Abstract
Methionine motifs are methionine-rich metal-binding segments found in many human, yeast, and bacterial proteins involved in the transportation of copper ion to other cellular pathways, and in protecting copper from oxidation. Methionine motifs are found to bind Ag(I) and Cu(I) ions. Proteins or peptides that can bind different metal ions should have the ability to differentiate between them, to be able to shuttle them to various pathways in the cell. This study utilizes electron paramagnetic resonance spectroscopy together with circular dichroism and nuclear magnetic resonance to probe structural changes in the methionine segment upon coordinating Cu(I) and Ag(I) metal ions. The data collected here indicate that methionine segments experience structural changes while coordinating Cu(I) and Ag(I), however, the differences between the coordination of Cu(I) vs. Ag(I) to the methionine segment are mild. Since Cu(I) and Ag(I) metal ions are pretty similar in their nature and charge, the minor structural changes reported here are significant towards the understanding of the differences in the transport mechanism of these two metal ions in prokaryotic and eukaryotic cells.
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Abbreviations
- CD:
-
Circular dichroism
- CW:
-
Continuous wave
- DEER:
-
Double electron–electron resonance
- EPR:
-
Electron paramagnetic resonance
- Met:
-
Methionine
- 5-MSL:
-
3-Maleimido-proxyl
- MTSSL:
-
(1-Oxyl-2,2,5,5-tetramethyl-2,5-pyrroline-3-methyl) methanethiosulfonate
- NMR:
-
Nuclear magnetic resonance
- SDSL:
-
Site-directed spin-labeling
References
Fabisiak JP, Tyurin VA, Tyurina YY, Borisenko GG, Korotaeve A, Pitt BR, Lazo JS, Kagan VE (1999) Arch Biochem Biophys 363:171–181
Haas KL, Putterman AB, White DR, Thiele DJ, Franz KJ (2011) J Am Chem Soc 133:4427–4437
Jiang J, Nadas IA, Alison Kim M, Franz KJ (2005) Inorg Chem 44:9787–9794
Rubino JT, Riggs-Gelasco P, Franz KJ (2010) J Biol Inorg Chem 15:1033–1049
Aller SG, Unger VM (2006) Proc Natl Acad Sci 103:3627–3632
De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM (2009) Proc Natl Acad Sci 106:4237–4242
De Feo CJ, Aller SG, Unger VM (2007) Biometals 20:705–716
Maryon EB, Molloy SA, Ivy K, Yu H, Kaplan JH (2013) J Biol Chem 288:18035–18046
Xue Y, Davis AV, Balakrishan G, Stasser JP, Staehlin BM, Focia P, Spiro TG, Penner-Hahn JE, O’Halloran TV (2008) Nat Chem Biol 4:107–109
Huffman DL, Huyett J, Wayne Outten F, Doan PE, Finney LA, Hoffmann BM, O’Halloran TV (2002) Biochem 41:10046–10055
Skvortsov AN, Zatulovskiy EA, Puchkova LV (2012) Mol Biol 46:335–347
Cason JS, Lowbury EJ (1968) Lancet 1:651–654
Drake PL, Hazelwood KJ (2005) Ann Occup Hyg 49:575–585
Modak SM, Sampath L, Fox CL Jr (1988) J Burn Care Rehabil 9:359–363
Fung MC, Bowen DL (1996) J Toxicol Clin Toxicol 34:119–126
Gulbranson SH, Hud JA, Hansen RC (2000) Cutis 66:373–374
Shelley WB, Shelley ED, Burmeister V (1987) J Am Acad Deratol 16:211–217
Bertinato J, Cheung L, Hoque R, Plouffe LJ (2010) J Trace Elem Med Biol 24:178–184
Ibricevic A, Brody SL, Youngs WJ, Cannon CL (2010) Toxic Appl Pharm 243:315–322
Lee J, Pena MMO, Nose Y, Thiele DJ (2002) J Biol Chem 277:4380–4387
Wernimont AK, Huffman DL, Finney LA, Demeler B, O’Halloran TV, Rosenzweig AC (2003) J Biol Inorg Chem 8:185–194
Banham JE, Baker CM, Ceola S, Day IJ, Grant GH, Groenen EJJ, Rodgers CT, Jeschke G, Timmel CR (2008) J Magn Reson 191:202–218
Banham JE, Jeschke G, Timmel CR (2007) Mol Phys 105:2041–2047
Bennati M, Robblee JH, Mugnaini V, Stubbe J, Freed JH, Borbat P (2005) J Am Chem Soc 127:15014–15015
Borbat PP, Surendhran K, Bortolus M, Zou P, Freed JH, Mchaourab HS (2007) PLoS Biol 5:2211–2219
Hemminga MA, Berliner LJ (2007) ESR Spectroscopy in Membrane Biophysics. Springer Science + Business Media, LLC
Hilger D, Jung H, Padan E, Wegener C, Vogel KP, Steinhoff HJ, Jeschke G (2005) Biophys J 89:1328–1338
Jeschke G, Polyhach Y (2007) Phys Chem Chem Phys 9:1895–1910
Raitsimring AM, Gunanathan C, Potapov A, Efremenko I, Martin JML, Milstein D, Goldfarb D (2007) J Am Chem Soc 129:14138–14139
Sicoli G, Mathis G, Delalande O, Boulard Y, Gasparutto D, Garnbarelli S (2008) Angew Chem Int Ed 47:735–737
Xu Q, Ellena JF, Kim M, Cafiso DS (2006) Biochem 45:10847–10854
Sahu ID, Kroncke BM, Zhang R, Dunagan MM, Smith HJ, Craig A, McCarrick RM, Sanders CR, Lorigan GA (2014) Biochem 53:6391–6401
Atherton NM (1993) Principles of electron spin resonance. Ellis Horwood PTR Prentice Hall, England
Weil JA, Bolton JR (2007) Electron paramagnetic resonance. Wiley, Hoboken
Schweiger A, Jeschke G (2001) Principles of electron paramgnetic resonance. University Press, Oxford
Pannier M, Veit S, Godt A, Jeschke G, Spiess HW (2000) J Magn Reson 142:331–340
Milov AD, Tsvetkov YD (1997) Appl Magn Reson 12:495–504
Joseph B, Morkhov VM, Yulikov M, Jeschke G, Bordignon E (2014) J Biol Chem 289:3176–3185
Sahu ID, McCarrick RM, Troxel KR, Zhang R, Smith HJ, Dunagan MM, Swartz MS, Rajan PV, Kroncke BM, Sanders CR, Lorigan GA (2013) Biochem 52:6627–6632
Hubbell WL, Gross A, Langen R, Lietzow MA (1998) Curr Opin Struct Biol 8:649–656
Columbus L, Hubbell WL (2002) Trend Biochem Sci 27:288–295
Hubbell WL, Mchaourab HS, Altenbach C, Lietzow MA (1996) Structure 4:779–783
Shenberger Y, Yarmiayev V, Ruthstein S (2013) Mol Phys 111:2980–2991
Jeschke G (2007) Bio Magn Res 27:287–288
Acknowledgments
This study was supported by the Israel Science Foundation, Grant No. 280/12. The Elexsys E580 Bruker EPR spectrometer was partially supported by the Israel Science Foundation, Grant No. 564/12.
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Shenberger, Y., Gottlieb, H.E. & Ruthstein, S. EPR and NMR spectroscopies provide input on the coordination of Cu(I) and Ag(I) to a disordered methionine segment. J Biol Inorg Chem 20, 719–727 (2015). https://doi.org/10.1007/s00775-015-1259-1
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DOI: https://doi.org/10.1007/s00775-015-1259-1