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Science 289 (5486): 1925-1928

Copyright © 2000 by the American Association for the Advancement of Science

Signal Transduction Through Prion Protein

S. Mouillet-Richard,1* M. Ermonval,1 C. Chebassier,12 J. L. Laplanche,2 S. Lehmann,3 J. M. Launay,2 O. Kellermann1

The cellular prion protein PrPc is a glycosylphosphatidylinositol-anchored cell-surface protein whose biological function is unclear. We used the murine 1C11 neuronal differentiation model to search for PrPc-dependent signal transduction through antibody-mediated cross-linking. A caveolin-1-dependent coupling of PrPc to the tyrosine kinase Fyn was observed. Clathrin might also contribute to this coupling. The ability of the 1C11 cell line to trigger PrPc-dependent Fyn activation was restricted to its fully differentiated serotonergic or noradrenergic progenies. Moreover, the signaling activity of PrPc occurred mainly at neurites. Thus, PrPc may be a signal transduction protein.

1 Différenciation Cellulaire, CNRS-Institut Pasteur, 75724 Paris Cedex 15, France.
2 CR Claude Bernard, Service de Biochimie, Hôpital Lariboisière, 75009 Paris, and Faculté de Pharmacie, 75005 Paris, France.
3 IGH du CNRS, UPR 1142, 34396 Montpellier Cedex 5, France.
*   To whom correspondence should be addressed. E-mail: srichard{at}

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Live imaging of prions reveals nascent PrPSc in cell-surface, raft-associated amyloid strings and webs.
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Prion Protein-mediated Toxicity of Amyloid-{beta} Oligomers Requires Lipid Rafts and the Transmembrane LRP1.
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Prion Protein Promotes Growth Cone Development through Reggie/Flotillin-Dependent N-Cadherin Trafficking.
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Analysis of nucleic acid chaperoning by the prion protein and its inhibition by oligonucleotides.
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Developmental influence of the cellular prion protein on the gene expression profile in mouse hippocampus.
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Physiol Genomics 43, 711-725
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Conditional Modulation of Membrane Protein Expression in Cultured Cells Mediated by Prion Protein Recognition of Short Phosphorothioate Oligodeoxynucleotides.
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Metabotropic glutamate receptors transduce signals for neurite outgrowth after binding of the prion protein to laminin {gamma}1 chain.
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Epitope-specific anti-prion antibodies upregulate apolipoprotein E and disrupt membrane cholesterol homeostasis.
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Anionic Phospholipid Interactions of the Prion Protein N Terminus Are Minimally Perturbing and Not Driven Solely by the Octapeptide Repeat Domain.
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Cellular Form of Prion Protein Inhibits Reelin-Mediated Shedding of Caspr from the Neuronal Cell Surface to Potentiate Caspr-Mediated Inhibition of Neurite Outgrowth.
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Neuron Dysfunction Is Induced by Prion Protein with an Insertional Mutation via a Fyn Kinase and Reversed by Sirtuin Activation in Caenorhabditis elegans.
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J. Neurosci. 30, 5394-5403
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Mutant Prion Protein Expression Is Associated with an Alteration of the Rab GDP Dissociation Inhibitor {alpha} (GDI)/Rab11 Pathway.
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Immunological mimicry of PrPC-PrPSc interactions: antibody-induced PrP misfolding.
L. Li, W. Guest, A. Huang, S. S. Plotkin, and N. R. Cashman (2009)
Protein Eng. Des. Sel. 22, 523-529
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p53-Dependent Transcriptional Control of Cellular Prion by Presenilins.
B. Vincent, C. Sunyach, H.-D. Orzechowski, P. St George-Hyslop, and F. Checler (2009)
J. Neurosci. 29, 6752-6760
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Cryo-Immunogold Electron Microscopy for Prions: Toward Identification of a Conversion Site.
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J. Neurosci. 28, 12489-12499
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Prions Impair Bioaminergic Functions through Serotonin- or Catecholamine-derived Neurotoxins in Neuronal Cells.
