Copper binding sites in the C-terminal domain of mouse prion protein: A hybrid (QM/MM) molecular dynamics study

Proteins: Structure, Function and Genetics

Volumn 70, Issue 3, 2008, Pages 1084-1098

  Colombo, Maria Carola ^a   VandeVondele, Joost ^b,d   Van Doorslaer, Sabine ^c   Laio, Alessandro ^b,e   Guidoni, Leonardo ^a,f   Rothlisberger, Ursula ^a,g  

^a EPFL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e SISSA   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g Inst of Chem Sci and Engineering   (Switzerland)

Author keywords

Copper binding protein; Creutzfeldt Jacob disease; ENDOR; EPR; Molecular simulations

Indexed keywords

COPPER; PRION PROTEIN;

BINDING SITE; ELECTRON SPIN RESONANCE; METAL BINDING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIMULATION;

ANIMALS; BINDING SITES; COMPUTER SIMULATION; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; MICE; MODELS, MOLECULAR; PRIONS; PROTEIN CONFORMATION;

EID: 38549135029     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21604     Document Type: Note

References (106)

1. Prusiner SB. Prions. Proc Natl Acad Sci USA 1998;95:13363-13383.
2. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, Wuthrich K. NMR structure of the mouse prion protein domain PrP(121-231). Nature 1996;382:180-182.
3. Liu H, Farr-Jones S, Ulyanov NB, Llinas M, Marqusee S, Groth D, Cohen FE, Prusiner SB, James TL. Solution structure of Syrian hamster prion protein rPrP(90-231). Biochemistry 1999;38:5362-5377.
4. Knaus KJ, Morillas M, Swietnicki W, Malone M, Surewicz WK, Yee VC. Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat Struct Biol 2001;8:770-774.
5. Haire LF, Whyte SM, Vasisht N, Gill AC, Verma C, Dodson EJ, Dodson GG, Bayley PM. The crystal structure of the globular domain of sheep prion protein. J Mol Biol 2004;336:1175-1183.
6. Brown DR, Qin KF, Herms JW, Madlung A, Manson J, Strome R, Fraser PE, Kruck T, von Bohlen A, SchulzSchaeffer W, Giese A, Westaway D, Kretzschmar H. The cellular prion protein binds copper in vivo. Nature 1997;390:684-687.
7. Brown DR. Metallic prions. Biochem Soc Symp 2004;71:193-202.
8. Brown DR, Kozlowski H. Biological inorganic and bioinorganic chemistry of neurodegeneration based on prion and Alzheimer diseases. Dalton Trans 2004;13:1907-1917.
9. Vassallo N, Herms J. Cellular prion protein function in copper homeostasis and redox signalling at the synapse. J Neurochem 2003;86:538-544.
10. Lehmann S. Metal ions and prion diseases. Curr Opin Chem Biol 2002;6:187-192.
11. Viles JH, Cohen FE, Prusiner SB, Goodin DB, Wright PE, Dyson HJ. Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci USA 1999;96:2042-2047.
12. Rachidi W, Vilette D, Guiraud P, Arlotto M, Riondel J, Laude H, Lehmann S, Favier A. Expression of prion protein increases cellular copper binding and antioxidant enzyme activities but not copper delivery. J Biol Chem 2003;278:9064-9072.
13. Hornshaw MP, McDermott JR, Candy JM. Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 1995;207:621-629.
14. Jackson GS, Murray I, Hosszu LLP, Gibbs N, Waltho JP, Clarke AR, Collinge J. Location and properties of metal-binding sites on the human prion protein. Proc Natl Acad Sci USA 2001;98:8531-8535.
15. Pauly PC, Harris DA. Copper stimulates endocytosis of the prion protein. J Biol Chem 1998;273:33107-33110.
16. Whittal RM, Ball HL, Cohen FE, Burlingame AL, Prusiner SB, Baldwin MA. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci 2000;9:332-343.
17. Burns CS, Aronoff-Spencer E, Dunham CM, Lario P, Avdievich NI, Antholine WE, Olmstead MM, Vrielink A, Gerfen GJ, Peisach J, Scott WG, Millhauser GL. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 2002;41:3991-4001.
18. Shiraishi N, Ohta Y, Nishikimi M. The octapeptide repeat region of prion protein binds Cu(II) in the redox-inactive state. Biochem Biophys Res Commun 2000;267:398-402.
