665
Views
12
CrossRef citations to date
0
Altmetric
Research Paper

Slow spontaneous α-to-β structural conversion in a non-denaturing neutral condition reveals the intrinsically disordered property of the disulfide-reduced recombinant mouse prion protein

, , , , &
Pages 489-497 | Published online: 17 Sep 2012

References

  • Prusiner SB. Prions. Proc Natl Acad Sci U S A 1998; 95:13363 - 83; http://dx.doi.org/10.1073/pnas.95.23.13363; PMID: 9811807
  • Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, et al. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci U S A 1993; 90:10962 - 6; http://dx.doi.org/10.1073/pnas.90.23.10962; PMID: 7902575
  • Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, et al. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc Natl Acad Sci U S A 1997; 94:13452 - 7; http://dx.doi.org/10.1073/pnas.94.25.13452; PMID: 9391046
  • Ryou C, Mays CE. Prion propagation in vitro: are we there yet?. Int J Med Sci 2008; 5:347 - 53; http://dx.doi.org/10.7150/ijms.5.347; PMID: 19015743
  • Bocharova OV, Breydo L, Parfenov AS, Salnikov VV, Baskakov IV. In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J Mol Biol 2005; 346:645 - 59; http://dx.doi.org/10.1016/j.jmb.2004.11.068; PMID: 15670611
  • Baskakov IV. Autocatalytic conversion of recombinant prion proteins displays a species barrier. J Biol Chem 2004; 279:7671 - 7; http://dx.doi.org/10.1074/jbc.M310594200; PMID: 14668351
  • Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, Lansbury PT, et al. Cell-free formation of protease-resistant prion protein. Nature 1994; 370:471 - 4; http://dx.doi.org/10.1038/370471a0; PMID: 7913989
  • Bessen RA, Kocisko DA, Raymond GJ, Nandan S, Lansbury PT, Caughey B. Non-genetic propagation of strain-specific properties of scrapie prion protein. Nature 1995; 375:698 - 700; http://dx.doi.org/10.1038/375698a0; PMID: 7791905
  • Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 2001; 411:810 - 3; http://dx.doi.org/10.1038/35081095; PMID: 11459061
  • Soto C, Saborio GP, Anderes L. Cyclic amplification of protein misfolding: application to prion-related disorders and beyond. Trends Neurosci 2002; 25:390 - 4; http://dx.doi.org/10.1016/S0166-2236(02)02195-1; PMID: 12127750
  • Gonzalez-Montalban N, Makarava N, Ostapchenko VG, Savtchenk R, Alexeeva I, Rohwer RG, et al. Highly efficient protein misfolding cyclic amplification. PLoS Pathog 2011; 7:e1001277; http://dx.doi.org/10.1371/journal.ppat.1001277; PMID: 21347353
  • Mays CE, Yeom J, Kang HE, Bian J, Khaychuk V, Kim Y, et al. In vitro amplification of misfolded prion protein using lysate of cultured cells. PLoS One 2011; 6:e18047; http://dx.doi.org/10.1371/journal.pone.0018047; PMID: 21464935
  • Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, et al. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods 2008; 5:211 - 2; http://dx.doi.org/10.1038/nmeth0308-211; PMID: 18309304
  • Baskakov IV, Legname G, Baldwin MA, Prusiner SB, Cohen FE. Pathway complexity of prion protein assembly into amyloid. J Biol Chem 2002; 277:21140 - 8; http://dx.doi.org/10.1074/jbc.M111402200; PMID: 11912192
  • Jackson GS, Hosszu LL, Power A, Hill AF, Kenney J, Saibil H, et al. Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 1999; 283:1935 - 7; http://dx.doi.org/10.1126/science.283.5409.1935; PMID: 10082469
  • Sokolowski F, Modler AJ, Masuch R, Zirwer D, Baier M, Lutsch G, et al. Formation of critical oligomers is a key event during conformational transition of recombinant syrian hamster prion protein. J Biol Chem 2003; 278:40481 - 92; http://dx.doi.org/10.1074/jbc.M304391200; PMID: 12917432
