Transgenic mice recapitulate the phenotypic heterogeneity of genetic prion diseases without developing prion infectivity: Role of intracellular PrP retention in neurotoxicity

REFERENCES

• Mastrianni JA. The genetics of prion diseases. Genet Med 2010; 12:187-95; PMID:20216075; http://dx.doi.org/10.1097/GIM.0b013e3181cd7374
   PubMed Web of Science ®Google Scholar
• Mead S, Gandhi S, Beck J, Caine D, Gajulapalli D, Carswell C, Hyare H, Joiner S, Ayling H, Lashley T, et al. A novel prion disease associated with diarrhea and autonomic neuropathy. N Engl J Med 2013; 369:1904-14; PMID:24224623; http://dx.doi.org/10.1056/NEJMoa1214747
   PubMed Web of Science ®Google Scholar
• Prusiner SB. Prions. Proc Natl Acad Sci U S A 1998; 95:13363-83; PMID:9811807; http://dx.doi.org/10.1073/pnas.95.23.13363
   PubMed Web of Science ®Google Scholar
• Telling GC, Parchi P, DeArmond SJ, Cortelli P, Montagna P, Gabizon R, Mastrianni J, Lugaresi E, Gambetti P, Prusiner SB. Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science 1996; 274:2079-82; PMID:8953038; http://dx.doi.org/10.1126/science.274.5295.2079
   PubMed Web of Science ®Google Scholar
• Tateishi J, Kitamoto T. Inherited prion diseases and transmission to rodents. Brain Pathol 1995; 5:53-9; PMID:7767491; http://dx.doi.org/10.1111/j.1750-3639.1995.tb00577.x
   PubMed Web of Science ®Google Scholar
• Dossena S, Imeri L, Mangieri M, Garofoli A, Ferrari L, Senatore A, Restelli E, Balducci C, Fiordaliso F, Salio M, et al. Mutant prion protein expression causes motor and memory deficits and abnormal sleep patterns in a transgenic mouse model. Neuron 2008; 60:598-609; PMID:19038218; http://dx.doi.org/10.1016/j.neuron.2008.09.008
   PubMed Web of Science ®Google Scholar
• Bouybayoune I, Mantovani S, Del Gallo F, Bertani I, Restelli E, Comerio L, Tapella L, Baracchi F, Fernández-Borges N, Mangieri M, et al. Transgenic fatal familial insomnia mice indicate prion infectivity-independent mechanisms of pathogenesis and phenotypic expression of disease. PLoS Pathog 2015; 11:e1004796; PMID:25880443; http://dx.doi.org/10.1371/journal.ppat.1004796
   PubMed Web of Science ®Google Scholar
• Chiesa R, Piccardo P, Ghetti B, Harris DA. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 1998; 21:1339-51; PMID:9883727; http://dx.doi.org/10.1016/S0896-6273(00)80653-4
   PubMed Web of Science ®Google Scholar
• Lugaresi E, Medori R, Montagna P, Baruzzi A, Cortelli P, Lugaresi A, Tinuper P, Zucconi M, Gambetti P. Fatal familial insomnia and dysautonomia with selective degeneration of thalamic nuclei. N Engl J Med 1986; 315:997-1003; PMID:3762620; http://dx.doi.org/10.1056/NEJM198610163151605
   PubMed Web of Science ®Google Scholar
• Cortelli P, Gambetti P, Montagna P, Lugaresi E. Fatal familial insomnia: clinical features and molecular genetics. J Sleep Res 1999; 8 Suppl 1:23-9; PMID:10389103; http://dx.doi.org/10.1046/j.1365-2869.1999.00005.x
   PubMed Web of Science ®Google Scholar
• Minikel EV, Vallabh SM, Lek M, Estrada K, Samocha KE, Sathirapongsasuti JF, McLean CY, Tung JY, Yu LP, Gambetti P, et al. Quantifying prion disease penetrance using large population control cohorts. Sci Transl Med 2016; 8(322):322ra9; PMID:26791950; http://dx.doi.org/10.1126/scitranslmed.aad5169
   Google Scholar
• Forloni G, Tettamanti M, Lucca U, Albanese Y, Quaglio E, Chiesa R, Erbetta A, Villani F, Redaelli V, Tagliavini F, et al. Preventive study in subjects at risk of fatal familial insomnia: Innovative approach to rare diseases. Prion 2015; 9:75-9; PMID:25996399; http://dx.doi.org/10.1080/19336896.2015.1027857
   PubMed Web of Science ®Google Scholar