19. Brown DR, Wong BS, Hafiz F, Clive C, Haswell SJ, Jones IM. Normal prion protein has an activity like that of superoxide dismutase. Biochem J 1999;344:1-5.
20. Wong BS, Pan T, Liu T, Li RL, Gambetti P, Sy MS. Differential contribution of superoxide dismutase activity by prion protein in vivo. Biochem Biophys Res Commun 2000;273:136-139.
21. Cui T, Daniels M, Wong BS, Li RL, Sy MS, Sassoon J, Brown DR. Mapping the functional domain of the prion protein. Eur J Biochem 2003;270:3368-3376.
22. Sakudo A, Lee DC, Nishimura T, Li SM, Tsuji S, Nakamura T, Matsumoto Y, Saeki K, Itohara S, Ikuta K, Onodera T. Octapeptide repeat region and N-terminal half of hydrophobic region of prion protein (PrP) mediate PrP-dependent activation of superoxide dismutase. Biochem Biophys Res Commun 2005;326:600-606.
23. Hutter G, Heppner FL, Aguzzi A. No superoxide dismutase activity of cellular prion protein in vivo. Biol Chem 2003;384:1279-1285.
24. Sakudo A, Hamaishi M, Hosokawa-Kanai T, Tuchiya K, Nishimura T, Saeki K, Matsumoto ,Y, Ueda S, Onodera T. Absence of superoxide dismutase activity in a soluble cellular isoform of prion protein produced by baculovirus expression system. Biochem Biophys Res Commun 2003;307:678-683.
25. 2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry 2000;39:13760-13771.
26. Burns CS, Aronoff-Spencer E, Legname G, Prusiner SB, Antholine WE, Gerfen GJ, Peisach J, Millhauser GL. Copper coordination in the full-length, recombinant prion protein. Biochemistry 2003;42: 6794-6803.
27. Burns CS, Aronoff-Spencer E, Dunham CM, Lario P, Avdievich NI, Antholine WE, Olmstead MM, Vrielink A, Gerfen GJ, Peisach J, Scott WG, Millhauser GL. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 2002;41:3991-4001.
28. Miura T, Hori-IA, Mototani H,Takeuchi H. Raman spectroscopic study on the copper(II) binding mode of prion octapeptide and its pH dependence. Biochemistry 1999;38:11560-11569.
29. Garnett AP, Viles JH. Copper binding to the octarepeats of the prion protein - affinity, specificity, folding, and cooperativity: insights from circular dichroism. J Biol Chem 2003;278:6795-6802.
30. Kramer ML, Kratzin HD, Schmidt B, Romer A, Windl O, Liemann S, Hornemann S, Kretzschmar H. Prion protein binds copper within the physiological concentration range. J Biol Chem 2001; 276:16711-16719.
31. Morante S, González-Iglesias R, Potrich C, Meneghini C, Meyer-Klaucke W, Menestrina G, Gasset M. Inter- and intra-octarepeat Cu(II) site geometries in the prion protein. J Biol Chem 2004;279: 11753-11759.
32. 2+ to the C-terminal domain of the murine prion protein. Biophys J 2001;81:516-525.
33. 2+ binding sites in the C-terminal domain of the murine prion protein: a pulse EPR and ENDOR study. J Phys Chem B 2001;105:1631-1639.
34. Cereghetti GM, Schweiger A, Glockshuber R, Van Doorslaer S. Stability and Cu(II) binding of prion protein variants related to inherited human prion diseases. Biophys J 2003;84:1985-1997.
35. Brown DR, Guantieri V, Grasso G, Impellizzeri G, Pappalardo G, Rizzarelli E. Copper(II) complexes of peptide fragments of the prion protein. Conformation changes induced by copper(II) and the binding motif in C-terminal protein region. J Inorg Biochem 2004;98:133-143.
36. Hasnain SS, Murphy LM, Strange RW, Grossmann JG, Clarke AR, Jackson GS, Collinge J. XAFS study of the high-affinity copper-binding site of human PrP91-231 and its low-resolution structure in solution. J Mol Biol 2001;311:467-473.
37. Stockel J, Safar J, Wallace AC, Cohen FE, Prusiner SB. Prion protein selectively binds copper(II) ions. Biochemistry 1998;37:7185-7193.
38. Flechsig E, Shmerling D, Hegyi I, Raeber AJ, Fischer M, Cozzio A, von Mering C, Aguzzi A, Weissmann C. Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice. Neuron 2000;27:399-408.
