Differential roles of Met10, Thr11, and Lys60 in structural dynamics of human copper chaperone atox

Biochemistry

Volumn 48, Issue 5, 2009, Pages 960-972

  Rodriguez Granillo, Agustina ^a   Wittung Stafshede, Pernilla ^a,b  

^a RICE UNIVERSITY   (United States)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CORRELATED MOTIONS; CYS RESIDUES; DYNAMIC PARAMETERS; DYNAMIC PROTEINS; HYDROPHOBIC CORES; IN-VIVO; LOOP DYNAMICS; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN FLEXIBILITIES; SOLVENT EXPOSURES; STRUCTURAL CHANGES;

ELECTROSTATICS; MOLECULAR DYNAMICS; SOLVENTS; STRUCTURAL DYNAMICS;

DYNAMICS;

CHAPERONE; COPPER; LYSINE; METHIONINE; PROTEIN ATOX1; THREONINE; UNCLASSIFIED DRUG; ATOX1 PROTEIN, HUMAN; CATION TRANSPORT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CRYSTAL STRUCTURE; ELECTRICITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; HUMAN; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

EUKARYOTA; PROKARYOTA;

CATION TRANSPORT PROTEINS; COPPER; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROPHOBICITY; LYSINE; METHIONINE; MOLECULAR CHAPERONES; PROTEIN STRUCTURE, SECONDARY; STATIC ELECTRICITY; THERMODYNAMICS; THREONINE;

EID: 61449184570     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8018652     Document Type: Article

References (41)

