Роль гена ATOX1 в метаболизме меди и в патогенезе медь-индуцированных заболеваний
- Авторы: Жалсанова И.Ж.1, Фонова Е.А.1, Жигалина Д.И.1, Скрябин Н.А.1
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Учреждения:
- Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
- Выпуск: Том 59, № 3 (2023)
- Страницы: 283-293
- Раздел: ОБЗОРНЫЕ И ТЕОРЕТИЧЕСКИЕ СТАТЬИ
- URL: https://journals.rcsi.science/0016-6758/article/view/134565
- DOI: https://doi.org/10.31857/S0016675823030128
- EDN: https://elibrary.ru/IQRALQ
- ID: 134565
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Аннотация
Белок ATOX1 (Antioxidant Protein 1) представляет собой медный металлошаперон человека, который играет важную роль в клеточном гомеостазе меди. Белок ответственен за захват цитозольной меди с CTR1 (транспортер меди 1) и перенос на медные насосы в транс-сети Гольджи к белкам ATP7A и ATP7B. В настоящем обзоре были собраны данные об антиоксидантной роли ATOX1, роли гена в регулировании ангиогенеза и пролиферации раковых клеток, а также роли в патогенезе медь-индуцированных заболеваний – болезни Вильсона–Коновалова и болезни Менкеса.
Ключевые слова
Об авторах
И. Ж. Жалсанова
Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
Автор, ответственный за переписку.
Email: irina.zhalsanova@medgenetics.ru
Россия, 634050, Томск
Е. А. Фонова
Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
Email: irina.zhalsanova@medgenetics.ru
Россия, 634050, Томск
Д. И. Жигалина
Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
Email: irina.zhalsanova@medgenetics.ru
Россия, 634050, Томск
Н. А. Скрябин
Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
Email: irina.zhalsanova@medgenetics.ru
Россия, 634050, Томск
Список литературы
- Linder M.C. Biochemistry of Copper // Biochem. Copp. Springer US. 1991. https://doi.org/10.1007/978-1-4757-9432-8
- Van Den Berghe P.V.E., Klomp L.W.J. New developments in the regulation of intestinal copper absorption // Nutr. Rev. 2009. V. 67. № 11. P. 658–672. https://doi.org/10.1111/J.1753-4887.2009.00250.X
- Gaetke L.M., Chow-Johnson H.S., Chow C.K. Copper: toxicological relevance and mechanisms // Arch. Toxicol. 2014. V. 88. № 11. P. 1929–1938. https://doi.org/10.1007/S00204-014-1355-Y
- Korte J.J., Prohaska J.R. Dietary copper deficiency alters protein and lipid composition of murine lymphocyte plasma membranes // J. Nutr. 1987. V. 117. № 6. P. 1076–1084. https://doi.org/10.1093/JN/117.6.1076
- Leah Harris Z., Gitlin J.D. Genetic and molecular basis for copper toxicity // Am. J. Clin. Nutr. 1996. V. 63. № 5. P. 836–841. https://doi.org/10.1093/AJCN/63.5.836
- O’Halloran T.V., Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions // J. Biol. Chem. 2000. V. 275. № 33. P. 25057–25060. https://doi.org/10.1074/JBC.R000006200
- Klomp L.W.J., Lin S.J., Yuan D.S. et al. Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis // J. Biol. Chem. 1997. V. 272. № 14. P. 9221–9226. https://doi.org/10.1074/JBC.272.14.9221
- Portnoy M.E., Rosenzweig A.C., Rae T. et al. Structure-function analyses of the ATX1 metallochaperone // J. Biol. Chem. 1999. V. 274. № 21. P. 15041–15045. https://doi.org/10.1074/JBC.274.21.15041
- Kelner G.S., Lee M.H., Clark M.E. et al. The copper transport protein Atox1 promotes neuronal survival // J. Biol. Chem. 2000. V. 275. № 1. P. 580–584. https://doi.org/10.1074/JBC.275.1.580
- Hatori Y., Clasen S., Hasan N.M. et al. Functional partnership of the copper export machinery and glutathione balance in human cells // J. Biol. Chem. 2012. V. 287. № 32. P. 26678–26687. https://doi.org/10.1074/JBC.M112.381178
- Hatori Y., Lutsenko S. The role of copper chaperone atox1 in coupling redox homeostasis to intracellular copper distribution // Antioxidants (Basel, Switzerland). 2016. V. 5. № 3. https://doi.org/10.3390/ANTIOX5030025
- Walker J.M., Tsivkovskii R., Lutsenko S. Metallochaperone Atox1 transfers copper to the NH2-terminal domain of the Wilson’s disease protein and regulates its catalytic activity // J. Biol. Chem. 2002. V. 277. № 31. P. 27953–27959. https://doi.org/10.1074/JBC.M203845200
- Culotta V.C., Klomp L.W.J., Strain J. et al. The copper chaperone for superoxide dismutase // J. Biol. Chem. Elsevier. 1997. V. 272. № 38. P. 23469–23472. https://doi.org/10.1074/JBC.272.38.23469
