Crystal Structures of Polymorphic Prion Protein β1 Peptides Reveal Variable Steric Zipper Conformations

Biochemistry

Volumn 54, Issue 23, 2015, Pages 3640-3648

  Yu, Lu ^a   Lee, Seung Joo ^a,b   Yee, Vivien C ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Warp Drive Bio LLC ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; PEPTIDES;

BETA-SHEET; CONFORMATIONAL CONVERSION; CONFORMATIONAL DIFFERENCES; DISEASE SUSCEPTIBILITY; INITIATION SITES; PRION DISEASE; PRION PROTEIN; RIGOROUS APPROACH;

PROTEINS;

LEUCINE; METHIONINE; PEPTIDE; PRION PROTEIN; PRION PROTEIN BETA 1; UNCLASSIFIED DRUG; VALINE; OLIGOPEPTIDE; PEPTIDE FRAGMENT; PRION; PRNP PROTEIN, HUMAN;

ARTICLE; BETA SHEET; CRYSTAL; CRYSTAL STRUCTURE; GENETIC SUSCEPTIBILITY; GEOMETRY; HUMAN; HYDROGEN BOND; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; CRYSTALLIZATION; GENETIC POLYMORPHISM; GENETICS; MOLECULAR WEIGHT; PRION; PROTEIN DATABASE; PROTEIN MOTIF; STEREOISOMERISM; SURFACE PROPERTY;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; CRYSTALLIZATION; DATABASES, PROTEIN; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR WEIGHT; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; POLYMORPHISM, GENETIC; PRIONS; PROTEIN CONFORMATION; STEREOISOMERISM; SURFACE PROPERTIES;

EID: 84934987870     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00425     Document Type: Article

References (53)

