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TECHNICAL REPORT

Prion formation, but not clearance, is supported by protein misfolding cyclic amplification

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Pages 415-420 | Received 08 Aug 2014, Accepted 03 Oct 2014, Published online: 08 Jan 2015

References

  • Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y, Marino S, Weissmann C, Aguzzi A. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 1996; 379:339-43; PMID:8552188; http://dx.doi.org/10.1038/379339a0
  • Miller MB, Wang DW, Wang F, Noble GP, Ma J, Woods VL, Li S, Supattapone S. Cofactor molecules induce structural transformation during infectious prion formation. Structure 2013; 21:2061-8; PMID:24120764; http://dx.doi.org/10.1016/j.str.2013.08.025
  • Westaway D, Mirenda C, Foster D, Zebarjadian Y, Scott M, Torchia M, Yang S, Serban H, DeArmond S, Ebeling C, et al. Paradoxical shortening of scrapie incubation times by expression of prion protein transgenes derived from long incubation period mice. Neuron 1991; 7:59-68; PMID:1676894; http://dx.doi.org/10.1016/0896-6273(91)90074-A
  • Smirnovas V, Baron GS, Offerdahl DK, Raymond GJ, Caughey B, Surewicz WK. Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat Struct Mol Biol 2011; 18:504-6; PMID:21441913; http://dx.doi.org/10.1038/nsmb.2035
  • Marzo L, Marijanovic Z, Browman D, Chamoun Z, Caputo A, Zurzolo C. 4-hydroxytamoxifen leads to PrPSc clearance by conveying both PrPC and PrPSc to lysosomes independently of autophagy. J Cell Sci 2013; 126:1345-54; PMID:23418355; http://dx.doi.org/10.1242/jcs.114801
  • Bolton D, Bendheim P. A modified host protein model of scrapie. Ciba Found Symp 1988; 135:164-81; PMID:3136999
  • Joshi-Barr S, Bett C, Chiang W-C, Trejo M, Goebel HH, Sikorska B, Liberski P, Raeber A, Lin JH, Masliah E, et al. De novo prion aggregates trigger autophagy in skeletal muscle. J Virol 2013; PMID:24307586
  • Heiseke A, Aguib Y, Riemer C, Baier M, Schätzl HM. Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J Neurochem 2009; 109:25-34; PMID:19183256; http://dx.doi.org/10.1111/j.1471-4159.2009.05906.x
  • Soto C, Saborio GP, Anderes L. Cyclic amplification of protein misfolding: application to prion-related disorders and beyond. Trends Neurosci 2002; 25:390-4; PMID:12127750; http://dx.doi.org/10.1016/S0166-2236(02)02195-1
  • Bessen R, Marsh R. Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J Virol 1992; 66:2096-101; PMID:1347795
  • Castilla J, Saa P, Hetz C, Soto C. In vitro generation of infectious scrapie prions. Cell 2005; 121:195-206; PMID:15851027; http://dx.doi.org/10.1016/j.cell.2005.02.011
  • Caughey B, Raymond GJ, Bessen RA. Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J Biol Chem 1998; 273:32230-5; PMID:9822701; http://dx.doi.org/10.1074/jbc.273.48.32230
  • Shikiya RA, Bartz JC. In vitro generation of high titer prions. J Virol 2011; 85:13439-13442; http://dx.doi.org/10.1128/JVI.06134-11
  • Gonzalez-Montalban N, Makarava N, Savtchenko R, Baskakov IV. Relationship between conformational stability and amplification efficiency of prions. Biochemistry 2011; 50:6815-23; PMID:21749158; http://dx.doi.org/10.1021/bi200950v
  • Moroncini G, Kanu N, Solforosi L, Abalos G, Telling GC, Head M, Ironside J, Brockes JP, Burton DR, Williamson RA. Motif-grafted antibodies containing the replicative interface of cellular PrP are specific for PrPSc. Proc Natl Acad Sci U S A 2004; 101:10404-9; PMID:15240877; http://dx.doi.org/10.1073/pnas.0403522101
  • Solforosi L, Bellon A, Schaller M, Cruite JT, Abalos GC, Williamson RA. Toward molecular dissection of PrPC-PrPSc interactions. J Biol Chem 2007; 282:7465-71; PMID:17218310; http://dx.doi.org/10.1074/jbc.M610051200
