Prion strain-dependent differences in conversion of mutant prion proteins in cell culture

Journal of Virology

Volumn 80, Issue 16, 2006, Pages 7854-7862

  Atarashi, Ryuichiro ^a,b   Sim, Valerie L ^b   Nishida, Noriyuki ^a   Caughey, Byron ^b   Katamine, Shigeru ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLUTAMINE; HISTIDINE; LYSINE; MUTANT PROTEIN; PRION PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CODON; CONTROLLED STUDY; HUMAN; INFRARED SPECTROSCOPY; MOUSE; MUTATION; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SCRAPIE; VIRUS STRAIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES; CELLS, CULTURED; CODON; CRICETINAE; EPITOPES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PRIONS; PROTEIN CONFORMATION; PRPSC PROTEINS;

EID: 33746849285     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00424-06     Document Type: Article

References (59)

1. Alonso, D. O., S. J. DeArmond, F. E. Cohen, and V. Daggett. 2001. Mapping the early steps in the pH-induced conformational conversion of the prion protein. Proc. Natl. Acad. Sci. USA 98:2985-2989.
2. Arima, K., N. Nishida, S. Sakaguchi, K. Shigematsu, R. Atarashi, N. Yamaguchi, D. Yoshikawa, J. Yoon, K. Watanabe, N. Kobayashi, S. Mouillet-Richard, S. Lehmann, and S. Katamine. 2005. Biological and biochemical characteristics of prion strains conserved in persistently infected cell cultures. J. Virol. 79:7104-7112.
3. Atarashi, R., N. Nishida, K. Shigematsu, S. Goto, T. Kondo, S. Sakaguchi, and S. Katamine. 2003. Deletion of N-terminal residues 23-88 from prion protein (PrP) abrogates the potential to rescue PrP-deficient mice from PrP-like protein/Doppel-induced neurodegeneration. J. Biol. Chem. 278: 28944-28949.
4. Belt, P. B., I. H. Muileman, B. E. Schreuder, R. Bos-de Ruijter, A. L. Gielkens, and M. A. Smits. 1995. Identification of five allelic variants of the sheep PrP gene and their association with natural scrapie. J. Gen. Virol. 76:509-517.
5. Ben-Zaken, O., S. Tzaban, Y. Tal, L. Horonchik, J. D. Esko, I. Vlodavsky, and A. Taraboulos. 2003. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278:40041-40049.
6. Bessen, R. A., D. A. Kocisko, G. J. Raymond, S. Nandan, P. T. Lansbury, and B. Caughey. 1995. Non-genetic propagation of strain-specific properties of scrapie prion protein. Nature 375:698-700.
7. Bessen, R. A., and R. F. Marsh. 1992. Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J. Virol. 66:2096-2101.
8. Birkett, C. R., R. M. Hennion, D. A. Bembridge, M. C. Clarke, A. Chree, M. E. Bruce, and C. J. Bostock. 2001. Scrapie strains maintain biological phenotypes on propagation in a cell line in culture. EMBO J. 20:3351-3358.
9. Bruce, M. E. 1993. Scrapie strain variation and mutation. Br. Med. Bull. 49:822-838.
10. Bruce, M. E. 2003. TSE strain variation. Br. Med. Bull. 66:99-108.
11. Bruce, M. E., I. McConnell, H. Fraser, and A. G. Dickinson. 1991. The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J. Gen. Virol. 72:595-603.
12. Caughey, B., and G. J. Raymond. 1993. Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J. Virol. 67:643-650.
13. Caughey, B., G. J. Raymond, and R. A. Bessen. 1998. Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J. Biol. Chem. 273:32230-32235.
14. Caughey, B. W., A. Dong, K. S. Bhat, D. Ernst, S. F. Hayes, and W. S. Caughey. 1991. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30:7672-7680.
15. Chesebro, B. 2003. Introduction to the transmissible spongiform encephalopathies or prion diseases. Br. Med. Bull. 66:1-20.
16. Collinge, J., K. C. Sidle, J. Meads, J. Ironside, and A. F. Hill. 1996. Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 383:685-690.
17. Deleault, N. R., R. W. Lucassen, and S. Supattapone. 2003. RNA molecules stimulate prion protein conversion. Nature 425:717-720.
18. DePace, A. H., A. Santoso, P. Hillner, and J. S. Weissman. 1998. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93:1241-1252.
