Prion Protein Repeat Expansion Results in Increased Aggregation and Reveals Phenotypic Variability

REFERENCES

• Bagriantsev, S., and S. W. Liebman. 2004. Specificity of prion assembly in vivo. J. Biol. Chem. 279:51042–51048.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bessen, R. A., and R. F. Marsh. 1992. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J. Gen. Virol. 73(Pt. 2):329–334.
   PubMedGoogle Scholar
• Borchsenius, A. S., S. Muller, G. P. Newnam, S. G. Inge-Vechtomov, and Y. O. Chernoff. 2006. Prion variant maintained only at high levels of the Hsp104 disaggregase. Curr. Genet. 49:21–29.
   PubMed Web of Science ®Google Scholar
• Borchsenius, A. S., R. D. Wegrzyn, G. P. Newnam, S. G. Inge-Vechtomov, and Y. O. Chernoff. 2001. Yeast prion protein derivative defective in aggregate shearing and production of new ‘seeds’. EMBO J. 20:6683–6691.
   PubMed Web of Science ®Google Scholar
• Bousset, L., and R. Melki. 2002. Similar and divergent features in mammalian and yeast prions. Microbes Infect. 4:461–469.
   PubMedGoogle Scholar
• Brown, P., C. J. Gibbs, Jr., P. Rodgers-Johnson, D. M. Asher, M. P. Sulima, A. Bacote, L. G. Goldfarb, and D. C. Gajdusek. 1994. Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease. Ann. Neurol. 35:513–529.
   PubMed Web of Science ®Google Scholar
• Castilla, J., A. Gutierrez-Adan, A. Brun, B. Pintado, F. J. Salguero, B. Parra, F. D. Segundo, M. A. Ramirez, A. Rabano, M. J. Cano, and J. M. Torres. 2005. Transgenic mice expressing bovine PrP with a four extra repeat octapeptide insert mutation show a spontaneous, non-transmissible, neurodegenerative disease and an expedited course of BSE infection. FEBS Lett. 579:6237–6246.
   PubMedGoogle Scholar
• Chen, S. G., P. Parchi, P. Brown, S. Capellari, W. Zou, E. J. Cochran, C. L. Vnencak-Jones, J. Julien, C. Vital, J. Mikol, E. Lugaresi, L. Autilio-Gambetti, and P. Gambetti. 1997. Allelic origin of the abnormal prion protein isoform in familial prion diseases. Nat. Med. 3:1009–1015.
   PubMedGoogle Scholar
• Chernoff, Y. O., S. L. Lindquist, B. Ono, S. G. Inge-Vechtomov, and S. W. Liebman. 1995. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268:880–884.
   PubMed Web of Science ®Google Scholar
• Chernoff, Y. O., S. M. Uptain, and S. L. Lindquist. 2002. Analysis of prion factors in yeast. Methods Enzymol. 351:499–538.
   PubMed Web of Science ®Google Scholar
• Chiesa, R., B. Drisaldi, E. Quaglio, A. Migheli, P. Piccardo, B. Ghetti, and D. A. Harris. 2000. Accumulation of protease-resistant prion protein (PrP) and apoptosis of cerebellar granule cells in transgenic mice expressing a PrP insertional mutation. Proc. Natl. Acad. Sci. USA 97:5574–5579.
   PubMed Web of Science ®Google Scholar
• Chiesa, R., P. Piccardo, B. Ghetti, and D. A. Harris. 1998. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21:1339–1351.
   PubMed Web of Science ®Google Scholar
• Chiesa, R., P. Piccardo, E. Quaglio, B. Drisaldi, S. L. Si-Hoe, M. Takao, B. Ghetti, and D. A. Harris. 2003. Molecular distinction between pathogenic and infectious properties of the prion protein. J. Virol. 77:7611–7622.
   PubMed Web of Science ®Google Scholar
• Collinge, J. 2001. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24:519–550.
   PubMed Web of Science ®Google Scholar
• Croes, E. A., J. Theuns, J. J. Houwing-Duistermaat, B. Dermaut, K. Sleegers, G. Roks, M. Van den Broeck, B. van Harten, J. C. van Swieten, M. Cruts, C. Van Broeckhoven, and C. M. van Duijn. 2004. Octapeptide repeat insertions in the prion protein gene and early onset dementia. J. Neurol. Neurosurg. Psychiatry 75:1166–1170.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Derkatch, I. L., M. E. Bradley, J. Y. Hong, and S. W. Liebman. 2001. Prions affect the appearance of other prions: the story of [PIN+]. Cell 106:171–182.
