Physiological role of the cellular prion protein

Veterinary Research

Volumn 39, Issue 4, 2008, Pages

  Zomosa Signoret, Viviana ^a   Arnaud, Jacques Damien ^a   Fontes, Pascaline ^a   Alvarez Martinez, Maria Terresa ^a   Liautard, Jean Pierre ^a  

^a UNIV MONTPELLIER   (France)

Author keywords

Biology; Physiology; Prion; PrPC

Indexed keywords

CELL PROTEIN; CELL SURFACE PROTEIN; CLATHRIN; COPPER ION; ISOPROTEIN; PRION PROTEIN; COPPER;

APOPTOSIS; CELL MEMBRANE; CELL SURFACE; CELL TRANSPORT; CENTRAL NERVOUS SYSTEM; CIRCADIAN RHYTHM; CROSS LINKING; ENDOPLASMIC RETICULUM; ENDOSOME; GENE DELETION; GOLGI COMPLEX; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; LIPID RAFT; METAL BINDING; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRION DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SEIZURE THRESHOLD; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; T LYMPHOCYTE ACTIVATION; UPREGULATION; ANIMAL; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PRION;

MUS;

ANIMALS; CELL MEMBRANE; COPPER; MICE; PRIONS; PROTEIN ISOFORMS;

EID: 50049122656     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres:2007048     Document Type: Review

References (115)

