Dominant-negative effects in prion diseases: Insights from molecular dynamics simulations on mouse prion protein chimeras

Journal of Biomolecular Structure and Dynamics

Volumn 31, Issue 8, 2013, Pages 829-840

  Cong, Xiaojing ^a,e   Bongarzone, Salvatore ^a,d   Giachin, Gabriele ^a   Rossetti, Giulia ^b,c,d,e   Carloni, Paolo ^c,e   Legname, Giuseppe ^a,f  

^a SISSA   (Italy)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c Forschungszentrum Jülich ^*  (Germany)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e RWTH AACHEN UNIVERSITY   (Germany)

^f SINCROTRONE TRIESTE   (Italy)

Author keywords

Dominant negative; Molecular dynamics; Prion protein

Indexed keywords

PRION PROTEIN; SOLVENT;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATOM; CHIMERA; CONTROLLED STUDY; DISEASE PREDISPOSITION; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOUSE; MUTATION; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SCRAPIE; SIMULATION; TRANSGENIC MOUSE; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; GENES, DOMINANT; MICE; MOLECULAR DYNAMICS SIMULATION; PRION DISEASES; PRIONS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 84875123041     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2012.712477     Document Type: Article

References (88)

1. Adrover, M., Pauwels, K., Prigent, S., de Chiara, C., Xu, Z., Chapuis, C., ... Rezaei, H. (2010). Prion fibrillization is mediated by a native structural element that comprises helices H2 and H3. Journal of Biological Chemistry, 285, 21004-21012.
2. Agrimi, U., Nonno, R., Dell'Omo, G., Di Bari, M.A., Conte, M., Chiappini, B., ... Lipp, H.P. (2008). Prion protein amino acid determinants of differential susceptibility and molecular feature of prion strains in mice and voles. Plos Pathogens 4, e1000113.
3. Alonso, D.O.V., DeArmond, S.J., Cohen, F.E., & Daggett, V. (2001). Mapping the early steps in the pH-induced conformational conversion of the prion protein. Proceedings of the National Academy of Sciences of the United States of America, 98, 2985-2989.
4. Andersen, H.C. (1980). Molecular-dynamics simulations at constant pressure and-or temperature. Journal of Chemical Physics, 72, 2384-2393.
5. Aqvist, J. (1990). Ion water interaction potentials derived from free-energy perturbation simulations. Journal of Physical Chemistry, 94, 8021-8024.
6. Bamdad, K., & Naderi-Manesh, H. (2007). Contribution of a putative salt bridge and backbone dynamics in the structural instability of human prion protein upon R208H mutation. Biochemical and Biophysical Research Communications, 364, 719-724.
7. Baylis, M., & Goldmann, W. (2004). The genetics of scrapie in sheep and goats. Current Molecular Medicine, 4, 385-396.
8. Biljan, I., Giachin, G., Ilc, G., Zhukov, I., Plavec, J. & Legname, G. (2012). Structural basis for the protective effect of the human prion protein carrying the dominant-negative E219K polymorphism. Biochemistry Journal, 446, 243-251.
9. Bishop, M.T., Pennington, C., Heath, C.A., Will, R.G., & Knight, R.S. (2009). PRNP variation in UK sporadic and variant Creutzfeldt Jakob disease highlights genetic risk factors and a novel non-synonymous polymorphism. BMC Medical Genetics, 10, 146.
10. Bossers, A., Schreuder, B.E., Muileman, I.H., Belt, P.B., & Smits, M.A. (1996). PrP genotype contributes to determining survival times of sheep with natural scrapie. Journal of General Virology, 77(Pt 10), 2669-2673.
11. Brandner, S., Raeber, A., Sailer, A., Blattler, T., Fischer, M., Weissmann, C., & Aguzzi, A. (1996). Normal host prion protein (PrPC) is required for scrapie spread within the central nervous system. Proceedings of the National Academy of Sciences of the USA, 93, 13148-13151.
12. Bueler, H., Aguzzi, A., Sailer, A., Greiner, R.A., Autenried, P., Aguet, M., & Weissmann, C. (1993). Mice devoid of PrP are resistant to scrapie. Cell, 73, 1339-1347.
