Conformation of Prion Protein Repeat Peptides Probed by FRET Measurements and Molecular Dynamics Simulations

Biophysical Journal

Volumn 86, Issue 4, 2004, Pages 2467-2483

  Gustiananda, Marsia ^a   Liggins, John R ^a   Cummins, Peter L ^a   Gready, Jill E ^a  

^a Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATION; DANSYL CHLORIDE; HISTIDINE; PEPTIDE; PHENYLALANINE; PRION PROTEIN; TRYPTOPHAN;

ANISOTROPY; ARTICLE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MARSUPIAL; MOLECULAR DYNAMICS; PH; PROTEIN CONFORMATION; SIMULATION; TEMPERATURE;

METATHERIA;

EID: 1942519322     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74303-9     Document Type: Article

References (68)

1. Aronoff-Spencer, E., C. S. Burns, N. I. Avdievich, G. J. Gerfen, J. Peisach, W. E. Antholine, H. L. Ball, F. Cohen, S. B. Prusiner, and G. L. Millhauser. 2000. Identification of the Cu(2+) binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry. 39:13760-13771.
2. Bauemschmitt, R., and R. Ahlrichs. 1996. Treatment of electronic excitations within the adiabatic approximation of time dependent density functional theory. Chem. Phys. Lett. 256:454-464.
3. Bonomo, R. P., G. Imperllizzeri, G. Pappalardo, E. Rizzarelli, and G. Tabbi. 2000. Copper(II) binding modes in the prion octapeptide PHGGGWGQ: a spectroscopic and voltammetric study. Chem. 6:4195-4202.
4. Brown, D. R. 1999. Prion protein expression aids cellular uptake and veratridine-induced release of copper. J. Neurosci. Res. 58:717-725.
5. Brown, D. R., K. Qin, J. W. Herms, A. Madlung, J. Manson, R. Strome, P. E. Fraser, T. Kruck, A. von Bohlen, W. Schulz-Schaeffer, A. Giese, D. Westaway, and H. Kretzschmar. 1997. The cellular prion protein binds copper in vivo. Nature. 390:684-687.
6. Burns, C. S., E. Aronoff-Spencer, C. M. Dunham, P. Lario, N. I. Avdievich, W. E. Antholine, M. M. Olmstead, A. Vrielink, G. J. Gerfen, J. Peisach, W. G. Scott, and G. L. Millhauser. 2002. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry. 41:3991-4001.
7. Burns, C. S., E. Aronoff-Spencer, G. Legname, S. B. Prusiner, W. E. Antholine, G. J. Gerfen, J. Peisach, and G. L. Millhauser. 2003. Copper coordination in the full-length, recombinant prion protein. Biochemistry. 42:6794-6803.
8. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1996. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:5179-5197.
9. Creighton, T. E. 1983. Proteins: Structures and Molecular Principles. W. H. Freeman, New York.
10. Cummins, P. L., and J. E. Gready. 1994. The electrostatic potential in the semiempirical molecular orbital approximation. Chem. Phys. Lett. 225:11-17.
11. Cummins, P. L., and J. E. Gready. 1996. Solvent effects in active-site molecular dynamics simulations on the binding of 8-methyl-N5-deazapterin and 8-methyl-pterin to dihydrofolate reductase. J. Comput. Chem. 17:1598-1611.
12. Cummins, P. L. 1996. Molecular Orbital Programs for Simulations (MOPS), Australian National University, Canberra, Australia.
13. de Souza, E. S., I. Y. Hirata, L. Juliano, and A. S. Ito. 2000. End-to-end distance distribution in bradykinin observed by Förster resonance energy transfer. Biochim. Biophys. Acta. 1474:251-261.
14. dos Remedios, C. G., and P. D. Moens. 1995. Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor. J. Struct. Biol. 115:175-185.
15. Dunn, B. M., C. Pham, L. Raney, D. Abayasekara, W. Gillespie, and A. Hsu. 1981. Interaction of alpha-dansylated peptide inhibitors with porcine pepsin: detection of complex formation by fluorescence energy transfer and chromatography and evidence for a two-step binding scheme. Biochemistry. 20:7206-7211.
16. Fernandez-Recio, J., A. Vazquez, C. Civera, P. Sevilla, and J. Sancho. 1997. The tryptophan/histidine interaction in alpha-helices. J. Mol. Biol. 267:184-197.
17. Flechsig, E., D. Shmerling, I. Hegyi, A. J. Raeber, M. Fischer, A. Cozzio, C. von Mering, A. Aguzzi, and C. Weissmann. 2000. Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice. Neuron. 27:399-408.
18. Foresman, J. B., M. Head-Gordon, J. A. Pople, and M. J. Frisch. 1992. Toward a systematic molecular orbital theory for excited states. J. Phys. Chem. 96:135-149.
19. Förster, T. 1948. Intermolecular energy migration and fluorescence. Ann. Phys. 2:55-75.