1. Aguzzi A., Prions and the immune system: a journey through gut, spleen, and nerves, Adv. Immunol. (2003) 81:123-171.
2. Antoine N., Cesbron J.Y., Coumans B., Jolois O., Zorzi W., Heinen E., Differential expression of cellular prion protein on human blood and tonsil lymphocytes, Haematologica (2000) 85:475-480.
3. Ballerini C., Gourdain P., Bachy V., Blanchard N., Levavasseur E., Gregoire S., Fontes P., Aucouturier P., Hivroz C., Carnaud C., Functional implication of cellular prion protein in antigen-driven interactions between T cells and dendritic cells, J. Immunol. (2006) 176:7254-7262.
4. Barclay G.R., Hope J., Birkett C.R., Turner M.L., Distribution of cell-associated prion protein in normal adult blood determined by flow cytometry, Br. J. Haematol. (1999) 107:804-814.
5. Barmada S., Piccardo P., Yamaguchi K., Ghetti B., Harris D.A., GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice, Neurobiol. Dis. (2004) 16:527-537.
6. Borchelt D.R., Koliatsos V.E., Guarnieri M., Pardo C.A., Sisodia S.S., Price D.L., Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems, J. Biol. Chem. (1994) 269:14711-14714.
7. Bounhar Y., Zhang Y., Goodyer C.G., LeBlanc A., Prion protein protects human neurons against Bax-mediated apoptosis, J. Biol. Chem. (2001) 276:39145-39149.
8. Brown D.R., Qin K., Herms J.W., Madlung A., Manson J., Strome R., Fraser P.E., Kruck T., von Bohlen A., Schulz-Schaeffer W., Giese A., Westaway D., Kretzschmar H., The cellular prion protein binds copper in vivo, Nature (1997) 390:684-687.
9. Brown D.R., Wong B.S., Hafiz F., Clive C., Haswell S.J., Jones I.M., Normal prion protein has an activity like that of superoxide dismutase, Biochem. J. (1999) 344:1-5.
10. Brown D.R., Copper and prion disease, Brain Res. Bull. (2001) 55:165-173.
11. Brown K.L., Stewart K., Ritchie D.L., Mabbott N.A., Williams A., Fraser H., Morrison W.I., Bruce M.E., Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells, Nat. Med. (1999) 5:1308-1312.
12. Brunet A., Datta S.R., Greenberg M.E., Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway, Curr. Opin. Neurobiol. (2001) 11:297-305.
13. Bueler H., Fischer M., Lang Y., Bluethmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., Weissmann C., Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein, Nature (1992) 356:577-582.
14. Bueler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., Weissmann C., Mice devoid of PrP are resistant to scrapie, Cell (1993) 73:1339-1347.
15. Burthem J., Urban B., Pain A., Roberts D.J., The normal cellular prion protein is strongly expressed by myeloid dendritic cells, Blood (2001) 98:3733-3738.
16. Carleton A., Tremblay P., Vincent J.D., Lledo P.M., Dose-dependent, prion protein (PrP)-mediated facilitation of excitatory synaptic transmission in the mouse hippocampus, Pflugers Arch. (2001) 442:223-229.
17. Cashman N.R., Loertscher R., Nalbantoglu J., Shaw I., Kascsak R.J., Bolton D.C., Bendheim P.E., Cellular isoform of the scrapie agent protein participates in lymphocyte activation, Cell (1990) 61:185-192.
18. Chen Z., Lund R., Aittokallio T., Kosonen M., Nevalainen O., Lahesmaa R., Identification of novel IL-4/Stat6-regulated genes in T lymphocytes, J. Immunol. (2003) 171:3627-3635.
19. Coitinho A.S., Roesler R., Martins V.R., Brentani R.R., Izquierdo I., Cellular prion protein ablation impairs behavior as a function of age, Neuroreport (2003) 14:1375-1379.
20. Coitinho A.S., Freitas A.R., Lopes M.H., Hajj G.N., Roesler R., Walz R., Rossato J.I., Cammarota M., Izquierdo I., Martins V.R., Brentani R.R., The interaction between prion protein and laminin modulates memory consolidation, Eur. J. Neurosci. (2006) 24:3255-3264.