S. Mouillet-Richard, N. Nishida, E. Pradines, H. Laude, B. Schneider, C. Feraudet, J. Grassi, J.-M. Launay, S. Lehmann, and O. Kellermann (2008)
J. Biol. Chem. 283, 23782-23790
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Endocytosis of Prion Protein Is Required for ERK1/2 Signaling Induced by Stress-Inducible Protein 1.
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Implications for Creutzfeldt-Jakob Disease (CJD) in Dentistry: a Review of Current Knowledge.
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Journal of Dental Research 87, 511-519
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Manganese Binding to the Prion Protein.
M. W. Brazier, P. Davies, E. Player, F. Marken, J. H. Viles, and D. R. Brown (2008)
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Physiology of the Prion Protein.
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Physiol Rev 88, 673-728
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Cyclodextrins Inhibit Replication of Scrapie Prion Protein in Cell Culture.
M. Prior, S. Lehmann, M.-S. Sy, B. Molloy, and H. E. M. McMahon (2007)
J. Virol. 81, 11195-11207
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Prion Protein Expression Differences in Microglia and Astroglia Influence Scrapie-Induced Neurodegeneration in the Retina and Brain of Transgenic Mice.
L. Kercher, C. Favara, J. F. Striebel, R. LaCasse, and B. Chesebro (2007)
J. Virol. 81, 10340-10351
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Cellular prion protein promotes proliferation and G1/S transition of human gastric cancer cells SGC7901 and AGS.
J. Liang, Y. Pan, D. Zhang, C. Guo, Y. Shi, J. Wang, Y. Chen, X. Wang, J. Liu, X. Guo, et al. (2007)
FASEB J 21, 2247-2256
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Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins.
G. N. M. Hajj, M. H. Lopes, A. F. Mercadante, S. S. Veiga, R. B. da Silveira, T. G. Santos, K. C. B. Ribeiro, M. A. Juliano, S. G. Jacchieri, S. M. Zanata, et al. (2007)
J. Cell Sci. 120, 1915-1926
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Identification and Characterization of two Bovine Spongiform Encephalopathy cases Diagnosed in the United States.
J. A. Richt, R. A. Kunkle, D. Alt, E. M. Nicholson, A. N. Hamir, S. Czub, J. Kluge, A. J. Davis, and S. M. Hall (2007)
Journal of Veterinary Diagnostic Investigation 19, 142-154
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Lethal recessive myelin toxicity of prion protein lacking its central domain.
F. Baumann, M. Tolnay, C. Brabeck, J. Pahnke, U. Kloz, H. H. Niemann, M. Heikenwalder, T. Rulicke, A. Burkle, and A. Aguzzi (2007)
EMBO J. 26, 538-547
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The C-terminal Products of Cellular Prion Protein Processing, C1 and C2, Exert Distinct Influence on p53-dependent Staurosporine-induced Caspase-3 Activation.
C. Sunyach, M. A. Cisse, C. A. da Costa, B. Vincent, and F. Checler (2007)
J. Biol. Chem. 282, 1956-1963
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Junctional expression of the prion protein PrPC by brain endothelial cells: a role in trans-endothelial migration of human monocytes.
P. Viegas, N. Chaverot, H. Enslen, N. Perriere, P.-O. Couraud, and S. Cazaubon (2006)
J. Cell Sci. 119, 4634-4643
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Prion Protein Expression by Mouse Dendritic Cells Is Restricted to the Nonplasmacytoid Subsets and Correlates with the Maturation State.
G. Martinez del Hoyo, M. Lopez-Bravo, P. Metharom, C. Ardavin, and P. Aucouturier (2006)
J. Immunol. 177, 6137-6142
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Overstimulation of PrPC Signaling Pathways by Prion Peptide 106-126 Causes Oxidative Injury of Bioaminergic Neuronal Cells.
M. Pietri, A. Caprini, S. Mouillet-Richard, E. Pradines, M. Ermonval, J. Grassi, O. Kellermann, and B. Schneider (2006)
J. Biol. Chem. 281, 28470-28479
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Cellular prion protein promotes invasion and metastasis of gastric cancer.
