The Mitochondrial Metallochaperone SCO1 Is Required to Sustain Expression of the High-Affinity Copper Transporter CTR1 and Preserve Copper Homeostasis

Cell Reports

Volumn 10, Issue 6, 2015, Pages 933-943

  Hlynialuk, Christopher J ^a   Ling, Binbing ^a   Baker, Zakery N ^a   Cobine, Paul A ^b   Yu, Lisa D ^a   Boulet, Aren ^a   Wai, Timothy ^c   Hossain, Amzad ^a   ElZawily, Amr M ^a,f   McFie, Pamela J ^a   Stone, Scot J ^a   Diaz, Francisca ^d   Moraes, Carlos T ^d   Viswanathan, Deepa ^e   Petris, Michael J ^e   Leary, Scot C ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b AUBURN UNIVERSITY   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e University of Missouri   (United States)

^f Damanhour University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER TRANSPORTER 1 PROTEIN; CYTOCHROME C OXIDASE; FAT DROPLET; MEMBRANE PROTEIN; MESSENGER RNA; METALLOCHAPERONE; SCO1 PROTEIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; COPPER DEFICIENCY; COPPER METABOLISM; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; LIFE EXPECTANCY; LIVER; MITOCHONDRION; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84923093655     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.01.019     Document Type: Article

References (55)