1. Prusiner, S. B. (1998) Prions Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
2. Collinge, J. (2001) Prion diseases of humans and animals: Their causes and molecular basis Annu. Rev. Neurosci. 24, 519-550
3. Aguzzi, A., Baumann, F., and Bremer, J. (2008) The prions elusive reason for being Annu. Rev. Neurosci. 31, 439-477
4. Knight, R. (2006) Creutzfeldt-Jakob disease: A rare cause of dementia in elderly persons Clin. Infect. Dis. 43, 340-346
5. Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., and Cohen, F. E. 1993, Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
6. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wuthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-231) Nature 382, 180-182
7. James, T. L., Liu, H., Ulyanov, N. B., Farr-Jones, S., Zhang, H., Donne, D. G., Kaneko, K., Groth, D., Mehlhorn, I., Prusiner, S. B., and Cohen, F. E. (1997) Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform Proc. Natl. Acad. Sci. U.S.A. 94, 10086-10091
8. Zahn, R., Liu, A., Luhrs, T., Riek, R., von Schroetter, C., Lopez Garcia, F., Billeter, M., Calzolai, L., Wider, G., and Wuthrich, K. (2000) NMR solution structure of the human prion protein Proc. Natl. Acad. Sci. U.S.A. 97, 145-150
9. Knaus, K. J., Morillas, M., Swietnicki, W., Malone, M., Surewicz, W. K., and Yee, V. C. (2001) Crystal structure of the human prion protein reveals a mechanism for oligomerization Nat. Struct. Biol. 8, 770-774
10. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F., and Caughey, W. S. (1991) Secondary Structure-Analysis of the Scrapie-Associated Protein Prp 27-30 in Water by Infrared-Spectroscopy Biochemistry 30, 7672-7680
11. Surewicz, W. K. and Apostol, M. I. (2011) Prion protein and its conformational conversion: A structural perspective Top. Curr. Chem. 305, 135-167
12. Sweeting, B., Brown, E., Khan, M. Q., Chakrabartty, A., and Pai, E. F. (2013) N-Terminal Helix-Cap in α-Helix 2 Modulates β-State Misfolding in Rabbit and Hamster Prion Proteins PLoS One 8, e63047
13. Khan, M. Q., Sweeting, B., Mulligan, V. K., Arslan, P. E., Cashman, N. R., Pai, E. F., and Chakrabartty, A. (2010) Prion disease susceptibility is affected by β-structure folding propensity and local side-chain interactions in PrP Proc. Natl. Acad. Sci. U.S.A. 107, 19808-19813
14. Lee, S., Antony, L., Hartmann, R., Knaus, K. J., Surewicz, K., Surewicz, W. K., and Yee, V. C. (2010) Conformational diversity in prion protein variants influences intermolecular β-sheet formation EMBO J. 29, 251-262
15. Haire, L. F., Whyte, S. M., Vasisht, N., Gill, A. C., Verma, C., Dodson, E. J., Dodson, G. G., and Bayley, P. M. (2004) The crystal structure of the globular domain of sheep prion protein J. Mol. Biol. 336, 1175-1183
16. Antonyuk, S. V., Trevitt, C. R., Strange, R. W., Jackson, G. S., Sangar, D., Batchelor, M., Cooper, S., Fraser, C., Jones, S., Georgiou, T., Khalili-Shirazi, A., Clarke, A. R., Hasnain, S. S., and Collinge, J. (2009) Crystal structure of human prion protein bound to a therapeutic antibody Proc. Natl. Acad. Sci. U.S.A. 106, 2554-2558
17. Baral, P. K., Swayampakula, M., Rout, M. K., Kav, N. N., Spyracopoulos, L., Aguzzi, A., and James, M. N. (2014) Structural basis of prion inhibition by phenothiazine compounds Structure 22, 291-303
18. Abskharon, R. N., Giachin, G., Wohlkonig, A., Soror, S. H., Pardon, E., Legname, G., and Steyaert, J. (2014) Probing the N-terminal β-sheet conversion in the crystal structure of the human prion protein bound to a nanobody J. Am. Chem. Soc. 136, 937-944
19. Palmer, M. S., Dryden, A. J., Hughes, J. T., and Collinge, J. (1991) Homozygous prion protein genotype predisposes to sporadic Creutzfeldt-Jakob disease Nature 352, 340-342
20. Goldfarb, L. G., Petersen, R. B., Tabaton, M., Brown, P., LeBlanc, A. C., Montagna, P., Cortelli, P., Julien, J., Vital, C., and Pendelbury, W. W. 1992, Fatal familial insomnia and familial Creutzfeldt-Jakob disease: Disease phenotype determined by a DNA polymorphism Science 258, 806-808
21. Mead, S., Stumpf, M. P., Whitfield, J., Beck, J. A., Poulter, M., Campbell, T., Uphill, J. B., Goldstein, D., Alpers, M., Fisher, E. M., and Collinge, J. (2003) Balancing selection at the prion protein gene consistent with prehistoric kurulike epidemics Science 300, 640-643
22. Green, K. M., Browning, S. R., Seward, T. S., Jewell, J. E., Ross, D. L., Green, M. A., Williams, E. S., Hoover, E. A., and Telling, G. C. (2008) The elk PRNP codon 132 polymorphism controls cervid and scrapie prion propagation J. Gen. Virol. 89, 598-608
23. Peletto, S., Perucchini, M., Acin, C., Dalgleish, M. P., Reid, H. W., Rasero, R., Sacchi, P., Stewart, P., Caramelli, M., Ferroglio, E., Bozzetta, E., Meloni, D., Orusa, R., Robetto, S., Gennero, S., Goldmann, W., and Acutis, P. L. (2009) Genetic variability of the prion protein gene (PRNP) in wild ruminants from Italy and Scotland J. Vet. Sci. 10, 115-120