• Montagna P, Gambetti P, Cortelli P, Lugaresi E. Familial and sporadic fatal insomnia. Lancet Neurol 2003; 2:167-76; PMID:12849238; http://dx.doi.org/10.1016/S1474-4422(03)00323-5
   PubMed Web of Science ®Google Scholar
• Parchi P, Castellani R, Cortelli P, Montagna P, Chen SG, Petersen RB, Manetto V, Vnencak-Jones CL, McLean MJ, Sheller JR, et al. Regional distribution of protease-resistant prion protein in fatal familial insomnia. Ann Neurol 1995; 38:21-9; PMID:7611720; http://dx.doi.org/10.1002/ana.410380107
   PubMed Web of Science ®Google Scholar
• Supattapone S, Muramoto T, Legname G, Mehlhorn I, Cohen FE, DeArmond SJ, Prusiner SB, Scott MR. Identification of two prion protein regions that modify scrapie incubation time. J Virol 2001; 75:1408-13; PMID:11152514; http://dx.doi.org/10.1128/JVI.75.3.1408-1413.2001
   PubMed Web of Science ®Google Scholar
• Chiesa R, Piccardo P, Quaglio E, Drisaldi B, Si-Hoe SL, Takao M, Ghetti B, Harris DA. Molecular distinction between pathogenic and infectious properties of the prion protein. J Virol 2003; 77:7611-22; PMID:12805461; http://dx.doi.org/10.1128/JVI.77.13.7611-7622.2003
   PubMed Web of Science ®Google Scholar
• Jackson WS, Borkowski AW, Faas H, Steele AD, King OD, Watson N, Jasanoff A, Lindquist S. Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron 2009; 63:438-50; PMID:19709627; http://dx.doi.org/10.1016/j.neuron.2009.07.026
   PubMed Web of Science ®Google Scholar
• Landolt HP, Glatzel M, Blattler T, Achermann P, Roth C, Mathis J, Weis J, Tobler I, Aguzzi A, Bassetti CL. Sleep-wake disturbances in sporadic Creutzfeldt-Jakob disease. Neurology 2006; 66:1418-24; PMID:16682677; http://dx.doi.org/10.1212/01.wnl.0000210445.16135.56
   PubMed Web of Science ®Google Scholar
• Wu MA, Tobaldini E, Bianchi S, Del Gallo F, Bouybayoune I, Mantovani S, Bertani I, Chiesa R, Montano N, Imeri L. Neurovegetative control is altered in transgenic mice expressing the prion protein mutation associated with fatal familial insomnia. Autonomic Neuroscience 2015; 192:107; http://dx.doi.org/10.1016/j.autneu.2015.07.169
   Google Scholar
• Prusiner SB, Scott M, Foster D, Pan KM, Groth D, Mirenda C, Torchia M, Yang SL, Serban D, Carlson GA, et al. Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 1990; 63:673-86; PMID:1977523; http://dx.doi.org/10.1016/0092-8674(90)90134-Z
   PubMed Web of Science ®Google Scholar
• Telling GC, Haga T, Torchia M, Tremblay P, DeArmond SJ, Prusiner SB. Interactions between wild-type and mutant prion proteins modulate neurodegeneration in transgenic mice. Genes Dev 1996; 10:1736-50; PMID:8698234; http://dx.doi.org/10.1101/gad.10.14.1736
   PubMed Web of Science ®Google Scholar
• Nazor KE, Kuhn F, Seward T, Green M, Zwald D, Purro M, Schmid J, Biffiger K, Power AM, Oesch B, et al. Immunodetection of disease-associated mutant PrP, which accelerates disease in GSS transgenic mice. EMBO J 2005; 24:2472-80; PMID:15962001; http://dx.doi.org/10.1038/sj.emboj.7600717
   PubMed Web of Science ®Google Scholar
• Yang W, Cook J, Rassbach B, Lemus A, DeArmond SJ, Mastrianni JA. A new transgenic mouse model of Gerstmann-Straussler-Scheinker syndrome caused by the A117V mutation of PRNP. J Neurosci 2009; 29:10072-80; PMID:19675240; http://dx.doi.org/10.1523/JNEUROSCI.2542-09.2009
   PubMed Web of Science ®Google Scholar
• Drisaldi B, Stewart RS, Adles C, Stewart LR, Quaglio E, Biasini E, Fioriti L, Chiesa R, Harris DA. 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; PMID:12663673; http://dx.doi.org/10.1074/jbc.M213247200
   PubMed Web of Science ®Google Scholar
