The activity of Menkes disease protein ATP7A is essential for redox balance in mitochondria

Journal of Biological Chemistry

Volumn 291, Issue 32, 2016, Pages 16644-16658

  Bhattacharjee, Ashima ^a,e   Yang, Haojun ^a   Duffy, Megan ^b   Robinson, Emily ^b,f   Conrad Antoville, Arianrhod ^b   Lu, Ya Wen ^a   Capps, Tony ^b   Braiterman, Lelita ^a   Wolfgang, Michael ^a   Murphy, Michael P ^c   Yi, Ling ^d   Kaler, Stephen G ^d   Lutsenko, Svetlana ^a   Ralle, Martina ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e UNIVERSITY OF CALCUTTA   (India)

^f AbSci LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; COPPER; CYTOLOGY; MAMMALS; OXIDATION; PATHOLOGY; PEPTIDES;

CELL SENSITIVITY; COPPER HOMEOSTASIS; COPPER TRANSPORT; QUANTITATIVE IMAGING; REDOX BALANCES; RENAL EPITHELIA; RESPIRATORY COMPLEX; SECRETORY PATHWAYS;

MITOCHONDRIA;

HYDROGEN PEROXIDE; MENKES PROTEIN; ADENOSINE TRIPHOSPHATASE; ATP7A PROTEIN, HUMAN; ATP7A PROTEIN, MOUSE; CATION TRANSPORT PROTEIN; COPPER;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME LOCALIZATION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; 3T3-L1 CELL LINE; ACTIVE TRANSPORT; ANIMAL; ENZYMOLOGY; FIBROBLAST; GENETICS; MENKES SYNDROME; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; TRANSFORMED CELL LINE;

3T3-L1 CELLS; ADENOSINE TRIPHOSPHATASES; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CATION TRANSPORT PROTEINS; CELL LINE, TRANSFORMED; COPPER; FIBROBLASTS; HUMANS; HYDROGEN PEROXIDE; MENKES KINKY HAIR SYNDROME; MICE; MITOCHONDRIA; OXIDATION-REDUCTION;

EID: 84982812274     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.727248     Document Type: Article

References (52)

