Membrane interactions and conformational preferences of human and avian prion N-terminal tandem repeats: The role of copper(II) ions, pH, and membrane mimicking environments
Membrane interactions and conformational preferences of human and avian prion N-terminal tandem repeats: The role of copper(II) ions, pH, and membrane mimicking environments(494 views) Di Natale G, Pappalardo G, Milardi D, Sciacca MF, Attanasio F, La Mendola D, Rizzarelli E
J Phys Chem B (ISSN: 1520-6106, 1520-5207, 1520-5207electronic), 2010 Nov 4; 114(43): 13830-13838.
Dipartimento di Scienze Chimiche, Università degli Studi di Catania, Viale Andrea Doria 6, 95125 Catania, Italy
Istituto di Biostrutture e Bioimmagini - Catania, Consiglio Nazionale delle Ricerche, Viale Andrea Doria 6, 95125 Catania, Italy
References: Prusiner, S.B., Prions (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 13363-1338
Prusiner, S.B., (2004) Prion Biology and Diseases, , 2nd ed.
Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, U. S
Zahn, R., Liu, A., Luhrs, T., Riek, R., Von Schroetter, C., Garcia, F.L., Billeter, M., Wuthrich, K., NMR solution structure of the human prion protein (2000) Proc. Natl. Acad. Sci. U. S. A., 97, pp. 145-150
Donne, D.G., Viles, J.H., Groth, D., Mehlhorn, I., James, T.L., Cohen, F.E., Prusiner, S.B., Dyson, H.J., Structure of the recombinant full-length hamster prion protein PrP (29-231): The N terminus is highly flexible (1997) Proc. Natl. Acad. Sci. U. S. A., 94, pp. 13452-13456
Zahn, R., The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site (2003) J. Mol. Biol., 334, pp. 477-488
Govaerts, C., Wille, H., Prusiner, S.B., Cohen, F.E., Evidence for assembly of prions with left-handed β
-helices into trimers (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 8342-8347
Wille, H., Michelitsch, M.D., Guenebaut, V., Supattapone, S., Serban, A., Cohen, F.E., Agard, D.A., Prusiner, S.B., Structural studies of the scrapie prion protein by electron crystallography (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 3563-3568
Harris, D.A., Falls, D.L., Johnson, F.A., Fischbach, G.D., A prion-like protein from chicken brain copurifies with an acetylcholine receptor-inducing activity (1991) Proc. Natl. Acad. Sci. U. S. A., 88, pp. 7664-7668
Schätzl, H.M., Costa, D.M., Taylor, L., Cohen, F.E., Prusiner, S.B., Prion protein gene variation among primates (1995) J. Mol. Biol., 245, pp. 362-374
Calzolai, L., Lysek, D.A., Perez, D.R., Guntert, P., Wuthrich, K., Prion protein NMR structures of chickens, turtles, and frogs (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 651-655
Pietropaolo, A., Muccioli, L., Zannoni, C., Rizzarelli, E., Conformational preferences of the full chicken prion protein in solution and its differences with respect to mammals (2009) Chem. Phys. Chem., 10, pp. 1500-1510
Marcotte, E.M., Eisemberg, D., Chicken prion tandem repeats form a stable, protease-resistant domain (1999) Biochemistry, 38, pp. 667-676
Matthews, D., Cooke, B.C., The potential for transmissible spongiform encephalopathies in non-ruminant livestock and fish (2003) Rev. Sci. Technol., 22, pp. 283-296
Mllhauser, G.L., Copper binding in the prion protein (2004) Acc. Chem. Res., 37, pp. 79-85
Vassallo, N., Herms, J., Cellular prion protein function in copper homeostasis and redox signalling at the synapse (2003) J. Neurochem., 86, pp. 538-544
Miura, T., Sasaki, S., Toyama, A., Takeuchi, H., Copper reduction by the octapeptide repeat region of prion protein: pH dependence and implications in cellular copper uptake (2005) Biochemistry, 44, pp. 8712-8720
Daniels, M., Brown, D.R., Purification and preparation of prion protein: The synaptic superoxide dismutase (2002) Methods Enzymol, 349, pp. 258-267
Pauly, P.C., Harris, D.A., Copper stimulates endocytosis of the prion protein (1998) J. Biol. Chem., 273, pp. 33107-33119
Taylor, D.R., Watt, N.T., Sumudhu, W., Perera, S., Hooper, N.M., Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis (2005) J. Cell. Sci., 118, pp. 5141-5153