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FASEB J 20, 1886-1888
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Functional Implication of Cellular Prion Protein in Antigen-Driven Interactions between T Cells and Dendritic Cells.
C. Ballerini, P. Gourdain, V. Bachy, N. Blanchard, E. Levavasseur, S. Gregoire, P. Fontes, P. Aucouturier, C. Hivroz, and C. Carnaud (2006)
J. Immunol. 176, 7254-7262
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Deletion of Cellular Prion Protein Results in Reduced Akt Activation, Enhanced Postischemic Caspase-3 Activation, and Exacerbation of Ischemic Brain Injury.
J. Weise, R. Sandau, S. Schwarting, O. Crome, A. Wrede, W. Schulz-Schaeffer, I. Zerr, and M. Bahr (2006)
Stroke 37, 1296-1300
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Overexpression of Cellular Prion Protein Induces an Antioxidant Environment Altering T Cell Development in the Thymus.
E. Jouvin-Marche, V. Attuil-Audenis, C. Aude-Garcia, W. Rachidi, M. Zabel, V. Podevin-Dimster, C. Siret, C. Huber, M. Martinic, J. Riondel, et al. (2006)
J. Immunol. 176, 3490-3497
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Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal.
C. C. Zhang, A. D. Steele, S. Lindquist, and H. F. Lodish (2006)
PNAS 103, 2184-2189
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Interaction of Cellular Prion and Stress-Inducible Protein 1 Promotes Neuritogenesis and Neuroprotection by Distinct Signaling Pathways.
M. H. Lopes, G. N. M. Hajj, A. G. Muras, G. L. Mancini, R. M. P. S. Castro, K. C. B. Ribeiro, R. R. Brentani, R. Linden, and V. R. Martins (2005)
J. Neurosci. 25, 11330-11339
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Charged bipolar suramin derivatives induce aggregation of the prion protein at the cell surface and inhibit PrPSc replication.
M. Nunziante, C. Kehler, E. Maas, M. U. Kassack, M. Groschup, and H. M. Schatzl (2005)
J. Cell Sci. 118, 4959-4973
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High Incidence of Scrapie Induced by Repeated Injections of Subinfectious Prion Doses.
C. Jacquemot, C. Cuche, D. Dormont, and F. Lazarini (2005)
J. Virol. 79, 8904-8908
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Biological and Biochemical Characteristics of Prion Strains Conserved in Persistently Infected Cell Cultures.
K. Arima, N. Nishida, S. Sakaguchi, K. Shigematsu, R. Atarashi, N. Yamaguchi, D. Yoshikawa, J. Yoon, K. Watanabe, N. Kobayashi, et al. (2005)
J. Virol. 79, 7104-7112
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Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth.
A. Santuccione, V. Sytnyk, I. Leshchyns'ka, and M. Schachner (2005)
J. Cell Biol. 169, 341-354
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A Transmembrane Form of the Prion Protein Is Localized in the Golgi Apparatus of Neurons.
R. S. Stewart and D. A. Harris (2005)
J. Biol. Chem. 280, 15855-15864
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Modulation of Serotonergic Receptor Signaling and Cross-talk by Prion Protein.
S. Mouillet-Richard, M. Pietri, B. Schneider, C. Vidal, V. Mutel, J.-M. Launay, and O. Kellermann (2005)
J. Biol. Chem. 280, 4592-4601
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The cellular prion protein modulates phagocytosis and inflammatory response.
C. J. G. de Almeida, L. B. Chiarini, J. P. da Silva, P. M. R. e Silva, M. A. Martins, and R. Linden (2005)
J. Leukoc. Biol. 77, 238-246
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Prion-associated Increases in Src-family Kinases.
R. R. Nixon (2005)
J. Biol. Chem. 280, 2455-2462
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The Tyrosine Kinase Inhibitor STI571 Induces Cellular Clearance of PrPSc in Prion-infected Cells.
A. Ertmer, S. Gilch, S.-W. Yun, E. Flechsig, B. Klebl, M. Stein-Gerlach, M. A. Klein, and H. M. Schatzl (2004)
J. Biol. Chem. 279, 41918-41927
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Phospholipase A2 Inhibitors or Platelet-activating Factor Antagonists Prevent Prion Replication.
