A novel copper(II) coordination at His186 in full-length murine prion protein

Biochemical and Biophysical Research Communications

Volumn 394, Issue 3, 2010, Pages 522-528

  Watanabe, Yasuko ^a   Hiraoka, Wakako ^b   Igarashi, Manabu ^c   Ito, Kimihito ^c   Shimoyama, Yuhei ^d   Horiuchi, Motohiro ^a   Yamamori, Tohru ^a   Yasui, Hironobu ^a   Kuwabara, Mikinori ^a   Inagaki, Fuyuhiko ^c   Inanami, Osamu ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b MEIJI UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d MURORAN INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

C terminal domain; Cu(II); Dipolar interaction; ESR; Histidine residue; Interspin distance; MTSSL; Prion protein; SDSL

Indexed keywords

COPPER COMPLEX; CUPRIC ION; PRION PROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; COMPUTER SIMULATION; DIPOLE; ELECTRON SPIN RESONANCE; METAL BINDING; PRIORITY JOURNAL;

ANIMALS; COPPER; HISTIDINE; HYDROPHOBICITY; MICE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PRPC PROTEINS;

MURINAE;

EID: 77950515898     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.03.003     Document Type: Article

References (32)

1. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. USA 95 (1998) 13363-13383
2. Hornemann S., and Glockshuber R. A scrapie-like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH. Proc. Natl. Acad. Sci. USA 95 (1998) 6010-6014
3. Quaglio E., Chiesa R., and Harris D.A. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 276 (2001) 11432-11438
4. res. FASEB J. 19 (2005) 783-785
5. Vey M., Pilkuhn S., Wille H., Nixon R., DeArmond S.J., Smart E.J., Anderson R.G., Taraboulos A., and Prusiner S.B. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl. Acad. Sci. USA 93 (1996) 14945-14949
6. Riek R., Hornemann S., Wider G., Billeter M., Glockshuber R., and Wüthrich K. NMR structure of the mouse prion protein domain PrP(121-231). Nature 382 (1996) 180-182
7. Whittal R.M., Ball H.L., Cohen F.E., Burlingame A.L., Prusiner S.B., and Baldwin M.A. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci. 9 (2000) 332-343
8. Jackson G.S., Murray I., Hosszu L.L.P., Gibbs N., Waltho J.P., Clarke A.R., and Collinge J. Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. USA 98 (2001) 8531-8535
9. Hornemann S., Korth C., Oesch B., Rieka R., Widera G., Wüthrich K., and Glockshubera R. Recombinant full-length murine prion protein, mPrP(23-231): purification and spectroscopic characterization. FEBS Lett. 413 (1997) 277-281
10. Burns C.S., Aronoff-Spencer E., Dunham C.M., Lario P., Avdievich N.I., Antholine W.E., Olmstead M.M., Vrielink A., Gerfen G.J., Peisach J., Scott W.G., and Millhauser G.L. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41 (2002) 3991-4001
11. 2+ binding region in full-length human prion protein, Eur. Biophys. J. 36 (2007) 239-252.
12. 2+ binding region in full-length human prion protein compared with the isolated octapeptide. Vet. Microbiol. 123 (2007) 358-366
13. Hasnain S.S., Murphy L.M., Strange R.W., Grossmann J.G., Clarke A.R., Jackson G.S., and Collinge J. XAFS study of the high-affinity copper-binding site of human PrP(91-231) and its low-resolution structure in solution. J. Mol. Biol. 311 (2001) 467-473
14. 2+ coordination by His96 and His111 induces β-sheet formation in the unstructured amyloidogenic region of the prion protein, J. Biol. Chem. 279 (2004) 32018-32027.
15. Berti F., Gaggelli E., Guerrini R., Janicka A., Kozlowski H., Legowska A., Miecznikowska H., Migliorini C., Pogni R., Remelli M., Rolka K., Valensin D., and Valensin G. Structural and dynamic characterization of copper(II) binding of the human prion protein outside the octarepeat region. Chemistry 13 (2007) 1991-2001
16. 2+ to the C-terminal domain of the murine prion protein. Biophys. J. 81 (2001) 516-525
17. Brown D.R., Guantieri V., Grasso G., Impellizzeri G., Pappalardo G., and 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. 98 (2004) 133-143
18. Grasso D., Grasso G., Guantieri V., Impellizzeri G., La Rosa C., Milardi D., Micera G., Õsz K., Pappalardo G., Rizzarelli E., Sanna D., and Sóvágó I. Environmental effects on a prion's helix II domain: copper(II) and membrane interactions with PrP180-193 and its analogues. Chemistry 12 (2005) 537-547
19. Inanami O., Hashida S., Iizuka D., Horiuchi M., Hiraoka W., Shimoyama Y., Nakamura H., Inagaki F., and Kuwabara M. Conformational change in full-length mouse prion: a site-directed spin-labeling study. Biochem. Biophys. Res. Commun. 335 (2005) 785-792
20. Watanabe Y., Inanami O., Horiuchi M., Hiraoka W., Shimoyama Y., Inagaki F., and Kuwabara M. Identification of pH-sensitive regions in the mouse prion by the cysteine-scanning spin-labeling ESR technique. Biochem. Biophys. Res. Commun. 350 (2006) 549-556
21. Watanabe Y., Hiraoka W., Shimoyama Y., Horiuchi M., Kuwabara M., and Inanami O. Instability of familial spongiform encephalopathy-related prion mutants. Biochem. Biophys. Res. Commun. 366 (2008) 244-249
22. Chiang Y.W., Otoshima Y., Watanabe Y., Inanami O., and Shimoyama Y. Dynamics and local ordering of spin-labeled prion protein: an ESR simulation study of a highly pH-sensitive site. J. Biomol. Struct. Dyn. 26 (2008) 355-366
23. Hubbell W.L., Mchaourab H.S., Altenbach C., and Lietzow M.A. Watching proteins move using site-directed spin labeling. Structure 4 (1996) 779-783
24. Hubbell W.L., Cafiso D.S., and Altenbach C. Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7 (2000) 735-739
25. Leigh Jr. J.S. ESR rigid-lattice line shape in a system of two interacting spins. J. Chem. Phys. 52 (1970) 2608-2612
26. Voss J., Salwiński L., Kaback H.R., and Hubbell W.L. A method for distance determination in proteins using a designed metal ion binding site and site-directed spin labeling: evaluation with T4 lysozyme. Proc. Natl. Acad. Sci. USA 92 (1995) 12295-12299
27. Kim C.L., Umetani A., Matsui T., Ishiguro N., Shinagawa M., and Horiuchi M. Antigenic characterization of an abnormal isoform of prion protein using a new diverse panel of monoclonal antibodies. Virology 320 (2004) 40-51
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., and Karplus M. CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4 (1983) 187-217
30. K. Sale, C. Sar, K.A. Sharp, K. Hideg, P.G. Fajer, Structural determination of spin label immobilization and orientation: a Monte Carlo minimization approach, J. Magn. Reson. 156 (104) (2002) 12.
31. Langella E., Improta R., and Barone V. Checking the pH-induced conformational transition of prion protein by molecular dynamics simulations: effect of protonation of histidine residues. Biophys. J. 87 (2004) 3623-3632
32. Cervenakova L., Buetefisch C., Lee H.S., Taller I., Stone G., Gibbs Jr. C.J., Brown P., Hallett M., and Goldfarb L.G. Novel PRNP sequence variant associated with familial encephalopathy. Am. J. Med. Genet. 88 (1999) 653-656