Klein, T.R., Kirsch, D., Kaufmann, R., Riesner, D., Prion rods contain small amounts of two host sphingolipids as revealed by thin-layer chromatography and mass spectrometry (1998) Biol. Chem., 379, pp. 655-666
Morillas, M., Swietnicki, W., Gambetti, P., Surewicz, W.K., Membrane environment alters the conformational structure of the recombinant human prion protein (1999) J. Biol. Chem., 274, pp. 36859-36865
Mura, T., Yoda, M., Takaku, N., Hirose, T., Takeuchi, H., Clustered negative charges on the lipid membrane surface induce β-sheet formation of prion protein fragment 106-126 (2007) Biochemistry, 46, pp. 11589-11597
Smith, C.J., Drakeb, A.F., Anfield, B.A., Bloomberga, G.B., Palmerc, M.S., Clarkea, A.R., Collinge, J., Conformational properties of the prion octa-repeat and hydrophobic sequences (1997) FEBS Lett., 405, pp. 378-384
Dong, S.L., Cadamuro, S.A., Fiorino, F., Bertsch, U., Moroder, L., Renner, C., Copper binding and conformation of the N-terminal octarepeat of the prion protein in the presence of DPC micelles as membrane mimetic (2007) Biopolymers, 88, pp. 840-847
Berti, F., Gaggelli, E., Guerrini, R., Janicka, A., Kozlowski, H., Legowska, A., Mecznikowska, H., Valensin, G., Structural and dynamic characterization of copper (II) binding of the human prion protein outside the octarepeat region (2007) Chem.-Eur. J., 13, pp. 1991-2001
Burns, C.S., Aronoff-Spencer, E., Legname, G., Prusiner, S.B., Antholine, W.E., Gerfen, G.J., Peisach, J., Millhauser, G.L., Copper coordination in the full-length, recombinant prion protein (2003) Biochemistry, 42, pp. 6794-6803
Mendola, D., Pietropaolo, A., Pappalardo, G., Zannoni, C., Rizzarelli, E., Prion proteins leading to neurodegeneration (2008) Curr. Alzheimer Res., 5, pp. 579-590
(2009) Curr. Alzheimer Res., 6, p. 321. , Erratum
Mendola, D., Bonomo, R.P., Caminati, S., Di Natale, G., Emmi, S.S., Hansson, O., Maccarrone, G., Rizzarelli, E., Copper (II) complexes with an avian prion N-terminal region and their potential SOD-like activity (2009) J. Inorg. Biochem., 103, pp. 195-204
Valensin, D., Luczkowski, M., Mancini, F.M., Legowska, A., Gaggelli, E., Valensin, G., Rolka, K., Kozlowski, H., The dimeric and tetrameric octarepeat fragments of prion protein behave differently to its monomeric unit (2004) Dalton Trans., pp. 1284-1293
Di Natale, G., Grasso, G., Impellizzeri, G., Mendola, D., Micera, G., Mihala, N., Nagy, Z., Sovago, I., Copper (II) interaction with unstructured prion domain outside the octarepeat region: Speciation, stability and binding details of copper (II) complexes with PrP106-126 peptides (2005) Inorg. Chem., 44, pp. 7214-7125
Gralka, E., Valensin, D., Gajda, K., Bacco, D., Szyrwiel, L., Remelli, M., Valensin, G., Kozlowski, H., Copper (II) coordination outside the tandem repeat region of an unstructured domain of chicken prion protein (2009) Mol. Biosyst, 5, pp. 497-510
Di Natale, G., Impellizzeri, G., Pappalardo, G., Conformational properties of peptide fragments homologous to the 106-114 and 106-126 residues of the human prion protein: A CD and NMR spectroscopicstudy (2005) Org. Biol. Chem., 3, pp. 490-497
Choi, G., Guo, J., Makriyannis, A., The conformation of the cytoplasmic helix 8 of the CB1 cannabinoid receptor using NMR and circular dichroism (2005) Biochim. Biophys. Acta, 1668, pp. 1-9
Grasso, D., Milardi, D., Rosa, C., Rizzarelli, E., DSC study of the interaction of the prion peptide PrP106-126 with artificial membranes (2001) New J. Chem., 25, pp. 1543-1548
Chen, G.C., Yang, J.T., Two-point calibration of circular dichrometer with d-10-camphorsulfonic acid (1977) Anal. Lett., 10, pp. 1195-1207
Tatham, A.S., Drake, A.F., Shewry, P.R., Conformational studies of a synthetic peptide corresponding to the repeat motif of C hordein (1989) Biochem. J., 259, pp. 471-476
Timasheff, S.N., Susi, H., Townend, R., Stevens, L., Gorbunoff, M.J., Kumosinski, T.F., (1967) Conformation of Biopolymers, 1. , Ramachandran, G. N., Ed.