24. Hamir, A. N., Gidlewski, T., Spraker, T. R., Miller, J. M., Creekmore, L., Crocheck, M., Cline, T., and ORourke, K. I. (2006) Preliminary observations of genetic susceptibility of elk (Cervus elaphus nelsoni) to chronic wasting disease by experimental oral inoculation J. Vet. Diagn. Invest. 18, 110-114
25. Perucchini, M., Griffin, K., Miller, M. W., and Goldmann, W. (2008) PrP genotypes of free-ranging wapiti (Cervus elaphus nelsoni) with chronic wasting disease J. Gen. Virol. 89, 1324-1328
26. Hosszu, L. L., Jackson, G. S., Trevitt, C. R., Jones, S., Batchelor, M., Bhelt, D., Prodromidou, K., Clarke, A. R., Waltho, J. P., and Collinge, J. (2004) The residue 129 polymorphism in human prion protein does not confer susceptibility to Creutzfeldt-Jakob disease by altering the structure or global stability of PrPC J. Biol. Chem. 279, 28515-28521
27. Apostol, M. I., Sawaya, M. R., Cascio, D., and Eisenberg, D. (2010) Crystallographic Studies of Prion Protein (PrP) Segments Suggest How Structural Changes Encoded by Polymorphism at Residue 129 Modulate Susceptibility to Human Prion Disease J. Biol. Chem. 285, 29671-29675
28. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. O., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers Nature 447, 453-457
29. Wiltzius, J. J., Landau, M., Nelson, R., Sawaya, M. R., Apostol, M. I., Goldschmidt, L., Soriaga, A. B., Cascio, D., Rajashankar, K., and Eisenberg, D. (2009) Molecular mechanisms for protein-encoded inheritance Nat. Struct. Mol. Biol. 16, 973-978
30. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R., and Eisenberg, D. (2005) Structure of the cross-β spine of amyloid-like fibrils Nature 435, 773-778
31. Wiltzius, J. J., Sievers, S. A., Sawaya, M. R., Cascio, D., Popov, D., Riekel, C., and Eisenberg, D. (2008) Atomic structure of the cross-β spine of islet amyloid polypeptide (amylin) Protein Sci. 17, 1467-1474
32. Colletier, J. P., Laganowsky, A., Landau, M., Zhao, M., Soriaga, A. B., Goldschmidt, L., Flot, D., Cascio, D., Sawaya, M. R., and Eisenberg, D. (2011) Molecular basis for amyloid-β polymorphism Proc. Natl. Acad. Sci. U.S.A. 108, 16938-16943
33. Apostol, M. I., Perry, K., and Surewicz, W. K. (2013) Crystal structure of a human prion protein fragment reveals a motif for oligomer formation J. Am. Chem. Soc. 135, 10202-10205
34. Apostol, M. I., Wiltzius, J. J. W., Sawaya, M. R., Cascio, D., and Eisenberg, D. (2011) Atomic Structures Suggest Determinants of Transmission Barriers in Mammalian Prion Disease Biochemistry 50, 2456-2463
35. Yau, J. and Sharpe, S. (2012) Structures of amyloid fibrils formed by the prion protein derived peptides PrP(244-249) and PrP(245-250) J. Struct. Biol. 180, 290-302
36. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
37. Sheldrick, G. M. (2008) A short history of SHELX Acta Crystallogr. A64, 112-122
38. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
39. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr. D67, 235-242
40. Kissinger, C. R., Gehlhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search Acta Crystallogr. D55, 484-491
41. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
42. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
43. Lee, B. and Richards, F. M. (1971) The interpretation of protein structures: Estimation of static accessibility J. Mol. Biol. 55, 379-400
44. Saff, E. B. and Kuijlaars, A. B. J. (1997) Distributing many points on a sphere The Mathematical Intelligencer 19, 5-11
45. Lawrence, M. C. and Colman, P. M. (1993) Shape Complementarity at Protein-Protein Interfaces J. Mol. Biol. 234, 946-950
46. Richards, F. M. (1977) Areas, Volumes, Packing, and Protein-Structure Annu. Rev. Biophys. Bioeng. 6, 151-176
47. Connolly, M. L. (1983) Analytical Molecular-Surface Calculation J. Appl. Crystallogr. 16, 548-558
48. Nicholls, A., Bharadwaj, R., and Honig, B. (1993) Grasp: Graphical Representation and Analysis of Surface-Properties Biophys. J. 64, A166
49. Zeidler, M., Stewart, G., Cousens, S. N., Estibeiro, K., and Will, R. G. (1997) Codon 129 genotype and new variant CJD Lancet 350, 668
50. Collinge, J. and Clarke, A. R. (2007) A general model of prion strains and their pathogenicity Science 318, 930-936
51. Haik, S. and Brandel, J. P. (2011) Biochemical and strain properties of CJD prions: Complexity versus simplicity J. Neurochem. 119, 251-261
52. Weissmann, C., Li, J. L., Mahal, S. P., and Browning, S. (2011) Prions on the move EMBO Rep. 12, 1109-1117
53. Telling, G. C. (2011) Transgenic mouse models and prion strains Top. Curr. Chem. 305, 79-99