19. Derkatch, I. L., M. E. Bradley, P. Zhou, and S. W. Liebman. 1999. The PNM2 mutation in the prion protein domain of SUP35 has distinct effects on different variants of the [PSI+] prion in yeast. Curr. Genet. 35:59-67.
20. Derkatch, I. L., Y. O. Chernoff, V. V. Kushnirov, S. G. Inge-Vechtomov, and S. W. Liebman. 1996. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144:1375-1386.
21. Goldfarb, L. G., R. B. Petersen, M. Tabaton, P. Brown, A. C. LeBlanc, P. Montagna, P. Cortelli, J. Julien, C. Vital, W. W. Pendelbury, M. Haltia, P. R. Wills, J. J. Hauw, P. E. McKeever, L. Monari, B. Schrank, G. D. Swergold, L. Autilio-Gambetti, D. C. Gajdusek, E. Lugaresi, and P. Gambetti. 1992. Fatal familial insomnia and familial Creutzfeldt-Jakob disease: disease phenotype determined by a DNA polymorphism. Science 258:806-808.
22. Herrmann, L. M., and B. Caughey. 1998. The importance of the disulfide bond in prion protein conversion. Neuroreport 9:2457-2461.
23. Hill, A. F., M. Desbruslais, S. Joiner, K. C. Sidle, I. Gowland, J. Collinge, L. J. Doey, and P. Lantos. 1997. The same prion strain causes vCJD and BSE. Nature 389:448-450, 526.
24. Horiuchi, M., S. A. Priola, J. Chabry, and B. Caughey. 2000. Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers. Proc. Natl. Acad. Sci. USA 97:5836-5841.
25. Jones, E. M., and W. K. Surewicz. 2005. Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121:63-72.
26. Kaneko, K., L. Zulianello, M. Scott, C. M. Cooper, A. C. Wallace, T. L. James, F. E. Cohen, and S. B. Prusiner. 1997. Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. USA 94:10069-10074.
27. Kimberlin, R. H. 1982. Scrapie agent: prions or virions? Nature 297:107-108.
28. Kimberlin, R. H., S. Cole, and C. A. Walker. 1987. Temporary and permanent modifications to a single strain of mouse scrapie on transmission to rats and hamsters. J. Gen. Virol. 68:1875-1881.
29. Kimberlin, R. H., C. A. Walker, and H. Fraser. 1989. The genomic identity of different strains of mouse scrapie is expressed in hamsters and preserved on reisolation in mice. J. Gen. Virol. 70:2017-2025.
30. King, C. Y. 2001. Supporting the structural basis of prion strains: induction and identification of [PSI] variants. J. Mol. Biol. 307:1247-1260.
31. King, C. Y., and R. Diaz-Avalos. 2004. Protein-only transmission of three yeast prion strains. Nature 428:319-323.
32. Korth, C., K. Kaneko, D. Groth, N. Heye, G. Telling, J. Mastrianni, P. Parchi, P. Gambetti, R. Will, J. Ironside, C. Heinrich, P. Tremblay, S. J. DeArmond, and S. B. Prusiner. 2003. Abbreviated incubation times for human prions in mice expressing a chimeric mouse-human prion protein transgene. Proc. Natl. Acad. Sci. USA 100:4784-4789.
33. Leucht, C., S. Simoneau, C. Rey, K. Vana, R. Rieger, C. I. Lasmezas, and S. Weiss. 2003. The 37 kDa/67 kDa laminin receptor is required for PrP(Sc) propagation in scrapie-infected neuronal cells. EMBO Rep. 4:290-295.
34. Manuelidis, L. 2003. Transmissible encephalopathies: speculations and realities. Viral Immunol. 16:123-139.
35. Meyer, R. K., M. P. McKinley, K. A. Bowman, M. B. Braunfeld, R. A. Barry, and S. B. Prusiner. 1986. Separation and properties of cellular and scrapie prion proteins. Proc. Natl. Acad. Sci. USA 83:2310-2314.
36. Muramoto, T., M. Scott, F. E. Cohen, and S. B. Prusiner. 1996. Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc. Natl. Acad. Sci. USA 93:15457-15462.
37. Nishida, N., D. A. Harris, D. Vilette, H. Laude, Y. Frobert, J. Grassi, D. Casanova, O. Milhavet, and S. Lehmann. 2000. Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J. Virol. 74:320-325.
38. Pan, K. M., M. Baldwin, J. Nguyen, M. Gasset, A. Serban, D. Groth, I. Mehlhorn, Z. Huang, R. J. Fletterick, F. E. Cohen, and S. B. Prusiner. 1993. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90:10962-10966.
