Impaired transport of intrinsically disordered proteins through the Sec61 and SecY translocon; implications for prion diseases

References

• Haraguchi T, Fisher S, Olofsson S, et al. Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Arch Biochem Biophys. 1989;274:1–13. doi:10.1016/0003-9861(89)90409-8
   PubMed Web of Science ®Google Scholar
• Stahl N, Borchelt DR, Hsiao K, et al. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell. 1987;51:229–40. doi:10.1016/0092-8674(87)90150-4
   PubMed Web of Science ®Google Scholar
• Yost CS, Lopez CD, Prusiner SB, et al. Non-hydrophobic extracytoplasmic determinant of stop transfer in the prion protein. Nature. 1990;343:669–72. doi:10.1038/343669a0
   PubMed Web of Science ®Google Scholar
• Hegde RS, Mastrianni JA, Scott MR, et al. A transmembrane form of the prion protein in neurodegenerative disease. Science. 1998;279:827–34. doi:10.1126/science.279.5352.827
   PubMed Web of Science ®Google Scholar
• Ma J, Wollmann R, Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science. 2002;298:1781–5. doi:10.1126/science.1073725
   PubMed Web of Science ®Google Scholar
• Rambold AS, Miesbauer M, Rapaport D, et al. Association of Bcl-2 with misfolded prion protein is linked to the toxic potential of cytosolic PrP. Mol Biol Cell. 2006;17:3356–68. doi:10.1091/mbc.E06-01-0083
   PubMed Web of Science ®Google Scholar
• Winklhofer KF, Tatzelt J, Haass C. The two faces of protein misfolding: Gain and loss of function in neurodegenerative diseases. EMBO J. 2008;27:336–49. doi:10.1038/sj.emboj.7601930
   PubMed Web of Science ®Google Scholar
• Rambold AS, Miesbauer M, Rapaport D, et al. Association of Bcl-2 with misfolded prion protein is linked to the toxic potential of cytosolic PrP. Mol Biol Cell. 2006;17:3356–68. doi:10.1091/mbc.E06-01-0083
   PubMed Web of Science ®Google Scholar
• Chakrabarti O, Hegde RS. Functional depletion of mahogunin by cytosolically exposed prion protein contributes to neurodegeneration. Cell. 2009;137:1136–47. doi:10.1016/j.cell.2009.03.042
   PubMed Web of Science ®Google Scholar
• Kristiansen M, Deriziotis P, Dimcheff DE, et al. Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol Cell. 2007;26:175–88. doi:10.1016/j.molcel.2007.04.001
   PubMed Web of Science ®Google Scholar
• Mironov AJ, Latawiec D, Wille H, et al. Cytosolic prion protein in neurons. J Neurosci. 2003;23:7183–93.
   PubMed Web of Science ®Google Scholar
• Donne DG, Viles JH, Groth D, et al. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc Natl Acad Sci USA. 1997;94:13452–57. doi:10.1073/pnas.94.25.13452
   PubMed Web of Science ®Google Scholar
• Riek R, Hornemann S, Wider G, et al. NMR structure of the mouse prion protein domain PrP(121-321). Nature. 1996;382:180–2. doi:10.1038/382180a0.
