An expanding range of functions for the copper chaperone/antioxidant protein atox1

Antioxidants and Redox Signaling

Volumn 19, Issue 9, 2013, Pages 945-957

  Hatori, Yuta ^a   Lutsenko, Svetlana ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COPPER; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; GLUTATHIONE; PEROXIREDOXIN 3;

BINDING SITE; CATALYSIS; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); HOMEOSTASIS; HUMAN; METAL BINDING; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ALIGNMENT; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTIOXIDANTS; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; COPPER; HUMANS; METALLOCHAPERONES; OXIDATION-REDUCTION;

EID: 84883391469     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.5086     Document Type: Review

References (101)

1. Allen KG, Arthur JR, Morrice PC, Nicol F, and Mills CF. Copper deficiency and tissue glutathione concentration in the rat. Proc Soc Exp Biol Med 187: 38-43, 1988.
2. Alvarez HM, Xue Y, Robinson CD, Canalizo-Hernandez MA, Marvin RG, Kelly RA, Mondragon A, Penner-Hahn JE, and O'Halloran TV. Tetrathiomolybdate inhibits copper trafficking proteins through metal cluster formation. Science 327: 331-334, 2010.
3. Anastassopoulou I, Banci L, Bertini I, Cantini F, Katsari E, and Rosato A. Solution structure of the apo and copper(I)-loaded human metallochaperone HAH1. Biochemistry 43: 13046-13053, 2004.
4. Arnesano F, Banci L, Bertini I, Cantini F, Ciofi-Baffoni S, Huffman DL, and O'Halloran TV. Characterization of the binding interface between the copper chaperone Atx1 and the first cytosolic domain of Ccc2 ATPase. J Biol Chem 276: 41365-41376, 2001.
5. Arnesano F, Banci L, Bertini I, Felli IC, Losacco M, and Natile G. Probing the interaction of cisplatin with the human copper chaperone Atox1 by solution and in-cell NMR spectroscopy. J Am Chem Soc 133: 18361-18369, 2011.
6. Arnesano F, Banci L, Bertini I, Huffman DL, and O'Halloran TV. Solution structure of the Cu(I) and apo forms of the yeast metallochaperone, Atx1. Biochemistry 40: 1528-1539, 2001.
7. Badarau A and Dennison C. Copper trafficking mechanism of CXXC-containing domains: insight from the pHdependence of their Cu(I) affinities. J Am Chem Soc 133: 2983-2988, 2011.
8. Banci L, Bertini I, Cantini F, Felli IC, Gonnelli L, Hadjiliadis N, Pierattelli R, Rosato A, and Voulgaris P. The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nat Chem Biol 2: 367-368, 2006.
9. Banci L, Bertini I, Ciofi-Baffoni S, Hadjiloi T, Martinelli M, and Palumaa P. Mitochondrial copper(I) transfer from Cox17 to Sco1 is coupled to electron transfer. Proc Natl Acad Sci USA 105: 6803-6808, 2008.
10. Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, and Palumaa P. Affinity gradients drive copper to cellular destinations. Nature 465: 645-648, 2010.
11. Barry AN, Otoikhian A, Bhatt S, Shinde U, Tsivkovskii R, Blackburn NJ, and Lutsenko S. The lumenal loop Met672-Pro707 of copper-transporting ATPase ATP7A binds metals and facilitates copper release from the intramembrane sites. J Biol Chem 286: 26585-26594, 2011.
12. Beeder J, Nilsen RK, Rosnes JT, Torsvik T, and Lien T. Archaeoglobus fulgidus isolated from hot north sea oil field waters. Appl Environ Microbiol 60: 1227-1231, 1994.
13. Boal AK and Rosenzweig AC. Crystal structures of cisplatin bound to a human copper chaperone. J Am Chem Soc 131: 14196-14197, 2009.
14. Carafoli E, Garcia-Martin E, and Guerini D. The plasma membrane calcium pump: recent developments and future perspectives. Experientia 52: 1091-1100, 1996.
15. Carr HS, George GN, and Winge DR. Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J Biol Chem 277: 31237-31242, 2002.
16. Chen Y, Saari JT, and Kang YJ. Expression of gammaglutamylcysteine synthetase in the liver of copper-deficient rats. Proc Soc for Exp BiolMed Soc Exp Biol Med 210: 102-106, 1995.
17. Culotta VC, Klomp LW, Strain J, Casareno RL, Krems B, and Gitlin JD. The copper chaperone for superoxide dismutase. J Biol Chem 272: 23469-23472, 1997.