21. Coitinho A.S., Lopes M.H., Hajj G.N., Rossato J.I., Freitas A.R., Castro C.C., Cammarota M., Brentani R.R., Izquierdo I., Martins V.R., Short-term memory formation and long-term memory consolidation are enhanced by cellular prion association to stress-inducible protein 1, Neurobiol. Dis. (2007) 26:282-290.
22. Colling S.B., Khana M., Collinge J., Jefferys J.G., Mossy fibre reorganization in the hippocampus of prion protein null mice, Brain Res. (1997) 755:28-35.
23. Collinge J., Whittington M.A., Sidle K.C., Smith C.J., Palmer M.S., Clarke A.R., Jefferys J.G., Prion protein is necessary for normal synaptic function, Nature (1994) 370:295-297.
24. Criado J.R., Sanchez-Alavez M., Conti B., Giacchino J.L., Wills D.N., Henriksen S.J., Race R., Manson J.C., Chesebro B., Oldstone M.B., Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons, Neurobiol. Dis. (2005) 19:255-265.
25. Crozet C., Vezilier J., Delfieu V., Nishimura T., Onodera T., Casanova D., Lehmann S., Beranger F., The truncated 23-230 form of the prion protein localizes to the nuclei of inducible cell lines independently of its nuclear localization signals and is not cytotoxic, Mol. Cell. Neurosci. (2006) 32:315-323.
26. De Almeida C.J., Chiarini L.B., da Silva J.P., e Silva P.M., Martins M.A., Linden R., The cellular prion protein modulates phagocytosis and inflammatory response, J. Leukoc. Biol. (2005) 77:238-246.
27. Dodelet V.C., Cashman N.R., Prion protein expression in human leukocyte differentiation, Blood (1998) 91:1556-1561.
28. Durig J., Giese A., Schmucker U., Kretzschmar H.A., Duhrsen U., Decreased prion protein expression in human peripheral blood leucocytes from patients with paroxysmal nocturnal haemoglobinuria, Br. J. Haematol. (2001) 112:658-662.
29. Eaton S.L., Rocchi M., Gonzalez L., Hamilton S., Finlayson J., Sales J., Jeffrey M., Steele P.J., Dagleish M.P., Rodger S.M., Reid H.W., Chianini F., Immunological differences between susceptible and resistant sheep during the preclinical phase of scrapie infection, J. Gen. Virol. (2007) 88:1384-1391.
30. Flechsig E., Hegyi I., Leimeroth R., Zuniga A., Rossi D., Cozzio A., Schwarz P., Rulicke T., Gotz J., Aguzzi A., Weissmann C., Expression of truncated PrP targeted to Purkinje cells of PrP knockout mice causes Purkinje cell death and ataxia, EMBO J. (2003) 22:3095-3101.
31. Fontes P., Alvarez-Martinez M.T., Gross A., Carnaud C., Kohler S., Liautard J.P., Absence of evidence for the participation of the macrophage cellular prion protein in infection with Brucella suis, Infect. Immun. (2005) 73:6229-6236.
32. Ford M.J., Burton L.J., Morris R.J., Hall S.M., Selective expression of prion protein in peripheral tissues of the adult mouse, Neuroscience (2002) 113:177-192.
33. Fournier J.G., Escaig-Haye F., Grigoriev V., Ultrastructural localization of prion proteins: physiological and pathological implications, Microsc. Res. Tech. (2000) 50:76-88.
34. 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.
35. Golding M.C., Long C.R., Carmell M.A., Hannon G.J., Westhusin M.E., Suppression of prion protein in livestock by RNA interference, Proc. Natl. Acad. Sci. USA (2006) 103:5285-5290.
36. Graner E., Mercadante A.F., Zanata S.M., Forlenza O.V., Cabral A.L., Veiga S.S., Juliano M.A., Roesler R., Walz R., Minetti A., Izquierdo I., Martins V.R., Brentani R.R., Cellular prion protein binds laminin and mediates neuritogenesis, Brain Res. Mol. Brain Res. (2000) 76:85-92.
37. Grant S.G., O'Dell T.J., Karl K.A., Stein P.L., Soriano P., Kandel E.R., Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice, Science (1992) 258:1903-1910.
38. Hachiya N.S., Watanabe K., Sakasegawa Y., Kaneko K., Microtubules- associated intracellular localization of the NH2-terminal cellular prion protein fragment, Biochem. Biophys. Res. Commun. (2004) 313:818-823.
