Developing predictive rules for coordination geometry from visible circular dichroism of copper(II) and nickel(II) ions in histidine and amide main-chain complexes

FEBS Journal

Volumn 281, Issue 17, 2014, Pages 3945-3954

  Stanyon, Helen F ^a   Cong, Xiaojing ^b,c   Chen, Yan ^a   Shahidullah, Nabeela ^a   Rossetti, Giulia ^b,c,e   Dreyer, Jens ^b,c   Papamokos, George ^b,c,d   Carloni, Paolo ^b,c,d   Viles, John H ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d SISSA   (Italy)

^e Institute of Neuroscience and Medicine   (Germany)

Author keywords

CD; density functional theory; protein

Indexed keywords

CD; CU2+; DENSITY FUNCTIONAL THEORY; NI2+; PROTEIN;

AMIDES; CIRCULAR DICHROISM; COPPER; HISTIDINE; NICKEL; OLIGOPEPTIDES; PROTEIN CONFORMATION; QUANTUM THEORY;

EID: 84906871655     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12934     Document Type: Article

References (42)

1. Martin RB, (1974) Optical properties of transition metal ion complexes of amino acids and peptides. Met Ions Biol Syst 1, 129-156.
2. Tsangaris JM, &, Martin RB, (1970) Visible circular dichroism of copper (II) complexes of amino acids and peptides. J Am Chem Soc 92, 4255-4260.
3. Stephens PJ, &, Harada N, (2010) ECD cotton effect approximated by the Gaussian curve and other methods. Chirality 22, 229-233.
4. Autschbach J, (2009) Computing chiroptical properties with first-principles theoretical methods: background and illustrative examples. Chirality 21, E116-E152.
5. Mori T, &, Inoue Y, (2011) Recent theoretical and experimental advances in the electronic circular dichroisms of planar chiral cyclophanes. Top Curr Chem 298, 99-128.
6. Pescitelli G, Kurtan T, Florke U, &, Krohn K, (2009) Absolute structural elucidation of natural products-a focus on quantum-mechanical calculations of solid-state CD spectra. Chirality 21, E181-E201.
7. 2+ binding modes of full-length prion protein. J Biol Chem 283, 1870-1881.
8. Viles JH, Cohen FE, Prusiner SB, Goodin DB, Wright PE, &, Dyson HJ, (1999) Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci USA 96, 2042-2047.
9. Binolfi A, Quintanar L, Bertoncini CW, Griesinger C, &, Fernández CO, (2012) Bioinorganic chemistry of copper coordination to alpha-synuclein: relevance to Parkinson's disease. Coord Chem Rev 256, 2188-2201.
10. Rasia RM, Bertoncini CW, Marsh D, Hoyer W, Cherny D, Zweckstetter M, Griesinger C, Jovin TM, &, Fernández CO, (2005) Structural characterization of copper(II) binding to α-synuclein: insights into the bioinorganic chemistry of Parkinson's disease. Proc Natl Acad Sci USA 102, 4294-4299.
11. Bal W, Christodoulou J, Sadler PJ, &, Tucker A, (1998) Multi-metal binding site of serum albumin. J Inorg Biochem 70, 33-39.
12. Garnett AP, &, Viles JH, (2003) Copper binding to the octarepeats of the prion protein: affinity, specificity, folding, and cooperativity: insights from circular dichroism. J Biol Chem 278, 6795-6802.
13. Younan ND, Klewpatinond M, Davies P, Ruban AV, Brown DR, &, Viles JH, (2011) Copper(II)-induced secondary structure changes and reduced folding stability of the prion protein. J Mol Biol 410, 369-382.
14. Hasnip PJ, Refson K, Probert MI, Yates JR, Clark SJ, &, Pickard CJ, (2014) Density functional theory in the solid state. Philos Trans A Math Phys Eng Sci 372.
15. Bauernschmitt R, &, Ahlrichs R, (1996) Treatment of electronic excitations within the adiabatic approximation of time dependent density functional theory. Chem Phys Lett 256, 454-464.
16. Berti F, Gaggelli E, Guerrini R, Janicka A, Kozlowski H, Legowska A, Miecznikowska H, Migliorini C, Pogni R, Remelli M, et al,. (2007) Structural and dynamic characterization of copper(II) binding of the human prion protein outside the octarepeat region. Chemistry 13, 1991-2001.
17. Di Natale G, Osz K, Nagy ZN, Sanna D, Micera G, Pappalardo G, Sõvágõ I, &, Rizzarell E, (2009) Interaction of copper(II) with the prion peptide fragment HuPrP(76-114) encompassing four histidyl residues within and outside the octarepeat domain. Inorg Chem 48, 4239-4250.
18. Gralka E, Valensin D, Porciatti E, Gajda C, Gaggelli E, Valensin G, Kamysz W, Nadolny R, Guerrini R, Bacco D, et al,. (2008) CuII binding sites located at His-96 and His-111 of the human prion protein: thermodynamic and spectroscopic studies on model peptides. Dalton Trans 22, 5207-5219.