• Fioriti L, Dossena S, Stewart LR, Stewart RS, Harris DA, Forloni G, Chiesa R. Cytosolic prion protein (PrP) is not toxic in N2a cells and primary neurons expressing pathogenic PrP mutations. J Biol Chem 2005; 280:11320-8; PMID:15632159; http://dx.doi.org/10.1074/jbc.M412441200
   PubMed Web of Science ®Google Scholar
• Quaglio E, Restelli E, Garofoli A, Dossena S, De Luigi A, Tagliavacca L, Imperiale D, Migheli A, Salmona M, Sitia R, et al. Expression of mutant or cytosolic PrP in transgenic mice and cells is not associated with endoplasmic reticulum stress or proteasome dysfunction. PLoS One 2011; 6:e19339; PMID:21559407; http://dx.doi.org/10.1371/journal.pone.0019339
   PubMed Web of Science ®Google Scholar
• Senatore A, Restelli E, Chiesa R. Synaptic dysfunction in prion diseases: a trafficking problem? Int J Cell Biol 2013; 2013:543803; PMID:24369467; http://dx.doi.org/10.1155/2013/543803
   PubMedGoogle Scholar
• Tapella L, Stravalaci M, Bastone A, Biasini E, Gobbi M, Chiesa R. Epitope scanning indicates structural differences in brain-derived monomeric and aggregated mutant prion proteins related to genetic prion diseases. Biochem J 2013; 454:417-25; PMID:23808898; http://dx.doi.org/10.1042/BJ20130563
   PubMed Web of Science ®Google Scholar
• Biasini E, Tapella L, Restelli E, Pozzoli M, Massignan T, Chiesa R. The hydrophobic core region governs mutant prion protein aggregation and intracellular retention. Biochem J 2010; 430:477-86; PMID:20626348; http://dx.doi.org/10.1042/BJ20100615
   PubMed Web of Science ®Google Scholar
• Senatore A, Colleoni S, Verderio C, Restelli E, Morini R, Condliffe SB, Bertani I, Mantovani S, Canovi M, Micotti E, et al. Mutant PrP suppresses glutamatergic neurotransmission in cerebellar granule neurons by impairing membrane delivery of VGCC alpha(2)delta-1 subunit. Neuron 2012; 74:300-13; PMID:22542184; http://dx.doi.org/10.1016/j.neuron.2012.02.027
   PubMed Web of Science ®Google Scholar
• Chiesa R. The elusive role of the prion protein and the mechanism of toxicity in prion disease. PLoS Pathog 2015; 11:e1004745; PMID:25951168; http://dx.doi.org/10.1371/journal.ppat.1004745
   PubMedGoogle Scholar
• Khosravani H, Zhang Y, Tsutsui S, Hameed S, Altier C, Hamid J, Chen L, Villemaire M, Ali Z, Jirik FR, et al. Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J Cell Biol 2008; 181:551-65; PMID:18443219; http://dx.doi.org/10.1083/jcb.200711002
   PubMed Web of Science ®Google Scholar
• Watt NT, Taylor DR, Kerrigan TL, Griffiths HH, Rushworth JV, Whitehouse IJ, Hooper NM. Prion protein facilitates uptake of zinc into neuronal cells. Nat Commun 2012; 3:1134; PMID:23072804; http://dx.doi.org/10.1038/ncomms2135
   PubMed Web of Science ®Google Scholar
• Hsiao KK, Scott M, Foster D, Groth DF, DeArmond SJ, Prusiner SB. Spontaneous neurodegeneration in transgenic mice with mutant prion protein. Science 1990; 250:1587-90; PMID:1980379; http://dx.doi.org/10.1126/science.1980379
   PubMed Web of Science ®Google Scholar
• Friedman-Levi Y, Meiner Z, Canello T, Frid K, Kovacs GG, Budka H, Avrahami D, Gabizon R. Fatal prion disease in a mouse model of genetic E200K Creutzfeldt-Jakob disease. PLoS Pathog 2011; 7:e1002350; PMID:22072968; http://dx.doi.org/10.1371/journal.ppat.1002350
   PubMed Web of Science ®Google Scholar
• Jackson WS, Borkowski AW, Watson NE, King OD, Faas H, Jasanoff A, Lindquist S. Profoundly different prion diseases in knock-in mice carrying single PrP codon substitutions associated with human diseases. Proc Natl Acad Sci U S A 2013; 110:14759-64; PMID:23959875; http://dx.doi.org/10.1073/pnas.1312006110
   PubMed Web of Science ®Google Scholar