  • Bocharova OV, Breydo L, Salnikov VV, Gill AC, Baskakov IV. Synthetic prions generated in vitro are similar to a newly identified subpopulation of PrPSc from sporadic Creutzfeldt-Jakob Disease. Protein Sci 2005; 14:1222 - 32; http://dx.doi.org/10.1110/ps.041186605; PMID: 15802644
  • Bjorndahl TC, Zhou GP, Liu X, Perez-Pineiro R, Semenchenko V, Saleem F, et al. Detailed biophysical characterization of the acid-induced PrP(c) to PrP(β) conversion process. Biochemistry 2011; 50:1162 - 73; http://dx.doi.org/10.1021/bi101435c; PMID: 21189021
  • Novitskaya V, Bocharova OV, Bronstein I, Baskakov IV. Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J Biol Chem 2006; 281:13828 - 36; http://dx.doi.org/10.1074/jbc.M511174200; PMID: 16554307
  • Khan MQ, Sweeting B, Mulligan VK, Arslan PE, Cashman NR, Pai EF, et al. Prion disease susceptibility is affected by beta-structure folding propensity and local side-chain interactions in PrP. Proc Natl Acad Sci U S A 2010; 107:19808 - 13; http://dx.doi.org/10.1073/pnas.1005267107; PMID: 21041683
  • Fanucci GE, Cafiso DS. Recent advances and applications of site-directed spin labeling. Curr Opin Struct Biol 2006; 16:644 - 53; http://dx.doi.org/10.1016/j.sbi.2006.08.008; PMID: 16949813
  • Chen PY, Lin CC, Chang YT, Lin SC, Chan SI. One O-linked sugar can affect the coil-to-β structural transition of the prion peptide. Proc Natl Acad Sci U S A 2002; 99:12633 - 8; http://dx.doi.org/10.1073/pnas.192137799; PMID: 12235358
  • Lee LY, Chen RP. Quantifying the sequence-dependent species barrier between hamster and mouse prions. J Am Chem Soc 2007; 129:1644 - 52; http://dx.doi.org/10.1021/ja0667413; PMID: 17243682
  • Ho CC, Lee LY, Huang KT, Lin CC, Ku MY, Yang CC, et al. Tuning the conformational properties of the prion peptide. Proteins 2009; 76:213 - 25; http://dx.doi.org/10.1002/prot.22341; PMID: 19137620
  • Zhang H, Stockel J, Mehlhorn I, Groth D, Baldwin MA, Prusiner SB, et al. Physical studies of conformational plasticity in a recombinant prion protein. Biochemistry 1997; 36:3543 - 53; http://dx.doi.org/10.1021/bi961965r; PMID: 9132005
  • Pan KM, Stahl N, Prusiner SB. Purification and properties of the cellular prion protein from Syrian hamster brain. Protein Sci 1992; 1:1343 - 52; http://dx.doi.org/10.1002/pro.5560011014; PMID: 1363897
  • Chang ES, Liao TY, Lim TS, Fann W, Chen RP. A new amyloid-like β-aggregate with amyloid characteristics, except fibril morphology. J Mol Biol 2009; 385:1257 - 65; http://dx.doi.org/10.1016/j.jmb.2008.11.009; PMID: 19041877
  • Watanabe Y, Hiraoka W, Shimoyama Y, Horiuchi M, Kuwabara M, Inanami O. Instability of familial spongiform encephalopathy-related prion mutants. Biochem Biophys Res Commun 2008; 366:244 - 9; http://dx.doi.org/10.1016/j.bbrc.2007.11.145; PMID: 18062918
  • Chiang YW, Otoshima Y, Watanabe Y, Inanami O, Shimoyama Y. Dynamics and local ordering of spin-labeled prion protein: an ESR simulation study of a highly PH-sensitive site. J Biomol Struct Dyn 2008; 26:355 - 66; http://dx.doi.org/10.1080/07391102.2008.10507250; PMID: 18808201
  • Hosszu LL, Trevitt CR, Jones S, Batchelor M, Scott DJ, Jackson GS, et al. Conformational properties of β-PrP. J Biol Chem 2009; 284:21981 - 90; http://dx.doi.org/10.1074/jbc.M809173200; PMID: 19369250
  • Bateman DA, Tycko R, Wickner RB. Experimentally derived structural constraints for amyloid fibrils of wild-type transthyretin. Biophys J 2011; 101:2485 - 92; http://dx.doi.org/10.1016/j.bpj.2011.10.009; PMID: 22098747