13. Bussi, G., Donadio, D. & Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics 126, 014101.
14. Calzolai, L., & Zahn, R. (2003). Influence of pH on NMR structure and stability of the human prion protein globular domain. Journal of Biological Chemistry, 278, 35592-35596.
15. Capellari, S., Strammiello, R., Saverioni, D., Kretzschmar, H., & Parchi, P. (2011). Genetic Creutzfeldt-Jakob disease and fatal familial insomnia: insights into phenotypic variability and disease pathogenesis. Acta Neuropathologica, 121, 21-37.
16. Chakroun, N., Prigent, S., Dreiss, C.A., Noinville, S., Chapuis, C., Fraternali, F., & Rezaei, H. (2010). The oligomerization properties of prion protein are restricted to the H2H3 domain. Faseb Journal, 24, 3222-3231.
17. Chebaro, Y., & Derreumaux, P. (2009). The conversion of helix H2 to beta-sheet is accelerated in the monomer and dimer of the prion protein upon T183A mutation. Journal of Physical Chemistry B, 113, 6942-6948.
18. Christen, B., Hornemann, S., Damberger, F.F., & Wuthrich, K. (2009). Prion protein NMR structure from tammar wallaby (Macropus eugenii) shows that the beta2-alpha2 loop is modulated by long-range sequence effects. Journal of Molecular Biology, 389, 833-845.
19. Christen, B., Perez, D.R., Hornemann, S., & Wuthrich, K. (2008). NMR structure of the bank vole prion protein at 20 degrees C contains a structured loop of residues 165-171. Journal of Molecular Biology, 383, 306-312.
20. Cobb, N.J., Sonnichsen, F.D., McHaourab, H., & Surewicz, W. K. (2007). Molecular architecture of human prion protein amyloid: A parallel, in-register beta-structure. Proceedings of the National Academy of Sciences of the USA, 104, 18946-18951.
21. Cohen, F.E., & Kelly, J.W. (2003). Therapeutic approaches to protein-misfolding diseases. Nature, 426, 905-909.
22. Damberger, F.F., Christen, B., Perez, D.R., Hornemann, S., & Wuthrich, K. (2011). Cellular prion protein conformation and function. Proceedings of the National Academy of Sciences of the United States of America, 108, 17308-17313.
23. Damo, S.M., Phillips, A.H., Young, A.L., Li, S., Woods, V.L. Jr., & Wemmer, D.E. (2010). Probing the conformation of a prion protein fibril with hydrogen exchange. Journal of Biological Chemistry, 285, 32303-32311.
24. Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald: An N. log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98, 10089-10092.
25. Deleault, N.R., Lucassen, R.W., & Supattapone, S. (2003). RNA molecules stimulate prion protein conversion. Nature, 425, 717-720.
26. Deleault, N.R., Piro, J.R., Walsh, D.J., Wang, F., Ma, J., Geoghegan, J.C., & Supattapone, S. (2012a). Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proceedings of the National Academy of Sciences of the USA, 109, 8546-8551.
27. Deleault, N.R., Walsh, D.J., Piro, J.R., Wang, F., Wang, X., Ma, J., .... Supattapone, S. (2012b). Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proceedings of the National Academy of Sciences of the USA, 109, E1938-E1946.
28. Dossena, S., Imeri, L., Mangieri, M., Garofoli, A., Ferrari, L., Senatore, A., ... Chiesa, R. (2008). Mutant prion protein expression causes motor and memory deficits and abnormal sleep patterns in a transgenic mouse model. Neuron, 60, 598-609.
29. Fink, J.K., Peacock, M.L., Warren, J.T., Roses, A.D., & Prusiner, S.B. (1994). Detecting prion protein gene-mutations by denaturing gradient gel-electrophoresis. Human Mutation, 4, 42-50.
30. Friedman-Levi, Y., Meiner, Z., Canello, T., Frid, K., Kovacs, G.G., Budka, H., ... Gabizon, R. (2011). Fatal prion disease in a mouse model of genetic E200K Creutzfeldt-Jakob disease. Plos Pathogens 7, e1002350.
31. Geoghegan, J.C., Miller, M.B., Kwak, A.H., Harris, B.T., & Supattapone, S. (2009). Trans-dominant inhibition of prion propagation in vitro is not mediated by an accessory cofactor. Plos Pathogens, 5, e1000535.