   PubMed Web of Science ®Google Scholar
• Riek R, Hornemann S, Wider G, et al. NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett. 1997;413:282–8. doi:10.1016/S0014-5793(97)00920-4
   PubMed Web of Science ®Google Scholar
• Zanusso G, Petersen RB, Jin T, et al. Proteasomal degradation and N-terminal protease resistance of the codon 145 mutant prion protein. J Biol Chem. 1999;274:23396–404. doi:10.1074/jbc.274.33.23396
   PubMed Web of Science ®Google Scholar
• Heske J, Heller U, Winklhofer KF, et al. The C-terminal domain of the prion protein is necessary and sufficient for import into the endoplasmic reticulum. J Biol Chem. 2004;279:5435–43. doi:10.1074/jbc.M309570200
   PubMed Web of Science ®Google Scholar
• Minikel EV, Vallabh SM, Lek M, et al. Quantifying prion disease penetrance using large population control cohorts. Sci Transl Med. 2016;8:322.ra9. doi:10.1126/scitranslmed.aad5169
   Web of Science ®Google Scholar
• Miesbauer M, Pfeiffer NV, Rambold AS, et al. Alpha-helical domains promote translocation of intrinsically disordered polypeptides into the endoplasmic reticulum. J Biol Chem. 2009;284:24384–93. doi:10.1074/jbc.M109.023135
   PubMed Web of Science ®Google Scholar
• Miesbauer M, Rambold AS, Winklhofer KF, et al. Targeting of the prion protein to the cytosol: mechanisms and consequences. Curr Issues Mol Biol. 2010;12:109–18.
   PubMed Web of Science ®Google Scholar
• Dirndorfer D, Seidel RP, Nimrod G, et al. The alpha-helical structure of prodomains promotes translocation of intrinsically disordered neuropeptide hormones into the endoplasmic reticulum. J Biol Chem. 2013;288:13961–73. doi:10.1074/jbc.M112.430264
   PubMed Web of Science ®Google Scholar
• Pfeiffer NV, Dirndorfer D, Lang S, et al. Structural features within the nascent chain regulate alternative targeting of secretory proteins to mitochondria. EMBO J. 2013;32:1036–51. doi:10.1038/emboj.2013.46
   PubMed Web of Science ®Google Scholar
• Rapoport TA, Li L, Park E. Structural and Mechanistic Insights into Protein Translocation. Annual review of cell and developmental biology. 2017;33:369–90. doi:10.1146/annurev-cellbio-100616-060439
   PubMed Web of Science ®Google Scholar
• Gonsberg A, Jung S, Ulbrich S, et al. The Sec61/SecY complex is inherently deficient in translocating intrinsically disordered proteins. J Biol Chem. 2017. doi:10.1074/jbc.M117.788067
   PubMed Web of Science ®Google Scholar
• Mori H, Ito K. The Sec protein-translocation pathway. Trends Microbiol. 2001;9:494–500. doi:10.1016/S0966-842X(01)02174-6
   PubMed Web of Science ®Google Scholar
• Daude N, Ng V, Watts JC, et al. Wild-type Shadoo proteins convert to amyloid-like forms under native conditions. J Neurochem. 2010;113:92–104. doi:10.1111/j.1471-4159.2010.06575.x
   PubMed Web of Science ®Google Scholar
• Watts JC, Drisaldi B, Ng V, et al. The CNS glycoprotein Shadoo has PrP(C)-like protective properties and displays reduced levels in prion infections. EMBO J. 2007;26:4038–50. doi:10.1038/sj.emboj.7601830
   PubMed Web of Science ®Google Scholar
• Ma J, Lindquist S. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc Natl Acad Sci U S A. 2001;98:14955–60. doi:10.1073/pnas.011578098
   PubMed Web of Science ®Google Scholar
• Drisaldi B, Stewart RS, Adles C, et al. Mutant PrP is delayed in its exit from the endoplasmic reticulum, but neither wild-type nor mutant PrP undergoes retrotranslocation prior to proteasomal degradation. J Biol Chem. 2003;278:21732–43. doi:10.1074/jbc.M213247200
   PubMed Web of Science ®Google Scholar
• Chakrabarti O, Ashok A, Hegde RS. Prion protein biosynthesis and its emerging role in neurodegeneration. Trends Biochem Sci. 2009;34:287–95. doi:10.1016/j.tibs.2009.03.001
   PubMed Web of Science ®Google Scholar
• Xue B, Dunker AK, Uversky VN. Orderly order in protein intrinsic disorder distribution: disorder in 3500 proteomes from viruses and the three domains of life. J Biomol Struct Dyn. 2012;30:137–49. doi:10.1080/07391102.2012.675145
   PubMed Web of Science ®Google Scholar