1. Menkes, J. H., Alter, M., Steigleder, G. K., Weakley, D. R., and Sung, J. H. (1962) A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29, 764-779
2. Vulpe, C., Levinson, B., Whitney, S., Packman, S., and Gitschier, J. (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat. Genet. 3, 7-13
3. Maryon, E. B., Molloy, S. A., and Kaplan, J. H. (2013) Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1. Am. J. Physiol. Cell Physiol. 304, C768-779
4. Kaler, S. G. (2011) ATP7A-related copper transport diseases: emerging concepts and future trends. Nat. Rev. Neurol. 7, 15-29
5. Grimes, A., Hearn, C. J., Lockhart, P., Newgreen, D. F., and Mercer, J. F. (1997) Molecular basis of the brindled mouse mutant (Mo(br)): a murine model of Menkes disease. Hum. Mol. Genet. 6, 1037-1042
6. La Fontaine, S., Theophilos, M. B., Firth, S. D., Gould, R., Parton, R. G., and Mercer, J. F. (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, 361-370
7. Mercer, J. F., Grimes, A., Ambrosini, L., Lockhart, P., Paynter, J. A., Dierick, H., and Glover, T. W. (1994) Mutations in the murine homologue of the Menkes gene in dappled and blotchy mice. Nat. Genet. 6, 374-378
8. Hodgkinson, V. L., Dale, J. M., Garcia, M. L., Weisman, G. A., Lee, J., Gitlin, J. D., and Petris, M. J. (2015) X-linked spinal muscular atrophy in mice caused by autonomous loss of ATP7A in the motor neuron. J. Pathol. 236, 241-250
9. La Fontaine, S., Ackland, M. L., and Mercer, J. F. (2010) Mammalian copper-transporting P-type ATPases, ATP7A and ATP7B: emerging roles. Int. J. Biochem. Cell Biol. 42, 206-209
10. Liu, P. C., Chen, Y. W., Centeno, J. A., Quezado, M., Lem, K., and Kaler, S. G. (2005) Downregulation of myelination, energy, and translational genes in Menkes disease brain. Mol. Genet. Metab. 85, 291-300
11. Lenartowicz, M., Sasuła, K., and Zawadowska, B. (2001) Alterations in kidney morphology in mice with mosaic mutation. Folia Histochem. Cytobiol. 39, 275-281
12. Kodama, H., Sato, E., Gu, Y. H., Shiga, K., Fujisawa, C., and Kozuma, T. (2005) Effect of copper and diethyldithiocarbamate combination therapy on the macular mouse, an animal model of Menkes disease. J. Inherit. Metab. Dis. 28, 971-978
13. Lenartowicz, M., Windak, R., Tylko, G., Kowal, M., and Styrna, J. (2010) Effects of copper supplementation on the structure and content of elements in kidneys of mosaic mutant mice. Biol. Trace Elem. Res. 136, 204-220
14. Nomura, S., Nozaki, S., Hamazaki, T., Takeda, T., Ninomiya, E., Kudo, S., Hayashinaka, E., Wada, Y., Hiroki, T., Fujisawa, C., Kodama, H., Shintaku, H., and Watanabe, Y. (2014) PET imaging analysis with 64Cu in disulfiram treatment for aberrant copper biodistribution in Menkes disease mouse model. J. Nucl. Med. 55, 845-851
15. Du, T., La Fontaine, S. L., Abdo, M., Bellingham, S. A., Greenough, M., Volitakis, I., Cherny, R. A., Bush, A. I., Hudson, P. J., Camakaris, J., Mercer, J. F., Crouch, P. J., Masters, C. L., Perreau, V. M., and White, A. R. (2008) Investigating copper-regulated protein expression in Menkes fibroblasts using antibody microarrays. Proteomics 8, 1819-1831
16. Leary, S. C., Cobine, P. A., Nishimura, T., Verdijk, R. M., de Krijger, R., de Coo, R., Tarnopolsky, M. A., Winge, D. R., and Shoubridge, E. A. (2013) COX19 mediates the transduction of a mitochondrial redox signal from SCO1 that regulates ATP7A-mediated cellular copper efflux. Mol. Biol. Cell 24, 683-691
17. Guo, Y., Nyasae, L., Braiterman, L. T., and Hubbard, A. L. (2005) NH2-terminal signals in ATP7B Cu-ATPase mediate its Cu-dependent anterograde traffic in polarized hepatic cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G904-916
18. Kaler, S. G., Buist, N. R., Holmes, C. S., Goldstein, D. S., Miller, R. C., and Gahl, W. A. (1995) Early copper therapy in classic Menkes disease patients with a novel splicing mutation. Ann. Neurol. 38, 921-928
19. Kaler, S. G., Das, S., Levinson, B., Goldstein, D. S., Holmes, C. S., Patronas, N. J., Packman, S., and Gahl, W. A. (1996) Successful early copper therapy in Menkes disease associated with a mutant transcript containing a small in-frame deletion. Biochem. Mol. Med. 57, 37-46
20. Vogt, S. (2003) Maps: a set of software tools for analysis and visualization of 3D x-ray fluorescent datasets. Journal de Physique IV 104, 635-638
21. Gutscher, M., Pauleau, A. L., Marty, L., Brach, T., Wabnitz, G. H., Samstag, Y., Meyer, A. J., and Dick, T. P. (2008) Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553-559
22. Malinouski, M., Zhou, Y., Belousov, V. V., Hatfield, D. L., and Gladyshev, V. N. (2011) Hydrogen peroxide probes directed to different cellular compartments. PLoS ONE 6, e14564
23. Anderson, M. E. (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 113, 548-555
24. Watson, W. H., Pohl, J., Montfort, W. R., Stuchlik, O., Reed, M. S., Powis, G., and Jones, D. P. (2003) Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J. Biol. Chem. 278, 33408-33415
25. Bersani, N. A., Merwin, J. R., Lopez, N. I., Pearson, G. D., and Merrill, G. F. (2002) Protein electrophoretic mobility shift assay to monitor redox state of thioredoxin in cells. Methods Enzymol. 347, 317-326
26. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., and Church, G. M. (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826