Academic Press: London
Drake, A.F., Siligardi, G., Gibbons, W.A., Reassessment of the electronic circular dichroism criteria for random coil conformations of poly (L-lysine) and the implications for protein folding and denaturation studies (1988) Biophys. Chem., 31, pp. 143-146
Brahms, S., Brahms, J., Determination of protein secondary structure in solution by vacuum ultraviolet circular dischroism (1980) J. Mol. Biol., 138, pp. 149-178
Johnson Jr., W.C., Protein secondary structure and circular dichroism: A practical guide (1990) Proteins Struct. Funct. Genet., 7, pp. 205-214
Leliveld, S.R., Stitz, L., Korth, C., Expansion of the octarepeat domain alters the misfolding pathway but not the folding pathway of the prion protein (2008) Biochemistry, 47, pp. 6267-6278
Pietropaolo, A., Raiola, L., Muccioli, L., Tiberio, G., Zannoni, C., Fattorusso, R., Isernia, C., Rizzarelli, E., An NMR and molecular dynamics investigation of the avian prion hexarepeat conformational features in solution (2007) Chem. Phys. Lett., 442, pp. 110-118
Monserret, R., Leish, M.M.J., Beckmann, A., Geonzjann, C., Penin, F., Involvement of electrostatic interactions in the mechanism of peptide folding induced by sodium dodecyl sulfate binding (2000) Biochemistry, 39, pp. 8362-8373
Chattopadhyay, M., Walter, E.D., Newell, D.J., Jackson, P.J., Aronoff-Spencer, E., Peisach, J., Gerfen, G.J., Millhauser, G.L., The octarepeat domain of the prion protein binds Cu (II) with three distinct coordination modes at pH 7.4 (2005) J. Am. Chem. Soc., 36, pp. 12649-12656
Wells, M.A., Jelinska, C., Hosszu, L.L.P., Craven, C.J., Clarke, A.R., Collinge, J., Waltho, J.P., Jackson, G.S., Multiple forms of copper (II) co-ordination occur throughout the disordered N-terminal region of the prion protein at pH 7.4 (2006) Biochem. J., 400, pp. 501-510
Viles, J.H., Cohen, F.E., Prusiner, S.B., Goodin, D.B., Wright, P.E., Dyson, H.J., Copper binding to the prion protein: Structural implications of four identical cooperative binding sites (1999) Proc. Natl. Acad. Sci. U. S. A., 96, pp. 2042-2047
Dawson, R.M.C., Elliott, D.C., Elliott, W.H., Jones, K.M., (1986) Data for Biochemical Research, , Oxford University Press: Oxford, U. K
McDonald, R.C., McDonald, R.I., Menco, B.P.M., Takeshita, K., Subbarao, N.K., Hu, L., Small-volume extrusion apparatus for preparations of large unilamellar vesicles (1991) Biochim. Biophys. Acta, 1061, pp. 297-303
Sanderson, J.M., Peptide-lipid interactions: Insights and perspectives (2005) Org. Biomol. Chem., 3, pp. 201-212
Nagle, J.F., Theory of the main lipid bilayer phase transition (1980) Annu. Rev. Phys. Chem., 31, pp. 157-195
Pappalardo, G., Milardi, D., Magrì, A., Attanasio, F., Impellizzeri, G., Rosa, C., Grasso, D., Rizzarelli, E., Environmental factors differently affect rat and human IAPP: Conformational preferences and membrane activity of IAPP 17-29 peptide derivatives (2007) Chem.-Eur. J., 13, pp. 10204-10215
