Prions and their partners in crime

Nature

Volumn 443, Issue 7113, 2006, Pages 803-810

  Caughey, Byron ^a   Baron, Gerald S ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DISEASES; NUCLEIC ACIDS; PATHOLOGY; PROTEINS;

CELL FREE SYSTEMS; PHYSIOLOGICAL FUNCTIONS; TRANSMISSIBLE SPONGIFORM ENCEPHALOPATHIES (TSE);

BIOMEDICAL ENGINEERING;

PRION PROTEIN;

NUCLEIC ACID; PHYSIOLOGICAL RESPONSE; PRION DISEASE;

DISEASE COURSE; HUMAN; MEDICAL RESEARCH; MOLECULAR DYNAMICS; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW;

EID: 33750310849     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature05294     Document Type: Review

References (96)

1. Silveira, J. R., Caughey, B. & Baron, G. S. Prion protein and the molecular features of transmissible spongiform encephalopathy agents. Curr. Top. Microbiol. Immunol. 284, 1-50 (2004).
2. Hill, A. F., Antoniou, M. & Collinge, J. Protease-resistant prion protein produced in vitro lacks detectable infectivity. J. Gen. Virol. 80, 11-14 (1999).
3. Legname, G. et al. Synthetic mammalian prions. Science 305, 673-676 (2004).
4. Legname, G. et al. Strain-specified characteristics of mouse synthetic prions. Proc. Natl Acad. Sci. USA 102, 2168-2173 (2005).
5. Hsiao, K. K. et al. Serial transmission in rodents of neurodegeneration from transgenic mice expressing mutant prion protein. Proc. Natl Acad. Sci. USA 91, 9126-9130 (1994).
6. Nazor, K. E. et al. Immunodetection of disease-associated mutant PrP, which accelerates disease in GSS transgenic mice. EMBO J. 24, 2472-2480 (2005).
7. Castilla, J., Saa, P., Hetz, C. & Soto, C. In vitro generation of infectious scrapie prions. Cell 121, 195-206 (2005).
8. Deleault, N. R. et al. Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J. Biol. Chem. 280, 26873-26879 (2005).
9. Sc dependent cell-free formation of protease-resistant prion protein. EMBO J. 20, 377-386 (2001).
10. Horonchik, L. et al. Heparan sulfate is a cellular receptor for purified infectious prions. J. Biol. Chem. 280, 17062-17067 (2005).
11. Sc incorporation to cells requires endogenous glycosaminoglycan expression. J. Biol. Chem. 280, 17057-17061 (2005).
12. Kovalchuk, O. et al. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278, 40041-40049 (2003).
13. Shaked, G. M., Meiner, Z., Avraham, I., Taraboulos, A. & Gabizon, R. Reconstitution of prion infectivity from solubilized protease-resistant PrP and nonprotein components of prion rods. J. Biol. Chem. 276, 14324-14328 (2001).
14. Weissmann, C. A unified theory of prion propagation. Nature 352, 679-683 (1991).
15. Cordeiro, Y. & Silva, J. L. The hypothesis of the catalytic action of nucleic acid on the conversion of prion protein. Protein Pept. Lett. 12, 251-255 (2005).
16. Sc propagation in scrapie-infected neuronal cells. EMBO Rep. 4, 290-295 (2003).
17. Silveira, J. R. et al. The most infectious prion protein particles. Nature 437, 257-261 (2005).
18. Caughey, B. & Lansbury, P. T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298 (2003).
19. Chesebro, B. et al. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308, 1435-1439 (2005).
20. Brandner, S. et al. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379, 339-343 (1996).
21. Mallucci, G. et al. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302, 871-874 (2003).
22. Kristiansen, M. et al. Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis. J. Biol. Chem. 280, 38851-38861 (2005).
23. Hetz, C. et al. The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J. Neurosci. 25, 2793-2802 (2005).
24. Raeber, A. J. et al. Astrocyte-specific expression of hamster prion protein (PrP) renders PrP knockout mice susceptible to hamster scrapie. EMBO J. 16, 6057-6065 (1997).
25. Jeffrey, M., Goodsir, C. M., Race, R. E. & Chesebro, B. Scrapie-specific neuronal lesions are independent of neuronal PrP expression. Ann. Neurol. 55, 781-792 (2004).
26. Marella, M. et al. Pathological prion protein exposure switches on neuronal mitogenactivated protein kinase pathway resulting in microglia recruitment. J. Biol. Chem. 280, 1529-1534 (2005).
27. Harris, D. A. & True, H. L. New insights into prion structure and toxicity. Neuron 50, 353-357 (2006).
