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EPR and NMR spectroscopies provide input on the coordination of Cu(I) and Ag(I) to a disordered methionine segment

  • Yulia Shenberger
  • Hugo E. Gottlieb
  • Sharon RuthsteinEmail author
Original Paper

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.

Keywords

Methionine segments Cu(I)/Ag(I) transport DEER Q-band Site-directed spin labeling 

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

Notes

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.

References

  1. 1.
    Fabisiak JP, Tyurin VA, Tyurina YY, Borisenko GG, Korotaeve A, Pitt BR, Lazo JS, Kagan VE (1999) Arch Biochem Biophys 363:171–181CrossRefPubMedGoogle Scholar
  2. 2.
    Haas KL, Putterman AB, White DR, Thiele DJ, Franz KJ (2011) J Am Chem Soc 133:4427–4437CrossRefPubMedCentralPubMedGoogle Scholar
  3. 3.
    Jiang J, Nadas IA, Alison Kim M, Franz KJ (2005) Inorg Chem 44:9787–9794CrossRefPubMedGoogle Scholar
  4. 4.
    Rubino JT, Riggs-Gelasco P, Franz KJ (2010) J Biol Inorg Chem 15:1033–1049CrossRefPubMedGoogle Scholar
  5. 5.
    Aller SG, Unger VM (2006) Proc Natl Acad Sci 103:3627–3632CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM (2009) Proc Natl Acad Sci 106:4237–4242CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    De Feo CJ, Aller SG, Unger VM (2007) Biometals 20:705–716CrossRefPubMedGoogle Scholar
  8. 8.
    Maryon EB, Molloy SA, Ivy K, Yu H, Kaplan JH (2013) J Biol Chem 288:18035–18046CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Xue Y, Davis AV, Balakrishan G, Stasser JP, Staehlin BM, Focia P, Spiro TG, Penner-Hahn JE, O’Halloran TV (2008) Nat Chem Biol 4:107–109CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Huffman DL, Huyett J, Wayne Outten F, Doan PE, Finney LA, Hoffmann BM, O’Halloran TV (2002) Biochem 41:10046–10055CrossRefGoogle Scholar
  11. 11.
    Skvortsov AN, Zatulovskiy EA, Puchkova LV (2012) Mol Biol 46:335–347CrossRefGoogle Scholar
  12. 12.
    Cason JS, Lowbury EJ (1968) Lancet 1:651–654CrossRefPubMedGoogle Scholar
  13. 13.
    Drake PL, Hazelwood KJ (2005) Ann Occup Hyg 49:575–585CrossRefPubMedGoogle Scholar
  14. 14.
    Modak SM, Sampath L, Fox CL Jr (1988) J Burn Care Rehabil 9:359–363CrossRefPubMedGoogle Scholar
  15. 15.
    Fung MC, Bowen DL (1996) J Toxicol Clin Toxicol 34:119–126CrossRefPubMedGoogle Scholar
  16. 16.
    Gulbranson SH, Hud JA, Hansen RC (2000) Cutis 66:373–374PubMedGoogle Scholar
  17. 17.
    Shelley WB, Shelley ED, Burmeister V (1987) J Am Acad Deratol 16:211–217CrossRefGoogle Scholar
  18. 18.
    Bertinato J, Cheung L, Hoque R, Plouffe LJ (2010) J Trace Elem Med Biol 24:178–184CrossRefPubMedGoogle Scholar
  19. 19.
    Ibricevic A, Brody SL, Youngs WJ, Cannon CL (2010) Toxic Appl Pharm 243:315–322CrossRefGoogle Scholar
  20. 20.
    Lee J, Pena MMO, Nose Y, Thiele DJ (2002) J Biol Chem 277:4380–4387CrossRefPubMedGoogle Scholar
  21. 21.
    Wernimont AK, Huffman DL, Finney LA, Demeler B, O’Halloran TV, Rosenzweig AC (2003) J Biol Inorg Chem 8:185–194CrossRefPubMedGoogle Scholar
  22. 22.
    Banham JE, Baker CM, Ceola S, Day IJ, Grant GH, Groenen EJJ, Rodgers CT, Jeschke G, Timmel CR (2008) J Magn Reson 191:202–218CrossRefPubMedGoogle Scholar