Alston, R.W., Lasagna, M., Grimsley, G.R., Scholtz, J.M., Reinhart, G.D., Pace, C.N., Peptide sequence and conformation strongly influence tryptophan fluorescence (2008) Biophys. J., 94, pp. 2880-2887
Heyn, M.P., Blume, A., Rehorek, M., Dencher, N.A., Calorimetric and fluorescence depolarization studies on the lipid phase transition of bacteriorhodopsin-dimyristoylphosphatidylcholine vesicles (1981) Biochemistry, 20, pp. 7109-7115
Chiang, Y.C., Lin, Y.J., Horng, J.C., Stereoelectronic effects on the transition barrier of polyproline conformational interconversion (2009) Protein Sci., 18, pp. 1967-1977
Taubner, L.M., Bienkiewicz, E.A., Copié, V., Caughey, B., Structure of the flexible amino-terminal domain of prion protein bound to a sulfated glycan (2010) J. Mol. Biol., 395, pp. 475-490
Khemtemourian, L., Sani, M.A., Bathany, K., Grobner, G., Dufourc, E.J., Synthesis and secondary structure in membranes of the Bcl-2 anti-apoptotic domain BH4 (2006) J. Pept. Sci., 12, pp. 58-64
Sonnichsen, F.D., Van Eyk, J.E., Hodges, R.S., Sykes, B.D., Effect of trifluoroethanol on protein secondary structure: An NMR and CD study using a synthetic actin peptide (1992) Biochemistry, 31, pp. 8790-8798
Santiveri, C.M., Pantoja-Uceda, D., Rico, M., Jimenez, M.A., Betahairpin formation in aqueous solution and in the presence of trifluoroethanol: A 1H and 13C nuclear magnetic resonance conformational study of designed peptides (2005) Biopolymers, 79, pp. 150-162
Calamai, M., Chiti, F., Dobson, C.M., Amyloid fibril formation can proceed from different conformations of a partially unfolded protein (2005) Biophys. J., 89, pp. 4201-4210
Pallares, I., Vendrell, J., Aviles, F.X., Ventura, S., Amyloid fibril formation by a partially structured intermediate state of alpha-chymotrypsin (2004) J. Mol. Biol., 342, pp. 321-331
Shanmugam, G., Polavarapu, P.L., Gopinath, D., Jayakumar, R., The structure of antimicrobial pexiganan peptide in solution probed by Fourier transform infrared absorption, vibrational circular dichroism, and electronic circular dichroism spectroscopy (2005) Biopolymers, 80, pp. 636-642
Liu, Z., Chen, K., Ng, A., Shi, Z., Woody, R.W., Kallenbach, N.R., Solvent dependence of PPII conformation in model Alanine peptides (2004) J. Am. Chem. Soc., 126, pp. 15141-15150
Matthews, J.M., Ward, L.D., Hammacher, A., Norton, R.S., Simpson, R.J., Roles of histidine 31 and tryptophan 34 in the structure, self-association, and folding of murine interleukin-6 (1997) Biochemistry, 36, pp. 6187-6196
White, S.H., Wimley, W.C., Membrane protein folding and stability: Physical Principles (1999) Annu. Rev. Biophys. Biomol. Struct, 28, pp. 319-365
Bonomo, R.P., Cucinotta, V., Giuffrida, A., Impellizzeri, G., Magrì, A., Pappalardo, G., Rizzarelli, E., Vagliasindi, L.I., A re-investigation of copper coordination in the octa-repeats region of the prion protein (2005) Dalton Trans., pp. 150-158
Prusiner, S. B., Prions (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 13363-1338
Prusiner, S. B., (2004) Prion Biology and Diseases, , 2nd ed.