  • Gonzalez-Montalban N, Makarava N, Ostapchenko VG, Savtchenk R, Alexeeva I, Rohwer RG, Baskakov IV. Highly efficient protein misfolding cyclic amplification. PLoS Pathog 2011; 7:e1001277; PMID:21347353; http://dx.doi.org/10.1371/journal.ppat.1001277
  • Miller MB, Geoghegan JC, Supattapone S. Dissociation of infectivity from seeding ability in prions with alternate docking mechanism. PLoS Pathog 2011; 7:e1002128; PMID:21779169; http://dx.doi.org/10.1371/journal.ppat.1002128
  • Gong C, Hart DP. Ultrasound induced cavitation and sonochemical yields. J Acoust Soc Am 1998; 104:2675-82; http://dx.doi.org/10.1121/1.423851
  • Mulcahy ER, Bessen RA. Strain-specific kinetics of prion protein formation in vitro and in vivo. J Biol Chem 2004; 279:1643-9; PMID:14573620; http://dx.doi.org/10.1074/jbc.M307844200
  • Kimberlin R, Walker C. Pathogenesis of mouse scrapie: dynamics of agent replication in spleen, spinal cord and brain after infection by different routes. J Comp Pathol 1979; 89:551-62; PMID:120379; http://dx.doi.org/10.1016/0021-9975(79)90046-X
  • Lasmezas C, Deslys J, Demaimay R, Adjou K, Hauw J, Dormont D. Strain specific and common pathogenic events in murine models of scrapie and bovine spongiform encephalopathy. J Gen Virol 1996; 77:1601-9; PMID:8758005; http://dx.doi.org/10.1099/0022-1317-77-7-1601
  • Saunders SE, Bartz JC, Telling GC, Bartelt-Hunt SL. Environmentally-relevant forms of the prion protein. Environ Sci Technol 2008; 42:6573-9; PMID:18800532; http://dx.doi.org/10.1021/es800590k
  • Tanaka M, Collins S, Toyama B, Weissman J. The physical basis of how prion conformations determine strain phenotypes. Nature 2006; 442:585-9; PMID:16810177; http://dx.doi.org/10.1038/nature04922
  • Legname G, Nguyen H, Peretz D, Cohen F, DeArmond S, Prusiner S. Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc Natl Acad Sci U S A 2006; 103:19105-10; PMID:17142317; http://dx.doi.org/10.1073/pnas.0608970103
  • Deleault N, Harris B, Rees J, Supattapone S. Formation of native prions from minimal components in vitro. Proc Natl Acad Sci USA 2007; 104:9741-6; PMID:17535913
  • Colby DW, Giles K, Legname G, Wille H, Baskakov IV, Dearmond SJ, Prusiner SB. Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci USA 2009; 106:20417-22; PMID:19915150; http://dx.doi.org/10.1073/pnas.0910350106
  • Saunders SE, Shikiya RA, Langenfeld K, Bartelt-Hunt SL, Bartz JC. Replication efficiency of soil-bound prions varies with soil type. J Virol 2011; 85:5476-82; PMID:21430062; http://dx.doi.org/10.1128/JVI.00282-11
  • Stein KC, True HL. Extensive diversity of prion strains is defined by differential chaperone interactions and distinct amyloidogenic regions. PLoS Genet 2014; 10:e1004337; PMID:24811344; http://dx.doi.org/10.1371/journal.pgen.1004337
  • Shikiya RA, Ayers JI, Schutt CR, Kincaid AE, Bartz JC. Coinfecting prion strains compete for a limiting cellular resource. J Virol 2010; 84:5706-14; PMID:20237082; http://dx.doi.org/10.1128/JVI.00243-10
  • Peretz D, Scott MR, Groth D, Williamson RA, Burton DR, Cohen FE, Prusiner SB. Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 2001; 10:854-63; PMID:11274476; http://dx.doi.org/10.1110/ps.39201
  • Ayers JI, Schutt CR, Shikiya RA, Aguzzi A, Kincaid AE, Bartz JC. The strain-encoded relationship between PrP replication, stability and processing in neurons is predictive of the incubation period of disease. PLoS Pathog 2011; 7:e1001317; PMID:21437239; http://dx.doi.org/10.1371/journal.ppat.1001317
  • Green KM, Castilla J, Seward TS, Napier DL, Jewell JE, Soto C, Telling GC. Accelerated high fidelity prion amplification within and across prion species barriers. PLoS Pathog 2008; 4:e1000139; PMID:18769716