39. Wong BS, Chen SG, Colucci M, Xie ZL, Pan T, Liu T, Li RL, Gambetti P, Sy MS, Brown DR. Aberrant metal binding by prion protein in human prion disease. J Neurochem 2001;78:1400-1408.
40. Rachidi W, Mange A, Senator A, Guiraud P, Riondel J, Benboubetra M, Favier A, Lehmann S. Prion infection impairs copper binding of cultured cells. J Biol Chem 2003;278:14595-14598.
41. Sigurdsson EM, Brown DR, Alim MA, Scholtzova H, Carp R, Meeker HC, Prelli F, Frangione B, Wisniewski T. Copper chelation delays the onset of prion disease. J Biol Chem 2003;278:46199-46202.
42. Requena JR, Groth D, Legname G, Stadtman ER, Prusiner SB, Levine RL. Copper-catalyzed oxidation of the recombinant SHa(29-231) prion protein. Proc Natl Acad Sci USA 2001;98:7170-7175.
43. Giese A, Levin J, Bertsch U, Kretzschmar H. Effect of metal ions on de novo aggregation of full-length prion protein. Biochem Biophys Res Commun 2004;320:1240-1246.
44. Okimoto N, Yamanaka K, Suenaga A, Hata M, Hoshino T. Computational studies on prion proteins: effect of Ala(117) -> val mutation. Biophys J 2002;82:2746-2757.
45. El-Bastawissy E, Knaggs MH, Gilbert IH. Molecular dynamics simulations of wild-type and point mutation human prion protein at normal and elevated temperature. J Mol Graph Model 2001;20: 145-154.
46. Alonso DOV, DeArmond SJ, Cohen FE, Daggett V. Mapping the early steps in the pH-induced conformational conversion of the prion protein. Proc Natl Acad Sci USA 2001;98:2985-2989.
47. Parchment OG, Essex JW. Molecular dynamics of mouse and syrian hamster PrP: implications for activity. Proteins 2000;38:327-340.
48. Zuegg J, Gready JE. Molecular dynamics simulations of human prion protein: importance of correct treatment of electrostatic interactions. Biochemistry 1999;38:13862-13876.
49. Ji HF, Zhang HY, Shen LA. The role of electrostatic interaction in triggering the unraveling of stable helix 1 in normal prion protein. A molecular dynamics simulation investigation. J Biomol Struct Dyn 2005;22:563-570.
50. Dima RI, Thirumalai D. Probing the instabilities in the dynamics of helical fragments from mouse PrPc. Proc Natl Acad Sci USA 2004;101:15335-15340.
51. Karplus M, Petsko GA. Molecular-dynamics simulation in biology. Nature 1990;347:631-639.
52. Laio A, VandeVondele J, Rothlisberger U. A Hamiltonian electrostatic coupling scheme for hybrid Car-Parrinello molecular dynamics simulations. J Chem Phys 2002;116:6941-6947.
53. Dal Peraro M, Llarrull LI, Rothlisberger U, Vila AJ, Carloni P. Water-assisted reaction mechanism of monozinc β-lactamases. J Am Chem Soc 2004;126:12661-12668.
54. Guidoni L, Spiegel K, Zumstein M, Rothlisberger U. Green oxidation catalysts: computational design of high-efficiency models of galactose oxidase. Angew Chem Int Ed Engl 2004;43:3286-3289.
55. Spiegel K, Rothlisberger U, Carloni P. Cisplatin binding to DNA oligomers from hybrid Car-Parrinello/molecular dynamics simulations. J Phys Chem B 2004;108:2699-2707.
56. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger PKHC, Mark AE, Scott WRP, Tironi IG. Biomolecular simulation: the GROMOS96 manual and user guide. Zürich: vdf Hochschulverlag AG; 1996.
57. te Velde G, Bickelhaupt FM, van Gisbergen SJA, Fonseca Guerra C, Baerends EJ, Snijders JG, Ziegler T. Chemistry with ADF. J Comput Chem 2001;22:931-967.
58. Guerra CF, Snijders JG, te Velde G, Baerends EJ. Towards an order-N DFT method. Theor Chem Acc 1998;99:391-403.
59. ADF2002.01, SCM. Theoretical chemistry. Vrije Universiteit, Amsterdam, The Netherlands. http://www.scm.com.
60. Dolittle RF. Redundancies in protein sequences. In: Fasman GD, editor. Prediction of protein structure and the principles of protein conformation. New York: Plenum; 1989. pp 599-623.
61. Hünenberger PH. Optimal charge-shaping functions for the particle-particle-particle-mesh (P3M) method for computing electrostatic interactions in molecular simulations. J Chem Phys 2000; 113:10464-10476.