20. Frisch, M. J., G. W. Truck, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, V. G. Zakrzewski, J. A. Montgomery, Jr., R. E. Stratmann, J. C. Burant, S. Dapprich, J. M. Millam, A. D. Daniels, K. N. Kudin, M. C. Strain, O. Farkas, J. Tomasi, V. Barone, M. Cossi, R. Cammi, B. Mennucci, C. Pomelli, C. Adamo, S. Clifford, J. Ochterski, G. A. Petersson, P. Y. Ayala, Q. Cui, K. Morokuma, D. K. Malick, A. D. Rabuck, K. Raghavachari, J. B. Foresman, J. Cioslowski, J. V. Ortiz, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. Gomperts, R. L. Martin, D. J. Fox, T. Keith, M. A. Al-Laham, C. Y. Peng, A. Nanayakkara, C. Gonzalez, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, J. L. Andres, C. Gonzalez, M. Head-Gordon, E. S. Replogle, and J. A. Pople. 1998. Gaussian 98, Rev. A7. Gaussian, Inc., Pittsburgh, PA.
21. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. USA. 96:9459-9464.
22. Garnett, A. P., and J. H. Viles. 2003. Copper binding to the octarepeats of the prion protein. Affinity, specificity, folding and co-operativity; insights from circular dichroism. J. Biol. Chem. 278:6795-6802.
23. Gonzalez-Iglesias, R., M. A. Pajares, C. Ocal, J. C. Espinosa, B. Oesch, and M. Gasset. 2002. Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J. Mol. Biol. 319:527-540.
24. Gromiha, M. M. 2002. Influence of cation-π interactions in mesophilic and thermophilic proteins. J. Liq. Chromatography Rel. Technol. 25:3141-3149.
25. Gromiha, M. M., S. Thomas, and C. Santhosh. 2002. Role of cation-π interactions to the stability of thermophilic proteins. Prep. Biochem. Biotechnol. 32:355-362.
26. Gustiananda, M., P. I. Haris, P. J. Milbum, and J. E. Gready. 2002. Copper-induced conformational change in a marsupial prion protein repeat peptide probed using FTIR spectroscopy. FEBS Lett. 512:38-42.
27. Haughland, R. P. 2001. Handbook of Fluorescent Probes and Research Products, 8th. Ed. Molecular Probes, Inc., Eugene, OR.
28. Hornshaw, M. P., J. R. McDermott, J. M. Candy, and J. H. Lakey. 1995. Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem. Biophys. Res. Commun. 214:993-999.
29. Jackson, G. S., I. Murray, L. L. Hosszu, N. Gibbs, J. P. Waltho, A. R. Clarke, and J. Collinge. 2001. Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. USA. 98:8531-8535.
30. Johnson, W. C., Jr. 1990. Protein secondary structure and circular dichroism: a practical guide. Proteins. 7:205-214.
31. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
32. Kramer, M. L., H. D. Kratzin, B. Schmidt, A. Romer, O. Windl, S. Liemann, S. Hornemann, and H. Kretzschmar. 2001. Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276:16711-16719.
33. Kulinski, T., A. B. Wennerberg, R. Rigler, S. W. Provencher, M. Pooga, U. Langel, and T. Bartfai. 1997. Conformational analysis of galanin using end to end distance distribution observed by Förster resonance energy transfer. Eur. Biophys. J. 26:145-154.
34. Lagunoff, D., and P. Ottolenghi. 1966. Effect of pH on the fluorescence of dimethylaminonaphthalenesulphonate (DNS) and several derivatives. C. R. Trav. Lab. Carlsberg. 35:63-83.
35. Lakowicz, J. R., I. Gryczynski, G. Laczko, W. Wiczk, and M. L. Johnson. 1994. Distribution of distances between the tryptophan and the N-terminal residue of melittin in its complex with calmodulin, troponin C, and phospholipids. Protein Sci. 3:628-637.
36. Loewenthal, R., J. Sancho, and A. R. Fersht. 1992. Histidine-aromatic interactions in barnase. Elevation of histidine pKa and contribution to protein stability. J. Mol. Biol. 224:759-770.
37. Luczkowski, M., H. Kozlowski, M. Stawikowski, K. Rolka, E. Gaggelli, D. Valensin, and G. Valensin. 2002. Is the monomeric prion octapeptide repeat PHGGGWGQ a specific ligand for Cu2+ ions? J. Chem. Soc. Dalton Trans. 2269-2274.
38. Maliwal, B. P., J. R. Lakowicz, G. Kupryszewski, and P. Rekowski. 1993. Fluorescence study of conformational flexibility of RNase s-peptide: distance-distribution, end-to-end diffusion, and anisotropy decays. Biochemistry. 32:12337-12345.
39. Miura, T., A. Hori-i, and H. Takeuchi. 1996. Metal-dependent alpha-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett. 396:248-252.
40. Miura, T., A. Hori-i, H. Mototani, and H. Takeuchi. 1999. Raman spectroscopic study on the copper(II) binding mode of prion octapeptide and its pH dependence. Biochemistry. 38:11560-11569.
