Raman optical activity demonstrates poly(l-proline) II helix in the N-terminal region of the ovine prion protein: Implications for function and misfunction

Journal of Molecular Biology

Volumn 343, Issue 2, 2004, Pages 467-476

  Blanch, Ewan W ^a   Gill, Andrew C ^b   Rhie, Alexandre G O ^b   Hope, James ^b   Hecht, Lutz ^a   Nielsen, Kurt ^c   Barron, Laurence D ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

amyloid fibrils; ovine prion protein; poly(l proline) II helix; Raman optical activity; transmissible spongiform encephalopathy

Indexed keywords

PRION PROTEIN; PROLINE DERIVATIVE; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY;

CHAETODON; MURINAE; OVIS;

EID: 4644372554     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.058     Document Type: Article

References (65)

1. S.B. Prusiner Prions Proc. Natl Acad. Sci. USA 95 1998 13363 13383
2. F.E. Cohen, and S.B. Prusiner Pathologic conformations of prion proteins Annu. Rev. Biochem. 67 1998 793 819
3. K.M. Pan, M. Baldwin, J. Nguyen, M. Gasset, A. Serban, and D. Groth Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins Proc. Natl Acad. Sci. USA 90 1993 10962 10966
4. P. Pergamini, H. Jaffe, and J. Safar Semipreparative chromatographic method to purify the normal cellular isoform of the prion protein in nondenatured form Anal. Biochem. 236 1996 63 73
5. K. Wüthrich, and R. Riek Three-dimensional structures of prion proteins Advan. Protein Chem. 57 2001 55 82
6. J.H. Viles, F.E. Cohen, S.B. Prusiner, D.B. Goodin, P.E. Wright, and H.J. Dyson Copper binding to the prion protein: structural implications of four identical cooperative binding sites Proc. Natl Acad. Sci. USA 96 1999 2042 2047
7. L.F. Haire, S.M. Whyte, N. Vasisht, A.C. Gill, C. Verma, and E.J. Dodson The crystal structure of the globular domain of sheep prion protein J. Mol. Biol. 336 2004 1175 1183
8. M. Fischer, T. Rulicke, A. Raeber, A. Sailer, M. Moser, and B. Oesch Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie EMBO J. 15 1996 1255 1264
9. S. Supattapone, P. Bosque, T. Muramoto, H. Wille, C. Aagaard, and D. Peretz Prion protein of 106 residues creates an artificial transmission barrier for prion replication in transgenic mice Cell 96 1999 869 878
10. D. Peretz, R.A. Williamson, Y. Matsunaga, H. Serban, C. Pinilla, and R.B. Bastidas A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform J. Mol. Biol. 273 1997 614 622
11. Sc)-specific epitope defined by a monoclonal antibody Nature 389 1997 74 77
12. D.G. Donne, J.H. Viles, D. Groth, I. Mehlhorn, T.L. James, and F.E. Cohen Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible Proc. Natl Acad. Sci. USA 94 1997 13452 13457
13. V.A. Lawson, S.A. Priola, K. Meade-White, M. Lawson, and B. Chesebro Flexible N-terminal region of prion protein influences conformation of protease resistant prion protein isoforms associated with cross-species scrapie infection in vivo and in vitro J. Biol. Chem. 279 2004 13689 13695
14. C.S. Burns, E. Aronoff-Spencer, C.M. Dunham, P. Lario, N.I. Avdievich, and W.E. Antholine Molecular features of the copper binding sites in the octarepeat domain of the prion protein Biochemistry 41 2002 3991 4001
15. L.D. Barron, M.P. Bogaard, and A.D. Buckingham Raman scattering of circularly polarized light by optically active molecules J. Am. Chem. Soc. 95 1973 603 605
16. L.D. Barron, L. Hecht, E.W. Blanch, and A.F. Bell Solution structure and dynamics of biomolecules from Raman optical activity Prog. Biophys. Mol. Biol. 73 2000 1 49
17. L.D. Barron, L. Hecht, E.W. Blanch, and I.H. McColl Raman optical activity comes of age Mol. Phys. 102 2002 731 744
18. W. Hug Raman optical activity J.M. Chalmers P.R. Griffiths Handbook of Vibrational Spectroscopy vol. 1 2002 Wiley Chichester 745 758
19. L.D. Barron, E.W. Blanch, and L. Hecht Unfolded proteins studied by Raman optical activity Advan. Protein Chem. 62 2002 51 90
20. A.A. Adzhubei, and M.J.E. Sternberg Conservation of polyproline II helices in homologous proteins: implications for structure prediction by model building Protein Sci. 3 1994 2395 2410