- Petzoldt S., Kahra D., Kovermann M. et al. Human cytoplasmic copper chaperones Atox1 and CCS exchange copper ions in vitro // Biometals. 2015. V. 28. № 3. P. 577–585. https://doi.org/10.1007/S10534-015-9832-1
- Hatori Y., Inouye S., Akagi R. Thiol-based copper handling by the copper chaperone Atox1 // IUBMB Life. Blackwell Publ. Ltd. 2017. V. 69. № 4. P. 246–254. https://doi.org/10.1002/iub.1620
- Curnock R., Cullen P.J. Mammalian copper homeostasis requires retromer-dependent recycling of the high-affinity copper transporter 1 // J. Cell Sci. 2020. V. 133. № 16. https://doi.org/10.1242/JCS.249201
- Itoh S., Ha W.K., Nakagawa O. et al. Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation // J. Biol. Chem. 2008. V. 283. № 14. P. 9157–9167. https://doi.org/10.1074/JBC.M709463200
- Blockhuys S., Wittung-Stafshede P. Roles of copper-binding proteins in breast cancer // Int. J. Mol. Sci. 2017. V. 18. № 4. https://doi.org/10.3390/IJMS18040871
- Antoniades V., Sioga A., Dietrich E.M. et al. Is copper chelation an effective anti-angiogenic strategy for cancer treatment? // Med. Hypotheses. 2013. V. 81. № 6. P. 1159–1163. https://doi.org/10.1016/J.MEHY.2013.09.035
- Denoyer D., Masaldan S., La Fontaine S. et al. Targeting copper in cancer therapy: “Copper That Cancer” // Metallomics. 2015. V. 7. № 11. P. 1459–1476. https://doi.org/10.1039/C5MT00149H
- Gupte A., Mumper R.J. Elevated copper and oxidative stress in cancer cells as a target for cancer treatment // Cancer Treat. Rev. 2009. V. 35. № 1. P. 32–46. https://doi.org/10.1016/J.CTRV.2008.07.004
- Doñate F., Juarez J.C., Burnett M.E. et al. Identification of biomarkers for the antiangiogenic and antitumour activity of the superoxide dismutase 1 (SOD1) inhibitor tetrathiomolybdate (ATN-224) // Br. J. Cancer. 2008. V. 98. № 4. P. 776–783. https://doi.org/10.1038/SJ.BJC.6604226
- Wang J., Luo C., Shan C. et al. Inhibition of human copper trafficking by a small molecule significantly attenuates cancer cell proliferation // Nat. Chem. 2015. V. 7. № 12. P. 968–979. https://doi.org/10.1038/nchem.2381
- Jana A., Das A., Krett N.L. et al. Nuclear translocation of Atox1 potentiates activin A-induced cell migration and colony formation in colon cancer // PLoS One. 2020. V. 15. № 1. https://doi.org/10.1371/JOURNAL.PONE.0227916
- Blockhuys S., Brady D.C., Wittung-Stafshede P. Evaluation of copper chaperone ATOX1 as prognostic biomarker in breast cancer // Breast Cancer. 2020. V. 27. № 3. P. 505–509. https://doi.org/10.1007/S12282-019-01044-4
- Kim Y.J., Bond G.J., Tsang T. et al. Copper chaperone ATOX1 is required for MAPK signaling and growth in BRAF mutation-positive melanoma // Metallomics. 2019. V. 11. № 8. P. 1430–1440. https://doi.org/10.1039/C9MT00042A
- Kaler S.G., Ferreira C.R., Yam L.S. Estimated birth prevalence of Menkes disease and ATP7A-related disorders based on the Genome Aggregation Database (gnomAD) // Mol. Genet. Metab. Reports. Elsevier. 2020. V. 24. P. 100602. https://doi.org/10.1016/J.YMGMR.2020.100602
- Horn N., Wittung-Stafshede P. ATP7A-regulated enzyme metalation and trafficking in the menkes disease puzzle // Biomedicines. 2021. V. 9. № 4. https://doi.org/10.3390/BIOMEDICINES9040391
- Vulpe C., Levinson B., Whitney S. et al. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase // Nat. Genet. 1993. V. 3. № 1. P. 7–13. https://doi.org/10.1038/NG0193-7
- Tümer Z., Møller L.B. Menkes disease // Eur. J. Hum. Genet. 2009. V. 18. № 5. P. 511–518. https://doi.org/10.1038/ejhg.2009.187
- Chen J., Jiang Y., Shi H. et al. The molecular mechanisms of copper metabolism and its roles in human diseases // Pflugers Arch. 2020. V. 472. № 10. P. 1415–1429. https://doi.org/10.1007/S00424-020-02412-2
- Hamza I., Faisst A., Prohaska J. et al. The metallochaperone Atox1 plays a critical role in perinatal copper homeostasis // Proc. Natl Acad. Sci. USA. 2001. V. 98. № 12. P. 6848–6852. https://doi.org/10.1073/PNAS.111058498
- Liu P.C., Koeller D.M., Kaler S.G. Genomic organization of ATOXI, A human copper chaperone // BMC Genet. BioMed Central. 2003. V. 4. № 1. P. 1–4. https://doi.org/10.1186/1471-2156-4-4/TABLES/2
- Федеральные клинические рекомендации по диагностике и лечению болезни Вильсона–Коновалова (гепатолентикулярная дегенерация). М., 2015.
