Structural basis for the protective effect of the human prion protein carrying the dominant-negative E219K polymorphism

Biochemical Journal

Volumn 446, Issue 2, 2012, Pages 243-251

  Biljan, Ivana ^a,g   Giachin, Gabriele ^b   Ilc, Gregor ^c   Zhukov, Igor ^c,h   Plavec, Janez ^c,d   Legname, Giuseppe ^a,e,f  

^a NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^b SISSA   (Italy)

^c EN FIST Centre of Excellence   (Slovenia)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^f SINCROTRONE TRIESTE   (Italy)

^g UNIVERSITY OF ZAGREB   (Croatia)

^h INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Creutzfeldt Jakob disease (CJD); NMR structure; Prion protein; Protective polymorphism; Transmissible spongiform encephalopathy (TSE)

Indexed keywords

GLUTAMIC ACID; LYSINE; PRION PROTEIN; PROTEIN; PROTEIN E219K; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE; WILD TYPE;

ALLELES; AMINO ACID SUBSTITUTION; CREUTZFELDT-JAKOB SYNDROME; EPITOPES; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTANT PROTEINS; PEPTIDE FRAGMENTS; POLYMORPHISM, GENETIC; PRIONS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 84865187121     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111940     Document Type: Article

References (44)

1. Colby, D. W. and Prusiner, S. B. (2011) Prions. Cold Spring Harbor Perspect. Biol. 3, a006833
2. Kocisko, D. A., Come, J. H., Priola, S. A., Chesebro, B., Raymond, G. J., Lansbury, P. T. and Caughey, B. (1994) Cell-free formation of protease-resistant prion protein. Nature 370, 471-474 (Pubitemid 24263553)
3. Surewicz, W. K. and Apostol, M. I. (2011) Prion protein and its conformational conversion: a structural perspective. Top. Curr. Chem. 305, 135-167
4. Aguzzi, A., Sigurdson, C. and Heikenwaelder, M. (2008) Molecular mechanisms of prion pathogenesis. Annu. Rev. Pathol. 3, 11-40 (Pubitemid 351488275)
5. 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 (Pubitemid 30055798)
6. Riek, R., Hornemann, S., Wider, G., Glockshuber, R. and Wuthrich, K. (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett. 413, 282-288 (Pubitemid 27353285)
7. Jackson, W. S., Borkowski, A. W., Faas, H., Steele, A. D., King, O. D., Watson, N., Jasanoff, A. and Lindquist, S. (2009) Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron 63, 438-450
8. Sigurdson, C. J., Nilsson, K. P., Hornemann, S., Manco, G., Fernandez-Borges, N., Schwarz, P., Castilla, J., Wuthrich, K. and Aguzzi, A. (2010) A molecular switch controls interspecies prion disease transmission in mice. J. Clin. Invest. 120, 2590-2599
9. Nozaki, I., Hamaguchi, T., Sanjo, N., Noguchi-Shinohara, M., Sakai, K., Nakamura, Y., Sato, T., Kitamoto, T., Mizusawa, H., Moriwaka, F. et al. (2010) Prospective 10-year surveillance of human prion diseases in Japan. Brain 133, 3043-3057
10. Shibuya, S., Higuchi, J., Shin, R. W., Tateishi, J. and Kitamoto, T. (1998) Codon 219 Lys allele of PRNP is not found in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 43, 826-828 (Pubitemid 28280227)
11. Soldevila, M., Calafell, F., Andres, A. M., Yague, J., Helgason, A., Stefansson, K. and Bertranpetit, J. (2003) Prion susceptibility and protective alleles exhibit marked geographic differences. Hum. Mutat. 22, 104-105
12. Perrier, V., Kaneko, K., Safar, J., Vergara, J., Tremblay, P., DeArmond, S. J., Cohen, F. E., Prusiner, S. B. and Wallace, A. C. (2002) Dominant-negative inhibition of prion replication in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 99, 13079-13084
13. Hizume, M., Kobayashi, A., Teruya, K., Ohashi, H., Ironside, J. W., Mohri, S. and Kitamoto, T. (2009) Human prion protein (PrP) 219K is converted to PrPSc but shows heterozygous inhibition in variant Creutzfeldt-Jakob disease infection. J. Biol. Chem. 284, 3603-3609
14. Crozet, C., Lin, Y. L., Mettling, C., Mourton-Gilles, C., Corbeau, P., Lehmann, S. and Perrier, V. (2004) Inhibition of PrPSc formation by lentiviral gene transfer of PrP containing dominant negative mutations. J. Cell Sci. 117, 5591-5597 (Pubitemid 40012205)
15. Kaneko, K., Zulianello, L., Scott, M., Cooper, C. M., Wallace, A. C., James, T. L., Cohen, F. E. and Prusiner, S. B. (1997) Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. U.S.A. 94, 10069-10074
16. Lee, C. I., Yang, Q., Perrier, V. and Baskakov, I. V. (2007) The dominant-negative effect of the Q218K variant of the prion protein does not require protein X. Protein Sci. 16, 2166-2173 (Pubitemid 47481651)
