Cell models of prion infection

Veterinary Research

Volumn 39, Issue 4, 2008, Pages

  Vilette, Didier ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Apoptosis; Cell models; Prion diseases; Prion dissemination; PrP protein

Indexed keywords

AMPHOTERICIN B; CONGO RED; CR 36; HEPARAN SULFATE; HM 2602; HM 5004; ICSM 18; ICSM 19; ICSM 35; ICSM 37; ICSM 42; ICSM42; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 8B4; MONOCLONAL ANTIBODY 8H4; PENTOSAN POLYSULFATE; PHOSPHOROTHIOIC ACID; PRION PROTEIN; PRION PROTEIN ANTIBODY; TETRAPYRROLE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; BIOASSAY; CELL SPREADING; CHRONIC WASTING DISEASE; CYTOLOGY; DRUG MECHANISM; NERVE CELL CULTURE; NERVE DEGENERATION; NEURAL STEM CELL; NONHUMAN; PASSIVE IMMUNIZATION; PRION DISEASE; PROTEIN POLYMORPHISM; REVIEW; SCRAPIE; STRAIN IDENTIFICATION; ANIMAL; CELL CULTURE; METABOLISM; MOUSE; NERVE CELL; PRION;

OVIS ARIES;

ANIMALS; CELLS, CULTURED; MICE; NEURONS; PRION DISEASES; PRIONS;

EID: 50049128403     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres:2007049     Document Type: Review

References (152)

1. Adjou K.T., Simoneau S., Sales N., Lamoury F., Dormont D., Papy-Garcia D., Barritault D., Deslys J.P., Lasmezas C.I., A novel generation of heparan sulfate mimetics for the treatment of prion diseases, J. Gen. Virol. (2003) 84:2595-2603.
2. Amyx H., Salazar A.M., Gajduzek C.D., Gibbs C.J., Chemotherapeutic trials in experimental slow virus disease, Neurology (1984) 34:149.
3. Archer F., Bachelin C., Andreoletti O., Besnard N., Perrot G., Langevin C., Le Dur A., Vilette D., Baron-Van Evercooren A., Vilotte J.L., Laude H., Cultured peripheral neuroglial cells are highly permissive to sheep prion infection, J. Virol. (2004) 78:482-490.
4. Arima K., Nishida N., Sakaguchi S., Shigematsu K., Atarashi R., Yamaguchi N., Yoshikawa D., Yoon J., Watanabe K., Kobayashi N., Mouillet-Richard S., Lehmann S., Katamine S., Biological and biochemical characteristics of prion strains conserved in persistently infected cell cultures, J. Virol. (2005) 79:7104-7112.
5. Arjona A., Simarro L., Islinger F., Nishida N., Manuelidis L., Two Creutzfeldt-Jakob disease agents reproduce prion protein-independent identities in cell cultures, Proc. Natl. Acad. Sci. USA (2004) 101:8768-8773.
6. Atarashi R., Sim V.L., Nishida N., Caughey B., Katamine S., Prion strain-dependent differences in conversion of mutant prion proteins in cell culture, J. Virol. (2006) 80:7854-7862.
7. Baron G.S., Magalhaes A.C., Prado M.A., Caughey B., Mouse-adapted scrapie infection of SN56 cells: greater efficiency with microsome-associated versus purified PrP-res, J. Virol. (2006) 80:2106-2117.
8. Barret A., Tagliavini F., Forloni G., Bate C., Salmona M., Colombo L., De Luigi A., Limido L., Suardi S., Rossi G., Auvre F., Adjou K.T., Sales N., Williams A., Lasmezas C., Deslys J.P., Evaluation of quinacrine treatment for prion diseases, J. Virol. (2003) 77:8462-8469.
9. Beekes M., McBride P.A., Baldauf E., Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie, J. Gen. Virol. (1998) 79:601-607.
10. Benestad S.L., Sarradin P., Thu B., Schonheit J., Tranulis M.A., Bratberg B., Cases of scrapie with unusual features in Norway and designation of a new type, Nor98, Vet. Rec. (2003) 153:202-208.
11. Ben-Zaken O., Tzaban S., Tal Y., Horonchik L., Esko J.D., Vlodavsky I., Taraboulos A., Cellular heparan sulfate participates in the metabolism of prions, J. Biol. Chem. (2003) 278:40041-40049.
12. Beringue V., Vilette D., Mallinson G., Archer F., Kaisar M., Tayebi M., Jackson G.S., Clarke A.R., Laude H., Collinge J., Hawke S., PrPSc binding antibodies are potent inhibitors of prion replication in cell lines, J. Biol. Chem. (2004) 279:39671-39676.