21. T.P. Creamer, and M.N. Campbell Determinants of the polyproline II helix from modelling studies Advan. Protein Chem. 62 2002 263 282
22. Z. Shi, R.W. Woody, and N. Kallenbach Is polyproline II a major backbone conformation in unfolded proteins? Advan. Protein Chem. 62 2002 163 240
23. B. Bochicchio, and A.M. Tamburro Polyproline II structure in proteins: identification by chiroptical spectroscopies, stability and functions Chirality 14 2002 782 792
24. T.A. Keiderling Peptide and protein conformational studies with vibrational circular dichroism and related spectroscopies N. Berova K. Nakanishi R.W. Woody Circular Dichroism. Principles and Applications 2000 Wiley New York 621 666
25. R. Schweitzer-Stenner, F. Eker, K. Griebenow, X. Cao, and L.A. Nafie The conformation of tetraalanine in water determined by polarized Raman, FT-IR and VCD spectroscopy J. Am. Chem. Soc. 126 2004 2768 2776
26. S.A. Asher, A.V. Mikhonin, and S. Bykov UV Raman demonstrates that α-helical polyalanine peptides melt to polyproline II conformations J. Am. Chem. Soc. 126 2004 8433 8440
27. Z. Shi, C.A. Olson, G.D. Rose, R.L. Baldwin, and N.R. Kallenbach Polyproline II structure in a sequence of seven alanine residues Proc. Natl Acad. Sci. USA 99 2002 9190 9195
28. I.H. McColl, E.W. Blanch, L. Hecht, N.R. Kallenbach, and L.D. Barron Vibrational Raman optical activity characterization of poly(l-proline) II helix in alanine oligopeptides J. Am. Chem. Soc. 126 2004 5076 5077
29. II conformation for the molecular recognition of peptides Biopolymers 37 1995 281 292
30. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 1999 321 331
31. M.A. Kelly, B.W. Chellgren, A.L. Rucker, J.M. Troutman, M.G. Fried, A.F. Miller, and T.P. Creamer Host-guest study of left-handed polyproline II helix formation Biochemistry 40 2001 14376 14383
32. A.K. Dunker, C.J. Brown, J.D. Lawson, L.M. Iakoucheva, and Z. Obradovic Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582
33. C.D. Syme, E.W. Blanch, C. Holt, R. Jakes, M. Goedert, L. Hecht, and L.D. Barron A Raman optical activity study of rheomorphism in caseins, synucleins and tau. New insight into the structure and behaviour of natively unfolded proteins. Eur. J. Biochem. 269 2002 148 156
34. V.N. Uversky A protein-chameleon: conformational plasticity of α-synuclein, a disordered protein involved in neurodegenerative disorders J. Biomol. Struct. Dyn. 21 2003 211 234
35. C.J. Smith, A.F. Drake, B.A. Banfield, G.B. Bloomberg, M.S. Palmer, A.R. Clarke, and J. Collinge Conformational properties of the prion octa-repeat and hydrophobic sequences FEBS Letters 405 1997 378 384
36. R.M. Whittal, H.L. Ball, F.E. Cohen, A.L. Burlingame, S.B. Prusiner, and M.A. Baldwin Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry Protein Sci. 9 2000 332 343
37. A.C. Gill, M.A. Ritchie, L.G. Hunt, S.E. Steane, K.G. Davies, and S.P. Bocking Post-translational hydroxylation at the N-terminus of the prion protein reveals presence of PPII structure in vivo EMBO J. 19 2000 5324 5331
38. H. Yoshida, N. Matsushima, Y. Kumaki, M. Nakata, and K. Hikichi NMR studies of model peptides of PHGGGWGQ repeats within the N-terminus of prion proteins: a loop conformation with histidine and tryptophan in close proximity J. Biochem. 128 2000 271 281
39. R. Zahn The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site J. Mol. Biol. 334 2000 477 488
40. I.H. McColl, E.W. Blanch, A.C. Gill, A.G.O. Rhie, M.A. Ritchie, and L. Hecht A new perspective on β-sheet structures using vibrational Raman optical activity: from poly(l-lysine) to the prion protein J. Am. Chem. Soc. 125 2003 10019 10026
41. I.H. McColl, E.W. Blanch, L. Hecht, and L.D. Barron A study of α-helix hydration in polypeptides, proteins and viruses using vibrational Raman optical activity J. Am. Chem. Soc. 126 2004 8181 8188
42. F. Wopfner, G. Weidenhöfer, R. Schneider, A. von Brunn, S. Gilch, and T.F. Schwarz Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein J. Mol. Biol. 289 1999 1163 1178
