Communication between the N and C termini is required for copper-stimulated Ser/Thr phosphorylation of Cu(I)-ATPase

Journal of Biological Chemistry

Volumn 290, Issue 14, 2015, Pages 8803-8819

  Braiterman, Lelita T ^a   Gupta, Arnab ^a   Chaerkady, Raghothama ^a   Cole, Robert N ^a   Hubbard, Ann L ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; PHOSPHORYLATION; PLANTS (BOTANY);

C-TERMINAL DOMAINS; CONFORMATIONAL CHANGE; CYTOPLASMIC DOMAINS; HYPERPHOSPHORYLATED; HYPERPHOSPHORYLATION; METAL BINDING DOMAIN; PHOSPHORYLATION SITES; TRANS-GOLGI NETWORK;

COPPER;

COPPER; DIPEPTIDE; PHOSPHOPEPTIDE; SERINE; THREONINE; TRIPEPTIDE; WILSON DISEASE PROTEIN; ADENOSINE TRIPHOSPHATASE; CATION TRANSPORT PROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; LIVER CELL; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; PROTEOMICS; TRANS GOLGI NETWORK; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; CELL LINE; COPPER; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; SERINE; THREONINE;

EID: 84926482899     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.627414     Document Type: Article

References (45)

1. Ferenci, P. (2006) Regional distribution of mutations of the ATP7B gene in patients with Wilson disease: impact on genetic testing. Hum. Genet. 120, 151-159
2. Weiss, K. H., and Stremmel, W. (2012) Evolving perspectives in Wilson disease: diagnosis, treatment and monitoring. Curr. Gastroenterol. Rep. 14, 1-7
3. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046
4. Braiterman, L., Nyasae, L., Guo, Y., Bustos, R., Lutsenko, S., and Hubbard, A. (2009) Apical targeting and Golgi retention signals reside within a 9-amino acid sequence in the copper-ATPase, ATP7B. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G433-G444
5. Braiterman, L., Nyasae, L., Leves, F., and Hubbard, A. L. (2011) Critical roles for the COOH terminus of the Cu-ATPase ATP7B in protein stability, trans-Golgi network retention, copper sensing, and retrograde trafficking. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G69-G81
6. Nyasae, L. K., Schell, M. J., and Hubbard, A. L. (2014) Copper directs ATP7B to the apical domain of hepatic cells via basolateral endosomes. Traffic 15, 1344-1365
7. van den Berghe, P. V., and Klomp, L. W. (2010) Posttranslational regulation of copper transporters. J. Biol. Inorg. Chem. 15, 37-46
8. Polishchuk, R., and Lutsenko, S. (2013) Golgi in copper homeostasis: a view from the membrane trafficking field. Histochem. Cell Biol. 140, 285-295
9. Vanderwerf, S. M., Cooper, M. J., Stetsenko, I. V., and Lutsenko, S. (2001) Copper specifically regulates intracellular phosphorylation of the Wilson's disease protein, a human copper-transporting ATPase. J. Biol. Chem. 276, 36289-36294
10. Vanderwerf, S. M., and Lutsenko, S. (2002) The Wilson's disease protein expressed in Sf9 cells is phosphorylated. Biochem. Soc. Trans. 30, 739-741
11. Pilankatta, R., Lewis, D., Adams, C. M., and Inesi, G. (2009) High yield heterologous expression of wild-type and mutant Cu+-ATPase (ATP7B, Wilson disease protein) for functional characterization of catalytic activity and serine residues undergoing copper-dependent phosphorylation. J. Biol. Chem. 284, 21307-21316
12. Pilankatta, R., Lewis, D., and Inesi, G. (2011) Involvement of protein kinase D in expression and trafficking of ATP7B (copper ATPase). J. Biol. Chem. 286, 7389-7396
13. Hasan, N. M., Gupta, A., Polishchuk, E., Yu, C. H., Polishchuk, R., Dmitriev, O. Y., and Lutsenko, S. (2012) Molecular events initiating exit of a copper-transporting ATPase ATP7B from the trans-Golgi network. J. Biol. Chem. 287, 36041-36050
14. 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
15. Bartee, M. Y., Ralle, M., and Lutsenko, S. (2009) The loop connecting metal-binding domains 3 and 4 of ATP7B is a target of a kinase-mediated phosphorylation. Biochemistry 48, 5573-5581
16. Huttlin, E. L., Jedrychowski, M. P., Elias, J. E., Goswami, T., Rad, R., Beausoleil, S. A., Villén, J., Haas, W., Sowa, M. E., and Gygi, S. P. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189
17. Kettenbach, A. N., Schweppe, D. K., Faherty, B. K., Pechenick, D., Pletnev, A. A., and Gerber, S. A. (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signal. 4, rs5
18. Grimsrud, P. A., Carson, J. J., Hebert, A. S., Hubler, S. L., Niemi, N. M., Bailey, D. J., Jochem, A., Stapleton, D. S., Keller, M. P., Westphall, M. S., Yandell, B. S., Attie, A. D., Coon, J. J., and Pagliarini, D. J. (2012) A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis. Cell Metab. 16, 672-683
19. Wilson-Grady, J. T., Haas, W., and Gygi, S. P. (2013) Quantitative comparison of the fasted and re-fed mouse liver phosphoproteomes using lower pH reductive dimethylation. Methods 61, 277-286
20. Hornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., Latham, V., and Sullivan, M. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-D270