62. Becke AD. Density-functional exchange-energy approximation with correct asymptotic behaviour. Phys Rev A 1988;38:3098-3100.
63. Lee CT, Yang WT, Parr RG. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 1988;37:785-789.
64. Troullier N, Martins JL. Efficient pseudopotentials for plane wave calculations. Phys Rev B 1991;43:1993-2006.
65. Martyna GJ, Tuckerman ME. A reciprocal space based method for treating long range interactions in ab initio and force-field-based calculations in clusters. J Chem Phys 1999;110:2810-2821.
66. Laio A, Gervasio FL, VandeVondele J, Sulpizi M, Rothlisberger U. A variational definition of electrostatic potential derived charges. J Phys Chem B 2004;108:7963-7968.
67. van Lenthe E, Wormer PES, van der Avoird A. Density functional calculations of molecular g-tensors in the zero-order regular approximation for relativistic effects. J Chem Phys 1997;107:2488-2498.
68. van Lenthe E, van der Avoird A, Wormer PES. Density functional calculations of molecular hyperfine interactions in the zero order regular approximation for relativistic effects. J Chem Phys 1998; 108:4783-4796.
69. Saladino AC, Larsen SC. Relativistic DFT calculations of copper hyperfine coupling constants: effect of spin-orbit coupling. J Phys Chem A 2003;107:5583-5587.
70. Baute D, Arieli D, Neese F, Zimmermann H, Weckhuysen BM, Goldfarb D. Carboxylate binding in copper histidine complexes in solution and in zeolite Y: X- and W-band pulsed EPR/ENDOR combined with DFT calculations. J Am Chem Soc 2004;126: 11733-11745.
71. Naumov S, Reinhold J, Beckert D. Investigation of the molecular structure of the radical anions of some pyrimidine-type bases in aqueous solution by comparison of calculated hyperfine coupling constants with EPR results. Phys Chem Chem Phys 2003;5:64-72.
72. Vosko SH, Wilk L, Nusair M. Accurate spin dependent electron liquid correlation energies for local spin-densities calculations - a critical analysis. Can J Phys 1980;58:1200-1211.
73. Perdew JP. Density functional approximation for the correlation-energy of the inhomogeneous electon-gas. Phys Rev B 1986;33: 8822-8824.
74. van Lenthe E, Baerends EJ, Snijders JG. Relativistic regular two-component Hamiltonians. J Chem Phys 1993;99:4597-4610.
75. van Lenthe E, Baerends EJ, Snijders JG. Relativistic total energy using regular approximations. J Chem Phys 1994;101:9783-9792.
76. van Lenthe E, Ehlers A, Baerends EJ. Geometry optimizations in the zero order regular approximation for relativistic effects. J Chem Phys 1999;110:8943-8953.
77. Kallberg Y, Gustafsson M, Persson B, Thyberg J, Johansson J. Prediction of amyloid fibril-forming proteins J Biol Chem 2001;276: 12945-12950.
78. Messerschmidt A. Metal sites in small blue copper proteins, blue copper oxidases and vanadium-containing enzymes. Struct Bonding 1998;90:37-68.
79. Kivelson D, Neiman R. ESR studies on bonding in copper complexes. J Chem Phys 1961;35:149-155.
80. Vänngärd T. Copper proteins. In: Swartz HM, Bolton JR, Borg DC, editors. Biological applications of electron spin resonance. New York: Wiley-Interscience; 1972. pp 411-447.
81. Peisach J, Blumberg WE. Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch Biochem Biophys 1974;165:961-708.
82. Munzarova ML, Kaupp M. A density functional study of EPR parameters for vanadyl complexes containing Schiff base ligands. J Phys Chem B 2001;105:12644-12652.
83. Neese F. Metal and ligand hyperfine couplings in transition metal complexes: the effect of spin-orbit coupling as studied by coupled perturbed Kohn-Sham theory. J Chem Phys 2003;118:3939-3948.
84. Belanzoni P, Baerends EJ, Vanasselt S. Langewen PB. Density functional study of magnetic coupling parameters - reconciling theory and experiment for the TiF3 complex. J Phys Chem 1995;99:13094-13102.
85. Munzarova ML, Kubacek P, Kaupp M. Mechanisms of EPR hyperfine coupling in transition metal complexes. J Am Chem Soc 2000; 122:11900-11913.
