Small pH and salt variations radically alter the thermal stability of metal-binding domains in the copper transporter, Wilson disease protein

Journal of Physical Chemistry B

Volumn 117, Issue 42, 2013, Pages 13038-13050

  Nilsson, Lina ^a   Ådén, Jörgen ^a   Niemiec, Moritz S ^a   Nam, Kwangho ^a   Wittung Stafshede, Pernilla ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CHEMICAL SHIFT; COPPER; FREE ENERGY; NEURODEGENERATIVE DISEASES; PROTEINS; THERMODYNAMIC STABILITY;

CHARGE-CHARGE INTERACTIONS; FREE ENERGY LANDSCAPE; HIGH SALT CONCENTRATION; LOW SALT CONCENTRATION; METAL BINDING DOMAIN; SOLUTE CONCENTRATIONS; STRUCTURAL STABILITIES; TEMPORAL AND SPATIAL;

STABILITY;

ADENOSINE TRIPHOSPHATASE; ATOX1 PROTEIN, HUMAN; CATION TRANSPORT PROTEIN; COPPER; INORGANIC SALT; METALLOCHAPERONE; RECOMBINANT PROTEIN; SOLVENT; WILSON DISEASE PROTEIN;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; PH; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATASES; CATION TRANSPORT PROTEINS; COPPER; HUMANS; HYDROGEN-ION CONCENTRATION; METALLOCHAPERONES; MOLECULAR DYNAMICS SIMULATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SALTS; SOLVENTS; TEMPERATURE; THERMODYNAMICS;

EID: 84886667981     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp402415y     Document Type: Article

References (65)