17. Geoghegan, J. C., Miller, M. B., Kwak, A. H., Harris, B. T. and Supattapone, S. (2009) Trans-dominant inhibition of prion propagation in vitro is not mediated by an accessory cofactor. PLoS Pathog. 5, e1000535
18. Marijanovic, Z., Caputo, A., Campana, V. and Zurzolo, C. (2009) Identification of an intracellular site of prion conversion. PLoS Pathog. 5, e1000426
19. Ilc, G., Giachin, G., Jaremko, M., Jaremko, L., Benetti, F., Plavec, J., Zhukov, I. and Legname, G. (2010) NMR structure of the human prion protein with the pathological Q212P mutation reveals unique structural features. PLoS ONE 5, e11715
20. Biljan, I., Ilc, G., Giachin, G., Raspadori, A., Zhukov, I., Plavec, J. and Legname, G. (2011) Toward the molecular basis of inherited prion diseases: nmr structure of the human prion protein with V210I mutation. J. Mol. Biol. 412, 660-673
21. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6, 277-293
22. Reference deleted
23. Keller, R. L. (2004) The Computer Aided Resonance Assignment Tutorial, CANTINA Verlag, Goldau
24. Güntert, P., Mumenthaler, C. and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (Pubitemid 27460230)
25. Herrmann, T., Güntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227 (Pubitemid 34729497)
26. Krieger, E., Koraimann, G. and Vriend, G. (2002) Increasing the precision of comparative models with YASARA NOVA: a self-parameterizing force field. Proteins 47, 393-402 (Pubitemid 34438688)
27. Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
28. Vriend, G. (1990) WHAT IF: a molecular modelling and drug design program. J. Mol. Graph. 9, 52-56
29. Cavanagh, J., Fairbrother, W. F., Palmer, A. G., Rance, M. and Skelton, N. J. (2007) Protein NMR spectroscopy: principles and practice, Elsevier, San Diego
30. 13C NMR chemical shifts can predict disulfide bond formation. J. Biomol. NMR 18, 165-171
31. Shen, Y. and Bax, A. (2010) Prediction of Xaa-Pro peptide bond conformation from sequence and chemical shifts. J. Biomol. NMR 46, 199-204
32. Watzlawik, J., Skora, L., Frense, D., Griesinger, C., Zweckstetter, M., Shulz-Schaeffer, W. J. and Kramer, M. L. (2006) Prion protein helix 1 promotes aggregation but is not converted into β-sheet. J. Biol. Chem. 281, 30242-30250 (Pubitemid 44537031)
33. Zhang, Y. B., Swietnicki, W., Zagorski, M. G., Surewicz, W. K. and Sönnichsen, F. D. (2000) Solution structure of the E200K variant of human prion protein: implications for the mechanism of pathogenesis in familial prion diseases. J. Biol. Chem. 275, 33650-33654
34. Lee, S., Antony, L., Hartmann, R., Knaus, K. J., Surewicz, K., Surewicz, W. K. and Yee, V. C. (2009) Conformational diversity in prion protein variants influences intermolecular β-sheet formation. EMBO J. 29, 251-262
35. Meli, M., Gasset, M. and Colombo, G. (2011) Dynamic diagnosis of familial prion diseases supports the β2-α2 loop as a universal interference target. PLoS ONE 6, e19093
36. Rossetti, G., Cong, X., Caliandro, R., Legname, G. and Carloni, P. (2011) Common structural traits across pathogenic mutants of the human prion protein and their implications for familial prion diseases. J. Mol. Biol. 411, 700-712
37. van der Kamp, M. W. and Daggett, V. (2011) Molecular dynamics as an approach to study prion protein misfolding and the effect of pathogenic mutations. Top. Curr. Chem. 305, 169-197
38. Perez, D. R., Damberger, F. F. and Wuthrich, K. (2010) Horse prion protein NMR structure and comparisons with related variants of the mouse prion protein. J. Mol. Biol. 400, 121-128
39. Wen, Y., Li, J., Yao, W., Xiong, M., Hong, J., Peng, Y., Xiao, G. and Lin, D. (2010) Unique structural characteristics of the rabbit prion protein. J. Biol. Chem. 285, 31682-31693
40. Mastrianni, J. A. (2010) The genetics of prion diseases. Genet. Med. 12, 187-195
41. Fraczkiewicz, R. and Braun, W. (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19, 319-333 (Pubitemid 128592649)
42. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G. and Baker, N. A. (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res. 35, W522-W525
43. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041 (Pubitemid 32802969)
44. Li, H., Robertson, A. D. and Jensen, J. H. (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61, 704-721 (Pubitemid 41753142)