SpringerProtocols: Abstract: 13. Biophysical Investigations of the Prion Protein Using Electron Paramagnetic Resonance

13. Biophysical Investigations of the Prion Protein Using Electron Paramagnetic Resonance

By: Simon C. Drew^{3 4}, Kevin J. Barnham³

Abstract

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The binding of paramagnetic metal ions is thought to be an essential function of the prion protein and lends itself to interrogation by electron paramagnetic resonance (EPR), which probes the local coordination environment of bound metal ions to provide details of the metal-binding affinity, stoichiometry, and the symmetry and identity of its ligating atoms. It is also capable of identifying reactive oxygen/nitrogen species and peptide-derived radicals, in addition to monitoring protein-membrane dynamics and conformation by using site-directed spin labeling. An overview of the EPR technique as applied to the prion protein is given, key results are summarized, and some future experimental avenues are outlined.

Affiliation(s): (3) Department of Pathology and Mental Health Research Institute of Victoria, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Melbourne, Australia
(4) School of Physics, Monash University, Melbourne, Australia

Book Title: Prion Protein Protocols

Series: Methods in Molecular Biology | Volume: 459 | Pub. Date: Jun-04-2008 | Page Range: 173-196 | DOI: 10.1007/978-1-59745-234-2_13

Subject: Protein Science

Key Words: Magnetic resonance - metalloprotein - site-directed spin labeling - spin-trapping

References

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1.	Jószai V, Zoltán N, Ősz K, Sanna D, Di Natale G, La Mendola D, Pappalardo G, Rizzarelli E, Sóvágó I (2006) Transition metal complexes of terminally protected peptides containing histidyl residues. J. Inorg. Biochem. 100: 1399–1409.

2.	Deloncle R, Guillard O, Bind JL, Delaval J, Fleury N, Mauco G, Lesage G (2006) Free radical generation of protease-resistant prion after substitution of manganese for copper in bovine brain homogenate. Neurotoxicology 27: 437–444.

3.	Brown DR, Hafiz F, Glassmith LL, Wong B-S, Jones IM, Clive C, Haswell S (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19: 1180–1186.

4.	Gaggelli E, Bernardi F, Molteni F, Pogni R, Valensin D, Valensin G, Remelli M, Luczkowski M, Kozlowski H (2005) J. Am. Chem. Soc. 127: 996–1006.

5.	Sutoh Y, Nishida Y (2005) Formation of a Mn(IV) species in the reaction mixture of a manganese(II) complex and an aliphatic aldehyde. Synthesis and Reactivity in Inorganic, Metal-Organic and Nano-Metal Chemistry 35: 575–577.

6.	Pilbrow JR (1990) Transition Ion Electron Paramagnetic Resonance, Oxford, UK: Clarendon Press.

7.	Abragam A, Bleaney B (1970) Electron Paramagnetic Resonance of Transition Ions, Oxford, UK: Clarendon Press.

8.	Pake GE, Estle TL (1973) The Physical Principles of Electron Paramagnetic Resonance, New York: WA Benjamin.

9.	Schweiger A, Jeschke G (2001) Principles of Pulse Electron Paramagnetic Resonance, Oxford, UK: Oxford University Press.

10.	Berliner LJ (ed) (1976) Spin Labeling—Theory and Applications, New York: Academic Press.

11.	Boas JF, Pilbrow JR, Smith TD (1978) ESR of copper in biological systems. In: Biological Magnetic Resonance, Vol. 1, Berliner LJ and Reuben J (eds), New York: Plenum Press, 277–342.

12.	Boas JF (1984) Electron paramagnetic resonance of copper proteins. In: Copper Proteins and Copper Enzymes, Vol. 1, Lontie R (ed), Boca Raton, FL: CRC Press, 5–62.

13.	Deligiannakis Y, Louloudi M, Hadjiliadis N (2000) Electron spin echo envelope modulation (ESEEM) spectroscopy as a tool to investigate the coordination environment of metal centers. Coord Chem Rev 204: 1–112.

14.	Wong B-S, Vénien-Bryan C¯, Williamson RA, Burton DR, Gambetti P, Sy M-S, Brown DR, Jones IM (2000) Copper refolding of prion protein. Biochem. Biophys. Res. Commun. 276: 1217–1224.

15.	Kaupp M, Bühl M, Malkin VG (Eds) (2004) Calculation of NMR and EPR Parameters: Theory and Applications, Wiley-VCH, Germany: Weinheim.

16.	Peisach J, Blumberg WE (1974) Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch. Biochem. Biophys. 165: 691–708.

17.	Palmer G (1985) The electron paramagnetic resonance of metalloproteins. Biochem. Soc. Trans. 13: 548, 560.

18.	Pauly PC, Harris DA (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273: 33107–33110.

19.	Sakaguchi U, Addison AW (1979) Spectroscopic and redox studies of some copper(II) complexes with biomimetic donor atoms: implications for protein copper centres. J. Chem. Soc. Dalton Trans. 4: 600–608.