1. Niemiec, M. S.; Weise, C. F.; Wittung-Stafshede, P. In Vitro Thermodynamic Dissection of Human Copper Transfer from Chaperone to Target Protein PLoS One 2012, 7 (5) e36102
2. Barry, A. N.; Shinde, U.; Lutsenko, S. Structural Organization of Human Cu-Transporting Atpases: Learning from Building Blocks J. Biol. Inorg. Chem. 2010, 15 (1) 47-59
3. Huffman, D. L.; O'Halloran, T. V. Function, Structure, and Mechanism of Intracellular Copper Trafficking Proteins Annu. Rev. Biochem. 2001, 70, 677-701
4. Puig, S.; Thiele, D. J. Molecular Mechanisms of Copper Uptake and Distribution Curr. Opin. Chem. Biol. 2002, 6 (2) 171-180
5. Harris, E. D. Basic and Clinical Aspects of Copper Crit. Rev. Clin. Lab. Sci. 2003, 40 (5) 547-586
6. O'Halloran, T. V.; Culotta, V. C. Metallochaperones, an Intracellular Shuttle Service for Metal Ions J. Biol. Chem. 2000, 275 (33) 25057-25060
7. Robinson, N. J.; Winge, D. R. Copper Metallochaperones Annu. Rev. Biochem. 2010, 79, 537-562
8. Festa, R. A.; Thiele, D. J. Copper: An Essential Metal in Biology Curr. Biol. 2011, 21 (21) R877-883
9. Lutsenko, S.; Tsivkovskii, R.; Walker, J. M. Functional Properties of the Human Copper-Transporting Atpase Atp7b (the Wilson's Disease Protein) and Regulation by Metallochaperone Atox1 Ann. N.Y. Acad. Sci. 2003, 986, 204-211
10. Kim, B. E.; Nevitt, T.; Thiele, D. J. Mechanisms for Copper Acquisition, Distribution and Regulation Nat. Chem. Biol. 2008, 4 (3) 176-185
11. Lutsenko, S.; LeShane, E. S.; Shinde, U. Biochemical Basis of Regulation of Human Copper-Transporting Atpases Arch. Biochem. Biophys. 2007, 463 (2) 134-148
12. Arnesano, F.; Banci, L.; Bertini, I.; Ciofi-Baffoni, S.; Molteni, E.; Huffman, D. L.; O'Halloran, T. V. Metallochaperones and Metal-Transporting Atpases: A Comparative Analysis of Sequences and Structures Genome Res. 2002, 12 (2) 255-271
13. Huster, D.; 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. 2003, 278 (34) 32212-32218
14. Gourdon, P.; Liu, X. Y.; Skjorringe, T.; Morth, J. P.; Moller, L. B.; Pedersen, B. P.; Nissen, P. Crystal Structure of a Copper-Transporting Pib-Type Atpase Nature 2011, 475 (7354) 59-64
15. Gourdon, P.; Sitsel, O.; Lykkegaard Karlsen; Birk Moller, J.; Nissen, P. Structural Models of the Human Copper P-Type Atpases Atp7a and Atp7b Biol. Chem. 2012, 393 (4) 205-216
16. Schushan, M.; Bhattacharjee, A.; Ben-Tal, N.; Lutsenko, S. A Structural Model of the Copper Atpase Atp7b to Facilitate Analysis of Wilson Disease-Causing Mutations and Studies of the Transport Mechanism Metallomics 2012, 4 (7) 669-678
17. Tsivkovskii, R.; MacArthur, B. C.; Lutsenko, S. The Lys1010-Lys1325 Fragment of the Wilson's Disease Protein Binds Nucleotides and Interacts with the N-Terminal Domain of This Protein in a Copper-Dependent Manner J. Biol. Chem. 2001, 276 (3) 2234-2242
18. Hatori, Y.; Lutsenko, S. An Expanding Range of Functions for the Copper Chaperone/Antioxidant Protein Atox1. Antioxid. Redox Signaling, 2013.
19. Gonzalez-Guerrero, M.; Arguello, J. M. Mechanism of Cu+-Transporting Atpases: Soluble Cu+ Chaperones Directly Transfer Cu+ to Transmembrane Transport Sites Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (16) 5992-5997
20. Arumugam, K.; Crouzy, S. Dynamics and Stability of the Metal Binding Domains of the Menkes Atpase and Their Interaction with Metallochaperone Hah1 Biochemistry 2012, 51 (44) 8885-8906
21. Achila, D.; Banci, L.; Bertini, I.; Bunce, J.; Ciofi-Baffoni, S.; Huffman, D. L. Structure of Human Wilson Protein Domains 5 and 6 and Their Interplay with Domain 4 and the Copper Chaperone Hah1 in Copper Uptake Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (15) 5729-5734
22. Fatemi, N.; Korzhnev, D. M.; Velyvis, A.; Sarkar, B.; Forman-Kay, J. D. Nmr Characterization of Copper-Binding Domains 4-6 of Atp7b Biochemistry 2010, 49 (39) 8468-8477