13. Birkett C.R., Hennion R.M., Bembridge D.A., Clarke M.C., Chree A., Bruce M.E., Bostock C.J., Scrapie strains maintain biological phenotypes on propagation in a cell line in culture, EMBO J. (2001) 20:3351-3358.
14. Borchelt D.R., Scott M., Taraboulos A., Stahl N., Prusiner S.B., Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells, J. Cell Biol. (1990) 110:743-752.
15. Borchelt D.R., Taraboulos A., Prusiner S.B., Evidence for synthesis of scrapie prion proteins in the endocytic pathway, J. Biol. Chem. (1992) 267:16188-16199.
16. Bosque P.J., Prusiner S.B., Cultured cell sublines highly susceptible to prion infection, J. Virol. (2000) 74:4377-4386.
17. 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) 379:339-343.
18. Buschmann A., Luhken G., Schultz J., Erhardt G., Groschup M.H., Neuronal accumulation of abnormal prion protein in sheep carrying a scrapie-resistant genotype (PrPARR/ARR), J. Gen. Virol. (2004) 85:2727-2733.
19. Butler D.A., Scott M.R., Bockman J.M., Borchelt D.R., Taraboulos A., Hsiao K.K., Kingsbury D.T., Prusiner S.B., Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins, J. Virol. (1988) 62:1558-1564.
20. Campana V., Sarnataro D., Zurzolo C., The highways and byways of prion protein trafficking, Trends Cell Biol. (2005) 15:102-111.
21. Carimalo J., Cronier S., Petit G., Peyrin J.M., Boukhtouche F., Arbez N., Lemaigre-Dubreuil Y., Brugg B., Miquel M.C., Activation of the JNK-c-Jun pathway during the early phase of neuronal apoptosis induced by PrP106-126 and prion infection, Eur. J. Neurosci. (2005) 21:2311-2319.
22. Caspi S., Halimi M., Yanai A., Sasson S.B., Taraboulos A., Gabizon R., The anti-prion activity of Congo Red. Putative mechanism, J. Biol. Chem. (1998) 273:3484-3489.
23. Caughey B., Race R.E., Ernst D., Buchmeier M.J., Chesebro B., Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells, J. Virol. (1989) 63:175-181.
24. Caughey B., Neary K., Buller R., Ernst D., Perry L.L., Chesebro B., Race R.E., Normal and scrapie-associated forms of prion protein differ in their sensitivities to phospholipase and proteases in intact neuroblastoma cells, J. Virol. (1990) 64:1093-1101.
25. Caughey B., Raymond G.J., The scrapieassociated form of PrP is made from a cell surface precursor that is both protease- and phospholipase-sensitive, J. Biol. Chem. (1991) 266:18217-18223.
26. Caughey B., Raymond G.J., Ernst D., Race R.E., N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state, J. Virol. (1991) 65:6597-6603.
27. Caughey B., Race R.E., Potent inhibition of scrapie-associated PrP accumulation by Congo Red, J. Neurochem. (1992) 59:768-771.
28. Caughey B., Raymond G.J., Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells, J. Virol. (1993) 67:643-650.
29. Caughey B., Brown K., Raymond G.J., Katzenstein G.E., Thresher W., Binding of the protease-sensitive form of PrP (prion protein) to sulfated glycosaminoglycan and Congo Red, J. Virol. (1994) 68:2135-2141.
30. Caughey W.S., Raymond L.D., Horiuchi M., Caughey B., Inhibition of protease-resistant prion protein formation by porphyrins and phthalocyanines, Proc. Natl. Acad. Sci. USA (1998) 95:12117-12122.
31. Clarke M.C., Haig D.A., Evidence for the multiplication of scrapie agent in cell culture, Nature (1970) 225:100-101.
32. Collinge J., Prion diseases of humans and animals: their causes and molecular basis, Annu. Rev. Neurosci. (2001) 24:519-550.
33. Courageot M.P., Daude N., Nonno R., Paquet S., Di Bari M.A., Le Dur A., Chapuis J., Hill A.F., Agrimi U., Laude H., Vilette D., A cell line infectible by prion strains from different species, J. Gen. Virol. (2008) 89.
34. Cronier S., Laude H., Peyrin J.M., Prions can infect primary cultured neurons and astrocytes and promote neuronal cell death, Proc. Natl. Acad. Sci. USA (2004) 101:12271-12276.
35. Crozet C., Lin Y.L., Mettling C., Mourton-Gilles C., Corbeau P., Lehmann S., Perrier V., Inhibition of PrPSc formation by lentiviral gene transfer of PrP containing dominant negative mutations, J. Cell. Sci. (2004) 117:5591-5597.