20.	Jeschke G (1996) PhD thesis, Swiss Federal Institute of Technology, section 6.3.2.

21.	Janzen EG (1971) Spin trapping. Acc. Chem. Res. 4: 31–40.

22.	Mason RP, Buettner GR (2003) Spin-trapping methods for detecting superoxide and hydroxyl free radicals in vitro and in vivo. In: Critical Reviews of Oxidative Stress and Aging: Advances in Basic Science, Diagnostics and Intervention, Cutker RG and Rodriguez H (eds), Hackensack, NJ: World Scientific, 27–38.

23.	Kennedy CH, Maples KR, Mason RP (1990) In vivo detection of free radical metabolites. Pure Appl. Chem. 62: 95–299.

24.	Shi H, Timmins G, Monske M, Burdick A, Kalyanaraman B, Liu Y, Clément J-L, Burchiel S, Liu KJ (2005) Evaluation of spin trapping agents and trapping conditions for detection of cell-generated reactive oxygen species. Arch. Biochem. Biophys. 437: 59–68.

25.	Haya A, Burkittb MJ, Jones CM, Hartley RC (2005) Development of a new EPR spin trap DOD-8C for the trapping of lipid radicals at a predetermined depth within biological membranes. Arch. Biochem. Biophys. 435: 336–346.

26.	Turnbull S, Tabner BJ, Brown DR, Allsop D (2003) Copper-dependent generation of hydrogen peroxide from the toxic prion protein fragment PrP106—126. Neurosci. Lett. 336: 159–162.

27.	Turnbull S, Tabner BJ, Brown DR, Allsop D (2003) Generation of hydrogen peroxide from mutant forms of the prion protein fragment PrP121—231. Biochemistry 42: 7675–7681.

28.	Tabner BJ, Turnbull S, Fullwood NJ, German M, and Allsop D (2005) The production of hydrogen peroxide during early-stage protein aggregation: a common pathological mechanism in different neurodegenerative diseases? Biochem. Soc. Trans. 33: 548–550.

29.	Barnham KJ, Haeffner F, Ciccotosto GD, Curtain CC, Tew D, Carrington D, Mavros C, Beyreuther C, Carrington R, Masters CL, Cherny RA, Cappai R, Bush AI (2004) Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease β-amyloid. FASEB J. 2004; 18: 1427–1429.

30.	Barnham KJ, Cappai R, Beyreuther K, Masters CL, Hill AF (2006) Delineating common molecular mechanisms in Alzheimer's and prion diseases. Trends Biochem. Sci. 31: 465–472.

31.	Berliner L (1983) The spin-label approach to labeling membrane protein sulfhydryl groups. Ann. N Y Acad. Sci. 414: 153–161.

32.	Lundberg KM, Stenland CJ, Cohen FE, Prusiner SB, Millhauser GL (1997) Kinetics and mechanism of amyloid formation by the prion protein H1 peptide as determined by time-dependent ESR. Chem. Biol. 4: 345–355.

33.	Inanami O, Hashida S, Iizuka D, Horiuchi M, Hiraoka W, Shimoyama Y, Nakamura H, Inagaki F, Kuwabara M. (2005) Conformational change in full-length mouse prion: a site-directed spin-labeling study. Biochem. Biophys. Res. Commun. 335: 785–792.

34.	Watanabe Y, Inanami O, Horiuchi M, Hiraoka W, Shimoyama Y, Inagaki F, Kuwabara M (2006) Identification of pH-sensitive regions in the mouse prion by the cysteine-scanning spin-labeling ESR technique. Biochem. Biophys. Res. Commun. 350: 549–556.

35.	Aronoff-Spencer E, Burns CS, Avdievich NI, Gerfen GJ, Peisach J, Antholine WE, Ball HL, Cohen FE, Prusiner SB, Millhauser GL (2000) Identification of the Cu²⁺ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry 39: 13760–13771.

36.	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 (2002) Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41: 3991–4001.

37.	Millhauser GL (2004) Copper binding in the prion protein. Acc. Chem. Res. 37: 79–85.

38.	Chattopadhyay M, Walter ED, Newell DJ, Jackson PJ, Aronoff-Spencer E, Peisach J, Gerfen GJ, Bennett B, Antholine WE, Millhauser GL (2005) The octarepeat domain of the prion protein binds Cu(II) with three distinct coordination modes at pH 7.4. J. Am. Chem. Soc. 127: 12647–12656.

39.	Walter ED, Chattopadhyay M, Millhauser GL (2006) The affinity of copper binding to the prion protein octarepeat domain: evidence for negative cooperativity. Biochemistry 45: 13083–13092.