39. Harris D.A., True H.L., New insights into prion structure and toxicity, Neuron (2006) 50:353-357.
40. Harris E.D., Basic and clinical aspects of copper, Crit. Rev. Clin. Lab. Sci. (2003) 40:547-586.
41. Herms J., Tings T., Gall S., Madlung A., Giese A., Siebert H., Schurmann P., Windl O., Brose N., Kretzschmar H., Evidence of presynaptic location and function of the prion protein, J. Neurosci. (1999) 19:8866-8875.
42. Holada K., Vostal J.G., Different levels of prion protein (PrPc) expression on hamster, mouse and human blood cells, Br. J. Haematol. (2000) 110:472-480.
43. Horiuchi M., Yamazaki N., Ikeda T., Ishiguro N., Shinagawa M., A cellular form of prion protein (PrPC) exists in many non-neuronal tissues of sheep, J. Gen. Virol. (1995) 76:2583-2587.
44. Hugel B., Martinez M.C., Kunzelmann C., Blattler T., Aguzzi A., Freyssinet J.M., Modulation of signal transduction through the cellular prion protein is linked to its incorporation in lipid rafts, Cell. Mol. Life Sci. (2004) 61:2998-3007.
45. Kanaani J., Prusiner S.B., Diacovo J., Baekkeskov S., Legname G., Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro, J. Neurochem. (2005) 95:1373-1386.
46. Kim B.H., Lee H.G., Choi J.K., Kim J.I., Choi E.K., Carp R.I., Kim Y.S., The cellular prion protein (PrPC) prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation, Brain Res. Mol. Brain Res. (2004) 124:40-50.
47. Kurschner C., Morgan J.I., The cellular prion protein (PrP) selectively binds to Bcl-2 in the yeast two-hybrid system, Brain Res. Mol. Brain Res. (1995) 30:165-168.
48. Kurschner C., Morgan J.I., Analysis of interaction sites in homo- and heteromeric complexes containing Bcl-2 family members and the cellular prion protein, Brain Res. Mol. Brain Res. (1996) 37:249-258.
49. Kuwahara C., Takeuchi A.M., Nishimura T., Haraguchi K., Kubosaki A., Matsumoto Y., Saeki K., Matsumoto Y., Yokoyama T., Itohara S., Onodera T., Prions prevent neuronal cell-line death, Nature (1999) 400:225-226.
50. Laine J., Marc M.E., Sy M.S., Axelrad H., Cellular and subcellular morphological localization of normal prion protein in rodent cerebellum, Eur. J. Neurosci. (2001) 14:47-56.
51. Lee K.S., Linden R., Prado M.A., Brentani R.R., Martins V.R., Towards cellular receptors for prions, Rev. Med. Virol. (2003) 13:399-408.
52. Lehmann S., Metal ions and prion diseases, Curr. Opin. Chem. Biol. (2002) 6:187-192.
53. Li A., Harris D.A., Mammalian prion protein suppresses Bax-induced cell death in yeast, J. Biol. Chem. (2005) 280:17430-17434.
54. Li R., Liu D., Zanusso G., Liu T., Fayen J.D., Huang J.H., Petersen R.B., Gambetti P., Sy M.S., The expression and potential function of cellular prion protein in human lymphocytes, Cell. Immunol. (2001) 207:49-58.
55. Liu T., Li R., Wong B.S., Liu D., Pan T., Petersen R.B., Gambetti P., Sy M.S., Normal cellular prion protein is preferentially expressed on subpopulations of murine hemopoietic cells, J. Immunol. (2001) 166:3733-3742.
56. Lopes M.H., Hajj G.N., Muras A.G., Mancini G.L., Castro R.M., Ribeiro K.C., Brentani R.R., Linden R., Martins V.R., Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways, J. Neurosci. (2005) 25:11330-11339.
57. Ma J., Wollmann R., Lindquist S., Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol, Science (2002) 298:1781-1785.
58. Magalhaes A.C., Silva J.A., Lee K.S., Martins V.R., Prado V.F., Ferguson S.S., GomezM.V., Brentani R.R., Prado M.A., Endocytic intermediates involved with the intracellular trafficking of a fluorescent cellular prion protein, J. Biol. Chem. (2002) 277:33311-33318.
59. Mallucci G.R., Ratte S., Asante E.A., Linehan J., Gowland I., Jefferys J.G., Collinge J., Post-natal knock-out of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration, EMBO J. (2002) 21:202-210.