86. Abragam A, Bleaney B. Electron paramagnetic resonance of transition ions. Oxford, UK: Clarendon Press; 1970.
87. Carl PJ, Isley SL, Larsen SC. Combining theory and experiment to interpret the EPR spectra of VO21-exchanged zeolites. J Phys Chem A 2001;105:4563-4573.
88. Saladino AC, Larsen SC. Density functional theory calculations of the electron paramagnetic resonance parameters for VO2+ complexes. J Phys Chem A 2003;107:1872-1878.
89. van Lenthe E, Wormer PES, van der Avoird A. Density functional calculations of molecular g-tensors in the zero-order regular approximation for relativistic effects. J Chem Phys 1997;107:2488-2498.
90. Munzarova M, Kaupp M. A critical validation of density functional and coupled-cluster approaches for the calculation of EPR hyperfine coupling constants in transition metal complexes. J Phys Chem A 1999;103:9966-9983.
91. Saladino AC, Larsen SC. Computational study of the effect of the imidazole ring orientation on the EPR parameters for vanadylimidazole complexes. J Phys Chem A 2002;106:10444-10451.
92. Saladino AC, Larsen SC. Density functional theory calculations of nitrogen hyperfine and quadrupole coupling constants in Oxovanadium(IV) complexes. J Phys Chem A 2003;107:4735-4740.
93. Stein M, van Lenthe E, Baerends EJ, Lubitz W. g- and a-tensor calculations in the zero-order approximation for relativistic effects of Ni complexes Ni(mnt)(2)(-) and Ni(CO)(3)H as model complexes for the active center of [NiFe]-hydrogenase. J Phys Chem A 2001;105:416-425.
94. Schreckenbach G, Ziegler T. Calculation of the g-tensor of electron paramagnetic resonance spectroscopy using gauge-including atomic orbitals and density functional theory. J Phys Chem A 1997;101:3388-3399.
95. Patchkovskii S, Ziegler T. Calculation of the EPR g-tensors of high-spin radicals with density functional theory. J Phys Chem A 2001;105:5490-5497.
96. Kaupp M, Reviakine R, Malkina OL, Arbuznikov A, Schimmelpfennig B, Malkin VG. Calculation of electronic g-tensors for transition metal complexes using hybrid density functionals and atomic meanfield spin-orbit operators. J Comput Chem 2002;23:794-803.
97. Neese F. Configuration interaction calculation of electronic g tensors in transition metal complexes. Int J Quantum Chem 2001;83: 104-114.
98. Rinkevicius Z, Telyatnyk L, Salek P, Vahtras O, Agren H. Restricted density-functional linear response theory calculations of electronic g-tensors. J Chem Phys 2003;119:10489-10496.
99. Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S, Gotz J, Rulicke T, Flechsig E, Cozzio A, von Mering C, Hangartner C, Aguzzi A, Weissmann C. Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 1998;93:203-214.
100. Bocharova OV, Breydo L, Salnikov VV, Baskakov IV. Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 2005;44:6776-6787.
101. McKinley MP, Masiarz FR, Prusiner SB. Reversible chemical modification of the scrapie agent. Science 1981;214:1259-1261.
102. Cervenakova L, Buetefisch C, Lee HS, Taller I, Stone G, Gibbs CJ, Brown P, Hallett M, Goldfarb LG. Novel PRNP sequence variant associated with familial encephalopathy. Am J Med Genet 1999;88: 653-656.
103. Thompson A, White AR, McLean C, Masters CL, Cappai R, Barrow CJ. Amyloidgenicity and neurotoxicity of peptides corresponding to the helical regions of PrPC. J Neurosci Res 2000;62:293-301.
104. Bosques CJ, Imperiali B. The interplay of glycosylation and disulfide formation influences fibrillization in a prion protein fragment. Proc Natl Acad Sci USA 2003;100:7593-7598.
105. Kuwata K, Li H, Yamada H Legname G, Prusiner SB, Akasaka K, James TL. Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 2002;41:12277-12283.
106. Kuwata K, Kamatari YO, Akasaka K, James TL. Slow conformational dynamics in the hamster prion protein. Biochemistry 2004; 43:4439-4446.