  • Barria MA, Telling GC, Gambetti P, Mastrianni JA, Soto C. Generation of a new form of human PrPSc in vitro by interspecies transmission from cervid prions. J Biol Chem 2011; 286:7490-5; PMID:21209079; http://dx.doi.org/10.1074/jbc.M110.198465
  • Haldiman T, Kim C, Cohen Y, Chen W, Blevins J, Qing L, Cohen ML, Langeveld J, Telling GC, Kong Q, et al. Coexistence of distinct prion types enables conformational evolution of human PrPSc by competitive selection. J Biol Chem 2013; 288(41):29846-61; PMID:23974118; http://dx.doi.org/10.1074/jbc.M113.500108
  • Gonzalez-Montalban N, Lee YJ, Makarava N, Savtchenko R, Baskakov IV. Changes in prion replication environment cause prion strain mutation. FASEB J 2013; 27(9):3702-10; PMID:23729586; http://dx.doi.org/10.1096/fj.13-230466
  • Makarava N, Savtchenko R, Baskakov IV. Selective amplification of classical and atypical prions using modified protein misfolding cyclic amplification. J Biol Chem 2013; 288:33-41; PMID:23168413; http://dx.doi.org/10.1074/jbc.M112.419531
  • Castilla J, Morales R, Saá P, Barria M, Gambetti P, Soto C. Cell-free propagation of prion strains. EMBO J 2008; 27:2557-66; PMID:18800058; http://dx.doi.org/10.1038/emboj.2008.181
  • Gonzalez-Romero D, Barria MA, Leon P, Morales R, Soto C. Detection of infectious prions in urine. FEBS Lett 2008; 582:3161-6; PMID:18706416; http://dx.doi.org/10.1016/j.febslet.2008.08.003
  • Klingeborn M, Race B, Meade-White KD, Chesebro B. Lower specific infectivity of protease-resistant prion protein generated in cell-free reactions. Proc Natl Acad Sci USA 2011; 108(48):E1244-53; PMID:22065744; http://dx.doi.org/10.1073/pnas.1111255108
  • Deleault NR, Walsh DJ, Piro JR, Wang F, Wang X, Ma J, Rees JR, Supattapone S. Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc Natl Acad Sci U S A 2012; 109:E1938-46; PMID:22711839; http://dx.doi.org/10.1073/pnas.1206999109
  • Deleault NR, Kascsak R, Geoghegan JC, Supattapone S. Species-dependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 2010; 49:3928-34; PMID:20377181; http://dx.doi.org/10.1021/bi100370b
  • Saunders SE, Bartelt-Hunt SL, Bartz JC. Resistance of soil-bound prions to rumen digestion. PLoS ONE 2012; 7:e44051; PMID:22937149; http://dx.doi.org/10.1371/journal.pone.0044051
  • Safar JG, Dearmond SJ, Kociuba K, Deering C, Didorenko S, Bouzamondo-Bernstein E, Prusiner SB, Tremblay P. Prion clearance in bigenic mice. J Gen Virol 2005; 86:2913-23; PMID:16186247; http://dx.doi.org/10.1099/vir.0.80947-0
  • Nicholson EM, Richt JA, Rasmussen MA, Hamir AN, Lebepe-Mazur S, Horst RL. Exposure of sheep scrapie brain homogenate to rumen-simulating conditions does not result in a reduction of PrP(Sc) levels. Lett Appl Microbiol 2007; 44:631-6; PMID:17576225; http://dx.doi.org/10.1111/j.1472-765X.2007.02124.x
  • Mallucci G, Dickinson A, Linehan J, Klöhn P-C, Brandner S, Collinge J. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 2003; 302:871-4; PMID:14593181; http://dx.doi.org/10.1126/science.1090187
  • Brown P, Rau E, Johnson B, Bacote A, Gibbs C, Gajdusek D. New studies on the heat resistance of hamster-adapted scrapie agent: threshold survival after ashing at 600 degrees C suggests an inorganic template of replication. Proc Natl Acad Sci U S A 2000; 97:3418-21; PMID:10716712
  • Bartz JC, Kincaid AE, Bessen RA. Retrograde transport of transmissible mink encephalopathy within descending motor tracts. J Virol 2002; 76:5759-68; PMID:11992004; http://dx.doi.org/10.1128/JVI.76.11.5759-5768.2002
  • Beekes M, Baldauf E, Diringer H. Sequential appearance and accumulation of pathognomonic markers in the central nervous system of hamsters orally infected with scrapie. J Gen Virol 1996; 77:1925-34; PMID:8760444; http://dx.doi.org/10.1099/0022-1317-77-8-1925
  • Kimberlin R, Walker C. Pathogenesis of mouse scrapie: evidence for neural spread of infection to the CNS. J Gen Virol 1980; 51:183-7; PMID:6780656; http://dx.doi.org/10.1099/0022-1317-51-1-183