C. Bate, S. Reid, and A. Williams (2004)
J. Biol. Chem. 279, 36405-36411
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Cross-Linking Cellular Prion Protein Triggers Neuronal Apoptosis in Vivo.
L. Solforosi, J. R. Criado, D. B. McGavern, S. Wirz, M. Sanchez-Alavez, S. Sugama, L. A. DeGiorgio, B. T. Volpe, E. Wiseman, G. Abalos, et al. (2004)
Science 303, 1514-1516
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Quantitative Analysis of Prion-Protein Degradation by Constitutive and Immuno-20S Proteasomes Indicates Differences Correlated with Disease Susceptibility.
S. Tenzer, L. Stoltze, B. Schonfisch, J. Dengjel, M. Muller, S. Stevanovic, H.-G. Rammensee, and H. Schild (2004)
J. Immunol. 172, 1083-1091
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The Cellular Prion Protein PrPc Is Expressed in Human Enterocytes in Cell-Cell Junctional Domains.
E. Morel, S. Fouquet, D. Chateau, L. Yvernault, Y. Frobert, M. Pincon-Raymond, J. Chambaz, T. Pillot, and M. Rousset (2004)
J. Biol. Chem. 279, 1499-1505
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NADPH oxidase and extracellular regulated kinases 1/2 are targets of prion protein signaling in neuronal and nonneuronal cells.
B. Schneider, V. Mutel, M. Pietri, M. Ermonval, S. Mouillet-Richard, and O. Kellermann (2003)
PNAS 100, 13326-13331
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Prion, Amyloid {beta}-derived Cu(II) Ions, or Free Zn(II) Ions Support S-Nitroso-dependent Autocleavage of Glypican-1 Heparan Sulfate.
K. Mani, F. Cheng, B. Havsmark, M. Jonsson, M. Belting, and L.-A. Fransson (2003)
J. Biol. Chem. 278, 38956-38965
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Trafficking of prion proteins through a caveolae-mediated endosomal pathway.
P. J. Peters, A. Mironov Jr., D. Peretz, E. van Donselaar, E. Leclerc, S. Erpel, S. J. DeArmond, D. R. Burton, R. A. Williamson, M. Vey, et al. (2003)
J. Cell Biol. 162, 703-717
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Cytosolic Prion Protein in Neurons.
A. Mironov Jr, D. Latawiec, H. Wille, E. Bouzamondo-Bernstein, G. Legname, R. A. Williamson, D. Burton, S. J. DeArmond, S. B. Prusiner, and P. J. Peters (2003)
J. Neurosci. 23, 7183-7193
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Expression of truncated PrP targeted to Purkinje cells of PrP knockout mice causes Purkinje cell death and ataxia.
E. Flechsig, I. Hegyi, R. Leimeroth, A. Zuniga, D. Rossi, A. Cozzio, P. Schwarz, T. Rulicke, J. Gotz, A. Aguzzi, et al. (2003)
EMBO J. 22, 3095-3101
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Putative functions of PrPC.
C. I. Lasmezas (2003)
Br. Med. Bull. 66, 61-70
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Trafficking, turnover and membrane topology of PrP: Protein function in prion disease.
D. A Harris (2003)
Br. Med. Bull. 66, 71-85
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Determinants of the in Vivo Folding of the Prion Protein. A BIPARTITE FUNCTION OF HELIX 1 IN FOLDING AND AGGREGATION.
K. F. Winklhofer, J. Heske, U. Heller, A. Reintjes, W. Muranyi, I. Moarefi, and J. Tatzelt (2003)
J. Biol. Chem. 278, 14961-14970
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Cellular Prion Protein Sensitizes Neurons to Apoptotic Stimuli through Mdm2-regulated and p53-dependent Caspase 3-like Activation.
E. Paitel, R. Fahraeus, and F. Checler (2003)
J. Biol. Chem. 278, 10061-10066
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The PrP-like Protein Doppel Binds Copper.