36. DeArmond S.J., Sanchez H., Yehiely F., Qiu Y., Ninchak-Casey A., Daggett V., Camerino A.P., Cayetano J., Rogers M., Groth D., Torchia M., Tremblay P., Scott M.R., Cohen F.E., Prusiner S.B., Selective neuronal targeting in prion disease, Neuron (1997) 19:1337-1348.
37. Demaimay R., Chesebro B., Caughey B., Inhibition of formation of protease-resistant prion protein by Trypan Blue, Sirius Red and other Congo Red analogs, Arch. Virol. Suppl. (2000) 277-283.
38. Desgranges P., Barbaud C., Caruelle J.P., Barritault D., Gautron J., A substituted dextran enhances muscle fiber survival and regeneration in ischemic and denervated rat EDL muscle, FASEB J. (1999) 13:761-766.
39. Dlakic W.M., Grigg E., Bessen R.A., Prion infection of muscle cells in vitro, J. Virol. (2007) 81:4615-4624.
40. Ehlers B., Diringer H., Dextran sulphate 500 delays and prevents mouse scrapie by impairment of agent replication in spleen, J. Gen. Virol. (1984) 65:1325-1330.
41. Enari M., Flechsig E., Weissmann C., Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody, Proc. Natl. Acad. Sci. USA (2001) 98:9295-9299.
42. Ertmer A., Gilch S., Yun S.W., Flechsig E., Klebl B., Stein-Gerlach M., Klein M.A., Schatzl H.M., The tyrosine kinase inhibitor STI571 induces cellular clearance of PrPSc in prion-infected cells, J. Biol. Chem. (2004) 279:41918-41927.
43. Faure J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V., Kirchhoff F., Raposo G., Garin J., Sadoul R., Exosomes are released by cultured cortical neurones, Mol. Cell. Neurosci. (2006) 31:642-648.
44. Feraudet C., Morel N., Simon S., Volland H., Frobert Y.F., Creminon C., Vilette D., Lehmann S., Grassi J., Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells, J. Biol. Chem. (2004) 280:11247-11258.
45. Fevrier B., Raposo G., Exosomes: endosomal-derived vesicles shipping extracellular messages, Curr. Opin. Cell. Biol. (2004) 16:415-421.
46. Fevrier B., Vilette D., Archer F., Loew D., Faigle W., Vidal M., Laude H., Raposo G., Cells release prions in association with exosomes, Proc. Natl. Acad. Sci. USA (2004) 101:9683-9688.
47. Follet J., Lemaire-Vieille C., Blanquet-Grossard F., Podevin-Dimster V., Lehmann S., Chauvin J.P., Decavel J.P., Varea R., Grassi J., Fontes M., Cesbron J.Y., PrP expression and replication by Schwann cells: implications in prion spreading, J. Virol. (2002) 76:2434-2439.
48. Fraser H., Dickinson A.G., Scrapie in mice. Agent-strain differences in the distribution and intensity of grey matter vacuolation, J. Comp. Pathol. (1973) 83:29-40.
49. Gabizon R., Meiner Z., Halimi M., Ben-Sasson S.A., Heparin-like molecules bind differentially to prion-proteins and change their intracellular metabolic fate, J. Cell. Physiol. (1993) 157:319-325.
50. Gauczynski S., Peyrin J.M., Haik S., Leucht C., Hundt C., Rieger R., Krasemann S., Deslys J.P., Dormont D., Lasmezas C.I., Weiss S., The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein, EMBO J. (2001) 20:5863-5875.
51. Gauczynski S., Nikles D., El-Gogo S., Papy-Garcia D., Rey C., Alban S., Barritault D., Lasmezas C.I., Weiss S., The 37-kDa/67-kDa laminin receptor acts as a receptor for infectious prions and is inhibited by polysulfated glycans, J. Infect. Dis. (2006) 194:702-709.
52. Gilch S., Wopfner F., Renner-Muller I., Kremmer E., Bauer C., Wolf E., Brem G., Groschup M.H., Schatzl H.M., Polyclonal anti-PrP auto-antibodies induced with dimeric PrP interfere efficiently with PrPSc propagation in prion-infected cells, J. Biol. Chem. (2003) 278:18524-18531.
53. Giri R.K., Young R., Pitstick R., DeArmond S.J., Prusiner S.B., Carlson G.A., Prion infection of mouse neurospheres, Proc. Natl. Acad. Sci. USA (2006) 103:3875-3880.
54. Hetz C., Russelakis-Carneiro M., Maundrell K., Castilla J., Soto C., Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein, EMBO J. (2003) 22:5435-5445.