1. Aigner E., Strasser M., Haufe H., Sonnweber T., Hohla F., Stadlmayr A., Solioz M., Tilg H., Patsch W., Weiss G., et al. A role for low hepatic copper concentrations in nonalcoholic Fatty liver disease. Am. J. Gastroenterol. 2010, 105:1978-1985.
2. Bull P.C., Thomas G.R., Rommens J.M., Forbes J.R., Cox D.W. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat. Genet. 1993, 5:327-337.
3. Caruano-Yzermans A.L., Bartnikas T.B., Gitlin J.D. Mechanisms of the copper-dependent turnover of the copper chaperone for superoxide dismutase. J.Biol. Chem. 2006, 281:13581-13587.
4. +)-dependent activation of Sirt1 corrects the phenotype in a mouse model of mitochondrial disease. Cell Metab. 2014, 19:1042-1049.
5. Cobine P.A., Pierrel F., Winge D.R. Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim. Biophys. Acta 2006, 1763:759-772.
6. Desai V., Kaler S.G. Role of copper in human neurological disorders. Am. J. Clin. Nutr. 2008, 88:855S-858S.
7. Diaz F., Garcia S., Hernandez D., Regev A., Rebelo A., Oca-Cossio J., Moraes C.T. Pathophysiology and fate of hepatocytes in a mouse model of mitochondrial hepatopathies. Gut 2008, 57:232-242.
8. DiMauro S., Tanji K., Schon E.A. The many clinical faces of cytochrome c oxidase deficiency. Adv. Exp. Med. Biol. 2012, 748:341-357.
9. Dodani S.C., Leary S.C., Cobine P.A., Winge D.R., Chang C.J. A targetable fluorescent sensor reveals that copper-deficient SCO1 and SCO2 patient cells prioritize mitochondrial copper homeostasis. J.Am. Chem. Soc. 2011, 133:8606-8616.
10. Eisses J.F., Kaplan J.H. The mechanism of copper uptake mediated by human CTR1: a mutational analysis. J.Biol. Chem. 2005, 280:37159-37168.
11. Festa R.A., Thiele D.J. Copper: an essential metal in biology. Curr. Biol. 2011, 21:R877-R883.
12. Festa R.A., Thiele D.J. Copper at the front line of the host-pathogen battle. PLoS Pathog. 2012, 8:e1002887.
13. Gitlin D., Janeway C.A. Turnover of the copper and protein moieties of ceruloplasmin. Nature 1960, 185:693.
14. Glerum D.M., Shtanko A., Tzagoloff A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J.Biol. Chem. 1996, 271:14504-14509.
15. Glerum D.M., Shtanko A., Tzagoloff A. SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J.Biol. Chem. 1996, 271:20531-20535.
16. Guo Y., Smith K., Lee J., Thiele D.J., Petris M.J. Identification of methionine-rich clusters that regulate copper-stimulated endocytosis of the human Ctr1 copper transporter. J.Biol. Chem. 2004, 279:17428-17433.
17. Hamza I., Schaefer M., Klomp L.W., Gitlin J.D. Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc. Natl. Acad. Sci. USA 1999, 96:13363-13368.
18. Hasan N.M., Lutsenko S. Regulation of copper transporters in human cells. Curr. Top. Membr. 2012, 69:137-161.
19. Jaksch M., Ogilvie I., Yao J., Kortenhaus G., Bresser H.G., Gerbitz K.D., Shoubridge E.A. Mutations in SCO2 are associated with a distinct form of hypertrophic cardiomyopathy and cytochrome c oxidase deficiency. Hum. Mol. Genet. 2000, 9:795-801.
20. Kim B.E., Nevitt T., Thiele D.J. Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 2008, 4:176-185.
21. Kim H., Son H.Y., Bailey S.M., Lee J. Deletion of hepatic Ctr1 reveals its function in copper acquisition and compensatory mechanisms forcopper homeostasis. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296:G356-G364.
22. Lamb A.L., Torres A.S., O'Halloran T.V., Rosenzweig A.C. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat. Struct. Biol. 2001, 8:751-755.
23. Leary S.C. Redox regulation of SCO protein function: controlling copper at a mitochondrial crossroad. Antioxid. Redox Signal. 2010, 13:1403-1416.
24. Leary S.C., Hill B.C., Lyons C.N., Carlson C.G., Michaud D., Kraft C.S., Ko K., Glerum D.M., Moyes C.D. Chronic treatment with azide insitu leads to an irreversible loss of cytochrome c oxidase activity via holoenzyme dissociation. J.Biol. Chem. 2002, 277:11321-11328.
25. Leary S.C., Kaufman B.A., Pellecchia G., Guercin G.H., Mattman A., Jaksch M., Shoubridge E.A. Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase. Hum. Mol. Genet. 2004, 13:1839-1848.
26. Leary S.C., Cobine P.A., Kaufman B.A., Guercin G.H., Mattman A., Palaty J., Lockitch G., Winge D.R., Rustin P., Horvath R., Shoubridge E.A. The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. Cell Metab. 2007, 5:9-20.
27. Leary S.C., Sasarman F., Nishimura T., Shoubridge E.A. Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1. Hum. Mol. Genet. 2009, 18:2230-2240.
28. Leary S.C., Antonicka H., Sasarman F., Weraarpachai W., Cobine P.A., Pan M., Brown G.K., Brown R., Majewski J., Ha K.C., et al. Novel mutations in SCO1 as a cause of fatal infantile encephalopathy and lactic acidosis. Hum. Mutat. 2013, 34:1366-1370.