18. El Meskini R, Cline LB, Eipper BA, and Ronnett GV. The developmentally regulated expression of Menkes protein ATP7A suggests a role in axon extension and synaptogenesis. Dev Neurosci 27: 333-348, 2005.
19. Field LS, Luk E, and Culotta VC. Copper chaperones: personal escorts for metal ions. J Bioenerg Biomembr 34: 373-379, 2002.
20. Filomeni G and Ciriolo MR. Redox control of apoptosis: an update. Antioxid Redox Signal 8: 2187-2192, 2006.
21. Forman-Kay JD, Clore GM, and Gronenborn AM. Relationship between electrostatics and redox function in human thioredoxin: characterization of pH titration shifts using two-dimensional homo-and heteronuclear NMR. Biochemistry 31: 3442-3452, 1992.
22. Glerum DM, Shtanko A, and Tzagoloff A. SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J Biol Chem 271: 20531-20535, 1996.
23. Gonzalez-Guerrero M and Arguello JM. Mechanism of Cu +-transporting ATPases: soluble Cu + chaperones directly transfer Cu + to transmembrane transport sites. Proc Natl Acad Sci USA 105: 5992-5997, 2008.
24. Gonzalez-Guerrero M, Eren E, Rawat S, Stemmler TL, and Arguello JM. Structure of the two transmembrane Cu + transport sites of the Cu +-ATPases. J Biol Chem 283: 29753-29759, 2008.
25. Gonzalez-Guerrero M, Hong D, and Arguello JM. Chaperonemediated Cu+ delivery to Cu+ transport ATPases: requirement of nucleotide binding. J Biol Chem284: 20804-20811, 2009.
26. Goulet AC, Watts G, Lord JL, and Nelson MA. Profiling of selenomethionine responsive genes in colon cancer by microarray analysis. Cancer Biol Ther 6: 494-503, 2007.
27. Gourdon P, Liu XY, Skjorringe T, Morth JP, Moller LB, Pedersen BP, and Nissen P. Crystal structure of a coppertransporting PIB-type ATPase. Nature 475: 59-64, 2011.
28. Halliwell B and Gutteridge JM. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186: 1-85, 1990.
29. HamzaI,FaisstA,ProhaskaJ,ChenJ,GrussP,andGitlinJD.The metallochaperone Atox1 plays a critical role in perinatal copper homeostasis. Proc Natl Acad Sci USA 98: 6848-6852, 2001.
30. Hatori Y, Clasen S, Hasan NM, Barry AN, and Lutsenko S. Functional partnership of the copper export machinery and glutathione balance in human cells. J Biol Chem, 2012.
31. Hirota Y, Acar N, Tranguch S, Burnum KE, Xie H, Kodama A, Osuga Y, Ustunel I, Friedman DB, Caprioli RM, Daikoku T, and Dey SK. Uterine FK506-binding protein 52 (FKBP52)-peroxiredoxin-6 (PRDX6) signaling protects pregnancy from overt oxidative stress. Proc Natl Acad Sci USA 107: 15577-15582, 2010.
32. Horng YC, Cobine PA, Maxfield AB, Carr HS, and Winge DR. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J Biol Chem 279: 35334-35340, 2004.
33. Horng YC, Leary SC, Cobine PA, Young FB, George GN, Shoubridge EA, and Winge DR. Human Sco1 and Sco2 function as copper-binding proteins. J Biol Chem 280: 34113-34122, 2005.
34. Hua H, Gunther V, Georgiev O, and Schaffner W. Distorted copper homeostasis with decreased sensitivity to cisplatin upon chaperone Atox1 deletion in Drosophila. Biometals 24: 445-453, 2011.
35. Huffman DL and O'Halloran TV. Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J Biol Chem 275: 18611-18614, 2000.
36. Hung IH, Casareno RL, Labesse G, Mathews FS, and Gitlin JD. HAH1 is a copper-binding protein with distinct amino acid residues mediating copper homeostasis and antioxidant defense. J Biol Chem 273: 1749-1754, 1998.
37. Hussain F, Olson JS, and Wittung-Stafshede P. Conserved residues modulate copper release in human copper chaperone Atox1. Proc Natl Acad Sci USA 105: 11158-11163, 2008.
38. Hussain F, Rodriguez-Granillo A, and Wittung-Stafshede P. Lysine-60 in copper chaperone Atox1 plays an essential role in adduct formation with a target Wilson disease domain. J Am Chem Soc 131: 16371-16373, 2009.
39. Huster D and Lutsenko S. The distinct roles of the N-terminal copper-binding sites in regulation of catalytic activity of the Wilson's disease protein. J Biol Chem 278: 32212-32218, 2003.