55. Hijazi N., Kariv-Inbal Z., Gasset M., Gabizon R., PrPSc incorporation to cells requires endogenous glycosaminoglycan expression, J. Biol. Chem. (2005) 280:17057-17061.
56. Holscher C., Delius H., Burkle A., Overexpression of nonconvertible PrPC delta114-121 in scrapie-infected mouse neuroblastoma cells leads to trans-dominant inhibition of wild-type PrP(Sc) accumulation, J. Virol. (1998) 72:1153-1159.
57. Horiuchi M., Priola S.A., Chabry J., Caughey B., Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers, Proc. Natl. Acad. Sci. USA (2000) 97:5836-5841.
58. Horonchik L., Tzaban S., Ben-Zaken O., Yedidia Y., Rouvinski A., Papy-Garcia D., Barritault D., Vlodavsky I., Taraboulos A., Heparan sulfate is a cellular receptor for purified infectious prions, J. Biol. Chem. (2005) 280:17062-17067.
59. Hunter N., PrP genetics in sheep and the applications for scrapie and BSE, Trends Microbiol. (1997) 5:331-334.
60. Ingrosso L., Ladogana A., Pocchiari M., Congo Red prolongs the incubation period in scrapie-infected hamsters, J. Virol. (1995) 69:506-508.
61. Iwamaru Y., Takenouchi T., Ogihara K., Hoshino M., Takata M., Imamura M., Tagawa Y., Hayashi-Kato H., Ushiki-Kaku Y., Shimizu Y., Okada H., Shinagawa M., Kitani H., Yokoyama T., Microglial cell line established from prion protein-overexpressing mice is susceptible to various murine prion strains, J. Virol. (2007) 81:1524-1527.
62. Jeffrey M., Martin S., Gonzalez L., Ryder S.J., Bellworthy S.J., Jackman R., Differential diagnosis of infections with the bovine spongiform encephalopathy (BSE) and scrapie agents in sheep, J. Comp. Pathol. (2001) 125:271-284.
63. Kaneko K., Vey M., Scott M., Pilkuhn S., Cohen F.E., Prusiner S.B., COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scrapie isoform, Proc. Natl. Acad. Sci. USA (1997) 94:2333-2338.
64. Kaneko K., Zulianello L., Scott M., Cooper C.M., Wallace A.C., James T.L., Cohen F.E., Prusiner S.B., Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation, Proc. Natl. Acad. Sci. USA (1997) 94:10069-10074.
65. Kanu N., Imokawa Y., Drechsel D.N., Williamson R.A., Birkett C.R., Bostock C.J., Brockes J.P., Transfer of scrapie prion infectivity by cell contact in culture, Curr. Biol. (2002) 12:523-530.
66. Kim C.L., Karino A., Ishiguro N., Shinagawa M., Sato M., Horiuchi M., Cell-surface retention of PrPC by anti-PrP antibody prevents protease-resistant PrP formation, J. Gen. Virol. (2004) 85:3473-3482.
67. Klohn P.C., Stoltze L., Flechsig E., Enari M., Weissmann C., A quantitative, highly sensitive cell-based infectivity assay for mouse scrapie prions, Proc. Natl. Acad. Sci. USA (2003) 100:11666-11671.
68. Kocisko D.A., Baron G.S., Rubenstein R., Chen J., Kuizon S., Caughey B., New inhibitors of scrapie-associated prion protein formation in a library of 2000 drugs and natural products, J. Virol. (2003) 77:10288-10294.
69. Kocisko D.A., Caughey W.S., Race R.E., Roper G., Caughey B., Morrey J.D., A porphyrin increases survival time of mice after intracerebral prion infection, Antimicrob. Agents Chemother. (2006) 50:759-761.
70. Kocisko D.A., Vaillant A., Lee K.S., Arnold K.M., Bertholet N., Race R.E., Olsen E.A., Juteau J.M., Caughey B., Potent antiscrapie activities of degenerate phosphorothioate oligonucleotides, Antimicrob. Agents Chemother. (2006) 50:1034-1044.
71. Kristiansen M., Messenger M.J., Klohn P.C., Brandner S., Wadsworth J.D., Collinge J., Tabrizi S.J., Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis, J. Biol. Chem. (2005) 280:38851-38861.
72. Ladogana A., Casaccia P., Ingrosso L., Cibati M., Salvatore M., Xi Y.G., Masullo C., Pocchiari M., Sulphate polyanions prolong the incubation period of scrapie-infected hamsters, J. Gen. Virol. (1992) 73:661-665.