  23. 23.
    Banham JE, Jeschke G, Timmel CR (2007) Mol Phys 105:2041–2047CrossRefGoogle Scholar
  24. 24.
    Bennati M, Robblee JH, Mugnaini V, Stubbe J, Freed JH, Borbat P (2005) J Am Chem Soc 127:15014–15015CrossRefPubMedGoogle Scholar
  25. 25.
    Borbat PP, Surendhran K, Bortolus M, Zou P, Freed JH, Mchaourab HS (2007) PLoS Biol 5:2211–2219CrossRefGoogle Scholar
  26. 26.
    Hemminga MA, Berliner LJ (2007) ESR Spectroscopy in Membrane Biophysics. Springer Science + Business Media, LLCGoogle Scholar
  27. 27.
    Hilger D, Jung H, Padan E, Wegener C, Vogel KP, Steinhoff HJ, Jeschke G (2005) Biophys J 89:1328–1338CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Jeschke G, Polyhach Y (2007) Phys Chem Chem Phys 9:1895–1910CrossRefPubMedGoogle Scholar
  29. 29.
    Raitsimring AM, Gunanathan C, Potapov A, Efremenko I, Martin JML, Milstein D, Goldfarb D (2007) J Am Chem Soc 129:14138–14139CrossRefPubMedGoogle Scholar
  30. 30.
    Sicoli G, Mathis G, Delalande O, Boulard Y, Gasparutto D, Garnbarelli S (2008) Angew Chem Int Ed 47:735–737CrossRefGoogle Scholar
  31. 31.
    Xu Q, Ellena JF, Kim M, Cafiso DS (2006) Biochem 45:10847–10854CrossRefGoogle Scholar
  32. 32.
    Sahu ID, Kroncke BM, Zhang R, Dunagan MM, Smith HJ, Craig A, McCarrick RM, Sanders CR, Lorigan GA (2014) Biochem 53:6391–6401CrossRefGoogle Scholar
  33. 33.
    Atherton NM (1993) Principles of electron spin resonance. Ellis Horwood PTR Prentice Hall, EnglandGoogle Scholar
  34. 34.
    Weil JA, Bolton JR (2007) Electron paramagnetic resonance. Wiley, HobokenGoogle Scholar
  35. 35.
    Schweiger A, Jeschke G (2001) Principles of electron paramgnetic resonance. University Press, OxfordGoogle Scholar
  36. 36.
    Pannier M, Veit S, Godt A, Jeschke G, Spiess HW (2000) J Magn Reson 142:331–340CrossRefPubMedGoogle Scholar
  37. 37.
    Milov AD, Tsvetkov YD (1997) Appl Magn Reson 12:495–504CrossRefGoogle Scholar
  38. 38.
    Joseph B, Morkhov VM, Yulikov M, Jeschke G, Bordignon E (2014) J Biol Chem 289:3176–3185CrossRefPubMedCentralPubMedGoogle Scholar
  39. 39.
    Sahu ID, McCarrick RM, Troxel KR, Zhang R, Smith HJ, Dunagan MM, Swartz MS, Rajan PV, Kroncke BM, Sanders CR, Lorigan GA (2013) Biochem 52:6627–6632CrossRefGoogle Scholar
  40. 40.
    Hubbell WL, Gross A, Langen R, Lietzow MA (1998) Curr Opin Struct Biol 8:649–656CrossRefPubMedGoogle Scholar
  41. 41.
    Columbus L, Hubbell WL (2002) Trend Biochem Sci 27:288–295CrossRefPubMedGoogle Scholar
  42. 42.
    Hubbell WL, Mchaourab HS, Altenbach C, Lietzow MA (1996) Structure 4:779–783CrossRefPubMedGoogle Scholar
  43. 43.
    Shenberger Y, Yarmiayev V, Ruthstein S (2013) Mol Phys 111:2980–2991CrossRefGoogle Scholar
  44. 44.
    Jeschke G (2007) Bio Magn Res 27:287–288Google Scholar

Copyright information

© SBIC 2015

Authors and Affiliations

  • Yulia Shenberger
    • 1
  • Hugo E. Gottlieb
    • 1
  • Sharon Ruthstein
    • 1
    Email author
  1. 1.The Department of Chemistry, Faculty of Exact SciencesBar Ilan UniversityRamat-GanIsrael

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