21. Zhou, H., Di Palma, S., Preisinger, C., Peng, M., Polat, A. N., Heck, A. J., and Mohammed, S. (2013) Toward a comprehensive characterization of a human cancer cell phosphoproteome. J. Proteome Res. 12, 260-271
22. Braiterman, L. T., Murthy, A., Jayakanthan, S., Nyasae, L., Tzeng, E., Gromadzka, G., Woolf, T. B., Lutsenko, S., and Hubbard, A. L. (2014) Distinct phenotype of a Wilson disease mutation reveals a novel trafficking determinant in the copper transporter ATP7B. Proc. Natl. Acad. Sci. U.S.A. 111, E1364-E1373
23. 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-G916
24. Hardy, S., Kitamura, M., Harris-Stansil, T., Dai, Y., and Phipps, M. L. (1997) Construction of adenovirus vectors through Cre-lox recombination. J. Virol. 71, 1842-1849
25. Bastaki, M., Braiterman, L. T., Johns, D. C., Chen, Y. H., and Hubbard, A. L. (2002) Absence of direct delivery for single transmembrane apical proteins or their "secretory" forms in polarized hepatic cells. Mol. Biol. Cell 13, 225-237
26. Ihrke, G., Neufeld, E. B., Meads, T., Shanks, M. R., Cassio, D., Laurent, M., Schroer, T. A., Pagano, R. E., and Hubbard, A. L. (1993) WIF-B cells: an in vitro model for studies of hepatocyte polarity. J. Cell Biol. 123, 1761-1775
27. Shevchenko, A., Wilm, M., Vorm, O., Jensen, O. N., Podtelejnikov, A. V., Neubauer, G., Shevchenko, A., Mortensen, P., and Mann, M. (1996) A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem. Soc. Trans. 24, 893-896
28. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
29. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
30. Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A., and Lajoie, G. (2003) PEAKS: powerful software for peptide de novo sequencing by MS/MS. Rapid Commun. Mass Spectrom. 17, 2337-2342
31. Griffiths, G., Fuller, S. D., Back, R., Hollinshead, M., Pfeiffer, S., and Simons, K. (1989) The dynamic nature of the Golgi complex. J. Cell Biol. 108, 277-297
32. Ladinsky, M. S., Wu, C. C., McIntosh, S., McIntosh, J. R., and Howell, K. E. (2002) Structure of the Golgi and distribution of reporter molecules at 20°C reveals the complexity of the exit compartments. Mol. Biol. Cell 13, 2810-2825
33. Huster, D., and Lutsenko, S. (2003) 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
34. Banci, L., Bertini, I., Cantini, F., Rosenzweig, A. C., and Yatsunyk, L. A. (2008) Metal binding domains 3 and 4 of the Wilson disease protein: solution structure and interaction with the copper(I) chaperone HAH1. Biochemistry 47, 7423-7429
35. Tsivkovskii, R., MacArthur, B. C., and Lutsenko, S. (2001) The Lys1010-Lys1325 fragment of the Wilson's disease protein binds nucleotides and interacts with the N-terminal domain of this protein in a copperdependent manner. J. Biol. Chem. 276, 2234-2242
36. Christensen, G. L., Kelstrup, C. D., Lyngsø, C., Sarwar, U., Bøgebo, R., Sheikh, S. P., Gammeltoft, S., Olsen, J. V., and Hansen, J. L. (2010) Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol. Cell. Proteomics 9, 1540-1553
37. Brady, D. C., Crowe, M. S., Turski, M. L., Hobbs, G. A., Yao, X., Chaikuad, A., Knapp, S., Xiao, K., Campbell, S. L., Thiele, D. J., and Counter, C. M. (2014) Copper is required for oncogenic BRAF signalling and tumorigenesis. Nature 509, 492-496
38. Turski, M. L., Brady, D. C., Kim, H. J., Kim, B. E., Nose, Y., Counter, C. M., Winge, D. R., and Thiele, D. J. (2012) A novel role for copper in Ras/mitogen-activated protein kinase signaling. Mol. Cell. Biol. 32, 1284-1295
39. Cater, M. A., La Fontaine, S., and Mercer, J. F. (2007) Copper binding to the N-terminal metal-binding sites or the CPC motif is not essential for copper-induced trafficking of the human Wilson protein (ATP7B). Biochem. J. 401, 143-153
40. Borjigin, J., Payne, A. S., Deng, J., Li, X., Wang, M. M., Ovodenko, B., Gitlin, J. D., and Snyder, S. H. (1999) A novel pineal night-specific ATPase encoded by the Wilson disease gene. J. Neurosci. 19, 1018-1026
41. Baek, J. H., Cerda, O., and Trimmer, J. S. (2011) Mass spectrometry-based phosphoproteomics reveals multisite phosphorylation on mammalian brain voltage-gated sodium and potassium channels. Semin. Cell Dev. Biol. 22, 153-159
42. Arshavsky, V. Y. (2002) Rhodopsin phosphorylation: from terminating single photon responses to photoreceptor dark adaptation. Trends Neurosci. 25, 124-126
43. Valverde, R. H., Britto-Borges, T., Lowe, J., Einicker-Lamas, M., Mintz, E., Cuillel, M., and Vieyra, A. (2011) Two serine residues control sequential steps during catalysis of the yeast copper ATPase through different mechanisms that involve kinase-mediated phosphorylations. J. Biol. Chem. 286, 6879-6889
44. Cardoso, L. H., Britto-Borges, T., Vieyra, A., and Lowe, J. (2014) ATP7B activity is stimulated by PKCε in porcine liver. Int. J. Biochem. Cell Biol. 54, 60-67
45. Trinidad, J. C., Barkan, D. T., Gulledge, B. F., Thalhammer, A., Sali, A., Schoepfer, R., and Burlingame, A. L. (2012) Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol. Cell. Proteomics 11, 215-229