Donne, D. G., Viles, J. H., Groth, D., Mehlhorn, I., James, T. L., Cohen, F. E., Prusiner, S. B., Dyson, H. J., Structure of the recombinant full-length hamster prion protein PrP (29-231): The N terminus is highly flexible (1997) Proc. Natl. Acad. Sci. U. S. A., 94, pp. 13452-13456
Harris, D. A., Falls, D. L., Johnson, F. A., Fischbach, G. D., A prion-like protein from chicken brain copurifies with an acetylcholine receptor-inducing activity (1991) Proc. Natl. Acad. Sci. U. S. A., 88, pp. 7664-7668
Sch tzl, H. M., Costa, D. M., Taylor, L., Cohen, F. E., Prusiner, S. B., Prion protein gene variation among primates (1995) J. Mol. Biol., 245, pp. 362-374
Marcotte, E. M., Eisemberg, D., Chicken prion tandem repeats form a stable, protease-resistant domain (1999) Biochemistry, 38, pp. 667-676
Mllhauser, G. L., Copper binding in the prion protein (2004) Acc. Chem. Res., 37, pp. 79-85
Pauly, P. C., Harris, D. A., Copper stimulates endocytosis of the prion protein (1998) J. Biol. Chem., 273, pp. 33107-33119
Taylor, D. R., Watt, N. T., Sumudhu, W., Perera, S., Hooper, N. M., Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis (2005) J. Cell. Sci., 118, pp. 5141-5153
Klein, T. R., Kirsch, D., Kaufmann, R., Riesner, D., Prion rods contain small amounts of two host sphingolipids as revealed by thin-layer chromatography and mass spectrometry (1998) Biol. Chem., 379, pp. 655-666
Smith, C. J., Drakeb, A. F., Anfield, B. A., Bloomberga, G. B., Palmerc, M. S., Clarkea, A. R., Collinge, J., Conformational properties of the prion octa-repeat and hydrophobic sequences (1997) FEBS Lett., 405, pp. 378-384
Dong, S. L., Cadamuro, S. A., Fiorino, F., Bertsch, U., Moroder, L., Renner, C., Copper binding and conformation of the N-terminal octarepeat of the prion protein in the presence of DPC micelles as membrane mimetic (2007) Biopolymers, 88, pp. 840-847
Burns, C. S., Aronoff-Spencer, E., Legname, G., Prusiner, S. B., Antholine, W. E., Gerfen, G. J., Peisach, J., Millhauser, G. L., Copper coordination in the full-length, recombinant prion protein (2003) Biochemistry, 42, pp. 6794-6803
(2009) Curr. Alzheimer Res., 6, p. 321. , Erratum
Chen, G. C., Yang, J. T., Two-point calibration of circular dichrometer with d-10-camphorsulfonic acid (1977) Anal. Lett., 10, pp. 1195-1207
Tatham, A. S., Drake, A. F., Shewry, P. R., Conformational studies of a synthetic peptide corresponding to the repeat motif of C hordein (1989) Biochem. J., 259, pp. 471-476
Timasheff, S. N., Susi, H., Townend, R., Stevens, L., Gorbunoff, M. J., Kumosinski, T. F., (1967) Conformation of Biopolymers, 1. , Ramachandran, G. N., Ed.
