Structure of the β2-α2 loop and interspecies prion transmission

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 2868-2876

  Bett, Cyrus ^a,b   Fernández Borges, Natalia ^c   Kurt, Timothy D ^a,b   Lucero, Melanie ^a,b   Nilsson, K Peter R ^d   Castilla, Joaquín ^c,e   Sigurdson, Christina J ^a,b,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c CIC BIOGUNE   (Spain)

^d LINKÖPING UNIVERSITY   (Sweden)

^e BASQUE FOUNDATION FOR SCIENCE   (Spain)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid; Neurodegeneration; Transmissible spongiform encephalopathy; TSE

Indexed keywords

PRION PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; INOCULATION; MOUSE; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECONDARY STRUCTURE; RESIDUE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; VIRUS TRANSMISSION;

AMINO ACID SUBSTITUTION; ANIMALS; BRAIN; BRAIN CHEMISTRY; CATTLE; CRICETINAE; DEER; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRION DISEASES; PROTEIN CONFORMATION; PROTEIN FOLDING; PRPC PROTEINS; RECOMBINANT PROTEINS; SHEEP; SPECIES SPECIFICITY;

ANIMALIA; MUS;

EID: 84863186235     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-200923     Document Type: Article

References (53)

1. Wells, G. A., and Wilesmith, J. W. (1995) The neuropathology and epidemiology of bovine spongiform encephalopathy. Brain Pathol. 5, 91-103
2. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
3. Prusiner, S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522
4. Will, R. G., Ironside, J. W., Zeidler, M., Cousens, S. N., Estibeiro, K., Alperovitch, A., Poser, S., Pocchiari, M., Hofman, A., and Smith, P. G. (1996) A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347, 921-925 (Pubitemid 26102546)
5. Collinge, J., Sidle, K. C., Meads, J., Ironside, J., and Hill, A. F. (1996) Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 383, 685-690 (Pubitemid 26360638)
6. Bruce, M. E., Will, R. G., Ironside, J. W., McConnell, I., Drummond, D., Suttie, A., McCardle, L., Chree, A., Hope, J., Birkett, C., Cousens, S., Fraser, H., and Bostock, C. J. (1997) Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent Nature 389, 498-501 (Pubitemid 27435325)
7. Kirkwood, J. K., Cunningham, A. A., Wells, G. A., Wilesmith, J. W., and Barnett, J. E. (1993) Spongiform encephalopathy in a herd of greater kudu (Tragelaphus strepsiceros): epidemiological observations. Vet. Rec. 133, 360-364
8. Kirkwood, J. K., and Cunningham, A. A. (1994) Epidemiological observations on spongiform encephalopathies in captive wild animals in the British Isles. Vet. Rec. 135, 296-303
9. Ryder, S. J., Wells, G. A., Bradshaw, J. M., and Pearson, G. R. (2001) Inconsistent detection of PrP in extraneural tissues of cats with feline spongiform encephalopathy. Vet. Rec. 148, 437-441 (Pubitemid 33605914)
10. Piening, N., Nonno, R., Di Bari, M., Walter, S., Windl, O., Agrimi, U., Kretzschmar, H. A., and Bertsch, U. (2006) Conversion efficiency of bank vole prion protein in vitro is determined by residues 155 and 170, but does not correlate with the high susceptibility of bank voles to sheep scrapie in vivo. J. Biol. Chem. 281, 9373-9384 (Pubitemid 43864654)
11. Barron, R. M., Thomson, V., Jamieson, E., Melton, D. W., Ironside, J., Will, R., and Manson, J. C. (2001) Changing a single amino acid in the N-terminus of murine PrP alters TSE incubation time across three species barriers. EMBO J. 20, 5070-5078 (Pubitemid 32910903)
12. Priola, S. A., and Chesebro, B. (1995) A single hamster PrP amino acid blocks conversion to protease-resistant PrP in scrapieinfected mouse neuroblastoma cells. J. Virol. 69, 7754-7758
13. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wüthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature 382, 180-182 (Pubitemid 26242887)
14. Riek, R., Hornemann, S., Wider, G., Glockshuber, R., and Wüthrich, K. (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett. 413, 282-288 (Pubitemid 27353285)