73. Ladogana A., Liu Q., Xi Y.G., Pocchiari M., Proteinase-resistant protein in human neuroblastoma cells infected with brain material from Creutzfeldt-Jakob patient, Lancet (1995) 345:594-595.
74. Larramendy-Gozalo C., Barret A., Daudigeos E., Mathieu E., Antonangeli L., Riffet C., Petit E., Papy-Garcia D., Barritault D., Brown P., Deslys J.P., Comparison of CR36, a new heparan mimetic, and pentosan polysulfate in the treatment of prion diseases, J. Gen. Virol. (2007) 88:1062-1067.
75. Laude H., Vilette D., Le Dur A., Archer F., Soulier S., Besnard N., Essalmani R., Vilotte J.L., New in vivo and ex vivo models for the experimental study of sheep scrapie: development and perspectives, C. R. Biol. (2002) 325:49-57.
76. Leblanc P., Alais S., Porto-Carreiro I., Lehmann S., Grassi J., Raposo G., Darlix J.L., Retrovirus infection strongly enhances scrapie infectivity release in cell culture, EMBO J. (2006) 25:2674-2685.
77. Lehmann S., Harris D.A., Mutant and infectious prion proteins display common biochemical properties in cultured cells, J. Biol. Chem. (1996) 271:1633-1637.
78. Leucht C., Simoneau S., Rey C., Vana K., Rieger R., Lasmezas C.I., Weiss S., The 37 kDa/67 kDa laminin receptor is required for PrP(Sc) propagation in scrapie-infected neuronal cells, EMBO Rep. (2003) 4:290-295.
79. Luhr K.M., Nordstrom E.K., Low P., Kristensson K., Cathepsin B and L are involved in degradation of prions in GT1-1 neuronal cells, Neuroreport (2004) 15:1663-1667.
80. Maas E., Geissen M., Groschup M.H., Rost R., Onodera T., Schatzl H., Vorberg I.M., Scrapie infection of prion protein-deficient cell line upon ectopic expression of mutant prion proteins, J. Biol. Chem. (2007) 282:18702-18710.
81. Magalhaes A.C., Baron G.S., Lee K.S., Steele-Mortimer O., Dorward D., Prado M.A., Caughey B., Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells, J. Neurosci. (2005) 25:5207-5216.
82. Mallucci G., Dickinson A., Linehan J., Klohn P.C., Brandner S., Collinge J., Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis, Science (2003) 302:871-874.
83. Mange A., Nishida N., Milhavet O., McMahon H.E., Casanova D., Lehmann S., Amphotericin B inhibits the generation of the scrapie isoform of the prion protein in infected cultures, J. Virol. (2000) 74:3135-3140.
84. Mange A., Crozet C., Lehmann S., Beranger F., Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin, J. Cell. Sci. (2004) 117:2411-2416.
85. Marella M., Chabry J., Neurons and astrocytes respond to prion infection by inducing microglia recruitment, J. Neurosci. (2004) 24:620-627.
86. Markovits P., Mutel V., Dianoux L., Launay J.M., Haimart M., Dormont D., Court L., Cathala F., Effects of in vitro infection of mouse glial and neuroblastoma cells with the scrapie agent, Ann. Rech. Vet. (1985) 16:111-119.
87. McKay R., Stem cells in the central nervous system, Science (1997) 276:66-71.
88. McKinley M.P., Taraboulos A., Kenaga L., Serban D., Stieber A., DeArmond S.J., Prusiner S.B., Gonatas N., Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells, Lab. Invest. (1991) 65:622-630.
89. Milhavet O., McMahon H.E., Rachidi W., Nishida N., Katamine S., Mange A., Arlotto M., Casanova D., Riondel J., Favier A., Lehmann S., Prion infection impairs the cellular response to oxidative stress, Proc. Natl. Acad. Sci. USA (2000) 97:13937-13942.
90. Milhavet O., Casanova D., Chevallier N., McKay R.D., Lehmann S., Neural stem cell model for prion propagation, Stem Cells (2006) 24:2284-2291.
91. Miyamoto K., Nakamura N., Aosasa M., Nishida N., Yokoyama T., Horiuchi H., Furusawa S., Matsuda H., Inhibition of prion propagation in scrapie-infected mouse neuroblastoma cell lines using mouse monoclonal antibodies against prion protein, Biochem. Biophys. Res. Commun. (2005) 335:197-204.
92. Morel E., Andrieu T., Casagrande F., Gauczynski S., Weiss S., Grassi J., Rousset M., Dormont D., Chambaz J., Bovine prion is endocytosed by human enterocytes via the 37 kDa/67 kDa laminin receptor, Am. J. Pathol. (2005) 167:1033-1042.