41. Pace, C. N., and F. X. Schmid. 1997. How to determine the molar absorbance coefficient of a protein. In Protein Structure: A Practical Approach. T. E. Creighton, editor. IRL Press, Oxford, UK. 253-259.
42. Pauly, P. C., and D. A. Harris. 1998. Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273:33107-33110.
43. Perrin, D. D., and B. Dempsey. 1974. Buffers for pH and Metal Ion Control. Chapman and Hall, London, UK.
44. Pesce, A. J., C.-G. Rosen, and T. L. Pasby. 1971. Fluorescence Spectroscopy: An Introduction for Biology and Medicine. Marcel Dekker Inc., New York.
45. Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. USA. 95:13363-13383.
46. Qin, K. F., Y. Yang, P. Mastrangelo, and D. Westaway. 2002. Mapping Cu(II) binding sites in prion proteins by diethyl pyrocarbonate modification and matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometric footprinting. J. Biol. Chem. 277:1981-1990.
47. Ryckaert, J.-P., G. Ciccoti, and H. J. C. Berendsen. 1977. Numerical integration of Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
48. Schmid, F. X. 1997. Optical spectroscopy to characterize protein conformation and conformational changes. In Protein Structure: A Practical Approach. T. E. Creighton, editor. IRL Press, Oxford, UK. 261-297.
49. Selvin, P. R. 1995. Fluorescence resonance energy transfer. Methods Enzymol. 246:300-334.
50. Smith, C. J., A. F. Drake, B. A. Banfield, G. B. Bloomberg, M. S. Palmer, A. R. Clarke, and J. Collinge. 1997. Conformational properties of the prion octa-repeat and hydrophobic sequences. FEBS Lett. 405:378-384.
51. Stella, L., M. Venanzi, M. Carafa, E. Maccaroni, M. E. Straccamore, G. Zanotti, A. Palleschi, and B. Pispisa. 2002. Structural features of model glycopeptides in solution and in membrane phase: a spectroscopic and molecular mechanics investigation. Biopolymers. 64:44-56.
52. Stockel, J., J. Safar, A. C. Wallace, F. E. Cohen, and S. B. Prusiner. 1998. Prion protein selectively binds copper(II) ions. Biochemistry. 37:7185-7193.
53. Stultz, C. M., A. D. Levin, and E. R. Edelman. 2002. Phosphorylation-induced conformational changes in a MAP-kinase substrate: implications for tyrosine hydroxylase activation. J. Biol. Chem. 277:47653-47661.
54. Stryer, L. 1978. Fluorescence energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47:819-846.
55. Stryer, L., and R. P. Haughland. 1967. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. USA. 58:719-726.
56. Sugita, Y., and Y. Okamoto. 1999. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314:141-151.
57. van der Meer, B. W. 2002. Kappa-squared: from nuisance to new sense. Rev. Mol. Biotechnol. 82:181-196.
58. Viles, J. H., F. E. Cohen, S. B. Prusiner, D. B. Goodin, P. E. Wright, and H. J. Dyson. 1999. Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. USA. 96:2042-2047.
59. Warner, R. G., C. Hundt, S. Weiss, and J. E. Turnbull. 2002. Identification of the heparan sulfate binding sites in the cellular prion protein. J. Biol. Chem. 277:18421-18430.
60. Weber, G., and M. Shinitzky. 1970. Failure of energy transfer between identical aromatic molecules on the excitation at the long wavelength edge of absortion spectrum. Proc. Natl. Acad. Sci. USA. 65:823-830.
61. Whittal, R. M., H. L. Ball, F. E. Cohen, A. L. Burlingame, S. B. Prusiner, and M. A. Baldwin. 2000. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci. 9:332-343.
62. Woody, R. W. 1995. Circular dichroism. Methods Enzymol. 246:34-71.
63. Woody, R. W., and A. K. Durker. 1996. Aromatic and cystine side-chain circular dichroism in proteins. In Circular Dichroism and the Conformational Analysis of Biomolecules. G. D. Fasman, editor. Plenum Press, New York. 109-157.
64. Wootton, J. C. 1994. Sequences with 'unusual' amino acid compositions. Curr. Opin. Struct. Biol. 4:413-421.
65. Wright, P. E., and H. J. Dyson. 1999. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J. Mol. Biol. 293:321-331.
66. Wu, P., and L. Brand. 1994. Resonance energy transfer: methods and applications. Anal. Biochem. 218:1-13.
67. Yoshida, H., N. Matsushima, Y. Kumaki, M. Nakata, and K. Hikichi. 2000. 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. 128:271-281.
68. Zahn, R., A. Liu, T. Luhrs, R. Riek, C. von Schroetter, F. Lopez Garcia, M. Billeter, L. Calzolai, G. Wider, and K. Wuthrich. 2000. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. USA. 97:145-150.