Prion protein biology

Cell

Volumn 93, Issue 3, 1998, Pages 337-348

  Prusiner, Stanley B ^a   Scott, Michael R ^a   DeArmond, Stephen J ^a   Cohen, Fred E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

BOVINE SPONGIFORM ENCEPHALOPATHY; CREUTZFELDT JAKOB DISEASE; GENE DOSAGE; GENE OVEREXPRESSION; MOLECULAR GENETICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SPECIES DIFFERENCE; TRANSGENE; VIRUS MUTATION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSMISSION;

BOVINAE;

EID: 0032076463     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81163-0     Document Type: Review

References (96)

1. Alper, T., Cramp, W.A., Haig, D.A., and Clarke, M.C. (1967). Does the agent of scrapie replicate without nucleic acid? Nature 214, 764-766.
2. Anfinsen, C.B. (1973). Principles that govern the folding of protein chains. Science 181, 223-230.
3. Basler, K., Oesch, B., Scott, M., Westaway, D., Wälchli, M., Groth, D.F., McKinley, M.P., Prusiner, S.B., and Weissmann, C. (1986). Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 46, 417-428.
4. Bellinger-Kawahara, C.G., Kempner, E., Groth, D.F., Gabizon, R., and Prusiner, S.B. (1988). Scrapie prion liposomes and rods exhibit target sizes of 55,000 Da. Virology 164, 537-541.
5. Bessen, R.A., and Marsh, R.F. (1994). Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J. Virol. 68, 7859-7868.
6. Borchelt, D.R., Scott, M., Taraboulos, A., Stahl, N., and Prusiner, S.B. (1990). Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells. J. Cell Biol. 110, 743-752.
7. Bruce, M.E., McBride, P.A., and Farquhar, C.F. (1989). Precise targeting of the pathology of the sialoglycoprotein, PrP, and vacuolar degeneration in mouse scrapie. Neurosci. Lett. 102, 1-6.
8. Büeler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H.-P., DeArmond, S.J., Prusiner, S.B., Aguet, M., and Weissmann, C. (1992). Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582.
9. Büeler, H., Aguzzi, A., Sailer, A., Greiner, R.-A., Autenried, P., Aguet, M., and Weissmann, C. (1993). Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
10. Sc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol. Med. 1, 19-30.
11. Carlson, G.A., Kingsbury, D.T., Goodman, P.A., Coleman, S., Marshall, S.T., DeArmond, S.J., Westaway, D., and Prusiner, S.B. (1986). Linkage of prion protein and scrapie incubation time genes. Cell 46, 503-511.
12. Carlson, G.A., Ebeling, C., Yang, S.-L., Telling, G., Torchia, M., Groth, D., Westaway, D., DeArmond, S.J., and Prusiner, S.B. (1994). Prion isolate specified allotypic interactions between the cellular and scrapie prion proteins in congenic and transgenic mice. Proc. Natl. Acad. Sci. USA 91, 5690-5694.
13. Carp, R.I., Meeker, H., and Sersen, E. (1997). Scrapie strains retain their distinctive characteristics following passages of homogenates from different brain regions and spleen. J. Gen. Virol. 78, 283-290.
14. Caughey, B., and Raymond, G.J. (1991). The scrapie-associated form of PrP is made from a cell surface precursor that is both protease-and phospholipase-sensitive. J. Biol. Chem. 266, 18217-18223.
15. Caughey, B., Kocisko, D.A., Raymond, G.J., and Lansbury, P.T., Jr. (1995). Aggregates of scrapie-associated prion protein induce the cell-free conversion of protease-sensitive prion protein to the protease-resistant state. Chem. Biol. 2, 807-817.
16. Chernoff, Y.O., Lindquist, S.L., Ono, B., Inge-Vechtomov, S.G., and Liebman, S.W. (1995). Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268, 880-884.