93. Moum T., Olsaker I., Hopp P., Moldal T., Valheim M., Benestad S.L., Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases, J. Gen. Virol. (2005) 86:231-235.
94. Naslavsky N., Stein R., Yanai A., Friedlander G., Taraboulos A., Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform, J. Biol. Chem. (1997) 272:6324-6331.
95. Nishida N., Harris D.A., Vilette D., Laude H., Frobert Y., Grassi J., Casanova D., Milhavet O., Lehmann S., Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein, J. Virol. (2000) 74:320-325.
96. Nishida N., Katamine S., Manuelidis L., Reciprocal interference between specific CJD and scrapie agents in neural cell cultures, Science (2005) 310:493-496.
97. Nunziante M., Gilch S., Schatzl H.M., Essential role of the prion protein N terminus in subcellular trafficking and half-life of cellular prion protein, J. Biol. Chem. (2003) 278:3726-3734.
98. Paquet S., Daude N., Courageot M.P., Chapuis J., Laude H., Vilette D., PrPC does not mediate internalization of PrPSc but is required at an early stage for de novo prion infection of Rov cells, J. Virol. (2007).
99. Paquet S., Langevin C., Chapuis J., Jackson G.S., Laude H., Vilette D., Efficient dissemination of prions through preferential transmission to nearby cells, J. Gen. Virol. (2007) 88:706-713.
100. Parizek P., Roeckl C., Weber J., Flechsig E., Aguzzi A., Raeber A.J., Similar turnover and shedding of the cellular prion protein in primary lymphoid and neuronal cells, J. Biol. Chem. (2001) 276:44627-44632.
101. Pastrana M.A., Sajnani G., Onisko B., Castilla J., Morales R., Soto C., Requena J.R., Isolation and characterization of a proteinase K-sensitive PrP(Sc) fraction, Biochemistry (2006) 45:15710-15717.
102. Peretz D., Williamson R.A., Kaneko K., Vergara J., Leclerc E., Schmitt-Ulms G., Mehlhorn I.R., Legname G., Wormald M.R., Rudd P.M., Dwek R.A., Burton D.R., Prusiner S.B., Antibodies inhibit prion propagation and clear cell cultures of prion infectivity, Nature (2001) 412:739-743.
103. Perrier V., Kaneko K., Safar J., Vergara J., Tremblay P., DeArmond S.J., Cohen F.E., Prusiner S.B., Wallace A.C., Dominant-negative inhibition of prion replication in transgenic mice, Proc. Natl. Acad. Sci. USA (2002) 99:13079-13084.
104. Perrier V., Solassol J., Crozet C., Frobert Y., Mourton-Gilles C., Grassi J., Lehmann S., Anti-PrP antibodies block PrPSc replication in prion-infected cell cultures by accelerating PrPC degradation, J. Neurochem. (2004) 89:454-463.
105. Pfeifer A., Eigenbrod S., Al-Khadra S., Hofmann A., Mitteregger G., Moser M., Bertsch U., Kretzschmar H., Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice, J. Clin. Invest. (2006) 116:3204-3210.
106. Pimpinelli F., Lehmann S., Maridonneau-Parini I., The scrapie prion protein is present in flotillin-1-positive vesicles in central- but not peripheral-derived neuronal cell lines, Eur. J. Neurosci. (2005) 21:2063-2072.
107. Poli G., Martino P.A., Villa S., Carcassola G., Giannino M.L., Dall'Ara P., Pollera C., Iussich S., Tranquillo V.M., Bareggi S., Mantegazza P., Ponti W., Evaluation of anti-prion activity of Congo Red and its derivatives in experimentally infected hamsters, Arzneimittelforschung (2004) 54:406-415.
108. Porto-Carreiro I., Fevrier B., Paquet S., Vilette D., Raposo G., Prions and exosomes: from PrPC trafficking to PrPSc propagation, Blood Cells Mol. Dis. (2005) 35:143-148.
109. Prado M.A., Alves-Silva J., Magalhaes A.C., Prado V.F., Linden R., Martins V.R., Brentani R.R., PrPC on the road: trafficking of the cellular prion protein, J. Neurochem. (2004) 88:769-781.
110. Priola S.A., Caughey B., Race R.E., Chesebro B., Heterologous PrP molecules interfere with accumulation of protease-resistant PrP in scrapie-infected murine neuroblastoma cells, J. Virol. (1994) 68:4873-4878.
111. Priola S.A., Chesebro B., A single hamster PrP amino acid blocks conversion to protease-resistant PrP in scrapie-infected mouse neuroblastoma cells, J. Virol. (1995) 69:7754-7758.