23. Rodriguez-Granillo, A.; Wittung-Stafshede, P. Structure and Dynamics of Cu(I) Binding in Copper Chaperones Atox1 and Copz: A Computer Simulation Study J. Phys. Chem. B 2008, 112 (15) 4583-4593
24. Yatsunyk, L. A.; Rosenzweig, A. C. Cu(I) Binding and Transfer by the N Terminus of the Wilson Disease Protein J. Biol. Chem. 2007, 282 (12) 8622-8631
25. Delaglio, F.; Grzesiek, S.; Vuister, G. W.; Zhu, G.; Pfeifer, J.; Bax, A. Nmrpipe: A Multidimensional Spectral Processing System Based on Unix Pipes J. Biomol. NMR 1995, 6 (3) 277-293
26. Helgstrand, M.; Kraulis, P.; Allard, P.; Hard, T. Ansig for Windows: An Interactive Computer Program for Semiautomatic Assignment of Protein Nmr Spectra J. Biomol. NMR 2000, 18 (4) 329-336
27. Fushman, D.; Weisemann, R.; Thuring, H.; Ruterjans, H. Backbone Dynamics of Ribonuclease T1 and Its Complex with 2′gmp Studied by Two-Dimensional Heteronuclear Nmr Spectroscopy J. Biomol. NMR 1994, 4 (1) 61-78
28. Pelton, J. G.; Torchia, D. A.; Meadow, N. D.; Roseman, S. Tautomeric States of the Active-Site Histidines of Phosphorylated and Unphosphorylated Iiiglc, a Signal-Transducing Protein from Escherichia Coli, Using Two-Dimensional Heteronuclear Nmr Techniques Protein Sci. 1993, 2 (4) 543-558
29. Brünger, A.; Brooks, C. B.; Karplus, M. Stochastic Boundary Conditions for Molecular Dynamics Simulations of ST2 Water Chem. Phys. Lett. 1984, 105, 495-500
30. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of N-Alkanes J. Comput. Phys. 1977, 23, 327-341
31. Miyamoto, S.; Kollman, P. A. Settle: An Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
32. Patel, S.; Mackerell, A. D., Jr.; Brooks, C. L., 3rd Charmm Fluctuating Charge Force Field for Proteins: Ii Protein/Solvent Properties from Molecular Dynamics Simulations Using a Nonadditive Electrostatic Model J. Comput. Chem. 2004, 25 (12) 1504-1514
33. MacKerell, A. D., Jr.; Feig, M.; Brooks, C. L., III. Extending the Treatment of Backbone Energetic in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
34. Tirado-Rives, J.; Jorgensen, W. L. Molecular Dynamics Simulations of the Unfolding of Apomyoglobin in Water Biochemistry 1993, 32 (16) 4175-4184
35. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An Nlog(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
36. Brooks, B. R.; Brooks, C. L., 3rd; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S. Charmm: The Biomolecular Simulation Program J. Comput. Chem. 2009, 30 (10) 1545-1614
37. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with Namd J. Comput. Chem. 2005, 26 (16) 1781-1802
38. Badarau, A.; Dennison, C. Copper Trafficking Mechanism of Cxxc-Containing Domains: Insight from the Ph-Dependence of Their Cu(I) Affinities J. Am. Chem. Soc. 2011, 133 (9) 2983-2988
39. Marti, D. N. Apparent Pka Shifts of Titratable Residues at High Denaturant Concentration and the Impact on Protein Stability Biophys. Chem. 2005, 118 (2-3) 88-92
40. Palmer, A. G., 3rd. Probing Molecular Motion by Nmr Curr. Opin. Struct. Biol. 1997, 7 (5) 732-737
41. Bae, S. H.; Dyson, H. J.; Wright, P. E. Prediction of the Rotational Tumbling Time for Proteins with Disordered Segments J. Am. Chem. Soc. 2009, 131 (19) 6814-6821
42. Banci, L.; Bertini, I.; Cantini, F.; Massagni, C.; Migliardi, M.; Rosato, A. An Nmr Study of the Interaction of the N-Terminal Cytoplasmic Tail of the Wilson Disease Protein with Copper(I)-Hah1 J. Biol. Chem. 2009, 284 (14) 9354-9360
43. Llopis, J.; McCaffery, J. M.; Miyawaki, A.; Farquhar, M. G.; Tsien, R. Y. Measurement of Cytosolic, Mitochondrial, and Golgi Ph in Single Living Cells with Green Fluorescent Proteins Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (12) 6803-6808
44. Maouyo, D.; Chu, S.; Montrose, M. H. Ph Heterogeneity at Intracellular and Extracellular Plasma Membrane Sites in Ht29-C1 Cell Monolayers Am. J. Physiol.: Cell Physiol. 2000, 278 (5) C973-981