1. O'Halloran, T. V., and Culotta, V. C. (2000) Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275, 25057-25060.
2. Huffman, D. L., and O'Halloran, T. V. (2001) Function, structure, and mechanism of intracellular copper trafficking proteins. Annu. Rev. Biochem. 70, 677-701.
3. Puig, S., Rees, E. M., and Thiele, D. J. (2002) The ABCDs of periplasmic copper trafficking. Structure 10, 1292-1295.
4. Puig, S., and Thiele, D. J. (2002) Molecular mechanisms of copper uptake and distribution. Curr. Opin. Chem. Biol. 6, 171-180.
5. Harris, E. D. (2003) Basic and clinical aspects of copper. Crit. Rev. Clin. Lab. Sci. 40, 547-586.
6. Rosenzweig, A. C, and O'Halloran, T. V. (2000) Structure and chemistry of the copper chaperone proteins. Curr. Opin. Chem. Biol. 4, 140-147.
7. Harrison, M. D., Jones, C. E., Solioz, M., and Dameron, C. T. (2000) Intracellular copper routing: The role of copper chaperones. Trends Biochem. Sci. 25, 29-32.
8. Hamza, I., Schaefer, M., Klomp, L. W., and Gitlin, J. D. (1999) Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc. Natl. Acad. Sci. U.S.A. 96, 13363-13368.
9. Hung, I. H, Casareno, R. L., Labesse, G., Mathews, F. S., and Gitlin, J. D. (1998) HAH1 is a copper-binding protein with distinct amino acid residues mediating copper homeostasis and antioxidant defense. J. Biol. Chem. 273, 1749-1754.
10. Klomp, L. W., Lin, S. J., Yuan, D. S., Klausner, R. D., Culotta, V. C, and Gitlin, J. D. (1997) Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis. J. Biol. Chem. 272, 9221-9226.
11. Hung, I. H., Suzuki, M., Yamaguchi, Y., Yuan, D. S., Klausner, R. D., and Gitlin, J. D. (1997) Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272, 21461-21466.
12. Hellman, N. E., Kono, S., Mancini, G M., Hoogeboom, A. J., De Jong, G. J., and Gitlin, J. D. (2002) Mechanisms of copper incorporation into human ceruloplasmin. J. Biol. Chem. 277, 46632-46638.
13. Gitlin, J. D. (2003) Wilson disease. Gastroenterology 125, 1868-1877.
14. Tao, T. Y., and Gitlin, J. D. (2003) Hepatic copper metabolism: Insights from genetic disease. Hepatology 37, 1241-1247.
15. Kulkarni, P. P., She, Y. M., Smith, S. D., Roberts, E. A., and Sarkar, B. (2006) Proteomics of metal transport and metal-associated diseases. Chemistry 12, 2410-2422.
16. Miyajima, H, Takahashi, Y., Kamata, T., Shimizu, H, Sakai, N., and Gitlin, J. D. (1997) Use of desferoxamine in the treatment of aceruloplasminemia. Ann. Neurol. 41, 404-407.
17. Arnesano, F., Banci, L., Bertini, I., Ciofi-Baffoni, S., Molteni, E., Huffman, D. L., and O'Halloran, T. V. (2002) Metallochaperones and metal-transporting ATPases: A comparative analysis of sequences and structures. Genome Res. 12, 255-271.
18. DeSilva, T. M., Veglia, G., and Opella, S. J. (2005) Solution structures of the reduced and Cu(I) bound forms of the first metal binding sequence of ATP7A associated with Menkes disease. Proteins 61, 1038-1049.
19. Banci, L., Bertini, I., Ciofi-Baffoni, S., Huffman, D. L., and O'Halloran, T. V. (2001) Solution structure of the yeast copper transporter domain Ccc2a in the apo and Cu(I)-loaded states. J. Biol. Chem. 276, 8415-8426.
20. Banci, L., Bertini, I., Del Conte, R., Markey, J., and Ruiz-Duenas, F. J. (2001) Copper trafficking: The solution structure of Bacillus subtilis CopZ. Biochemistry 40, 15660-15668.
21. Pufahl, R. A., Singer, C. P., Peariso, K. L., Lin, S. J., Schmidt, P. J., Fahrni, C. J., Culotta, V. C, Penner-Hahn, J. E., and O'Halloran, T. V. (1997) Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278, 853-856.
22. Rosenzweig, A. C, Huffman, D. L., Hou, M. Y., Wernimont, A. K., Pufahl, R. A., and O'Halloran, T. V. (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 Å resolution. Structure 7, 605-617.
23. Arnesano, F., Banci, L., Bertini, I., Huffman, D. L., and O'Halloran, T. V. (2001) Solution structure of the Cu(I) and apo forms of the yeast metallochaperone, Atx1. Biochemistry 40, 1528-1539.
24. Rodriguez-Granillo, A., and Wittung-Stafshede, P. (2008) Structure and Dynamics of Cu(I) Binding in Copper Chaperones Atox1 and CopZ: A Computer Simulation Study. J. Phys. Chem. B 112, 4583-4593.
25. Poger, D., Fuchs, J. F., Nedev, H., Ferrand, M., and Crouzy, S. (2005) Molecular dynamics study of the metallochaperone Hah1 in its apo and Cu(I)-loaded states: Role of the conserved residue M10. FEBS Lett. 579, 5287-5292.
26. Wernimont, A. K., Huffman, D. L., Lamb, A. L., O'Halloran, T. V., and Rosenzweig, A. C. (2000) Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat. Struct. Biol. 7, 766-771.
27. Hussain, F., and Wittung-Stafshede, P. (2007) Impact of cofactor on stability of bacterial (CopZ) and human (Atox1) copper chaperones. Biochim. Biophys. Acta 1774, 1316-1322.
28. Anastassopoulou, I., Banci, L., Bertini, I., Cantini, F., Katsari, E., and Rosato, A. (2004) Solution structure of the apo and copper(I)-loaded human metallochaperone HAH1. Biochemistry 43, 13046-13053.
29. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C, Fox, T, Caldwell, J. W., and Kollman, P. A. (1995) A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules. J. Am. Chem. Soc. 117, 5179-5197.
30. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E., III., DeBolt, S., Ferguson, D., Seibel, G, and Kollman, P. (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91, 1-41.
31. Case, D. A., Cheatham, T. E., III., Darden, T, Gohlke, H, Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C, Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688.
32. Case, D. A., Darden, T. A., Cheatham, T. E., III., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Pearlman, D. A., Crowley, M., Walker, R. C, Zhang, W., Wang, B., Hayik, S., Roitberg, A., Seabra, G, Wong, K. F., Paesani, F., Wu, X., Brozell, S., Tsui, V., Gohlke, H, Yang, L., Tan, C, Mongan, J., Hornak, V., Cui, G., Beroza, P., Mathews, D. H, Schafmeister, C, Ross, W. S., and Kollman, P. A. (2006) AMBER 9, University of California, San Francisco.
33. Jorgensen, W. L., Chandrasekhar, J., Madura, J., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
34. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725.
35. Berendsen, H. J., Postma, J. P., van Gunsteren, W. F., Di Nola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690.
36. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical-integration of Cartesian equations of motion of a system with constraints: Molecular dynamics of N-alkanes. J. Comput. Phys. 23, 327-341.
37. Ichiye, T., and Karplus, M. (1991) Collective motions in proteins: A covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations. Proteins 11, 205-217.
38. Rod, T. H., Radkiewicz, J. L., and Brooks, C. L., III. (2003) Correlated motion and the effect of distal mutations in dihy-drofolate reductase. Proc. Natl. Acad. Sci. U.S.A. 100, 6980 6985.
39. Banci, L., Bertini, I., Cantini, F., Felli, I. C, Gonnelli, L., Hadjiliadis, N., Pierattelli, R., Rosato, A., and Voulgaris, P. (2006) The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nat. Chem. Biol. 2, 367-368.
40. Arnold, G. E., and Ornstein, R. L. (1997) Molecular dynamics study of time-correlated protein domain motions and molecular flexibility: Cytochrome P450BM-3. Biophys. J. 73, 1147-1159.
41. Hussain, F., Olson, J. S., and Wittung-Stafshede, P. (2008) Conserved residues modulate copper release in human copper chaperone Atox1. Proc. Natl. Acad. Sci. U.S.A. 105, 11158-11163.