112. Priola S.A., Raines A., Caughey W.S., Porphyrin and phthalocyanine antiscrapie compounds, Science (2000) 287:1503-1506.
113. Priola S.A., Raines A., Caughey W., Prophylactic and therapeutic effects of phthalocyanine tetrasulfonate in scrapie-infected mice, J. Infect. Dis. (2003) 188:699-705.
114. Race R., The scrapie agent in vitro, Curr. Top. Microbiol. Immunol. (1991) 172:181-193.
115. Race R.E., Fadness L.H., Chesebro B., Characterization of scrapie infection in mouse neuroblastoma cells, J. Gen. Virol. (1987) 68:1391-1399.
116. Raymond G.J., Olsen E.A., Lee K.S., Raymond L.D., Bryant P.K., 3rd, Baron G.S., Caughey W.S., Kocisko D.A., McHolland L.E., Favara C., Langeveld J.P., van Zijderveld F.G., Mayer R.T., Miller M.W., Williams E.S., Caughey B., Inhibition of protease-resistant prion protein formation in a transformed deer cell line infected with chronic wasting disease, J. Virol. (2006) 80:596-604.
117. Rigter A., Bossers A., Sheep scrapie susceptibility-linked polymorphisms do not modulate the initial binding of cellular to disease-associated prion protein prior to conversion, J. Gen. Virol. (2005) 86:2627-2634.
118. Rubenstein R., Carp R.I., Callahan S.M., In vitro replication of scrapie agent in a neuronal model: infection of PC12 cells, J. Gen. Virol. (1984) 65:2191-2198.
119. Rudyk H., Vasiljevic S., Hennion R.M., Birkett C.R., Hope J., Gilbert I.H., Screening Congo Red and its analogues for their ability to prevent the formation of PrP-res in scrapie-infected cells, J. Gen. Virol. (2000) 81:1155-1164.
120. Sabuncu E., Petit S., Le Dur A., Lan Lai T., Vilotte J.L., Laude H., Vilette D., PrP polymorphisms tightly control sheep prion replication in cultured cells, J. Virol. (2003) 77:2696-2700.
121. Sabuncu E., Paquet S., Chapuis J., Moudjou M., Lai T.L., Grassi J., Baron U., Laude H., Vilette D., Prion proteins from susceptible and resistant sheep exhibit some distinct cell biological features, Biochem. Biophys. Res. Commun. (2005) 337:791-798.
122. Safar J., Wille H., Itri V., Groth D., Serban H., Torchia M., Cohen F.E., Prusiner S.B., Eight prion strains have PrP(Sc) molecules with different conformations, Nat. Med. (1998) 4:1157-1165.
123. Saunders G.C., Cawthraw S., Mountjoy S.J., Hope J., Windl O., PrP genotypes of atypical scrapie cases in Great Britain, J. Gen. Virol. (2006) 87:3141-3149.
124. Schatzl H.M., Laszlo L., Holtzman D.M., Tatzelt J., DeArmond S.J., Weiner R.I., Mobley W.C., Prusiner S.B., A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis, J. Virol. (1997) 71:8821-8831.
125. Schiffer N.W., Broadley S.A., Hirschberger T., Tavan P., Kretzschmar H.A., Giese A., Haass C., Hartl F.U., Schmid B., Identification of anti-prion compounds as efficient inhibitors of polyglutamine protein aggregation in a zebrafish model, J. Biol. Chem. (2007) 282:9195-9203.
126. Schonberger O., Horonchik L., Gabizon R., Papy-Garcia D., Barritault D., Taraboulos A., Novel heparan mimetics potently inhibit the scrapie prion protein and its endocytosis, Biochem. Biophys. Res. Commun. (2003) 312:473-479.
127. Schulz-Schaeffer W.J., Tschoke S., Kranefuss N., Drose W., Hause-Reitner D., Giese A., Groschup M.H., Kretzschmar H.A., The paraffin-embedded tissue blot detects PrP(Sc) early in the incubation time in prion diseases, Am. J. Pathol. (2000) 156:51-56.
128. Scott M.R., Kohler R., Foster D., Prusiner S.B., Chimeric prion protein expression in cultured cells and transgenic mice, Protein Sci. (1992) 1:986-997.
129. Sellarajah S., Lekishvili T., Bowring C., Thompsett A.R., Rudyk H., Birkett C.R., Brown D.R., Gilbert I.H., Synthesis of analogues of Congo Red and evaluation of their anti-prion activity, J. Med. Chem. (2004) 47:5515-5534.