60. Manson J.C., Clarke A.R., Hooper M.L., Aitchison L., McConnell I., Hope J., 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal, Mol. Neurobiol. (1994) 8:121-127.
61. Martinez del Hoyo G., Lopez-Bravo M., Metharom P., Ardavin C., Aucouturier P., Prion protein expression by mouse dendritic cells is restricted to the nonplasmacytoid subsets and correlates with the maturation state, J. Immunol. (2006) 177:6137-6142.
62. Martins V.R., Graner E., Garcia-Abreu J., de Souza S.J., Mercadante A.F., Veiga S.S., Zanata S.M., Neto V.M., Brentani R.R., Complementary hydropathy identifies a cellular prion protein receptor, Nat. Med. (1997) 3:1376-1382.
63. Martins V.R., Brentani R.R., The biology of the cellular prion protein, Neurochem. Int. (2002) 41:353-355.
64. Mazzoni I.E., Ledebur H.C. Jr, Paramithiotis E., Cashman N., Lymphoid signal transduction mechanisms linked to cellular prion protein, Biochem. Cell Biol. (2005) 83:644-653.
65. McMahon H.E., Mange A., Nishida N., Creminon C., Casanova D., Lehmann S., Cleavage of the amino terminus of the prion protein by reactive oxygen species, J. Biol. Chem. (2001) 276:2286-2291.
66. Mironov A. Jr, Latawiec D., Wille H., Bouzamondo-Bernstein E., Legname G., Williamson R.A., Burton D., DeArmond S.J., Prusiner S.B., Peters P.J., Cytosolic prion protein in neurons, J. Neurosci. (2003) 23:7183-7193.
67. Mouillet-Richard S., Laurendeau I., Vidaud M., Kellermann O., Laplanche J.L., Prion protein and neuronal differentiation: quantitative analysis of prnp gene expression in a murine inducible neuroectodermal progenitor, Microbes Infect. (1999) 1:969-976.
68. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J.L., Lehmann S., Launay J.M., Kellermann O., Signal transduction through prion protein, Science (2000) 289:1925-1928.
69. Mouillet-Richard S., Schneider B., Pradines E., PietriM., Ermonval M., Grassi J., Richards J.G., Mutel V., Launay J.M., Kellermann O., Cellular prion protein signaling in serotonergic neuronal cells, Ann. NY Acad. Sci. (2007) 1096:106-119.
70. Moya K.L., Sales N., Hassig R., Creminon C., Grassi J., Di Giamberardino L., Immunolocalization of the cellular prion protein in normal brain, Microsc. Res. Tech. (2000) 50:58-65.
71. Moya K.L., Hassig R., Creminon C., Laffont I., Di Giamberardino L., Enhanced detection and retrograde axonal transport of PrPc in peripheral nerve, J. Neurochem. (2004) 88:155-160.
72. Negro A., Ballarin C., Bertoli A., Massimino M.L., Sorgato M.C., The metabolism and imaging in live cells of the bovine prion protein in its native form or carrying single amino acid substitutions, Mol. Cell. Neurosci. (2001) 17:521-538.
73. Nieznanski K., Podlubnaya Z.A., Nieznanska H., Prion protein inhibits microtubule assembly by inducing tubulin oligomerization, Biochem. Biophys. Res. Commun. (2006) 349:391-399.
74. Paar C., Wurm S., Pfarr W., Sonnleitner A., Wechselberger C., Prion protein resides in membrane microclusters of the immunological synapse during lymphocyte activation, Eur. J. Cell Biol. (2007).
75. Paisley D., Banks S., Selfridge J., McLennan N.F., Ritchie A.M., McEwan C., Irvine D.S., Saunders P.T., Manson J.C., Melton D.W., Male infertility and DNA damage in Doppel knockout and prion protein/ Doppel double-knockout mice, Am. J. Pathol. (2004) 164:2279-2288.
76. Paitel E., Alves da Costa C., Vilette D., Grassi J., Checler F., Overexpression of PrPc triggers caspase 3 activation: potentiation by proteasome inhibitors and blockade by anti-PrP antibodies, J. Neurochem. (2002) 83:1208-1214.
77. Paitel E., Fahraeus R., Checler F., Cellular prion protein sensitizes neurons to apoptotic stimuli through Mdm2-regulated and p53-dependent caspase 3-like activation, J. Biol. Chem. (2003) 278:10061-10066.