   PubMed Web of Science ®Google Scholar
• Derkatch, I. L., M. E. Bradley, and S. W. Liebman. 1998. Overexpression of the SUP45 gene encoding a Sup35p-binding protein inhibits the induction of the de novo appearance of the [PSI+] prion. Proc. Natl. Acad. Sci. USA 95:2400–2405.
   PubMed Web of Science ®Google Scholar
• Derkatch, I. L., M. E. Bradley, S. V. Masse, S. P. Zadorsky, G. V. Polozkov, S. G. Inge-Vechtomov, and S. W. Liebman. 2000. Dependence and independence of [PSI+] and [PIN+]: a two-prion system in yeast? EMBO J. 19:1942–1952.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Guthrie, C., and G. Fink. 2004. Guide to yeast genetics and molecular and cell biology, vol. 194. Elsevier Academic Press, San Diego, CA.
   Google Scholar
• Hill, A. F., S. Joiner, J. A. Beck, T. A. Campbell, A. Dickinson, M. Poulter, J. D. Wadsworth, and J. Collinge. 2006. Distinct glycoform ratios of protease resistant prion protein associated with PRNP point mutations. Brain 129:676–685.
   PubMedGoogle Scholar
• King, A., L. Doey, M. Rossor, S. Mead, J. Collinge, and P. Lantos. 2003. Phenotypic variability in the brains of a family with a prion disease characterized by a 144-base pair insertion in the prion protein gene. Neuropathol. Appl. Neurobiol. 29:98–105.
   PubMed Web of Science ®Google Scholar
• King, C. Y., and R. Diaz-Avalos. 2004. Protein-only transmission of three yeast prion strains. Nature 428:319–323.
   PubMed Web of Science ®Google Scholar
• Kochneva-Pervukhova, N. V., M. B. Chechenova, I. A. Valouev, V. V. Kushnirov, V. N. Smirnov, and M. D. Ter-Avanesyan. 2001. [Psi+] prion generation in yeast: characterization of the ‘strain’ difference. Yeast 18:489–497.
   PubMed Web of Science ®Google Scholar
• Kovács, G. G., G. Trabattoni, J. A. Hainfellner, J. W. Ironside, R. S. Knight, and H. Budka. 2002. Mutations of the prion protein gene phenotypic spectrum. J. Neurol. 249:1567–1582.
   PubMed Web of Science ®Google Scholar
• Krishnan, R., and S. L. Lindquist. 2005. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435:765–772.
   PubMed Web of Science ®Google Scholar
• Kryndushkin, D. S., I. M. Alexandrov, M. D. Ter-Avanesyan, and V. V. Kushnirov. 2003. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J. Biol. Chem. 278:49636–49643.
   PubMed Web of Science ®Google Scholar
• Li, L., and S. Lindquist. 2000. Creating a protein-based element of inheritance. Science 287:661–664.
   PubMed Web of Science ®Google Scholar
• Liu, J. J., and S. Lindquist. 1999. Oligopeptide-repeat expansions modulate ‘protein-only’ inheritance in yeast. Nature 400:573–576.
   PubMed Web of Science ®Google Scholar
• Manogaran, A. L., K. T. Kirkland, and S. W. Liebman. 2006. An engineered nonsense URA3 allele provides a versatile system to detect the presence, absence and appearance of the [PSI+] prion in Saccharomyces cerevisiae. Yeast 23:141–147.
   PubMed Web of Science ®Google Scholar
• Millhauser, G. L. 2007. Copper and the prion protein: methods, structures, function, and disease. Annu. Rev. Phys. Chem. 58:299–320.
   PubMed Web of Science ®Google Scholar
• Moore, R. A., C. Herzog, J. Errett, D. A. Kocisko, K. M. Arnold, S. F. Hayes, and S. A. Priola. 2006. Octapeptide repeat insertions increase the rate of protease-resistant prion protein formation. Protein Sci. 15:609–619.