40. Itoh S, Kim HW, Nakagawa O, Ozumi K, Lessner SM, Aoki H, Akram K, McKinney RD, Ushio-Fukai M, and Fukai T. Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation. J Biol Chem 283: 9157-9167, 2008.
41. Itoh S, Ozumi K, Kim HW, Nakagawa O, McKinney RD, Folz RJ, Zelko IN, Ushio-Fukai M, and Fukai T. Novel mechanism for regulation of extracellular SOD transcription and activity by copper: role of antioxidant-1. Free Radic Biol Med 46: 95-104, 2009.
42. Jeney V, Itoh S, Wendt M, Gradek Q, Ushio-Fukai M, Harrison DG, and Fukai T. Role of antioxidant-1 in extracellular superoxide dismutase function and expression. Circ Res 96: 723-729, 2005.
43. Jensen LT and Culotta VC. Activation of CuZn superoxide dismutases from Caenorhabditis elegans does not require the copper chaperone CCS. J Biol Chem 280: 41373-41379, 2005.
44. Jordan A, Aslund F, Pontis E, Reichard P, and Holmgren A. Characterization of Escherichia coli NrdH. A glutaredoxinlike protein with a thioredoxin-like activity profile. J Biol Chem 272: 18044-18050, 1997.
45. Katano K, Kondo A, Safaei R, Holzer A, Samimi G, Mishima M, Kuo YM, Rochdi M, and Howell SB. Acquisition of resistance to cisplatin is accompanied by changes in the cellular pharmacology of copper. Cancer Res 62: 6559-6565, 2002.
46. Kelner GS, Lee M, Clark ME, Maciejewski D, McGrath D, Rabizadeh S, Lyons T, Bredesen D, Jenner P, and Maki RA. The copper transport protein Atox1 promotes neuronal survival. J Biol Chem 275: 580-584, 2000.
47. Kirlin WG, Cai J, Thompson SA, Diaz D, Kavanagh TJ, and Jones DP. Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic Biol Med 27: 1208-1218, 1999.
48. Korte JJ and Prohaska JR. Dietary copper deficiency alters protein and lipid composition of murine lymphocyte plasma membranes. J Nutr 117: 1076-1084, 1987.
49. Krummeck G and Rodel G. Yeast SCO1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II. Curr Genet 18: 13-15, 1990.
50. Kumar C, Igbaria A, D'Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, and Toledano MB. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 30: 2044-2056, 2011.
51. Lamb AL, Wernimont AK, Pufahl RA, Culotta VC, O'Halloran TV, and Rosenzweig AC. Crystal structure of the copper chaperone for superoxide dismutase. Nat Struct Biol 6: 724-729, 1999.
52. Lassi KC and Prohaska JR. Erythrocyte copper chaperone for superoxide dismutase is increased following marginal copper deficiency in adult and postweanling mice. J Nutr 142: 292-297, 2012.
53. Lassi KC and Prohaska JR. Rapid alteration in rat red blood cell copper chaperone for superoxide dismutase after marginal copper deficiency and repletion. Nutr Res 31: 698-706, 2011.
54. Leary SC. Redox regulation of SCO protein function: controlling copper at a mitochondrial crossroad. Antioxid Redox Signal 13: 1403-1416, 2010.
55. Leitch JM, Jensen LT, Bouldin SD, Outten CE, Hart PJ, and Culotta VC. Activation of Cu,Zn-superoxide dismutase in the absence of oxygen and the copper chaperone CCS. J Biol Chem 284: 21863-21871, 2009.
56. Lim CM, Cater MA, Mercer JF, and La Fontaine S. Copperdependent interaction of glutaredoxin with the N termini of the copper-ATPases (ATP7A and ATP7B) defective in Menkes and Wilson diseases. Biochem Biophys Res Commun 348: 428-436, 2006.
57. Lin SJ and Culotta VC. The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity. Proc Natl Acad Sci USA 92: 3784-3788, 1995.
58. Lin SJ, Pufahl RA, Dancis A, O'Halloran TV, and Culotta VC. A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J Biol Chem 272: 9215-9220, 1997.
59. Lockhart PJ and Mercer JF. Identification of the copper chaperone SAH in Ovis aries: expression analysis and in vitro interaction of SAH with ATP7B. Biochim Biophys Acta 1490: 11-20, 2000.
60. Mandal AK, Cheung WD, and Arguello JM. Characterization of a thermophilic P-type Ag +/Cu +-ATPase from the extremophile Archaeoglobus fulgidus. J Biol Chem 277: 7201-7208, 2002.