15. Schatzl, H. M., Da Costa, M., Taylor, L., Cohen, F. E., and Prusiner, S. B. (1997) Prion protein gene variation among primates. J. Mol. Biol. 265, 257
16. Billeter, M., Riek, R., Wider, G., Hornemann, S., Glockshuber, R., and Wüthrich, K. (1997) Prion protein NMR structure and species barrier for prion diseases. Proc. Natl. Acad. Sci. U. S. A. 94, 7281-7285 (Pubitemid 27345306)
17. Christen, B., Perez, D. R., Hornemann, S., and Wüthrich, K. (2008) NMR structure of the bank vole prion protein at 20 °C contains a structured loop of residues 165-171. J. Mol. Biol. 383, 306-312
18. Gossert, A. D., Bonjour, S., Lysek, D. A., Fiorito, F., and Wüthrich, K. (2005) Prion protein NMR structures of elk and of mouse/elk hybrids. Proc. Natl. Acad. Sci. U. S. A. 102, 646-650 (Pubitemid 40282719)
19. 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-βspines reveal varied steric zippers. Nature 447, 453-457 (Pubitemid 46816731)
20. 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
21. 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
22. Kurt, T. D., Telling, G. T., Zabel, M. D., Hoover, E. A. (2009) Trans-species amplification of PrPCWD and correlation with rigid loop 170N. Virology 387, 235-243
23. Kurt, T. D., Seelig, D. M., Schneider, J. R., Johnson, C. J., Telling, G. C., Heisey, D. M., and Hoover, E. A. Alteration of the chronic wasting disease species barrier by in vitro prion amplification. J. Virol. 85, 8528-8537
24. Sigurdson, C. J., Nilsson, K. P., Hornemann, S., Manco, G., Fernandez-Borges, N., Schwarz, P., Castilla, J., Wüthrich, K., and Aguzzi, A. (2010) A molecular switch controls interspecies prion disease transmission in mice. J. Clin. Invest. 120, 2590-2599
25. Perez, D. R., Damberger, F. F., and Wüthrich, K. (2010) Horse prion protein NMR structure and comparisons with related variants of the mouse prion protein. J. Mol. Biol. 400, 121-128
26. Sigurdson, C. J., Joshi-Barr, S., Bett, C., Winson, O., Manco, G., Schwarz, P., Rulicke, T., Nilsson, K. P., Margalith, I., Raeber, A., Peretz, D., Hornemann, S., Wüthrich, K., and Aguzzi, A. (2011) Spongiform encephalopathy in transgenic mice expressing a point mutation in the β2-α2 loop of the prion protein. J. Neurosci. 31, 13840-13847
27. Sigurdson, C. J., Manco, G., Schwarz, P., Liberski, P., Hoover, E. A., Hornemann, S., Polymenidou, M., Miller, M. W., Glatzel, M., and Aguzzi, A. (2006) Strain fidelity of chronic wasting disease upon murine adaptation. J. Virol. 80, 12303-12311 (Pubitemid 44904380)
28. Wadsworth, J. D. F., Joiner, S., Hill, A. F., Campbell, T. A., Desbruslais, M., Luthert, P. J., Collinge, J. (2001) Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immuno-blotting assay. Lancet 358, 171-180 (Pubitemid 32718539)
29. Polymenidou, M., Moos, R., Scott, M., Sigurdson, C., Shi, Y. Z., Yajima, B., Hafner-Bratkovic, I., Jerala, R., Hornemann, S., Wüthrich, K., Bellon, A., Vey, M., Garen, G., James, M. N., Kav, N., and Aguzzi, A. (2008) The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS ONE 3, e3872
30. Lau, A. L., Yam, A. Y., Michelitsch, M. M., Wang, X., Gao, C., Goodson, R. J., Shimizu, R., Timoteo, G., Hall, J., Medina-Selby, A., Coit, D., McCoin, C., Phelps, B., Wu, P., Hu, C., Chien, D., and Peretz, D. (2007) Characterization of prion protein (PrP)- derived peptides that discriminate full-length PrPSc from PrPC. Proc. Natl. Acad. Sci. U. S. A. 104, 11551-11556 (Pubitemid 47175050)
31. Castilla, J., Saa, P., Morales, R., Abid, K., Maundrell, K., and Soto, C. (2006) Protein misfolding cyclic amplification for diagnosis and prion propagation studies. Methods Enzymol. 412, 3-21 (Pubitemid 44548570)
32. Saa, P., Castilla, J., and Soto, C. (2005) Cyclic amplification of protein misfolding and aggregation. Methods Mol. Biol. 299, 53-65
33. Castilla, J., Saa, P., Hetz, C., and Soto, C. (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206 (Pubitemid 40546388)
34. Ding, L., Jonforsen, M., Roman, L. S., Andersson, M. R., and Inganas, O. (2000) Photovoltaic cells with a conjugated polyelectrolyte. Synth. Met. 110, 133-140 (Pubitemid 30561124)