   PubMed Web of Science ®Google Scholar
• Mumberg, D., R. Muller, and M. Funk. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119–122.
   PubMed Web of Science ®Google Scholar
• Ness, F., P. Ferreira, B. S. Cox, and M. F. Tuite. 2002. Guanidine hydrochloride inhibits the generation of prion “seeds” but not prion protein aggregation in yeast. Mol. Cell. Biol. 22:5593–5605.
   PubMed Web of Science ®Google Scholar
• Osherovich, L. Z., and J. S. Weissman. 2001. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI+] prion. Cell 106:183–194.
   PubMed Web of Science ®Google Scholar
• Parham, S. N., C. G. Resende, and M. F. Tuite. 2001. Oligopeptide repeats in the yeast protein Sup35p stabilize intermolecular prion interactions. EMBO J. 20:2111–2119.
   PubMed Web of Science ®Google Scholar
• Patino, M. M., J. J. Liu, J. R. Glover, and S. Lindquist. 1996. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273:622–626.
   PubMed Web of Science ®Google Scholar
• Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. USA 95:13363–13383.
   PubMed Web of Science ®Google Scholar
• Rogers, M., F. Yehiely, M. Scott, and S. B. Prusiner. 1993. Conversion of truncated and elongated prion proteins into the scrapie isoform in cultured cells. Proc. Natl. Acad. Sci. USA 90:3182–3186.
   PubMed Web of Science ®Google Scholar
• Scheibel, T., and S. L. Lindquist. 2001. The role of conformational flexibility in prion propagation and maintenance for Sup35p. Nat. Struct. Biol. 8:958–962.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., P. Chien, K. Yonekura, and J. S. Weissman. 2005. Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 121:49–62.
   PubMed Web of Science ®Google Scholar
• Tateishi, J., T. Kitamoto, M. Z. Hoque, and H. Furukawa. 1996. Experimental transmission of Creutzfeldt-Jakob disease and related diseases to rodents. Neurology 46:532–537.
   PubMed Web of Science ®Google Scholar
• Ter-Avanesyan, M. D., A. R. Dagkesamanskaya, V. V. Kushnirov, and V. N. Smirnov. 1994. The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics 137:671–676.
   PubMed Web of Science ®Google Scholar
• True, H. L. 2006. The battle of the fold: chaperones take on prions. Trends Genet. 22:110–117.
   PubMed Web of Science ®Google Scholar
• Tuite, M. F., and B. S. Cox. 2003. Propagation of yeast prions. Nat. Rev. Mol. Cell Biol. 4:878–890.
   PubMed Web of Science ®Google Scholar
• Uptain, S. M., and S. Lindquist. 2002. Prions as protein-based genetic elements. Annu. Rev. Microbiol. 56:703–741.
   PubMed Web of Science ®Google Scholar
• Uptain, S. M., G. J. Sawicki, B. Caughey, and S. Lindquist. 2001. Strains of [PSI+] are distinguished by their efficiencies of prion-mediated conformational conversion. EMBO J. 20:6236–6245.
   PubMed Web of Science ®Google Scholar
• Viles, J. H., D. Donne, G. Kroon, S. B. Prusiner, F. E. Cohen, H. J. Dyson, and P. E. Wright. 2001. Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 40:2743–2753.
   PubMed Web of Science ®Google Scholar
• Wadsworth, J. D., A. F. Hill, J. A. Beck, and J. Collinge. 2003. Molecular and clinical classification of human prion disease. Br. Med. Bull. 66:241–254.
   PubMed Web of Science ®Google Scholar
• Yin, S., S. Yu, C. Li, P. Wong, B. Chang, F. Xiao, S. C. Kang, H. Yan, G. Xiao, J. Grassi, P. Tien, and M. S. Sy. 2006. Prion proteins with insertion mutations have altered N-terminal conformation and increased ligand binding activity and are more susceptible to oxidative attack. J. Biol. Chem. 281:10698–10705.
   PubMed Web of Science ®Google Scholar
• Zhouravleva, G., V. V. Alenin, S. Inge-Vechtomov, and Y. O. Chernoff. 2002. To stick or not to stick: prion domains from yeast to mammals. Recent Res. Dev. Mol. Cell. Biol. 3:185–218.
   Google Scholar