K. Qin, J. Coomaraswamy, P. Mastrangelo, Y. Yang, S. Lugowski, C. Petromilli, S. B. Prusiner, P. E. Fraser, J. M. Goldberg, A. Chakrabartty, et al. (2003)
J. Biol. Chem. 278, 8888-8896
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Expression of Prion Protein Increases Cellular Copper Binding and Antioxidant Enzyme Activities but Not Copper Delivery.
W. Rachidi, D. Vilette, P. Guiraud, M. Arlotto, J. Riondel, H. Laude, S. Lehmann, and A. Favier (2003)
J. Biol. Chem. 278, 9064-9072
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Molecular Evolution of the Mammalian Prion Protein.
T. van Rheede, M. M. W. Smolenaars, O. Madsen, and W. W. de Jong (2003)
Mol. Biol. Evol. 20, 111-121
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Prion and doppel proteins bind to granule cells of the cerebellum.
G. Legname, P. Nelken, Z. Guan, Z. F. Kanyo, S. J. DeArmond, and S. B. Prusiner (2002)
PNAS 99, 16285-16290
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Protein Conformation and Diagnostic Tests: The Prion Protein.
B. J. Bennion and V. Daggett (2002)
Clin. Chem. 48, 2105-2114
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Intercellular Transfer of the Cellular Prion Protein.
T. Liu, R. Li, T. Pan, D. Liu, R. B. Petersen, B.-S. Wong, P. Gambetti, and M. S. Sy (2002)
J. Biol. Chem. 277, 47671-47678
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Recombinant human prion protein mutants huPrP D178N/M129 (FFI) and huPrP+9OR (fCJD) reveal proteinase K resistance.
S. Gauczynski, S. Krasemann, W. Bodemer, and S. Weiss (2002)
J. Cell Sci. 115, 4025-4036
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The Human "Prion-like" Protein Doppel Is Expressed in Both Sertoli Cells and Spermatozoa.
K. Peoc'h, C. Serres, Y. Frobert, C. Martin, S. Lehmann, S. Chasseigneaux, V. Sazdovitch, J. Grassi, P. Jouannet, J.-M. Launay, et al. (2002)
J. Biol. Chem. 277, 43071-43078
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Endocytic Intermediates Involved with the Intracellular Trafficking of a Fluorescent Cellular Prion Protein.
A. C. Magalhaes, J. A. Silva, K. S. Lee, V. R. Martins, V. F. Prado, S. S. G. Ferguson, M. V. Gomez, R. R. Brentani, and M. A. M. Prado (2002)
J. Biol. Chem. 277, 33311-33318
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Prion Protein Is Secreted in Soluble Forms in the Epididymal Fluid and Proteolytically Processed and Transported in Seminal Plasma.
J.-L. Gatti, S. Metayer, M. Moudjou, O. Andreoletti, F. Lantier, J.-L. Dacheux, and P. Sarradin (2002)
Biol Reprod 67, 393-400
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Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection.
S. M. Zanata, M. H. Lopes, A. F. Mercadante, G. N. M. Hajj, L. B. Chiarini, R. Nomizo, A. R. O. Freitas, A. L. B. Cabral, K. S. Lee, M. A. Juliano, et al. (2002)
EMBO J. 21, 3307-3316
   Abstract »    Full Text »    PDF »
Cellular prion protein transduces neuroprotective signals.
L. B. Chiarini, A. R. O. Freitas, S. M. Zanata, R. R. Brentani, V. R. Martins, and R. Linden (2002)
EMBO J. 21, 3317-3326
   Abstract »    Full Text »    PDF »
Mutant prion protein acquires resistance to protease in mouse neuroblastoma cells.
C. Wegner, A. Romer, R. Schmalzbauer, H. Lorenz, O. Windl, and H. A. Kretzschmar (2002)
J. Gen. Virol. 83, 1237-1245
   Abstract »    Full Text »    PDF »
Cutting Edge: Recruitment of the Ancestral fyn Gene During Emergence of the Adaptive Immune System.
C. Picard, A. Gilles, P. Pontarotti, D. Olive, and Y. Collette (2002)
J. Immunol. 168, 2595-2598
   Abstract »    Full Text »    PDF »
PrPc Expression Influences the Establishment of Herpes Simplex Virus Type 1 Latency.