35. Ho, H.-A., Boissinot, M., Bergeron, M. G., Corbeil, G., Dore, K., Boudreau, D., and Leclerc, M. (2002) Colorimetric and fluorometric detection of nucleic acids using cationic polythiophene derivatives. Angew. Chem. Int. Ed. Engl. 41, 1548-1551 (Pubitemid 34534396)
36. Peretz, D., Williamson, R. A., Legname, G., Matsunaga, Y., Vergara, J., Burton, D. R., DeArmond, S. J., Prusiner, S. B., and Scott, M. R. (2002) A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34, 921-932 (Pubitemid 34722282)
37. Castilla, J., Morales, R., Saa, P., Barria, M., Gambetti, P., and Soto, C. (2008) Cell-free propagation of prion strains. EMBO J. 27, 2557-2566
38. Castilla, J., Gonzalez-Romero, D., Saa, P., Morales, R., De Castro, J., and Soto, C. (2008) Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions. Cell 134, 757-768
39. Green, K. M., Castilla, J., Seward, T. S., Napier, D. L., Jewell, J. E., Soto, C., and Telling, G. C. (2008) Accelerated high fidelity prion amplification within and across prion species barriers. PLoS Pathog. 4, e1000139
40. Qi, Y., Wang, J. K., McMillian, M., and Chikaraishi, D. M. (1997) Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J. Neurosci. 17, 1217-1225 (Pubitemid 27073725)
41. Sigurdson, C. J., Nilsson, K. P., Hornemann, S., Manco, G., Polymenidou, M., Schwarz, P., Leclerc, M., Hammarstrom, P., Wüthrich, K., and Aguzzi, A. (2007) Prion strain discrimination using luminescent conjugated polymers. Nat. Methods 4, 1023-1030 (Pubitemid 350201774)
42. Scott, M., Groth, D., Foster, D., Torchia, M., Yang, S. L., DeArmond, S. J., and Prusiner, S. B. (1993) Propagation of prions with artificial properties in transgenic mice expressing chimeric PrP genes. Cell 73, 979-988 (Pubitemid 23165612)
43. Kocisko, D. A., Priola, S. A., Raymond, G. J., Chesebro, B., Lansbury, P. T., Jr., and Caughey, B. (1995) Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc. Natl. Acad. Sci. U. S. A. 92, 3923-3927
44. Scott, M. R., Safar, J., Telling, G., Nguyen, O., Groth, D., Torchia, M., Koehler, R., Tremblay, P., Walther, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (1997) Identification of a prion protein epitope modulating transmission of bovine spongiform encephalopathy prions to transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 94, 14279-14284 (Pubitemid 28041364)
45. Vorberg, I., Groschup, M. H., Pfaff, E., and Priola, S. A. (2003) Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J. Virol. 77, 2003-2009 (Pubitemid 36110012)
46. Bruce, K. L., and Chernoff, Y. O. (2011) Sequence specificity and fidelity of prion transmission in yeast. Semin. Cell Dev. Biol. 22, 444-451
47. Chang, H. Y., Lin, J. Y., Lee, H. C., Wang, H. L., and King, C. Y. (2008) Strain-specific sequences required for yeast [PSI ] prion propagation. Proc. Natl. Acad. Sci. U. S. A. 105, 13345-13350
48. Tessier, P. M., and Lindquist, S. (2007) Prion recognition elements govern nucleation, strain specificity and species barriers. Nature 447, 556-561 (Pubitemid 46868043)
49. Chien, P., DePace, A. H., Collins, S. R., and Weissman, J. S. (2003) Generation of prion transmission barriers by mutational control of amyloid conformations. Nature 424, 948-951 (Pubitemid 37051686)
50. Verges, K. J., Smith, M. H., Toyama, B. H., and Weissman, J. S. (2011) Strain conformation, primary structure and the propagation of the yeast prion [PSI ]. Nat. Struct. Mol. Biol. 18, 493-499
51. Prusiner, S. B., Scott, M., Foster, D., Pan, K. M., Groth, D., Mirenda, C., Torchia, M., Yang, S. L., Serban, D., Carlson, G. A., Hoppe, P.C., Westaway, D., and DeArmond, S. J. (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63, 673-686 (Pubitemid 120035041)
52. Collinge, J., and Clarke, A. R. (2007) A general model of prion strains and their pathogenicity. Science 318, 930-936 (Pubitemid 350098981)
53. Bett, C., Joshi-Barr, S., Lucero, M., Trejo, M., Liberski, P., Kelly, J. W., Masliah, E., and Sigurdson, C. J. (2012) Biochemical properties of highly neuroinvasive prion strains. PLoS Pathog. 8, e1002522