi: 10.1016/j.ymgme.2007.08.127
pubmed: 17981064
Jonczy A, Lipinski P, Ogorek M, Starzynski RR, Krzysztofik D, Bednarz A, Krzeptowski W, Szudzik M, Haberkiewicz O, Milon A, Grzmil P, Lenartowicz M (2019) Functional iron deficiency in toxic milk mutant mice (tx-J) despite high hepatic ferroportin: a critical role of decreased GPI-ceruloplasmin expression in liver macrophages. Metallomics 11(6):1079–1092. https://doi.org/10.1039/c9mt00035f
doi: 10.1039/c9mt00035f
pubmed: 31011744
Bronson RT, Sweet HO, Davissin MT (1995) Acute cerebral neuronalnecrosis in copper deficient offspring of female mice with the toxic milkmutation. Mouse Genome 93:152–154
Zhou XX, Li XH, Chen DB, Wu C, Feng L, Qin HL, Pu XY, Liang XL (2019) Injury factors and pathological features of toxic milk mice during different disease stages. Brain Behav 9(12):e01459. https://doi.org/10.1002/brb3.1459
doi: 10.1002/brb3.1459
pubmed: 31742933
pmcid: 6908887
Terwel D, Loschmann YN, Schmidt HH, Scholer HR, Cantz T, Heneka MT (2011) Neuroinflammatory and behavioural changes in the Atp7B mutant mouse model of Wilson’s disease. J Neurochem 118(1):105–112. https://doi.org/10.1111/j.1471-4159.2011.07278.x
doi: 10.1111/j.1471-4159.2011.07278.x
pubmed: 21517843
Przybylkowski A, Gromadzka G, Wawer A, Bulska E, Jablonka-Salach K, Grygorowicz T, Schnejder-Pacholek A, Czlonkowski A (2013) Neurochemical and behavioral characteristics of toxic milk mice: an animal model of Wilson’s disease. Neurochem Res 38(10):2037–2045. https://doi.org/10.1007/s11064-013-1111-3
doi: 10.1007/s11064-013-1111-3
pubmed: 23877404
pmcid: 3779085
Czachor JD, Cherian MG, Koropatnick J (2002) Reduction of copper and metallothionein in toxic milk mice by tetrathiomolybdate, but not deferiprone. J Inorg Biochem 88(2):213–222
doi: 10.1016/S0162-0134(01)00383-X
Chan HW, Liu T, Verdile G, Bishop G, Haasl RJ, Smith MA, Perry G, Martins RN, Atwood CS (2008) Copper induces apoptosis of neuroblastoma cells via post-translational regulation of the expression of Bcl-2-family proteins and the tx mouse is a better model of hepatic than brain Cu toxicity. Int J Clin Exp Med 1(1):76–88
pubmed: 19079689
pmcid: 2596338
Goldschmith A, Infante C, Leiva J, Motles E, Palestini M (2005) Interference of chronically ingested copper in long-term potentiation (LTP) of rat hippocampus. Brain Res 1056(2):176–182. https://doi.org/10.1016/j.brainres.2005.07.030
doi: 10.1016/j.brainres.2005.07.030
pubmed: 16112097
Medici V, Shibata NM, Kharbanda KK, LaSalle JM, Woods R, Liu S, Engelberg JA, Devaraj S, Torok NJ, Jiang JX, Havel PJ, Lonnerdal B, Kim K, Halsted CH (2013) Wilson’s disease: changes in methionine metabolism and inflammation affect global DNA methylation in early liver disease. Hepatology (Baltimore, MD) 57(2):555–565. https://doi.org/10.1002/hep.26047
doi: 10.1002/hep.26047
Medici V, Shibata NM, Kharbanda KK, Islam MS, Keen CL, Kim K, Tillman B, French SW, Halsted CH, LaSalle JM (2014) Maternal choline modifies fetal liver copper, gene expression, DNA methylation, and neonatal growth in the tx-j mouse model of Wilson disease. Epigenetics 9(2):286–296. https://doi.org/10.4161/epi.27110
doi: 10.4161/epi.27110
pubmed: 24220304
Buiakova OI, Xu J, Lutsenko S, Zeitlin S, Das K, Das S, Ross BM, Mekios C, Scheinberg IH, Gilliam TC (1999) Null mutation of the murine ATP7B (Wilson disease) gene results in intracellular copper accumulation and late-onset hepatic nodular transformation. Hum Mol Genet 8(9):1665–1671. https://doi.org/10.1093/hmg/8.9.1665
doi: 10.1093/hmg/8.9.1665
pubmed: 10441329
Huster D, Finegold MJ, Morgan CT, Burkhead JL, Nixon R, Vanderwerf SM, Gilliam CT, Lutsenko S (2006) Consequences of copper accumulation in the livers of the Atp7b-/- (Wilson disease gene) knockout mice. Am J Pathol 168(2):423–434. https://doi.org/10.2353/ajpath.2006.050312
doi: 10.2353/ajpath.2006.050312
pubmed: 16436657
pmcid: 1606493
Polishchuk EV, Merolla A, Lichtmannegger J, Romano A, Indrieri A, Ilyechova EY, Concilli M, De Cegli R, Crispino R, Mariniello M, Petruzzelli R, Ranucci G, Iorio R, Pietrocola F, Einer C, Borchard S, Zibert A, Schmidt HH, Di Schiavi E, Puchkova LV, Franco B, Kroemer G, Zischka H, Polishchuk RS (2019) Activation of autophagy, observed in liver tissues from patients with Wilson disease and from ATP7B-deficient animals, protects hepatocytes from copper-induced apoptosis. Gastroenterology 156(4):1173-1189.e1175. https://doi.org/10.1053/j.gastro.2018.11.032
doi: 10.1053/j.gastro.2018.11.032
pubmed: 30452922
Wooton-Kee CR, Robertson M, Zhou Y, Dong B, Sun Z, Kim KH, Liu H, Xu Y, Putluri N, Saha P, Coarfa C, Moore DD, Nuotio-Antar AM (2020) Metabolic dysregulation in the Atp7b (-/-) Wilson’s disease mouse model. Proc Natl Acad Sci USA 117(4):2076–2083. https://doi.org/10.1073/pnas.1914267117
doi: 10.1073/pnas.1914267117
pubmed: 31924743
Huster D, Purnat TD, Burkhead JL, Ralle M, Fiehn O, Stuckert F, Olson NE, Teupser D, Lutsenko S (2007) High copper selectively alters lipid metabolism and cell cycle machinery in the mouse model of Wilson disease. J Biol Chem 282(11):8343–8355. https://doi.org/10.1074/jbc.M607496200
doi: 10.1074/jbc.M607496200
pubmed: 17205981
Barnes N, Tsivkovskii R, Tsivkovskaia N, Lutsenko S (2005) The copper-transporting ATPases, menkes and wilson disease proteins, have distinct roles in adult and developing cerebellum. J Biol Chem 280(10):9640–9645. https://doi.org/10.1074/jbc.M413840200
doi: 10.1074/jbc.M413840200
pubmed: 15634671