78. Paitel E., Sunyach C., Alves da Costa C., Bourdon J.C., Vincent B., Checler F., Primary cultured neurons devoid of cellular prion display lower responsiveness to staurosporine through the control of p53 at both transcriptional and post-transcriptional levels, J. Biol. Chem. (2004) 279:612-618.
79. Papassotiropoulos A., Wollmer M.A., Aguzzi A., Hock C., Nitsch R.M., de Quervain D.J., The prion gene is associated with human long-term memory, Hum. Mol. Genet. (2005) 14:2241-2246.
80. Petchanikow C., Saborio G.P., Anderes L., Frossard M.J., Olmedo M.I., Soto C., Biochemical and structural studies of the prion protein polymorphism, FEBS Lett. (2001) 509:451-456.
81. Peters P.J., Mironov A. Jr, Peretz D., van Donselaar E., Leclerc E., Erpel S., DeArmond S.J., Burton D.R., Williamson R.A., Vey M., Prusiner S.B., Trafficking of prion proteins through a caveolae-mediated endosomal pathway, J. Cell Biol. (2003) 162:703-717.
82. Petrakis S., Sklaviadis T., Identification of proteins with high affinity for refolded and native PrPC, Proteomics (2006) 6:6476-6484.
83. Politopoulou G., Seebach J.D., Schmugge M., Schwarz H.P., Aguzzi A., Age-related expression of the cellular prion protein in human peripheral blood leukocytes, Haematologica (2000) 85:580-587.
84. Prusiner S.B., Novel proteinaceous infectious particles cause scrapie, Science (1982) 216:136-144.
85. Prusiner S.B., Prions, Proc. Natl. Acad. Sci. USA (1998) 95:13363-13383.
86. Richt J.A., Kasinathan P., Hamir A.N., Castilla J., Sathiyaseelan T., Vargas F., Sathiyaseelan J., Wu H., Matsushita H., Koster J., Kato S., Ishida I., Soto C., Robl J.M., Kuroiwa Y., Production of cattle lacking prion protein, Nat. Biotechnol. (2007) 25:132-138.
87. Rieger R., Edenhofer F., Lasmezas C.I., Weiss S., The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells, Nat. Med. (1997) 3:1383-1388.
88. Rodolfo K., Hassig R., Moya K.L., Frobert Y., Grassi J., Di Giamberardino L., A novel cellular prion protein isoform present in rapid anterograde axonal transport, Neuroreport (1999) 10:3639-3644.
89. Roucou X., LeBlanc A.C., Cellular prion protein neuroprotective function: implications in prion diseases, J. Mol. Med. (2005) 83:3-11.
90. Sakudo A., Lee D.C., Saeki K., Nakamura Y., Inoue K., Matsumoto Y., Itohara S., Onodera T., Impairment of superoxide dismutase activation by N-terminally truncated prion protein (PrP) in PrP-deficient neuronal cell line, Biochem. Biophys. Res. Commun. (2003) 308:660-667.
91. Sales N., Rodolfo K., Hassig R., Faucheux B., Di Giamberardino L., Moya K.L., Cellular prion protein localization in rodent and primate brain, Eur. J. Neurosci. (1998) 10:2464-2471.
92. Schenkein J., Montagna P., Self management of fatal familial insomnia. Part 1: what is FFI?, MedGenMed (2006) 8:65.
93. Schneider B., Mutel V., Pietri M., Ermonval M., Mouillet-Richard S., Kellermann O., NADPH oxidase and extracellular regulated kinases 1/2 are targets of prion protein signaling in neuronal and nonneuronal cells, Proc. Natl. Acad. Sci. USA (2003) 100:13326-13331.
94. Shamsir M.S., Dalby A.R., One gene, two diseases and three conformations: molecular dynamics simulations of mutants of human prion protein at room temperature and elevated temperatures, Proteins (2005) 59:275-290.
95. Shmerling D., Hegyi I., Fischer M., Blattler T., Brandner S., Gotz J., Rulicke T., Flechsig E., Cozzio A., von Mering C., Hangartner C., Aguzzi A., Weissmann C., Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions, Cell (1998) 93:203-214.
96. Solforosi L., Criado J.R., McGavern D.B., Wirz S., Sanchez-Alavez M., Sugama S., DeGiorgio L.A., Volpe B.T., Wiseman E., Abalos G., Masliah E., Gilden D., Oldstone M.B., Conti B., Williamson R.A., Cross-linking cellular prion protein triggers neuronal apoptosis in vivo, Science (2004) 303:1514-1516.