  • Castilla J, Gonzalez-Romero D, Saá P, Morales R, De Castro J, Soto C. Crossing the species barrier by PrP(Sc) replication in vitro generates unique infectious prions. Cell 2008; 134:757-68; PMID:18775309; http://dx.doi.org/10.1016/j.cell.2008.07.030
  • Kurt TD, Telling GC, Zabel MD, Hoover EA. Trans-species amplification of PrP(CWD) and correlation with rigid loop 170N. Virology 2009; 387:235-43; PMID:19269662; http://dx.doi.org/10.1016/j.virol.2009.02.025
  • Chianini F, Fernandez-Borges N, Vidal E, Gibbard L, Pintado B, De Castro J, Priola SA, Hamilton S, Eaton SL, Finlayson J, et al. Rabbits are not resistant to prion infection. Proc Natl Acad Sci USA 2012; 109:5080-5085; http://dx.doi.org/10.1073/pnas.1120076109
  • Barria MA, Mukherjee A, Gonzalez-Romero D, Morales R, Soto C. De novo generation of infectious prions in vitro produces a new disease phenotype. PLoS Pathog 2009; 5:e1000421; PMID:19436715
  • Bartz JC, Bessen R, McKenzie D, Marsh R, Aiken JM. Adaptation and selection of prion protein strain conformations following interspecies transmission of transmissible Mink encephalopathy. J Virol 2000; 74:5542-7; PMID:10823860; http://dx.doi.org/10.1128/JVI.74.12.5542-5547.2000
  • Kimberlin R, Walker C. Evidence that the transmission of one source of scrapie agent to hamsters involves separation of agent strains from a mixture. J Gen Virol 1978; 39:487-96; PMID:96212; http://dx.doi.org/10.1099/0022-1317-39-3-487
  • Saijo E, Kang H-E, Bian J, Bowling KG, Browning S, Kim S, Hunter N, Telling GC. Epigenetic dominance of prion conformers. PLoS Pathog 2013; 9:e1003692-2; PMID:24204258; http://dx.doi.org/10.1371/journal.ppat.1003692
  • Bian J, Kang H-E, Telling GC. Quinacrine promotes replication and conformational mutation of chronic wasting disease prions. PNAS 2014; 111:6028-33; PMID:24711410; http://dx.doi.org/10.1073/pnas.1322377111
  • Li J, Browning S, Mahal SP, Oelschlegel AM, Weissmann C. Darwinian evolution of prions in cell culture. Science 2010; 327:869-72; PMID:20044542; http://dx.doi.org/10.1126/science.1183218
  • Li J, Mahal SP, Demczyk CA, Weissmann C. Mutability of prions. EMBO Rep 2011; 12:1243-1250; http://dx.doi.org/10.1038/embor.2011.191
  • Daus ML, Wagenführ K, Thomzig A, Boerner S, Hermann P, Hermelink A, Beekes M, Lasch P. Infrared microspectroscopy detects protein misfolding cyclic amplification (PMCA)-induced conformational alterations in hamster scrapie progeny seeds. J Biol Chem 2013; 288(49):35068-80; PMID:24163371; http://dx.doi.org/10.1074/jbc.M113.497131
  • Dickinson A, Fraser H, Meikle V, Outram G. Competition between different scrapie agents in mice. Nat New Biol 1972; 237:244-5; PMID:4624846
  • Bartz JC, Kramer ML, Sheehan MH, Hutter JAL, Ayers JI, Bessen RA, Kincaid AE. Prion interference is due to a reduction in strain-specific PrPSc levels. J Virol 2007; 81:689-97; PMID:17079313; http://dx.doi.org/10.1128/JVI.01751-06
  • Bueler H, Fischer M, Lang Y, Bluethmann H, Lipp H, DeArmond S, Prusiner S, Aguet M, Weissmann C. Normal development and behaviour of mice lacking the neuronal cell- surface PrP protein. Nature 1992; 356:577-82; PMID:1373228
  • Saunders SE, Bartz JC, Shikiya RA. Protein misfolding cyclic amplification of prions. J Vis Exp 2012; PMID:23168797; http://dx.doi.org/10.3791/4075
  • Ayers JI, Kincaid AE, Bartz JC. Prion strain targeting independent of strain-specific neuronal tropism. J Virol 2009; 83:81-7; PMID:18971281; http://dx.doi.org/10.1128/JVI.01745-08
  • Bessen R, Marsh R. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J Gen Virol 1992; 73:329-34; PMID:1531675; http://dx.doi.org/10.1099/0022-1317-73-2-329

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