17. Chesebro, B. (1998). Prion diseases: BSE and prions: uncertainties about the agent. Science 279, 42-43.
18. Chesebro, B., and Caughey, B. (1993). Scrapie agent replication without the prion protein? Curr. Biol. 3, 696-698.
19. Chesebro, B., Race, R., Wehrly, K., Nishio, J., Bloom, M., Lechner, D., Bergstrom, S., Robbins, K., Mayer, L., Keith, J.M., et al. (1985). Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain. Nature 315, 331-333.
20. Cohen, F.E., Pan, K.-M., Huang, Z., Baldwin, M., Fletterick, R.J., and Prusiner, S.B. (1994). Structural clues to prion replication. Science 264, 530-531.
21. Collinge, J., Whittington, M.A., Sidle, K.C., Smith, C.J., Palmer, M.S., Clarke, A.R., and Jefferys, J.G.R. (1994). Prion protein is necessary for normal synaptic function. Nature 370, 295-297.
22. Collinge, J., Sidle, K.C.L., 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.
23. Coustou, V., Deleu, C., Saupe, S., and Begueret, J. (1997). The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc. Natl. Acad. Sci. USA 94, 9773-9778.
24. DeArmond, S.J., Mobley, W.C., DeMott, D.L., Barry, R.A., Beckstead, J.H., and Prusiner, S.B. (1987). Changes in the localization of brain prion proteins during scrapie infection. Neurology 37, 1271-1280.
25. DeArmond, S.J., Sánchez, H., Yehiely, F., Qiu, Y., Ninchak-Casey, A., Daggett, V., Camerino, A.P., Cayetano, J., Rogers, M., Groth, D., Torchia, M., Tremblay, P., Scott, M.R., Cohen, F.E., and Prusiner, S.B. (1997). Selective neuronal targeting in prion disease. Neuron 19, 1337-1348.
26. Derkatch, I.L., Chernoff, Y.O., Kushnirov, V.V., Inge-Vechtomov, S.G., and Liebman, S.W. (1996). Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144, 1375-1386.
27. Dickinson, A.G., Meikle, V.M. H., and Fraser, H. (1968). Identification of a gene which controls the incubation period of some strains of scrapie agent in mice. J. Comp. Pathol. 78, 293-299.
28. Donne, D.G., Viles, J.H., Groth, D., Mehlhorn, I., James, T.L., Cohen, F.E., Prusiner, S.B., Wright, P.E., and Dyson, H.J. (1997). Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc. Natl. Acad. Sci. USA 94, 13452-13457.
29. Frankel, J. (1990). Positional order and cellular handedness. J. Cell Sci. 97, 205-211.
30. Fraser, H., and Dickinson, A.G. (1968). The sequential development of the brain lesions of scrapie in three strains of mice. J. Comp. Pathol. 78, 301-311.
31. Gabizon, R., McKinley, M.P., Groth, D.F., and Prusiner, S.B. (1988). Immunoaffinity purification and neutralization of scrapie prion infectivity. Proc. Natl. Acad. Sci. USA 85, 6617-6621.
32. Gabizon, R., Telling, G., Meiner, Z., Halimi, M., Kahana, I., and Prusiner, S.B. (1996). Insoluble wild-type and protease-resistant mutant prion protein in brains of patients with inherited prion disease. Nat. Med. 2, 59-64.
33. Gajdusek, D.C. (1988). Transmissible and non-transmissible amyloidoses: autocatalytic post-translational conversion of host precursor proteins to β-pleated sheet configurations. J. Neuroimmunol. 20, 95-110.
34. Gibbs, C.J., Jr., Gajdusek, D.C., Asher, D.M., Alpers, M.P., Beck, E., Daniel, P.M., and Matthews, W.B. (1968). Creutzfeldt-Jakob disease (spongiform encephalopathy): transmission to the chimpanzee. Science 161, 388-389.
35. Gorodinsky, A., and Harris, D.A. (1995). Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129, 619-627.
36. Griffith, J.S. (1967). Self-replication and scrapie. Nature 215, 1043-1044.
37. Hegde, R.S., Mastrianni, J.A., Scott, M.R., DeFea, K.A., Tremblay, P., Torchia, M., DeArmond, S.J., Prusiner, S.B., and Lingappa, V.R. (1998). A transmembrane form of the prion protein in neurodegenerative disease. Science 279, 827-834.