43. T. van Rheede, M.M.W. Smolenaars, O. Madsen, and W.W. de Jong Molecular evolution of the mammalian prion protein Mol. Biol. Evol. 20 2003 111 121
44. P. Bamborough, H. Wille, G.C. Telling, F. Yehiely, S.B. Prusiner, and F.E. Cohen Prion protein structure and scrapie replication: theoretical, spectroscopic and genetic investigations Cold Spring Harbor Symp. Quant. Biol. 61 1996 495 509
45. C.S. Burns, E. Aronoff-Spencer, G. Legname, S.B. Prusiner, W.E. Antholine, and G.J. Gerfen Copper coordination in the full-length, recombinant prion protein Biochemistry 42 2003 6794 6803
46. R.G. Warner, C. Hundt, S. Weiss, and J.E. Turnbull Identification of the heparin sulfate binding sites in the cellular prion protein J. Biol. Chem. 277 2002 18421 18430
47. C. Hundt, J.M. Peyrin, S. Haik, S. Gauczynski, C. Leucht, and R. Rieger Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor EMBO J. 20 2001 5876 5886
48. C. Gabus, E. Derrington, P. Leblanc, J. Chnaiderman, D. Dormont, and W. Swietnicki The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCp7 of HIV-1 J. Biol. Chem. 276 2001 19301 19309
49. E.W. Blanch, L.A. Morozova-Roche, D.A.E. Cochran, A.J. Doig, L. Hecht, and L.D. Barron Is polyproline II helix the killer conformation? A Raman optical activity study of the amyloidogenic prefibrillar intermediate of human lysozyme J. Mol. Biol. 301 2000 553 563
50. A. Cooper Heat capacity of hydrogen-bonded networks: an alternative view of protein folding thermodynamics Biophys. Chem. 85 2000 25 39
51. M. Fändrich, V. Forge, K. Buder, M. Kittler, C.M. Dobson, and S. Diekmann Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments Proc. Natl Acad. Sci. USA 100 2003 15463 15468
52. F. Chiti, M. Stefani, N. Taddei, G. Ramponi, and C.M. Dobson Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424 2003 805 808
53. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins: Struct. Funct. Genet. 41 2000 415 427
54. 1 helical conformation in the Alzheimer Aβ(12-28) peptide FEBS Letters 555 2003 371 374
55. 1-28 fragment of the amyloid peptide predominantly adopts a polyproline II conformation in acidic solution Biochemistry 43 2004 6893 6898
56. A.L. Rucker, C.T. Pager, M.N. Campbell, J.E. Qualls, and T.P. Creamer Host-guest scale of left-handed polyproline II helix formation Proteins: Struct. Funct. Bioinformatics 53 2003 68 75
57. B.W. Chellgren, and T.P. Creamer Short sequences of non-proline residues can adopt the polyproline II helical conformation Biochemistry 43 2004 5864 5869
58. F. Eker, K. Griebenow, X. Cao, L.A. Nafie, and R. Schweitzer-Stenner Preferred peptide backbone conformations in the unfolded state revealed by the structure analysis of alanine-based (AXA) tripeptides in aqueous solution Proc. Natl Acad. Sci. USA 101 2004 10054 10059
59. C.K. Smith, and L. Regan Construction and design of β-sheets Acc. Chem. Res. 30 1997 153 161
60. R. Zahn, A. Liu, T. Lührs, R. Riek, C. von Schroetter, and F. López Garcia NMR solution structure of the human prion protein Proc. Natl Acad. Sci. USA 97 2000 145 150
61. J.H. Viles, D. Donne, G. Kroon, S.B. Prusiner, F.E. Cohen, H.J. Dyson, and P.E. Wright Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics Biochemistry 40 2001 2743 2753
62. F.L. Garcia, R. Zahn, R. Riek, and K. Wüthrich NMR structure of the bovine prion protein Proc. Natl Acad. Sci. USA 97 2000 8334 8339
63. L. Kirby, C.R. Birkett, H. Rudyk, I.H. Gilbert, and J. Hope In vitro cell free conversion of bacterial recombinant PrP to PrPres as a model for conversion J. Gen. Virol. 84 2003 1013 1020
64. S.M. Whyte, I.D. Sylvester, S.R. Martin, A.C. Gill, F. Wopfner, and H.M. Schatzl Stability and conformational properties of doppel, a prion-like protein, and its single-disulphide mutant Biochem. J. 373 2003 485 494
65. L. Hecht, L.D. Barron, E.W. Blanch, A.F. Bell, and L.A. Day Raman optical activity instrument for studies of biopolymer structure and function J. Raman Spectrosc. 30 1999 815 825