97. Spudich A., Frigg R., Kilic E., Kilic U., Oesch B., Raeber A., Bassetti C.L., Hermann D.M., Aggravation of ischemic brain injury by prion protein deficiency: role of ERK-1/-2 and STAT-1, Neurobiol. Dis. (2005) 20:442-449.
98. Stahl N., Prusiner S.B., Prions and prion proteins, FASEB J. (1991) 5:2799-2807.
99. Steele A.D., Emsley J.G., Ozdinler P.H., Lindquist S., Macklis J.D., Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis, Proc. Natl. Acad. Sci. USA (2006) 103:3416-3421.
100. Stuermer C.A., Langhorst M.F., Wiechers M.F., Legler D.F., Von Hanwehr S.H., Guse A.H., Plattner H., PrPc capping in T cells promotes its association with the lipid raft proteins reggie-1 and reggie-2 and leads to signal transduction, FASEB J. (2004) 18:1731-1733.
101. Sugaya M., Nakamura K., Watanabe T., Asahina A., Yasaka N., Koyama Y., Kusubata M., Ushiki Y., Kimura K., Morooka A., Irie S., Yokoyama T., Inoue K., Itohara S., Tamaki K., Expression of cellular prion-related protein by murine Langerhans cells and keratinocytes, J. Dermatol. Sci. (2002) 28:126-134.
102. 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.
103. Taylor D.R., Hooper N.M., The prion protein and lipid rafts, Mol. Membr. Biol. (2006) 23:89-99.
104. Tobler I., Gaus S.E., Deboer T., Achermann P., Fischer M., Rulicke T., Moser M., Oesch B., McBride P.A., Manson J.C., Altered circadian activity rhythms and sleep in mice devoid of prion protein, Nature (1996) 380:639-642.
105. Vassallo N., Herms J., Behrens C., Krebs B., Saeki K., Onodera T., Windl O., Kretzschmar H.A., Activation of phosphatidylinositol 3-kinase by cellular prion protein and its role in cell survival, Biochem. Biophys. Res. Commun. (2005) 332:75-82.
106. 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.
107. Watarai M., Kim S., Erdenebaatar J., Makino S., Horiuchi M., Shirahata T., Sakaguchi S., Katamine S., Cellular prion protein promotes Brucella infection into macrophages, J. Exp. Med. (2003) 198:5-17.
108. Watt N.T., Taylor D.R., Gillott A., Thomas D.A., Perera W.S., Hooper N.M., Reactive oxygen species-mediated beta-cleavage of the prion protein in the cellular response to oxidative stress, J. Biol. Chem. (2005) 280:35914-35921.
109. Weise J., Crome O., Sandau R., Schulz-Schaeffer W., Bahr M., Zerr I., Upregulation of cellular prion protein (PrPc) after focal cerebral ischemia and influence of lesion severity, Neurosci. Lett. (2004) 372:146-150.
110. Weise J., Sandau R., Schwarting S., Crome O., Wrede A., Schulz-Schaeffer W., Zerr I., Bahr M., Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury, Stroke (2006) 37:1296-1300.
111. Weissmann C., Flechsig E., PrP knock-out and PrP transgenic mice in prion research, Br. Med. Bull. (2003) 66:43-60.
112. Wells M.A., Jackson G.S., Jones S., Hosszu L.L., Craven C.J., Clarke A.R., Collinge J., Waltho J.P., A reassessment of copper(II) binding in the full-length prion protein, Biochem. J. (2006) 399:435-444.
113. Westergard L., Christensen H.M., Harris D.A., The cellular prion protein (PrP(C)): its physiological function and role in disease, Biochim. Biophys. Acta (2007) 1772:629-644.
114. Zanata S.M., Lopes M.H., Mercadante A.F., Hajj G.N., Chiarini L.B., Nomizo R., Freitas A.R., Cabral A.L., Lee K.S., Juliano M.A., de Oliveira E., Jachieri S.G., Burlingame A., Huang L., Linden R., Brentani R.R., Martins V.R., Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection, EMBO J. (2002) 21:3307-3316.
115. Zhang C.C., Steele A.D., Lindquist S., Lodish H.F., Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal, Proc. Natl. Acad. Sci. USA (2006) 103:2184-2189.