45. Safaei, R.; Otani, S.; Larson, B. J.; Rasmussen, M. L.; Howell, S. B. Transport of Cisplatin by the Copper Efflux Transporter Atp7b Mol. Pharmacol. 2008, 73 (2) 461-468
46. Chavez-Crooker, P.; Garrido, N.; Ahearn, G. A. Copper Transport by Lobster Hepatopancreatic Epithelial Cells Separated by Centrifugal Elutriation: Measurements with the Fluorescent Dye Phen Green J. Exp. Biol. 2001, 204 (Pt 8) 1433-1444
47. Bhaskara, R. M.; Srinivasan, N. Stability of Domain Structures in Multi-Domain Proteins Sci. Rep. 2011, 1, 40
48. Vihinen, M. Relationship of Protein Flexibility to Thermostability Protein Eng. 1987, 1 (6) 477-480
49. Wintrode, P. L.; Zhang, D.; Vaidehi, N.; Arnold, F. H.; Goddard, W. A., 3rd. Protein Dynamics in a Family of Laboratory Evolved Thermophilic Enzymes J. Mol. Biol. 2003, 327 (3) 745-757
50. Baxter, E. L.; Zuris, J. A.; Wang, C.; Vo, P. L.; Axelrod, H. L.; Cohen, A. E.; Paddock, M. L.; Nechushtai, R.; Onuchic, J. N.; Jennings, P. A. Allosteric Control in a Metalloprotein Dramatically Alters Function Proc. Natl. Acad. Sci. U.S.A. 2013, 110 (3) 948-953
51. Keeler, C.; Tettamanzi, M. C.; Meshack, S.; Hodsdon, M. E. Contribution of Individual Histidines to the Global Stability of Human Prolactin Protein Sci. 2009, 18 (5) 909-920
52. Rodnin, M. V.; Kyrychenko, A.; Kienker, P.; Sharma, O.; Posokhov, Y. O.; Collier, R. J.; Finkelstein, A.; Ladokhin, A. S. Conformational Switching of the Diphtheria Toxin T Domain J. Mol. Biol. 2010, 402 (1) 1-7
53. Achilonu, I.; Fanucchi, S.; Cross, M.; Fernandes, M.; Dirr, H.W. Role of Individual Histidines in the Ph-Dependent Global Stability of Human Chloride Intracellular Channel 1 Biochemistry 2012, 51 (5) 995-1004
54. Vaughn, D. E.; Bjorkman, P. J. Structural Basis of Ph-Dependent Antibody Binding by the Neonatal Fc Receptor Structure 1998, 6 (1) 63-73
55. Maldonado, S.; Irun, M. P.; Campos, L. A.; Rubio, J. A.; Luquita, A.; Lostao, A.; Wang, R.; Garcia-Moreno, E. B.; Sancho, J. Salt-Induced Stabilization of Apoflavodoxin at Neutral Ph Is Mediated through Cation-Specific Effects Protein Sci. 2002, 11 (5) 1260-1273
56. Pradeep, L.; Udgaonkar, J. B. Differential Salt-Induced Stabilization of Structure in the Initial Folding Intermediate Ensemble of Barstar J. Mol. Biol. 2002, 324 (2) 331-347
57. Schoeffler, A. J.; Ruiz, C. R.; Joubert, A. M.; Yang, X.; LiCata, V. J. Salt Modulates the Stability and Lipid Binding Affinity of the Adipocyte Lipid-Binding Proteins J. Biol. Chem. 2003, 278 (35) 33268-33275
58. Honig, B.; Nicholls, A. Classical Electrostatics in Biology and Chemistry Science 1995, 268 (5214) 1144-1149
59. Warshel, A. Calculations of Enzymatic Reactions: Calculations of Pka, Proton Transfer Reactions, and General Acid Catalysis Reactions in Enzymes Biochemistry 1981, 20 (11) 3167-3177
60. Banci, L.; Bertini, I.; Cantini, F.; Felli, I. C.; Gonnelli, L.; Hadjiliadis, N.; Pierattelli, R.; Rosato, A.; Voulgaris, P. The Atx1-Ccc2 Complex Is a Metal-Mediated Protein-Protein Interaction Nat. Chem. Biol. 2006, 2 (7) 367-368
61. Hussain, F.; Rodriguez-Granillo, A.; 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. 2009, 131 (45) 16371-16373
62. Banci, L.; Bertini, I.; Calderone, V.; Della-Malva, N.; Felli, I. C.; Neri, S.; Pavelkova, A.; Rosato, A. Copper(I)-Mediated Protein-Protein Interactions Result from Suboptimal Interaction Surfaces Biochem. J. 2009, 422 (1) 37-42
63. Bryngelson, J. D.; Onuchic, J. N.; Socci, N. D.; Wolynes, P. G. Funnels, Pathways, and the Energy Landscape of Protein Folding: A Synthesis Proteins 1995, 21 (3) 167-195
64. Levy, Y.; Wolynes, P. G.; Onuchic, J. N. Protein Topology Determines Binding Mechanism Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (2) 511-516
65. Olsson, U.; Wolf-Watz, M. Overlap between Folding and Functional Energy Landscapes for Adenylate Kinase Conformational Change Nat. Commun. 2010, 1, 111