38. Hsiao, K., Baker, H.F., Crow, T.J., Poulter, M., Owen, F., Terwilliger, J.D., Westaway, D., Ott, J., and Prusiner, S.B. (1989). Linkage of a prion protein missense variant to Gerstmann-Sträussler syndrome. Nature 338, 342-345.
39. Huang, Z., Gabriel, J.-M., Baldwin, M.A., Fletterick, R.J., Prusiner, S.B., and Cohen, F.E. (1994). Proposed three-dimensional structure for the cellular prion protein. Proc. Natl. Acad. Sci. USA 91, 7139-7143.
40. Huang, Z., Prusiner, S.B., and Cohen, F.E. (1996). Scrapie prions: a three-dimensional model of an infectious fragment. Fold. Des. 1, 13-19.
41. Hunter, N., Goldmann, W., Benson, G., Foster, J.D., and Hope, J. (1993). Swaledale sheep affected by natural scrapie differ significantly in PrP genotype frequencies from healthy sheep and those selected for reduced incidence of scrapie. J. Gen. Virol. 74, 1025-1031.
42. 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. USA 94, 10086-10091.
43. Kaneko, K., Wille, H., Mehlhorn, I., Zhang, H., Ball, H., Cohen, F.E., Baldwin, M.A., and Prusiner, S.B. (1997a). Molecular properties of complexes formed between the prion protein and synthetic peptides. J. Mol. Biol. 270, 574-586.
44. Kaneko, K., Zulianello, L., Scott, M., Cooper, C.M., Wallace, A.C., James, T.L., Cohen, F.E., and Prusiner, S.B. (1997b). 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.
45. Kascsak, R.J., Rubenstein, R., Merz, P.A., Tonna-DeMasi, M., Fersko, R., Carp, R.I., Wisniewski, H.M., and Diringer, H. (1987). Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol. 61, 3688-3693.
46. Kenward, N., Hope, J., Landon, M., and Mayer, R.J. (1994). Expression of polyubiquitin and heat-shock protein 70 genes increases in the later stages of disease progression in scrapie-infected mouse brain. J. Neurochem. 62, 1870-1877.
47. Kocisko, D.A., Come, J.H., Priola, S.A., Chesebro, B., Raymond, G.J., Lansbury, P.T., Jr., and Caughey, B. (1994).Cell-free formation of protease-resistant prion protein. Nature 370, 471-474.
48. Sc)-specific epitope defined by a monoclonal antibody. Nature 389, 74-77.
49. Kurschner, C., and Morgan, J.I. (1996). Analysis of interaction sites in homo-and heteromeric complexes containing Bcl-2 family members and the cellular prion protein. Mol. Brain Res. 37, 249-258.
50. Landman, O.E. (1991). The inheritance of acquired characteristics. Annu. Rev. Genetics 25, 1-20.
51. Lasmézas, C.I., Deslys, J.-P., Robain, O., Jaegly, A., Beringue, V., Peyrin, J.-M., Fournier, J.-G., Hauw, J.-J., Rossier, J., and Dormont, D. (1997). Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275, 402-405.
52. Lehmann, S., and Harris, D.A. (1996). Two mutant prion proteins expressed in cultured cells acquire biochemical properties reminiscent of the scrapie isoform. Proc. Natl. Acad. Sci. USA 93, 5610-5614.
53. Lledo, P.-M., Tremblay, P., DeArmond, S.J., Prusiner, S.B., and Nicoll, R.A. (1996). Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc. Natl. Acad. Sci. USA 93, 2403-2407.
54. Manson, J.C., Clarke, A.R., Hooper, M.L., Aitchison, L., McConnell, I., and Hope, J. (1994). 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8, 121-127.
55. Manuelidis, L., and Fritch, W. (1996). Infectivity and host responses in Creutzfeldt-Jakob disease. Virology 216, 46-59.
56. Masters, C.L., and Richardson, E.P., Jr. (1978).Subacute spongiform encephalopathy Creutzfeldt-Jakob disease - the nature and progression of spongiform change. Brain 101, 333-344.