61. Marcil V, Lavoie JC, Emonnot L, Seidman E, and Levy E. Analysis of the effects of iron and vitamin C cosupplementation on oxidative damage, antioxidant response and inflammation in THP-1 macrophages. Clin Biochem 44: 873-883, 2011.
62. McRae R, Lai B, and Fahrni CJ. Copper redistribution in Atox1-deficient mouse fibroblast cells. J Biol Inorg Chem 15: 99-105, 2010.
63. Miyayama T, Suzuki KT, and Ogra Y. Copper accumulation and compartmentalization in mouse fibroblast lacking metallothionein and copper chaperone, Atox1. Toxicol Appl Pharmacol 237: 205-213, 2009.
64. Morin I, Gudin S, Mintz E, and Cuillel M. Dissecting the role of the N-terminal metal-binding domains in activating the yeast copper ATPase in vivo. FEBS J 276: 4483-4495, 2009.
65. Muller PA and Klomp LW. ATOX1: a novel copperresponsive transcription factor in mammals Int J Biochem Cell Biol 41: 1233-1236, 2009.
66. Naeve GS, Vana AM, Eggold JR, Kelner GS, Maki R, Desouza EB, and Foster AC. Expression profile of the copper homeostasis gene, rAtox1, in the rat brain. Neuroscience 93: 1179-1187, 1999.
67. Neave MJ, Streten-Joyce C, Nouwens AS, Glasby CJ, McGuinness KA, Parry DL, and Gibb KS. The transcriptome and proteome are altered in marine polychaetes (Annelida) exposed to elevated metal levels. J Proteomics 75: 2721-2735, 2012.
68. Nittis T, George GN, and Winge DR. Yeast Sco1, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J Biol Chem 276: 42520-42526, 2001.
69. Nkabyo YS, Ziegler TR, Gu LH, Watson WH, and Jones DP. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am J Physiol Gastrointest Liver Physiol 283: G1352-G1359, 2002.
70. O'Halloran TV and Culotta VC. Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275: 25057-25060, 2000.
71. O'Neil KT and DeGrado WF. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250: 646-651, 1990.
72. Ozumi K, Sudhahar V, Kim HW, Chen GF, Kohno T, Finney L, Vogt S, McKinney RD, Ushio-Fukai M, and Fukai T. Role of copper transport protein antioxidant 1 in angiotensin ii-induced hypertension: a key regulator of extracellular superoxide dismutase. Hypertension 60: 476-486, 2012.
73. Palm ME, Weise CF, Lundin C, Wingsle G, Nygren Y, Bjorn E, Naredi P, Wolf-Watz M, and Wittung-Stafshede P. Cisplatin binds human copper chaperone Atox1 and promotes unfolding in vitro. Proc Natl Acad Sci USA 108: 6951-6956, 2011.
74. Portnoy ME, Rosenzweig AC, Rae T, Huffman DL, O'Halloran TV, and Culotta VC. Structure-function analyses of the ATX1 metallochaperone. J Biol Chem 274: 15041-15045, 1999.
75. Prohaska JR and Brokate B. Copper deficiency alters rat dopamine beta-monooxygenase mRNA and activity. J Nutr 129: 2147-2153, 1999.
76. Prohaska JR and Brokate B. Dietary copper deficiency alters protein levels of rat dopamine beta-monooxygenase and tyrosine monooxygenase. Exp Biol Med (Maywood) 226: 199-207, 2001.
77. Prohaska JR and Lukasewycz OA. Copper deficiency during perinatal development: effects on the immune response of mice. J Nutr 119: 922-931, 1989.
78. Ralle M, Lutsenko S, and Blackburn NJ. X-ray absorption spectroscopy of the copper chaperone HAH1 reveals a linear two-coordinate Cu(I) center capable of adduct formation with exogenous thiols and phosphines. J Biol Chem 278: 23163-23170, 2003.
79. Rodriguez-Granillo A and Wittung-Stafshede P. Structure and dynamics of Cu(I) binding in copper chaperones Atox1 and CopZ: a computer simulation study. J Phys Chem B 112: 4583-4593, 2008.
80. Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, and Herrero E. Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121, 2002.
81. Rosenzweig AC, Huffman DL, Hou MY, Wernimont AK, Pufahl RA, and O'Halloran TV. Crystal structure of the Atx1 metallochaperone protein at 1.02A resolution. Structure 7: 605-617, 1999.
82. Saari JT. Copper deficiency and cardiovascular disease: role of peroxidation, glycation, and nitration. Can J Physiol Pharmacol 78: 848-855, 2000.