27. Rodriguez, S., and Wolfgang, M. J. (2012) Targeted chemical-genetic regulation of protein stability in vivo. Chem. Biol. 19, 391-398
28. Goka, T. J., Stevenson, R. E., Hefferan, P. M., and Howell, R. R. (1976) Menkes disease: a biochemical abnormality in cultured human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 73, 604-606
29. Royce, P. M., Camakaris, J., and Danks, D. M. (1980) Reduced lysyl oxidase activity in skin fibroblasts from patients with Menkes' syndrome. Biochem. J. 192, 579-586
30. Ralle, M., Huster, D., Vogt, S., Schirrmeister, W., Burkhead, J. L., Capps, T. R., Gray, L., Lai, B., Maryon, E., and Lutsenko, S. (2010) Wilson disease at a single cell level: intracellular copper trafficking activates compartment-specific responses in hepatocytes. J. Biol. Chem. 285, 30875-30883
31. Holmgren, A., Johansson, C., Berndt, C., Lönn, M. E., Hudemann, C., and Lillig, C. H. (2005) Thiol redox control via thioredoxin and glutaredoxin systems. Biochem. Soc. Trans. 33, 1375-1377
32. Jones, D. P. (2006) Disruption of mitochondrial redox circuitry in oxidative stress. Chem. Biol. Interact. 163, 38-53
33. Rota, C., Chignell, C. F., and Mason, R. P. (1999) Evidence for free radical formation during the oxidation of 2′-7′-dichlorofluorescin to the fluorescent dye 2′-7′-dichlorofluorescein by horseradish peroxidase: possible implications for oxidative stress measurements. Free Radic. Biol. Med. 27, 873-881
34. 2 with roGFP2-based redox probes. Free Radic. Biol. Med. 51, 1943-1951
35. Cobine, P. A., Pierrel, F., Bestwick, M. L., and Winge, D. R. (2006) Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J. Biol. Chem. 281, 36552-36559
36. Petris, M. J., Strausak, D., and Mercer, J. F. (2000) The Menkes copper transporter is required for the activation of tyrosinase. Hum. Mol. Genet. 9, 2845-2851
37. Gupta, A., Bhattacharjee, A., Dmitriev, O. Y., Nokhrin, S., Braiterman, L., Hubbard, A. L., and Lutsenko, S. (2011) Cellular copper levels determine the phenotype of the Arg875 variant of ATP7B/Wilson disease protein. Proc. Natl. Acad. Sci. U.S.A. 108, 5390-5395
38. Schushan, M., Bhattacharjee, A., Ben-Tal, N., and Lutsenko, S. (2012) A structural model of the copper ATPase ATP7B to facilitate analysis of Wilson disease-causing mutations and studies of the transport mechanism. Metallomics 4, 669-678
39. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V., and Lukyanov, S. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281-286
40. Marthandan, S., Murphy, M. P., Billett, E., and Barnett, Y. (2011) An investigation of the effects of MitoQ on human peripheral mononuclear cells. Free Radic. Res. 45, 351-358
41. Pletjushkina, O. Y., Fetisova, E. K., Lyamzaev, K. G., Ivanova, O. Y., Domnina, L. V., Vyssokikh, M. Y., Pustovidko, A. V., Alexeevski, A. V., Alexeevski, D. A., Vasiliev, J. M., Murphy, M. P., Chernyak, B. V., and Skulachev, V. P. (2006) Hydrogen peroxide produced inside mitochondria takes part in cell-to-cell transmission of apoptotic signal. Biochemistry Biokhimiia 71, 60-67
42. Kelso, G. F., Porteous, C. M., Coulter, C. V., Hughes, G., Porteous, W. K., Ledgerwood, E. C., Smith, R. A., and Murphy, M. P. (2001) Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J. Biol. Chem. 276, 4588-4596
43. Williams, T. D., Diab, A., Ortega, F., Sabine, V. S., Godfrey, R. E., Falciani, F., Chipman, J. K., and George, S. G. (2008) Transcriptomic responses of European flounder (Platichthys flesus) to model toxicants. Aquat. Toxicol. 90, 83-91
44. Hamilton, J. P., Koganti, L., Muchenditsi, A., Pendyala, V. S., Huso, D., Hankin, J., Murphy, R. C., Huster, D., Merle, U., Mangels, C., Yang, N., Potter, J. J., Mezey, E., and Lutsenko, S. (2016) Activation of LXR/RXR pathway ameliorates liver disease in atp7b (Wilson disease) mice. Hepatology 63, 1828-1841
45. Wooton-Kee, C. R., Jain, A. K., Wagner, M., Grusak, M. A., Finegold, M. J., Lutsenko, S., and Moore, D. D. (2015) Elevated copper impairs hepatic nuclear receptor function in Wilson's disease. J. Clin. Invest. 125, 3449-3460
46. Burkhead, J. L., Ralle, M., Wilmarth, P., David, L., and Lutsenko, S. (2011) Elevated copper remodels hepatic RNA processing machinery in the mouse model of Wilson's disease. J. Mol. Biol. 406, 44-58
47. -/- mouse model of Wilson's disease. Metallomics 4, 660-668
48. Roberts, E. A., Robinson, B. H., and 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, 54-65
49. Medici, V., Shibata, N. M., Kharbanda, K. K., Islam, M. S., Keen, C. L., Kim, K., Tillman, B., French, S. W., Halsted, C. H., and LaSalle, J. M. (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, 286-296
50. Huster, D., Purnat, T. D., Burkhead, J. L., Ralle, M., Fiehn, O., Stuckert, F., Olson, N. E., Teupser, D., and Lutsenko, S. (2007) High copper selectively alters lipid metabolism and cell cycle machinery in the mouse model of Wilson disease. J. Biol. Chem. 282, 8343-8355
51. 2+ toxicity inhibition of mitochondrial dehydrogenases in vitro and in vivo. Ann. Neurol. 55, 645-653
52. Zischka, H., Lichtmannegger, J., Schmitt, S., Jägemann, N., Schulz, S., Wartini, D., Jennen, L., Rust, C., Larochette, N., Galluzzi, L., Chajes, V., Bandow, N., Gilles, V. S., DiSpirito, A. A., Esposito, I., et al. (2011) Liver mitochondrial membrane crosslinking and destruction in a rat model of Wilson disease. J. Clin. Invest. 121, 1508-1518