29. Leary S.C., Cobine P.A., Nishimura T., Verdijk R.M., de Krijger R., de Coo R., Tarnopolsky M.A., Winge D.R., Shoubridge E.A. COX19 mediates the transduction of a mitochondrial redox signal from SCO1 that regulates ATP7A-mediated cellular copper efflux. Mol. Biol. Cell 2013, 24:683-691.
30. Lee J., Peña M.M., Nose Y., Thiele D.J. Biochemical characterization of the human copper transporter Ctr1. J.Biol. Chem. 2002, 277:4380-4387.
31. Lutsenko S., Barnes N.L., Bartee M.Y., Dmitriev O.Y. Function and regulation of human copper-transporting ATPases. Physiol. Rev. 2007, 87:1011-1046.
32. McKenzie M., Lazarou M., Thorburn D.R., Ryan M.T. Analysis of mitochondrial subunit assembly into respiratory chain complexes using Blue Native polyacrylamide gel electrophoresis. Anal. Biochem. 2007, 364:128-137.
33. Mendelsohn B.A., Yin C., Johnson S.L., Wilm T.P., Solnica-Krezel L., Gitlin J.D. Atp7a determines a hierarchy of copper metabolism essential for notochord development. Cell Metab. 2006, 4:155-162.
34. Mercer J.F., Livingston J., Hall B., Paynter J.A., Begy C., Chandrasekharappa S., Lockhart P., Grimes A., Bhave M., Siemieniak D., et al. Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat. Genet. 1993, 3:20-25.
35. Merchant S.S., Allen M.D., Kropat J., Moseley J.L., Long J.C., Tottey S., Terauchi A.M. Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim. Biophys. Acta 2006, 1763:578-594.
36. Nose Y., Kim B.E., Thiele D.J. Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metab. 2006, 4:235-244.
37. Öhrvik H., Nose Y., Wood L.K., Kim B.E., Gleber S.C., Ralle M., Thiele D.J. Ctr2 regulates biogenesis of a cleaved form of mammalian Ctr1 metal transporter lacking the copper- and cisplatin-binding ecto-domain. Proc. Natl. Acad. Sci. USA 2013, 110:E4279-E4288.
38. Papadopoulou L.C., Sue C.M., Davidson M.M., Tanji K., Nishino I., Sadlock J.E., Krishna S., Walker W., Selby J., Glerum D.M., et al. Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat. Genet. 1999, 23:333-337.
39. Petris M.J., Smith K., Lee J., Thiele D.J. Copper-stimulated endocytosis and degradation of the human copper transporter, hCtr1. J.Biol. Chem. 2003, 278:9639-9646.
40. Postic C., Shiota M., Niswender K.D., Jetton T.L., Chen Y., Moates J.M., Shelton K.D., Lindner J., Cherrington A.D., Magnuson M.A. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J.Biol. Chem. 1999, 274:305-315.
41. Potting C., Tatsuta T., König T., Haag M., Wai T., Aaltonen M.J., Langer T. TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid. Cell Metab. 2013, 18:287-295.
42. Puig S., Lee J., Lau M., Thiele D.J. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J.Biol. Chem. 2002, 277:26021-26030.
43. Sasarman F., Brunel-Guitton C., Antonicka H., Wai T., Shoubridge E.A. LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol. Biol. Cell 2010, 21:1315-1323. LSFC Consortium.
44. Sato M., Gitlin J.D. Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J.Biol. Chem. 1991, 266:5128-5134.
45. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
46. Stiburek L., Vesela K., Hansikova H., Hulkova H., Zeman J. Loss of function of Sco1 and its interaction with cytochrome c oxidase. Am. J. Physiol. Cell Physiol. 2009, 296:C1218-C1226.
47. Turski M.L., Thiele D.J. New roles for copper metabolism in cell proliferation, signaling, and disease. J.Biol. Chem. 2009, 284:717-721.
48. Valnot I., Osmond S., Gigarel N., Mehaye B., Amiel J., Cormier-Daire V., Munnich A., Bonnefont J.P., Rustin P., Rötig A. Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am. J. Hum. Genet. 2000, 67:1104-1109.
49. Vest K.E., Leary S.C., Winge D.R., Cobine P.A. Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J.Biol. Chem. 2013, 288:23884-23892.
50. Viscomi C., Bottani E., Civiletto G., Cerutti R., Moggio M., Fagiolari G., Schon E.A., Lamperti C., Zeviani M. Invivo correction of COX deficiency by activation of the AMPK/PGC-1α axis. Cell Metab. 2011, 14:80-90.
51. 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.
52. Wernimont A.K., Huffman D.L., Lamb A.L., O'Halloran T.V., Rosenzweig A.C. Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat. Struct. Biol. 2000, 7:766-771.
53. White C., Kambe T., Fulcher Y.G., Sachdev S.W., Bush A.I., Fritsche K., Lee J., Quinn T.P., Petris M.J. Copper transport into the secretory pathway is regulated by oxygen in macrophages. J.Cell Sci. 2009, 122:1315-1321.
54. Yamaguchi Y., Heiny M.E., Gitlin J.D. Isolation and characterization of a human liver cDNA as a candidate gene for Wilson disease. Biochem. Biophys. Res. Commun. 1993, 197:271-277.
55. Yang H., Brosel S., Acin-Perez R., Slavkovich V., Nishino I., Khan R., Goldberg I.J., Graziano J., Manfredi G., Schon E.A. Analysis of mouse models of cytochrome c oxidase deficiency owing to mutations in Sco2. Hum. Mol. Genet. 2010, 19:170-180.