83. Safaei R, Maktabi MH, Blair BG, Larson CA, and Howell SB. Effects of the loss of Atox1 on the cellular pharmacology of cisplatin. J Inorg Biochem 103: 333-341, 2009.
84. Sanokawa-Akakura R, Cao W, Allan K, Patel K, Ganesh A, Heiman G, Burke R, Kemp FW, Bogden JD, Camakaris J, Birge RB, and Konsolaki M. Control of Alzheimer's amyloid beta toxicity by the high molecular weight immunophilin FKBP52 and copper homeostasis in Drosophila. PLoS One 5: e8626, 2010.
85. Sanokawa-Akakura R, Dai H, Akakura S, Weinstein D, Fajardo JE, Lang SE, Wadsworth S, Siekierka J, and Birge RB. A novel role for the immunophilin FKBP52 in copper transport. J Biol Chem 279: 27845-27848, 2004.
86. Satoh T, Sakai N, Enokido Y, Uchiyama Y, and Hatanaka H. Survival factor-insensitive generation of reactive oxygen species induced by serum deprivation in neuronal cells. Brain Res 733: 9-14, 1996.
87. Schmidt PJ, Kunst C, and Culotta VC. Copper activation of superoxide dismutase 1 (SOD1) in vivo. Role for proteinprotein interactions with the copper chaperone for SOD1. J Biol Chem 275: 33771-33776, 2000.
88. Schmidt PJ, Rae TD, Pufahl RA, Hamma T, Strain J, O'Halloran TV, and Culotta VC. Multiple protein domains contribute to the action of the copper chaperone for superoxide dismutase. J Biol Chem 274: 23719-23725, 1999.
89. Singleton WC, McInnes KT, Cater MA, Winnall WR, McKirdy R, Yu Y, Taylor PE, Ke BX, Richardson DR, Mercer JF, and La Fontaine S. Role of glutaredoxin1 and glutathione in regulating the activity of the coppertransporting P-type ATPases, ATP7A and ATP7B. J Biol Chem 285: 27111-27121, 2010.
90. Southon A, Burke R, Norgate M, Batterham P, and Camakaris J. Copper homoeostasis in Drosophila melanogaster S2 cells. Biochem J 383: 303-309, 2004.
91. Thompson JD, Higgins DG, and Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680, 1994.
92. Tiffany-Castiglioni E, Hong S, and Qian Y. Copper handling by astrocytes: insights into neurodegenerative diseases. Int J Dev Neurosci 29: 811-818, 2011.
93. Tottey S, Patterson CJ, Banci L, Bertini I, Felli IC, Pavelkova A, Dainty SJ, Pernil R, Waldron KJ, Foster AW, and Robinson NJ. Cyanobacterial metallochaperone inhibits deleterious side reactions of copper. Proc Natl Acad Sci USA 109: 95-100, 2012.
94. Wakabayashi T, Nakamura N, Sambongi Y, Wada Y, Oka T, and Futai M. Identification of the copper chaperone, CUC-1, in Caenorhabditis elegans: tissue specific co-expression with the copper transporting ATPase, CUA-1. FEBS Lett 440: 141-146, 1998.
95. Walker JM, Huster D, Ralle M, Morgan CT, Blackburn NJ, and Lutsenko S. The N-terminal metal-binding site 2 of the Wilson's disease protein plays a key role in the transfer of copper from Atox1. J Biol Chem 279: 15376-15384, 2004.
96. Walker JM, Tsivkovskii R, and 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 277: 27953-27959, 2002.
97. Wernimont AK, Huffman DL, Lamb AL, O'Halloran TV, and Rosenzweig AC. Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat Struct Biol 7: 766-771, 2000.
98. White C, Kambe T, Fulcher YG, Sachdev SW, Bush AI, Fritsche K, Lee J, Quinn TP, and Petris MJ. Copper transport into the secretory pathway is regulated by oxygen in macrophages. J Cell Sci 122: 1315-1321, 2009.
99. Wimmer R, Herrmann T, Solioz M, and Wuthrich K. NMR structure and metal interactions of the CopZ copper chaperone. J Biol Chem 274: 22597-22603, 1999.
100. Xiao Z, Brose J, Schimo S, Ackland SM, La Fontaine S, and Wedd AG. Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1, and related proteins: detection probes and affinity standards. J Biol Chem 286: 11047-11055, 2011.
101. Yang Y, Mandal AK, Bredeston LM, Gonzalez-Flecha FL, and Arguello JM. Activation of Archaeoglobus fulgidus Cu( + )-ATPase CopA by cysteine. Biochim Biophys Acta 1768: 495-501, 2007.