- Shribman S., Warner T.T., Dooley J.S. Clinical presentations of Wilson disease // Ann. Transl. Med. 2019. V. 7. Suppl. 2. P. S60. https://doi.org/10.21037/ATM.2019.04.27
- Machado A., Chien H.F., Deguti M.M. et al. Neurological manifestations in Wilson’s disease: Report of 119 cases // Mov. Disord. 2006. V. 21. № 12. P. 2192–2196. https://doi.org/10.1002/MDS.21170
- Баязутдинова Г.М., Щагина О.А., Поляков А.В. Молекулярный патогенез болезни Вильсона–Коновалова // Мед. генетика. 2017. Т. 16. № 7. С. 18–24.
- Chang I.J., Hahn S.H. The genetics of Wilson disease // Handb. Clin. Neurol. 2017. V. 142. P. 19. https://doi.org/10.1016/B978-0-444-63625-6.00003-3
- Postrigan A.E., Zhalsanova I.Z., Fonova E.A. et al. Modifier genes as a cause of Wilson–Konovalov disease clinical polymorphism // Rus. J. Genet. 2021. V. 57. № 5. P. 522–532. https://doi.org/10.1134/S1022795421050094/TABLES/1
- Hamza I., Schaefer M., Klomp L.W.J. et al. Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis // Proc. Natl Acad. Sci. USA. 1999. V. 96. № 23. P. 13363–13368. https://doi.org/10.1073/PNAS.96.23.13363
- Simon I., Schaefer M., Reichert J. et al. Analysis of the human Atox 1 homologue in Wilson patients // World J. Gastroenterol. 2008. V. 14. № 15. P. 2383–2387. https://doi.org/10.3748/WJG.14.2383
- Bost M., Piguet-Lacroix G., Parant F. et al. Molecular analysis of Wilson patients: Direct sequencing and MLPA analysis in the ATP7B gene and Atox1 and COMMD1 gene analysis // J. Trace Elem. Med. Biol. 2012. V. 26. № 2–3. P. 97–101. https://doi.org/10.1016/J.JTEMB.2012.04.024
- Kumari N., Kumar A., Pal A. et al. In-silico analysis of novel p.(Gly14Ser) variant of ATOX1 gene: Plausible role in modulating ATOX1-ATP7B interaction // Mol. Biol. Rep. 2019. V. 46. № 3. P. 3307–3313. https://doi.org/10.1007/S11033-019-04791-X
- Reed E., Lutsenko S., Bandmann O. Animal models of Wilson disease // J. Neurochem. 2018. V. 146. № 4. P. 356–373. https://doi.org/10.1111/JNC.14323
- Medici V., Huster D. Animal models of Wilson disease // Handb. Clin. Neurol. 2017. V. 142. P. 57–70. https://doi.org/10.1016/B978-0-444-63625-6.00006-9
- Wu J., Forbes J.R., Chen H.S. et al. The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene // Nat. Genet. 1994. V. 7. № 4. P. 541–545. https://doi.org/10.1038/NG0894-541
- Suzuki M., Aoki T. Impaired hepatic copper homeostasis in long-evans Cinnamon rats: Reduced biliary excretion of copper // Pediatr. Res. 1994. V. 35. № 5. P. 598–601. https://doi.org/10.1203/00006450-199405000-00012
- Rauch H. Toxic milk, A new mutation affecting cooper metabolism in the mouse // J. Hered. 1983. V. 74. № 3. P. 141–144. https://doi.org/10.1093/OXFORDJOURNALS.JHE-RED.A109751
- La Fontaine S., Theophilos M.B., Firth S.D. et al. 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. V. 10. № 4. P. 361–370. https://doi.org/10.1093/HMG/10.4.361
- Voskoboinik I., Greenough M., La Fontaine S. et al. Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant // Biochem. Biophys. Res. 2001. V. 281. № 4. P. 966–970. https://doi.org/10.1006/BBRC.2001.4445
- Kasai N., Osanai T., Miyoshi I. et al. Clinico-pathological studies of LEC rats with hereditary hepatitis and hepatoma in the acute phase of hepatitis // Lab. Anim. Sci. 1990. V. 40. P. 502–505.