57. Mastrianni, J., Nixon, F., Layzer, R., DeArmond, S.J., and Prusiner, S.B. (1997). Fatal sporadic insomnia: fatal familial insomnia phenotype without a mutation of the prion protein gene. Neurology [Suppl.] 48, A296.
58. Meggendorfer, F. (1930). Klinische und genealogische Beobachtungen bei einem Fall von spastischer Pseudosklerose Jakobs. Z. Gesamte Neurol. Psychiatr. 128, 337-341.
59. Monari, L., Chen, S.G., Brown, P., Parchi, P., Petersen, R.B., Mikol, J., Gray, F., Cortelli, P., Montagna, P., Ghetti, B., et al. (1994). Fatal familial insomnia and familial Creutzfeldt-Jakob disease: different prion proteins determined by a DNA polymorphism. Proc. Natl. Acad. Sci. USA 91, 2839-2842.
60. Moore, R.C., Hope, J., McBride, P.A., McConnell, I., Selfridge, J., Melton, D.W., and Manson, J.C. (1998). Mice with gene targetted prion protein alterations show that Prn-p, Sinc and Prni are congruent. Nat. Genet. 18, 118-125.
61. Muramoto, T., Scott, M., Cohen, F., and Prusiner, S.B. (1996). Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc. Natl. Acad. Sci. USA 93, 15457-15462.
62. Oesch, B., Westaway, D., Wälchli, M., McKinley, M.P., Kent, S.B.H., Aebersold, R., Barry, R.A., Tempst, P., Teplow, D.B., Hood, L.E., et al. (1985). A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735-746.
63. Oesch, B., Teplow, D.B., Stahl, N., Serban, D., Hood, L.E., and Prusiner, S.B. (1990). Identification of cellular proteins binding to the scrapie prion protein. Biochemistry 29, 5848-5855.
64. Pan, K.-M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R.J., Cohen, F.E., and Prusiner, S.B. (1993). Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90, 10962-10966.
65. Parry, H.B. (1962). Scrapie: a transmissible and hereditary disease of sheep. Heredity 17, 75-105.
66. Paushkin, S.V., Kushnirov, V.V., Smirnov, V.N., and Ter-Avanesyan, M.D. (1997). In vitro propagation of the prion-like state of yeast Sup35 protein. Science 277, 381-383.
67. Peretz, D., Williamson, R.A., Matsunaga, Y., Serban, H., Pinilla, C., Bastidas, R., Rozenshteyn, R., James, T.L., Houghten, R.A., Cohen, F.E., et al. (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.
68. Prusiner, S.B. (1982). Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144.
69. Prusiner, S.B. (1991). Molecular biology of prion diseases. Science 252, 1515-1522.
70. Prusiner, S.B. (1997). Prion diseases and the BSE crisis. Science 278, 245-251.
71. Prusiner, S.B. (1998). Prions. Les Prix Nobel, in press.
72. Prusiner, S.B., Scott, M., Foster, D., Pan, K.-M., Groth, D., Mirenda, C., Torchia, M., Yang, S.-L., Serban, D., Carlson, G.A., et al. (1990). Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63, 673-686.
73. Prusiner, S.B., Groth, D., Serban, A., Koehler, R., Foster, D., Torchia, M., Burton, D., Yang, S.-L., and DeArmond, S.J. (1993). Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proc. Natl. Acad. Sci. USA 90, 10608-10612.
74. Rieger, R., Edenhofer, F., Lasmézas, C.I., and Weiss, S. (1997). The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat. Med. 3, 1383-1388.
75. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R., and Wüthrich, K. (1996). NMR structure of the mouse prion protein domain PrP(121-231). Nature 382, 180-182.
76. Roos, R., Gajdusek, D.C., and Gibbs, C.J., Jr. (1973). The clinical characteristics of transmissible Creutzfeldt-Jakob disease. Brain 96, 1-20.
77. Sailer, A., Büeler, H., Fischer, M., Aguzzi, A., and Weissmann, C. (1994). No propagation of prions in mice devoid of PrP. Cell 77, 967-968.