32. Goldmann, W., Hunter, N., Smith, G., Foster, J., & Hope, J. (1994). Prp genotype and agent effects in scrapie - change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. Journal of General Virology, 75, 989-995.
33. Gossert, A.D., Bonjour, S., Lysek, D.A., Fiorito, F., & Wuthrich, K. (2005). Prion protein NMR structures of elk and of mouse/elk hybrids. Proceedings of the National Academy of Sciences of the USA, 102, 646-650.
34. Guex, N., & Peitsch, M.C. (1997). SWISS-MODEL and the Swiss-PDB viewer: An environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
35. Helmus, J.J., Surewicz, K., Nadaud, P.S., Surewicz, W.K., & Jaroniec, C.P. (2008). Molecular conformation and dynamics of the Y145Stop variant of human prion protein in amyloid fibrils. Proceedings of the National Academy of Sciences of the USA, 105, 6284-6289.
36. Hess, B., Bekker, H., Berendsen, H.J.C., & Fraaije, J.G.E.M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463-1472.
37. Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4, 435-447.
38. Hizume, M., Kobayashi, A., Teruya, K., Ohashi, H., Ironside, J. W., Mohri, S., & Kitamoto, T. (2009). Human prion protein (PrP) 219K Is converted to PrP(Sc) but shows heterozygous inhibition in variant Creutzfeldt-Jakob disease infection. Journal of Biological Chemistry, 284, 3603-3609.
39. Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics & Modelling, 14, 33-38.
40. Jackson, W.S., Borkowski, A.W., Faas, H., Steele, A.D., King, O.D., Watson, N., ... Lindquist, S. (2009). Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron, 63, 438-450.
41. James, T.L., Liu, H., Ulyanov, N.B., Farr-Jones, S., Zhang, H., Donne, D.G., ... Cohen, F.E. (1997). Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proceedings of the National Academy of Sciences of the USA, 94, 10086-10091.
42. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., & Klein, M.L. (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics, 79, 926-935.
43. Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure - pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
44. Kallberg, Y., Gustafsson, M., Persson, B., Thyberg, J., & Johansson, J. (2001). Prediction of amyloid fibril-forming proteins. Journal of Biological Chemistry, 276, 12945-12950.
45. Kaneko, K., Zulianello, L., Scott, M., Cooper, C.M., Wallace, A.C., James, T.L., ... Prusiner, S.B. (1997). Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proceedings of the National Academy of Sciences of the USA, 94, 10069-10074.
46. Kobayashi, A., Hizume, M., Teruya, K., Mohri, S., & Kitamoto, T. (2009). Heterozygous inhibition in prion infection: The stone fence model. Prion, 3, 27-30.
47. Kuwata, K., Kamatari, Y.O., Akasaka, K., & James, T.L. (2004). Slow conformational dynamics in the hamster prion protein. Biochemistry, 43, 4439-4446.
48. Kuwata, K., Li, H., Yamada, H., Legname, G., Prusiner, S.B., Akasaka, K., & James, T.L. (2002). Locally disordered conformer of the hamster prion protein: A crucial intermediate to PrPSc? Biochemistry, 41, 12277-12283.
49. Lee, C.I., Yang, Q., Perrier, V., & Baskakov, I.V. (2007). The dominant-negative effect of the Q218K variant of the prion protein does not require protein X. Protein Science, 16, 2166-2173.
50. Legname, G., Nguyen, H.O.B., Baskakov, I.V., Cohen, F.E., DeArmond, S.J., & Prusiner, S.B. (2006). Strain-specified characteristics of mouse synthetic prions (vol 102, pg 2168, 2005). Proceedings of the National Academy of Sciences of the United States of America, 103, 14642-14642.
51. Lim, K.H., Nguyen, T.N., Damo, S.M., Mazur, T., Ball, H.L., Prusiner, S.B., ... Wemmer, D.E. (2006). Solid-state NMR structural studies of the fibril form of a mutant mouse prion peptide PrP89-143(P101L). Solid State Nuclear Magnetic Resonance, 29, 183-190.
52. Linden, R., Martins, V.R., Prado, M.A.M., Cammarota, M., Izquierdo, I., & Brentani, R.R. (2008). Physiology of the prion protein. Physiological Reviews, 88, 673-728.
53. Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J.L., Dror, R.O., & Shaw, D.E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins-Structure Function and Bioinformatics, 78, 1950-1958.
54. Lu, X., Wintrode, P.L., & Surewicz, W.K. (2007). Beta-sheet core of human prion protein amyloid fibrils as determined by hydrogen/deuterium exchange. Proceedings of the National Academy of Sciences of the USA, 104, 1510-1515.
55. Lysek, D.A., Schorn, C., Nivon, L.G., Esteve-Moya, V., Christen, B., Calzolai, L., ... Wuthrich, K. (2005). Prion protein NMR structures of cats, dogs, pigs, and sheep. Proceedings of the National Academy of Sciences of the USA, 102, 640-645.
56. Mastrianni, J.A. (2010). The genetics of prion diseases. Genetics in Medicine, 12, 187-195.
57. Mead, S., Stumpf, M.P.H., Whitfield, J., Beck, J.A., Poulter, M., Campbell, T., ... Collinge, J. (2003). Balancing selection at the prion protein gene consistent with prehistoric kurulike epidemics. Science, 300, 640-643.
58. Meli, M., Gasset, M., & Colombo, G. (2011). Dynamic diagnosis of familial prion diseases supports the beta 2-alpha 2 loop as a universal interference target. Plos One 6, e19093.
59. Micheletti, C., Seno, F., & Maritan, A. (2000). Recurrent oligomers in proteins: An optimal scheme reconciling accurate and concise backbone representations in automated folding and design studies. Proteins-Structure Function and Bioinformatics, 40, 662-674.
60. Nekooki-Machida, Y., Kurosawa, M., Nukina, N., Ito, K., Oda, T., & Tanaka, M. (2009). Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity. Proceedings of the National Academy of Sciences of the USA, 106, 9679-9684.
61. Pan, K.M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., ... Prusiner, S.B. (1993). Conversion of alphahelices into beta-sheets features in the formation of the scrapie prion proteins. Proceedings of the National Academy of Sciences of the United States of America, 90, 10962-10966.
62. Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single-crystals - a new molecular-dynamics method. Journal of Applied Physics, 52, 7182-7190.
63. Perez, D.R., Damberger, F.F., & Wuthrich, K. (2010). Horse prion protein NMR structure and comparisons with related variants of the mouse prion protein. Journal of Molecular Biology, 400, 121-128.
64. Perrier, V., Kaneko, K., Safar, J., Vergara, J., Tremblay, P., DeArmond, S.J., ... Wallace, A.C. (2002). Dominantnegative inhibition of prion replication in transgenic mice. Proceedings of the National Academy of Sciences of the USA, 99, 13079-13084.
65. Prusiner, S.B. (2001). Shattuck lecture - neurodegenerative diseases and prions. New England Journal of Medicine, 344, 1516-1526.
66. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., & Wuthrich, K. (1996). NMR structure of the mouse prion protein domain PrP(121-231). Nature, 382, 180-182.
67. Riek, R., Wider, G., Billeter, M., Hornemann, S., Glockshuber, R., & Wuthrich, K. (1998). Prion protein NMR structure and familial human spongiform encephalopathies. Proceedings of the National Academy of Sciences of the United States of America, 95, 11667-11672.
68. Rossetti, G., Cong, X.J., Caliandro, R., Legname, G., & Carloni, P. (2011). Common structural traits across pathogenic mutants of the human prion protein and their implications for familial prion diseases. Journal of Molecular Biology, 411, 700-712.
69. Rossetti, G., Giachin, G., Legname, G., & Carloni, P. (2010). Structural facets of disease-linked human prion protein mutants: A molecular dynamic study. Proteins-Structure Function and Bioinformatics, 78, 3270-3280.
70. Sabuncu, E., Petit, S., Le Dur, A., Lan Lai, T., Vilotte, J.L., Laude, H., & Vilette, D. (2003). PrP polymorphisms tightly control sheep prion replication in cultured cells. Journal of Virology, 77, 2696-2700.