Drake, A. F., Siligardi, G., Gibbons, W. A., Reassessment of the electronic circular dichroism criteria for random coil conformations of poly (L-lysine) and the implications for protein folding and denaturation studies (1988) Biophys. Chem., 31, pp. 143-146
Johnson Jr., W. C., Protein secondary structure and circular dichroism: A practical guide (1990) Proteins Struct. Funct. Genet., 7, pp. 205-214
Leliveld, S. R., Stitz, L., Korth, C., Expansion of the octarepeat domain alters the misfolding pathway but not the folding pathway of the prion protein (2008) Biochemistry, 47, pp. 6267-6278
Wells, M. A., Jelinska, C., Hosszu, L. L. P., Craven, C. J., Clarke, A. R., Collinge, J., Waltho, J. P., Jackson, G. S., Multiple forms of copper (II) co-ordination occur throughout the disordered N-terminal region of the prion protein at pH 7. 4 (2006) Biochem. J., 400, pp. 501-510
Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E., Dyson, H. J., Copper binding to the prion protein: Structural implications of four identical cooperative binding sites (1999) Proc. Natl. Acad. Sci. U. S. A., 96, pp. 2042-2047
Dawson, R. M. C., Elliott, D. C., Elliott, W. H., Jones, K. M., (1986) Data for Biochemical Research, , Oxford University Press: Oxford, U. K
McDonald, R. C., McDonald, R. I., Menco, B. P. M., Takeshita, K., Subbarao, N. K., Hu, L., Small-volume extrusion apparatus for preparations of large unilamellar vesicles (1991) Biochim. Biophys. Acta, 1061, pp. 297-303
Sanderson, J. M., Peptide-lipid interactions: Insights and perspectives (2005) Org. Biomol. Chem., 3, pp. 201-212
Nagle, J. F., Theory of the main lipid bilayer phase transition (1980) Annu. Rev. Phys. Chem., 31, pp. 157-195
Alston, R. W., Lasagna, M., Grimsley, G. R., Scholtz, J. M., Reinhart, G. D., Pace, C. N., Peptide sequence and conformation strongly influence tryptophan fluorescence (2008) Biophys. J., 94, pp. 2880-2887
Heyn, M. P., Blume, A., Rehorek, M., Dencher, N. A., Calorimetric and fluorescence depolarization studies on the lipid phase transition of bacteriorhodopsin-dimyristoylphosphatidylcholine vesicles (1981) Biochemistry, 20, pp. 7109-7115
Chiang, Y. C., Lin, Y. J., Horng, J. C., Stereoelectronic effects on the transition barrier of polyproline conformational interconversion (2009) Protein Sci., 18, pp. 1967-1977
Taubner, L. M., Bienkiewicz, E. A., Copi, V., Caughey, B., Structure of the flexible amino-terminal domain of prion protein bound to a sulfated glycan (2010) J. Mol. Biol., 395, pp. 475-490
Sonnichsen, F. D., Van Eyk, J. E., Hodges, R. S., Sykes, B. D., Effect of trifluoroethanol on protein secondary structure: An NMR and CD study using a synthetic actin peptide (1992) Biochemistry, 31, pp. 8790-8798
Santiveri, C. M., Pantoja-Uceda, D., Rico, M., Jimenez, M. A., Betahairpin formation in aqueous solution and in the presence of trifluoroethanol: A 1H and 13C nuclear magnetic resonance conformational study of designed peptides (2005) Biopolymers, 79, pp. 150-162
Matthews, J. M., Ward, L. D., Hammacher, A., Norton, R. S., Simpson, R. J., Roles of histidine 31 and tryptophan 34 in the structure, self-association, and folding of murine interleukin-6 (1997) Biochemistry, 36, pp. 6187-6196
White, S. H., Wimley, W. C., Membrane protein folding and stability: Physical Principles (1999) Annu. Rev. Biophys. Biomol. Struct, 28, pp. 319-365
Bonomo, R. P., Cucinotta, V., Giuffrida, A., Impellizzeri, G., Magr, A., Pappalardo, G., Rizzarelli, E., Vagliasindi, L. I., A re-investigation of copper coordination in the octa-repeats region of the prion protein (2005) Dalton Trans., pp. 150-158
Membrane interactions and conformational preferences of human and avian prion N-terminal tandem repeats: The role of copper(II) ions, pH, and membrane mimicking environments
Membrane interactions and conformational preferences of human and avian prion N-terminal tandem repeats: The role of copper(II) ions, pH, and membrane mimicking environments
Membrane interactions and conformational preferences of human and avian prion N-terminal tandem repeats: The role of copper(II) ions, pH, and membrane mimicking environments