- Smedley R., Mullaney T., Rumbeiha W. Copper-associated hepatitis in Labrador Retrievers // Vet. Pathol. 2009. V. 46. № 3. P. 484–490. https://doi.org/10.1354/VP.08-VP-0197-S-FL
- Fieten H., Gill Y., Martin A.J. et al. The Menkes and Wilson disease genes counteract in copper toxicosis in Labrador retrievers: A new canine model for copper-metabolism disorders // Dis. Model. Mech. 2016. V. 9. № 1. P. 25–38. https://doi.org/10.1242/DMM.020263
- Miyayama T., Suzuki K.T., Ogra Y. Copper accumulation and compartmentalization in mouse fibroblast lacking metallothionein and copper chaperone, Atox1 // Toxicol. Appl. Pharmacol. 2009. V. 237. № 2. P. 205–213. https://doi.org/10.1016/J.TAAP.2009.03.024
- Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease // Toxicology. 2011. V. 283. № 2–3. P. 65–87. https://doi.org/10.1016/J.TOX.2011.03.001
- Zhang J.W., Liu J.X., Hou H.M. et al. Effects of tetrathiomolybdate and penicillamine on brain hydroxyl radical and free copper levels: a microdialysis study in vivo // Biochem. Biophys. Res. Commun. 2015. V. 458. № 1. P. 82–85. https://doi.org/10.1016/J.BBRC.2015.01.071
- Alvarez H.M., Xue Y., Robinson C.D. et al. Tetrathiomolybdate inhibits copper trafficking proteins through metal cluster formation // Science. 2010. V. 327. № 5963. P. 331–334. https://doi.org/10.1126/SCIENCE.1179907
- Scheinberg I.H., Walshe J.M. Orphan Diseases and Orphan Drugs. Manchester: Univ. Press, 1986. V. 3. 228 p.
- Walshe J.M. The conquest of Wilson’s disease // Brain. 2009. V. 132. Pt 8. P. 2289–2295. https://doi.org/10.1093/BRAIN/AWP149
- Brewer G.J. Zinc and tetrathiomolybdate for the treatment of Wilson’s disease and the potential efficacy of anticopper therapy in a wide variety of diseases // Metallomics. 2009. V. 1. № 3. P. 199–206. https://doi.org/10.1039/B901614G
- Weiss K.H., Askari F.K., Czlonkowska A. et al. Bis-choline tetrathiomolybdate in patients with Wilson’s disease: An open-label, multicentre, phase 2 study // Lancet Gastroenterol Hepatol. 2017. V. 2. № 12. P. 869–876. https://doi.org/10.1016/S2468-1253(17)30293-5
- Stremmel W. Bis-choline tetrathiomolybdate as old drug in a new design for Wilson’s disease: Good for brain and liver? // Hepatology. 2019. V. 69. № 2. P. 901–903. https://doi.org/10.1002/HEP.30130
- Goodman V., Brewer G., Merajver S. Control of copper status for cancer therapy // Curr. Cancer Drug Targets. 2005. V. 5. № 7. P. 543–549. https://doi.org/10.2174/156800905774574066
- Tetrathiomolybdate, a copper chelator for the treatment of Wilson disease, pulmonary fibrosis and other indications – PubMed (Электронный ресурс). URL: https://pubmed.ncbi.nlm.nih.gov/18683094/ (accessed: 01.04.2022).
- Ishida S., McCormick F., Smith-McCune K. et al. Enhancing tumor-specific uptake of the anticancer drug cisplatin with a copper chelator // Cancer Cell. 2010. V. 17. № 6. P. 574–583. https://doi.org/10.1016/J.CCR.2010.04.011
- Blockhuys S., Celauro E., Hildesjö C. et al. Defining the human copper proteome and analysis of its expression variation in cancers // Metallomics. 2017. V. 9. № 2. P. 112–123. https://doi.org/10.1039/C6MT00202A
- Urso E., Maffia M. Behind the link between copper and angiogenesis: Established mechanisms and an overview on the role of vascular copper transport systems // J. Vasc. Res. 2015. V. 52. № 3. P. 172–196. https://doi.org/10.1159/000438485
- Maryon E.B., Molloy S.A., Kaplan J.H. Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1 // Am. J. Physiol. Cell Physiol. 2013. V. 304. № 8. https://doi.org/10.1152/AJPCELL.00417.2012
- Puig-Pijuan T., Souza L.R.Q., Da C. et al. Copper imbalance linked to oxidative stress and cell death during Zika virus infection in human astrocytes // bioRxiv. 2021. P. 2021.12.29.474370. https://doi.org/10.1101/2021.12.29.474370
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