39. Peretz, D., M. R. Scott, D. Groth, R. A. Williamson, D. R. Burton, F. E. Cohen, and S. B. Prusiner. 2001. Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci. 10:854-863.
40. Peretz, D., R. A. Williamson, Y. Matsunaga, H. Serban, C. Pinilla, R. B. Bastidas, R. Rozenshteyn, T. L. James, R. A. Houghten, F. E. Cohen, S. B. Prusiner, and D. R. Burton. 1997. A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J. Mol. Biol. 273:614-622.
41. Prusiner, S. B., M. R. Scott, S. J. DeArmond, and F. E. Cohen. 1998. Prion protein biology. Cell 93:337-348.
42. Riek, R., S. Hornemann, G. Wider, M. Billeter, R. Glockshuber, and K. Wuthrich. 1996. NMR structure of the mouse prion protein domain PrP(121-321). Nature 382:180-182.
43. Riek, R., G. Wider, M. Billeter, S. Hornemann, R. Glockshuber, and K. Wuthrich. 1998. Prion protein NMR structure and familial human spongiform encephalopathies. Proc. Natl. Acad. Sci. USA 95:11667-11672.
44. Safar, J., H. Wille, V. Itri, D. Groth, H. Serban, M. Torchia, F. E. Cohen, and S. B. Prusiner. 1998. Eight prion strains have PrP(Sc) molecules with different conformations. Nat. Med. 4:1157-1165.
45. Scott, M., D. Foster, C. Mirenda, D. Serban, F. Coufal, M. Walchli, M. Torchia, D. Groth, G. Carlson, S. J. DeArmond, D. Westaway, and S. B. Prusiner. 1989. Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59:847-857.
46. Shaked, G. M., Z. Meiner, I. Avraham, A. Taraboulos, and R. Gabizon. 2001. Reconstitution of prion infectivity from solubilized protease-resistant PrP and nonprotein components of prion rods. J. Biol. Chem. 276:14324-14328.
47. Shibuya, S., J. Higuchi, R. W. Shin, J. Tateishi, and T. Kitamoto. 1998. Codon 219 Lys allele of PRNP is not found in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 43:826-828.
48. Snow, A. D., R. Kisilevsky, J. Willmer, S. B. Prusiner, and S. J. DeArmond. 1989. Sulfated glycosaminoglycans in amyloid plaques of prion diseases. Acta Neuropathol. (Berlin) 77:337-342.
49. Tanaka, M., P. Chien, N. Naber, R. Cooke, and J. S. Weissman. 2004. Conformational variations in an infectious protein determine prion strain differences. Nature 428:323-328.
50. Telling, G. C., P. Parchi, S. J. DeArmond, P. Cortelli, P. Montagna, R. Gabizon, J. Mastrianni, E. Lugaresi, P. Gambetti, and S. B. Prusiner. 1996. Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 274:2079-2082.
51. Telling, G. C., M. Scott, J. Mastrianni, R. Gabizon, M. Torchia, F. E. Cohen, S. J. DeArmond, and S. B. Prusiner. 1995. Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83:79-90.
52. Thomzig, A., S. Spassov, M. Friedrich, D. Naumann, and M. Beekes. 2004. Discriminating scrapie and bovine spongiform encephalopathy isolates by infrared spectroscopy of pathological prion protein. J. Biol. Chem. 279:33847-33854.
53. Uptain, S. M., and S. Lindquist. 2002. Prions as protein-based genetic elements. Annu. Rev. Microbiol. 56:703-741.
54. Vorberg, I., A. Buschmann, S. Harmeyer, A. Saalmuller, E. Pfaff, and M. H. Groschup. 1999. A novel epitope for the specific detection of exogenous prion proteins in transgenic mice and transfected murine cell lines. Virology 255:26-31.
55. Vorberg, I., M. H. Groschup, E. Pfaff, and S. A. Priola. 2003. Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J. Virol. 77:2003-2009.
56. Weissmann, C. 2004. The state of the prion. Nat. Rev. Microbiol. 2:861-871.
57. Westaway, D., V. Zuliani, C. M. Cooper, M. Da Costa, S. Neuman, A. L. Jenny, L. Detwiler, and S. B. Prusiner. 1994. Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev. 8:959-969.
58. Wickner, R. B., H. K. Edskes, B. T. Roberts, U. Baxa, M. M. Pierce, E. D. Ross, and A. Brachmann. 2004. Prions: proteins as genes and infectious entities. Genes Dev. 18:470-485.
59. Wong, C., L. W. Xiong, M. Horiuchi, L. Raymond, K. Wehrly, B. Chesebro, and B. Caughey. 2001. Sulfated glycans and elevated temperature stimulate PrP(Sc)-dependent cell-free formation of protease-resistant prion protein. EMBO J. 20:377-386.