130. Sigurdsson E.M., Sy M.S., Li R., Scholtzova H., Kascsak R.J., Kascsak R., Carp R., Meeker H.C., Frangione B., Wisniewski T., Anti-prion antibodies for prophylaxis following prion exposure in mice, Neurosci. Lett. (2003) 336:185-187.
131. Simons K., Ikonen E., Functional rafts in cell membranes, Nature (1997) 387:569-572.
132. Solassol J., Crozet C., Lehmann S., Prion propagation in cultured cells, Br. Med. Bull. (2003) 66:87-97.
133. Somerville R.A., Host and transmissible spongiform encephalopathy agent strain control glycosylation of PrP, J. Gen. Virol. (1999) 80:1865-1872.
134. Stahl N., Borchelt D.R., Prusiner S.B., Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol- specific phospholipase C, Biochemistry (1990) 29:5405-5412.
135. Sunyach C., Jen A., Deng J., Fitzgerald K.T., Frobert Y., Grassi J., McCaffrey M.W., Morris R., The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein, EMBO J. (2003) 22:3591-3601.
136. Taraboulos A., Serban D., Prusiner S.B., Scrapie prion proteins accumulate in the cytoplasm of persistently infected cultured cells, J. Cell. Biol. (1990) 110:2117-2132.
137. Taraboulos A., Jendroska K., Serban D., Yang S.L., DeArmond S.J., Prusiner S.B., Regional mapping of prion proteins in brain, Proc. Natl. Acad. Sci. USA (1992) 89:7620-7624.
138. Taraboulos A., Scott M., Semenov A., Avrahami D., Laszlo L., Prusiner S.B., Avraham D., Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform, J. Cell. Biol. (1995) 129:121-132.
139. Trevitt C.R., Collinge J., A systematic review of prion therapeutics in experimental models, Brain (2006) 129:2241-2265.
140. Tribouillard D., Bach S., Gug F., Desban N., Beringue V., Andrieu T., Dormont D., Galons H., Laude H., Vilette D., Blondel M., Using budding yeast to screen for anti-prion drugs, Biotechnol. J. (2006) 1:58-67.
141. Turnbull J., Powell A., Guimond S., Heparan sulfate: decoding a dynamic multifunctional cell regulator, Trends Cell. Biol. (2001) 11:75-82.
142. Tzaban S., Friedlander G., Schonberger O., Horonchik L., Yedidia Y., Shaked G., Gabizon R., Taraboulos A., Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes, Biochemistry (2002) 41:12868-12875.
143. Vella L.J., Sharples R.A., Lawson V.A., Masters C.L., Cappai R., Hill A.F., Packaging of prions into exosomes is associated with a novel pathway of PrP processing, J. Pathol. (2007) 211:582-590.
144. Vey M., Pilkuhn S., Wille H., Nixon R., DeArmond S.J., Smart E.J., Anderson R.G., Taraboulos A., Prusiner S.B., Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains, Proc. Natl. Acad. Sci. USA (1996) 93:14945-14949.
145. Vilette D., Madelaine M.F., Laude H., Establishment of astrocyte cell lines from sheep genetically susceptible to scrapie, In Vitro Cell. Dev. Biol. Anim. (2000) 36:45-49.
146. Vilette D., Andreoletti O., Archer F., Madelaine M.F., Vilotte J.L., Lehmann S., Laude H., Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein, Proc. Natl. Acad. Sci. USA (2001) 98:4055-4059.
147. Vorberg I., Raines A., Story B., Priola S.A., Susceptibility of common fibroblast cell lines to transmissible spongiform encephalopathy agents, J. Infect. Dis. (2004) 189:431-439.
148. Walmsley A.R., Zeng F., Hooper N.M., The N-terminal region of the prion protein ectodomain contains a lipid raft targeting determinant, J. Biol. Chem. (2003) 278:37241-37248.
149. Warner R.G., Hundt C., Weiss S., Turnbull J.E., Identification of the heparan sulfate binding sites in the cellular prion protein, J. Biol. Chem. (2002) 277:18421-18430.
150. Weissmann C., The state of the prion, Nat. Rev. Microbiol. (2004) 2:861-871.
151. White A.R., Enever P., Tayebi M., Mushens R., Linehan J., Brandner S., Anstee D., Collinge J., Hawke S., Monoclonal antibodies inhibit prion replication and delay the development of prion disease, Nature (2003) 422:80-83.
152. Yadavalli R., Guttmann R.P., Seward T., Centers A.P., Williamson R.A., Telling G.C., Calpain-dependent endoproteolytic cleavage of PrPSc modulates scrapie prion propagation, J. Biol. Chem. (2004) 279:21948-21956.