78. Sakaguchi, S., Katamine, S., Nishida, N., Moriuchi, R., Shigematsu, K., Sugimoto, T., Nakatani, A., Kataoka, Y., Houtani, T., Shirabe, S., et al. (1996). Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380, 528-531.
79. Scott, M., Foster, D., Mirenda, C., Serban, D., Coufal, F., Wälchli, M., Torchia, M., Groth, D., Carlson, G., DeArmond, S.J., et al. (1989). Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59, 847-857.
80. Scott, M.R., Groth, D., Tatzelt, J., Torchia, M., Tremblay, P., DeArmond, S.J., and Prusiner, S.B. (1997). Propagation of prion strains through specific conformers of the prion protein. J. Virol. 71, 9032-9044.
81. Shibuya, S., Higuchi, J., Shin, R.-W., Tateishi, J., and Kitamoto, T. (1998). Protective prion protein polymorphisms against sporadic Creutzfeldt-Jakob disease. Lancet 351, 419.
82. Shinde, U.P., Liu, J.J., and Inouye, M. (1997). Protein memory through altered folding mediated by intramolecular chaperones. Nature 389, 520-522.
83. Somerville, R.A., Chong, A., Mulqueen, O.U., Birkett, C.R., Wood, S.C.E.R., and Hope, J. (1997). Biochemical typing of scrapie strains. Nature 386, 564.
84. Stahl, N., Borchelt, D.R., Hsiao, K., and Prusiner, S.B. (1987). Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240.
85. Stahl, N., Baldwin, M.A., Teplow, D.B., Hood, L., Gibson, B.W., Burlingame, A.L., and Prusiner, S.B. (1993). Structural analysis of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991-2002.
86. Taraboulos, A., Jendroska, K., Serban, D., Yang, S.-L., DeArmond, S.J., and Prusiner, S.B. (1992). Regional mapping of prion proteins in brains. Proc. Natl. Acad. Sci. USA 89, 7620-7624.
87. Taraboulos, A., Scott, M., Semenov, A., Avrahami, D., Laszlo, L., and Prusiner, S.B. (1995). Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibits formation of the scrapie isoform. J. Cell Biol. 129, 121-132.
88. Tatzelt, J., Zuo, J., Voellmy, R., Scott, M., Hartl, U., Prusiner, S.B., and Welch, W.J. (1995). Scrapie prions selectively modify the stress response in neuroblastoma cells. Proc. Natl. Acad. Sci. USA 92, 2944-2948.
89. Telling, G.C., Scott, M., Hsiao, K.K., Foster, D., Yang, S.-L., Torchia, M., Sidle, K.C.L., Collinge, J., DeArmond, S.J., and Prusiner, S.B. (1994). Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc. Natl. Acad. Sci. USA 91, 9936-9940.
90. Telling, G.C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F.E., DeArmond, S.J., and 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.
91. Telling, G.C., Parchi, P., DeArmond, S.J., Cortelli, P., Montagna, P., Gabizon, R., Mastrianni, J., Lugaresi, E., Gambetti, P., and Prusiner, S.B. (1996). Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 274, 2079-2082.
92. Tobler, I., Gaus, S.E., Deboer, T., Achermann, P., Fischer, M., Rülicke, T., Moser, M., Oesch, B., McBride, P.A., and Manson, J.C. (1996). Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380, 639-642.
93. Wells, G.A.H., Scott, A.C., Johnson, C.T., Gunning, R.F., Hancock, R.D., Jeffrey, M., Dawson, M., and Bradley, R. (1987). A novel progressive spongiform encephalopathy in cattle. Vet. Rec. 121, 419-420.
94. Westaway, D., Zuliani, V., Cooper, C.M., Da Costa, M., Neuman, S., Jenny, A.L., Detwiler, L., and Prusiner, S.B. (1994). Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev. 8, 959-969.
95. Wickner, R.B. (1994). [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566-569.
96. Wickner, R.B. (1997). A new prion controls fungal cell fusion incompatibility. Proc. Natl. Acad. Sci. USA 94, 10012-10014.