  • Mehlhorn I, Groth D, Stöckel J, Moffat B, Reilly D, Yansura D, et al. High-level expression and characterization of a purified 142-residue polypeptide of the prion protein. Biochemistry 1996; 35:5528 - 37; http://dx.doi.org/10.1021/bi952965e; PMID: 8611544
  • Dmitrenko O, Thorpe C, Bach RD. Mechanism of SN2 disulfide bond cleavage by phosphorus nucleophiles. Implications for biochemical disulfide reducing agents. J Org Chem 2007; 72:8298 - 307; http://dx.doi.org/10.1021/jo071271w; PMID: 17914842
  • Turk E, Teplow DB, Hood LE, Prusiner SB. Purification and properties of the cellular and scrapie hamster prion proteins. Eur J Biochem 1988; 176:21 - 30; http://dx.doi.org/10.1111/j.1432-1033.1988.tb14246.x; PMID: 3138115
  • Muramoto T, Scott M, Cohen FE, Prusiner SB. Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc Natl Acad Sci U S A 1996; 93:15457 - 62; http://dx.doi.org/10.1073/pnas.93.26.15457; PMID: 8986833
  • Welker E, Raymond LD, Scheraga HA, Caughey B. Intramolecular versus intermolecular disulfide bonds in prion proteins. J Biol Chem 2002; 277:33477 - 81; http://dx.doi.org/10.1074/jbc.M204273200; PMID: 12082114
  • Herrmann LM, Caughey B. The importance of the disulfide bond in prion protein conversion. Neuroreport 1998; 9:2457 - 61; http://dx.doi.org/10.1097/00001756-199808030-00006; PMID: 9721914
  • Imamura M, Kato N, Okada H, Iwamaru Y, Shimizu Y, Mohri S, et al. Strain-specific effects of reducing agents on the cell-free conversion of recombinant prion protein into a protease-resistant form. Microbiol Immunol 2011; 55:633 - 40; http://dx.doi.org/10.1111/j.1348-0421.2011.00357.x; PMID: 21645053
  • Maeda R, Ado K, Takeda N, Taniguchi Y. Promotion of insulin aggregation by protein disulfide isomerase. Biochim Biophys Acta 2007; 1774:1619 - 27; http://dx.doi.org/10.1016/j.bbapap.2007.08.016; PMID: 17920002
  • Baldwin AJ, Knowles TP, Tartaglia GG, Fitzpatrick AW, Devlin GL, Shammas SL, et al. Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc 2011; 133:14160 - 3; http://dx.doi.org/10.1021/ja2017703; PMID: 21650202
  • Turano C, Coppari S, Altieri F, Ferraro A. Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 2002; 193:154 - 63; http://dx.doi.org/10.1002/jcp.10172; PMID: 12384992
  • Yoo BC, Krapfenbauer K, Cairns N, Belay G, Bajo M, Lubec G. Overexpressed protein disulfide isomerase in brains of patients with sporadic Creutzfeldt-Jakob disease. Neurosci Lett 2002; 334:196 - 200; http://dx.doi.org/10.1016/S0304-3940(02)01071-6; PMID: 12453628
  • Hetz C, Russelakis-Carneiro M, Wälchli S, Carboni S, Vial-Knecht E, Maundrell K, et al. The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci 2005; 25:2793 - 802; http://dx.doi.org/10.1523/JNEUROSCI.4090-04.2005; PMID: 15772339
  • Smith AM, Chan J, Oksenberg D, Urfer R, Wexler DS, Ow A, et al. A high-throughput turbidometric assay for screening inhibitors of protein disulfide isomerase activity. J Biomol Screen 2004; 9:614 - 20; http://dx.doi.org/10.1177/1087057104265292; PMID: 15475481
  • Makarava N, Baskakov IV. Expression and purification of full-length recombinant PrP of high purity. Methods Mol Biol 2008; 459:131 - 43; http://dx.doi.org/10.1007/978-1-59745-234-2_10; PMID: 18576153
  • Shearman MS, Hawtin SR, Tailor VJ. The intracellular component of cellular 3-(4,5-dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide (MTT) reduction is specifically inhibited by beta-amyloid peptides. J Neurochem 1995; 65:218 - 27; http://dx.doi.org/10.1046/j.1471-4159.1995.65010218.x; PMID: 7790863