A. M. Thackray and R. Bujdoso (2002)
J. Virol. 76, 2498-2509
   Abstract »    Full Text »    PDF »
Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration.
G. R. Mallucci, S. Ratte, E. A. Asante, J. Linehan, I. Gowland, J. G. R. Jefferys, and J. Collinge (2002)
EMBO J. 21, 202-210
   Abstract »    Full Text »    PDF »
The normal cellular prion protein is strongly expressed by myeloid dendritic cells.
J. Burthem, B. Urban, A. Pain, and D. J. Roberts (2001)
Blood 98, 3733-3738
   Abstract »    Full Text »    PDF »
Prion Protein Fragment PrP-(106-126) Induces Apoptosis via Mitochondrial Disruption in Human Neuronal SH-SY5Y Cells.
C. N. O'Donovan, D. Tobin, and T. G. Cotter (2001)
J. Biol. Chem. 276, 43516-43523
   Abstract »    Full Text »    PDF »
Deletion of {beta}-Strand and {alpha}-Helix Secondary Structure in Normal Prion Protein Inhibits Formation of Its Protease-Resistant Isoform.
I. Vorberg, K. Chan, and S. A. Priola (2001)
J. Virol. 75, 10024-10032
   Abstract »    Full Text »    PDF »
The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein.
S. Gauczynski, J.-M. Peyrin, S. Haik, C. Leucht, C. Hundt, R. Rieger, S. Krasemann, J.-P. Deslys, D. Dormont, C. I. Lasmezas, et al. (2001)
EMBO J. 20, 5863-5875
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Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor.
C. Hundt, J.-M. Peyrin, S. Haik, S. Gauczynski, C. Leucht, R. Rieger, M. L. Riley, J.-P. Deslys, D. Dormont, C. I. Lasmezas, et al. (2001)
EMBO J. 20, 5876-5886
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Prion Protein Protects Human Neurons against Bax-mediated Apoptosis.
Y. Bounhar, Y. Zhang, C. G. Goodyer, and A. LeBlanc (2001)
J. Biol. Chem. 276, 39145-39149
   Abstract »    Full Text »    PDF »
Prion protein: Evolution caught en route.
P. Tompa, G. E. Tusnady, M. Cserzo, and I. Simon (2001)
PNAS 98, 4431-4436
   Abstract »    Full Text »    PDF »
Prion proteins and the gut: une liaison dangereuse?.
A N SHMAKOV and S GHOSH (2001)
Gut 48, 443-447
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Mapping the early steps in the pH-induced conformational conversion of the prion protein.
D. O. V. Alonso, S. J. DeArmond, F. E. Cohen, and V. Daggett (2001)
PNAS 98, 2985-2989
   Abstract »    Full Text »    PDF »
Two different neurodegenerative diseases caused by proteins with similar structures.
H. Mo, R. C. Moore, F. E. Cohen, D. Westaway, S. B. Prusiner, P. E. Wright, and H. J. Dyson (2001)
PNAS 98, 2352-2357
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Cleavage of the Amino Terminus of the Prion Protein by Reactive Oxygen Species.
H. E. M. McMahon, A. Mange, N. Nishida, C. Creminon, D. Casanova, and S. Lehmann (2001)
J. Biol. Chem. 276, 2286-2291
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The Prion Protein Has RNA Binding and Chaperoning Properties Characteristic of Nucleocapsid Protein NCp7 of HIV-1.
C. Gabus, E. Derrington, P. Leblanc, J. Chnaiderman, D. Dormont, W. Swietnicki, M. Morillas, W. K. Surewicz, D. Marc, P. Nandi, et al. (2001)
J. Biol. Chem. 276, 19301-19309
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Addition of a Glycophosphatidylinositol to Acetylcholinesterase. PROCESSING, DEGRADATION, AND SECRETION.
F. Coussen, A. Ayon, A. Le Goff, J. Leroy, J. Massoulie, and S. Bon (2001)
J. Biol. Chem. 276, 27881-27892
   Abstract »    Full Text »    PDF »

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