71. Santini, S., Claude, J.B., Audic, S., & Derreumaux, P. (2003). Impact of the tail and mutations G131V and M129V on prion protein flexibility. Proteins-Structure Function and Genetics, 51, 258-265.
72. Santini, S., & Derreumaux, P. (2004). Helix H1 of the prion protein is rather stable against environmental perturbations: Molecular dynamics of mutation and deletion variants of PrP(90-231). Cellular and Molecular Life Sciences, 61, 951-960.
73. Sekijima, M., Motono, C., Yamasaki, S., Kaneko, K., & Akiyama, Y. (2003). Molecular dynamics simulation of dimeric and monomeric forms of human prion protein: Insight into dynamics and properties. Biophysical Journal, 85, 1176-1185.
74. Shibuya, S., Higuchi, J., Shin, R.W., Tateishi, J., & Kitamoto, T. (1998). Codon 219 Lys allele of PRNP is not found in sporadic Creutzfeldt-Jakob disease. Annals of Neurolog, 43, 826-828.
75. Sigurdson, C.J., Joshi-Barr, S., Bett, C., Winson, O., Manco, G., Schwarz, P., ... Aguzzi, A. (2011). Spongiform encephalopathy in transgenic mice expressing a point mutation in the beta 2-alpha 2 loop of the prion protein. Journal of Neuroscience, 31, 13840-13847.
76. Sigurdson, C.J., Nilsson, K.P.R., Hornemann, S., Heikenwalder, M., Manco, G., Schwarz, P., ... Aguzzi, A. (2009). De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proceedings of the National Academy of Sciences of the United States of America, 106, 304-309.
77. Sigurdson, C.J., Nilsson, K.P.R., Hornemann, S., Manco, G., Fernandez-Borges, N., Schwarz, P., ... Aguzzi, A. (2010). A molecular switch controls interspecies prion disease transmission in mice. Journal of Clinical Investigation, 120, 2590-2599.
78. Soldevila, M., Calafell, F., Andres, A.M., Yague, J., Helgason, A., Stefansson, K., & Bertranpetit, J. (2003). Prion susceptibility and protective alleles exhibit marked geographic differences. Human Mutation, 22, 104-105.
79. Sutcliffe, M.J. (1993). Representing an ensemble of nmrderived protein structures by a single structure. Protein Science, 2, 936-944.
80. Telling, G.C., Scott, M., Hsiao, K.K., Foster, D., Yang, S.L., Torchia, M., ... Prusiner, S.B. (1994). Transmission of Creutzfeldt-Jakob-disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proceedings of the National Academy of Sciences of the United States of America, 91, 9936-9940.
81. Telling, G.C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F.E., ... Prusiner, S.B. (1995). Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell, 83, 79-90.
82. Tessier, P.M., & Lindquist, S. (2007). Prion recognition elements govern nucleation, strain specificity and species barriers. Nature, 447, 556-561.
83. Tycko, R., Savtchenko, R., Ostapchenko, V.G., Makarava, N., & Baskakov, I.V. (2010). The alpha-helical C-terminal domain of full-length recombinant PrP converts to an inregister parallel beta-sheet structure in PrP fibrils: Evidence from solid state nuclear magnetic resonance. Biochemistry, 49, 9488-9497.
84. van der Kamp, M.W., & Daggett, V. (2009). The consequences of pathogenic mutations to the human prion protein. Protein Engineering Design & Selection, 22, 461-468.
85. van der Kamp, M.W., & Daggett, V. (2010). Pathogenic mutations in the hydrophobic core of the human prion protein can promote structural instability and misfolding. Journal of Molecular Biology, 404, 732-748.
86. Wen, Y., Li, J., Yao, W., Xiong, M., Hong, J., Peng, Y., ... Lin, D. (2010). Unique structural characteristics of the rabbit prion protein. Journal of Biological Chemistry, 285, 31682-31693.
87. Westaway, D., Zuliani, V., Cooper, C.M., Dacosta, M., Neuman, S., Jenny, A.L., ... Prusiner, S.B. (1994). Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes & Development, 8, 959-969.
88. Zahn, R., Liu, A.Z., Luhrs, T., Riek, R., von Schroetter, C., Garcia, F.L., ... Wuthrich, K. (2000). NMR solution structure of the human prion protein. Proceedings of the National Academy of Sciences of the United States of America, 97, 145-150.