40.	del Pino P, Weiss A, Bertsch U, Renner C, Mentler M, Grantner K, Fiorino F, Meyer-Klaucke W, Moroder L, Kretzschmar HA, Parak FG (2007) The configuration of the Cu²⁺ binding region in full-length human prion protein. Eur. Biophys. J. 36: 239–252.

41.	Cereghetti GM, Schweiger A, Glockshuber R, Van Doorslaer SV (2001) Electron paramagnetic resonance evidence for binding of the Cu²⁺ to the C-terminal domain of the murine prion protein. Biophys. J. 81: 516–525.

42.	Van Doorslaer S V, Cereghetti GM, Glockshuber R, Schweiger A (2001) Unraveling the Cu²⁺ binding sites in the C-terminal domain of the murine prion protein: a pulse EPR and ENDOR study. J. Phys. Chem. B 105: 1631–1639.

43.	Burns CS, Aronoff-Spencer E, Legname G, Prusiner S, Antholine WE, Gerfen GJ, Peisach J, Millhauser GL. (2003) Copper coordination in the full-length prion protein. Biochemistry 42: 6794–6803.

44.	Hureau C, Charlet L, Dorlet P, Gonnet F, Spadini L, Anxolabéhère-Mallart E, Girerd J-J (2006) A spectroscopic and voltammetric study of the pH-dependent Cu(II) coordination to the peptide GGGTH: relevance to the fifth Cu(II) site in the prion protein. J. Biol. Inorg. Chem. 11: 735–744.

45.	Jobling MF, Huang X, Stewart LR, Barnham KJ, Curtain C,Volitakis I, Perugini M, White AR, Cherny RA, Masters CL, Barrow CJ, Collins SJ, Bush AI, Cappai R (2001) Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP1067#x2014;126. Biochemistry 40: 8073–8084.

46.	Belosi B, Gaggelli E, Guerrini R, Kozlowski H, Luczkowski M, Mancini FM, Remelli M, Valensin D, Valensin G. (2004) Copper binding to the neurotoxic peptide PrP_106–126: thermodynamic and structural studies. Chem. Biol. Chem. 5: 349–359.

47.	Jones CE, Abdelraheim SR, Brown DR, Viles JH (2004) Preferential Cu²⁺ coordination by His96 and His111 induces β sheet formation in the unstructured amyloidogenic region of the prion protein. J. Biol. Chem. 279: 32018–32027.

48.	Cereghetti GM, Schweiger A, Glockshuber R, Van Doorslaer S (2003) Stability and Cu(II) binding of prion protein variants related to inherited human prion diseases. Biophys. J. 84: 1985–1997.

49.	Grasso D, Grasso G, Guantieri V, Impellizzeri G, La Rosa C, Milardi D, Micera G, Õsz K, Pappalardo G, Rizzarelli E, Sanna D, Sóvágó I (2006) Environmental effects on a prion's Helix II domain: copper(II) and membrane interactions with PrP180—193 and its analogues. Chem. Eur. J. 12: 537–547.

50.	Brown DR, Guantieri V, Grasso G, Impellizzeri G, Pappalardo G, Rizzarelli E (2004) 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: 133–143.

51.	Renner C, Fiori S, Fiorino F, Landgraf D, Deluca D, Mentler M, Grantner K, Parak FG, Kretzschmar H, Moroder L (2004) Micellar environments induce structuring of the N-terminal tail of the prion protein. Biopolymers 73: 421–433.

52.	Hicks MR, Gill AC, Bath IK, Rullay AK, Sylvester ID, Crout DH,Pinheiro TJT (2006) Synthesis and structural characterization of a mimetic membrane-anchored prion protein. FEBS J. 273: 1285–1299.

53.	Blough NV, Simpson DJ (1998) Chemically mediated fluorescence yield switching in nitroxide-fluorophore adducts: optical sensors of radical/redox reactions. J. Am. Chem. Soc. 110: 1915–1917.

54.	Jiang J, Borisenko GG, Osipov A, Martin I, Chen R, Shvedova AA, Sorokin A, Tyurina YY, Potapovich A, Tyurin VA, Graham SH, KaganVE (2004) Arachidonic acid-induced carbon-centered radicals and phospholipid peroxidation in cyclo-oxygenase-2-transfected PC12 cells. J. Neurochem. 90: 1036–1049.

55.	Ramirez DC, Gomez Mejiba SE, Mason RP (2005) Copper-catalyzed protein oxidation and its modulation by carbon dioxide. J. Biol. Chem. 280: 27402–27411.

56.	Abdelraheim SR, Královicová S, Brown DR (2006) Hydrogen peroxide cleavage of the prion protein generates a fragment able to initiate polymerisation of full length prion protein. Int. J. Biochem. Cell Biol. 38: 1429–1440.

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