19. Jackson GS, Murray I, Hosszu LLP, Gibbs N, Waltho JP, Clarke AR, &, Collinge J, (2001) Location and properties of metal-binding sites on the human prion protein. Proc Natl Acad Sci USA 98, 8531-8535.
20. 2+ ions at physiological concentrations. J Mol Biol 346, 1393-1407.
21. 2+ histidine complexes: applications to the prion protein. FEBS Lett 581, 1430-1434.
22. 2+ binding to His96 or His111 of the prion protein and spectroscopic evidence for a multiple histidine binding only at low pH. Biochem J 404, 393-402.
23. Osz K, Nagy Z, Pappalardo G, Di Natale G, Sanna D, Micera G, Rizzarelli E, &, Sõvágõ I, (2007) Copper(II) interaction with prion peptide fragments encompassing histidine residues within and outside the octarepeat domain: speciation, stability constants and binding details. Chemistry 13, 7129-7143.
24. Stanyon HF, Patel K, Begum N, &, Viles JH, (2014) Copper(II) sequentially loads onto the N-terminal amino group of the cellular prion protein before the individual octarepeats. Biochemistry 53, 3934-3939.
25. Karavelas T, Mylonas M, Malandrinos G, Plakatouras JC, Hadjiliadis N, Mlynarz P, &, Kozlowski H, (2005) Coordination properties of Cu(II) and Ni(II) ions towards the C-terminal peptide fragment-ELAKHA-of histone H2B. J Inorg Biochem 99, 606-615.
26. Mylonas M, Krezel A, Plakatouras JC, Hadjiliadis N, &, Bal W, (2002) The binding of Ni(ii) ions to terminally blocked hexapeptides derived from the metal binding-ESHH-motif of histone H2A. J Chem Soc, Dalton Trans 38, 4296-4306.
27. Mylonas M, Plakatouras JC, Hadjiliadis N, Krȩzel A, &, Bal W, (2002) Potentiometric and spectroscopic studies of the interaction of Cu(II) ions with the hexapeptides AcThrAlaSerHisHisLysNH2, AcThrGluAlaHisHisLysNH2, AcThrGluSerAlaHisLysNH2 and AcThrGluSerHisAlaLysNH2, models of C-terminal tail of histone H2A. Inorg Chim Acta 339, 60-70.
28. Pace CN, Fu HL, Fryar KL, Landua J, Trevino SR, Shirley BA, Hendricks MM, Iimura S, Gajiwala K, Scholtz JM, et al,. (2011) Contribution of hydrophobic interactions to protein stability. J Mol Biol 408, 514-528.
29. 2+ bound single octarepeat. Dalton Trans 3, 509-518.
30. Sadler PJ, Tucker A, &, Viles JH, (1994) Involvement of a lysine residue in the N-terminal Ni2+ and Cu2+ binding site of serum albumins. Eur J Biochem 220, 193-200.
31. Bal W, Sokołowska M, Kurowska E, &, Faller P, (2013) Binding of transition metal ions to albumin: sites, affinities and rates. Biochim Biophys Acta 1830, 5444-5455.
32. Rõzga M, Sokołowska M, Protas AM, &, Bal W, (2007) Human serum albumin coordinates Cu (II) at its N-terminal binding site with 1 pM affinity. J Biol Inorg Chem 12, 913-918.
33. 2+. J Am Chem Soc 115, 9285-9286.
34. Bal W, Jeżowska-Bojczuk M, &, Kasprzak KS, (1997) Binding of nickel(II) and copper(II) to the N-terminal sequence of human protamine HP2. Chem Res Toxicol 10, 906-914.
35. Binolfi AS, Lamberto GR, Duran R, Quintanar L, Bertoncini CW, Souza JM, Cervenansky C, Zweckstetter M, Griesinger C, &, Fernandez CO, (2008) Site-specific interactions of Cu(II) with a and ß-synuclein: bridging the molecular gap between metal binding and aggregation. J Am Chem Soc 130, 11801-11812.
36. Asz K, Bõka B, Várnagy K, Sõvágõ I, Kurtán T, &, Antus S, (2002) The application of circular dichroism spectroscopy for the determination of metal ion speciation and coordination modes of peptide complexes. Polyhedron 21, 2149-2159.
37. 2+ affinities for the prion protein. Biochemistry 48, 8929-8931.
38. Heyd J, Scuseria GE, &, Ernzerhof M, (2003) Hybrid functionals based on a screened Coulomb potential. J Chem Phys 118, 8207-8215.
39. Strati GL, Willett JL, &, Momany FA, (2002) A DFT/ab initio study of hydrogen bonding and conformational preference in model cellobiose analogs using B3LYP/6-311 + +G. Carbohydr Res 337, 1851-1859.
40. Cossi M, Rega N, Scalmani G, &, Barone V, (2003) Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J Comput Chem 24, 669-681.
41. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, et al,. (2009) Gaussian 09, Gaussian, Inc., Wallingford, CT, USA.
42. O'Boyle NM, Tenderholt AL, &, Langner KM, (2008) cclib: a library for package-independent computational chemistry algorithms. J Comput Chem 29, 839-845.