28. Hetz, C., Maundrell, K. & Soto, C. Is loss of function of the prion protein the cause of prion disorders? Trends Mol. Med. 9, 237-243 (2003).
29. Mallucci, G. & Collinge, J. Rational targeting for prion therapeutics. Nature Rev. Neurosci. 6, 23-34 (2005).
30. Chiesa, R. & Harris, D. A. Prion diseases: what is the neurotoxic molecule? Neurobiol. Dis. 8, 743-763 (2001).
31. Roucou, X. & LeBlanc, A. C. Cellular prion protein neuroprotective function: implications in prion diseases. J. Mol. Med. 83, 3-11 (2005).
32. Martins, V. R. et al. Cellular prion protein: on the road for functions. FEBS Lett. 512, 25-28 (2002).
33. Watt, N. T. & Hooper, N. M. The prion protein and neuronal zinc homeostasis. Trends Biochem. Sci. 28, 406-410 (2003).
34. Vassallo, N. & Herms, J. Cellular prion protein function in copper homeostasis and redox signalling at the synapse. J. Neurochem. 86, 538-544 (2003).
35. Santuccione, A., Sytnyk, V., Leshchyns'ka, I. & Schachner, M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J. Cell Biol. 169, 341-354 (2005).
36. Lopes, M. H. et al. Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25, 11330-11339 (2005).
37. Moya, K. L., Hassig, R., Breen, K. C., Volland, H. & Di, G. L. Axonal transport of the cellular prion protein is increased during axon regeneration. J. Neurochem. 92, 1044-1053 (2005).
38. 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. 95, 1373-1386 (2005).
39. Tobler, I. et al. Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380, 639-642 (1996).
40. Collinge, J. et al. Prion protein is necessary for normal synaptic function. Nature 370, 295-297 (1994).
41. Criado, J. R. et al. Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiol. Dis. 19, 255-265 (2005).
42. Brown, D. R. et al. The cellular prion protein binds copper in vivo. Nature 390, 684-687 (1997).
43. C by adenovirus-mediated gene targeting reduces ischemic injury in a stroke rat model. J. Neurosci. 25, 8967-8977 (2005).
44. de Almeida, C. J. et al. The cellular prion protein modulates phagocytosis and inflammatory response. J. Leukoc. Biol. 77, 238-246 (2005).
45. 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 103, 2184-2189 (2006).
46. 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 103, 3416-3421 (2006).
47. Nico, P. B. et al. Altered behavioural response to acute stress in mice lacking cellular prion protein. Behav. Brain Res. 162, 173-181 (2005).
48. Lledo, P. M., Tremblay, P., DeArmond, S. J., Prusiner, S. B. & Nicoll, R. A. Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc. Natl Acad. Sci. USA 93, 2403-2407 (1996).
49. Waggoner, D. J. et al. Brain copper content and cuproenzyme activity do not vary with prion protein expression level. J. Biol. Chem. 275, 7455-7458 (2000).
50. Brown, D. R., Schmidt, B. & Kretzschmar, H. A. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345-347 (1996).
51. Kunz, B., Sandmeier, E. & Christen, P. Neurotoxicity of prion peptide 106-126 not confirmed. FEBS Lett. 458, 65-68 (1999).
52. Ma, J., Wollmann, R. & Lindquist, S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298, 1781-1785 (2002).
53. Drisaldi, B. et al. 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. 278, 21732-21743 (2003).
54. Watarai, M. et al. Cellular prion protein promotes Brucella infection into macrophages. J. Exp. Med. 198, 5-17 (2003).
55. Fontes, P. et al. Absence of evidence for the participation of the macrophage cellular prion protein in infection with Brucella suis. Infect. Immun. 73, 6229-6236 (2005).
56. Gonzalez-Iglesias, R. et al. Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J. Mol. Biol. 319, 527-540 (2002).
57. Kocisko, D. A. et al. Potent antiscrapie activities of degenerate phosphorothioate oligonucleotides. Antimicrob. Agents Chemother. 50, 1034-1044 (2006).
58. Sc propagation in scrapie-infected neuronal cells. J. Mol. Biol. 358, 57-66 (2006).
59. Morel, E. et al. Bovine prion is endocytosed by human enterocytes via the 37 kDa/67 kDa laminin receptor. Am. J. Pathol. 167, 1033-1042 (2005).
60. Hundt, C. et al. Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J. 20, 5876-5886 (2001).
61. Leucht, C. et al. Knock-down of the 37-kDa/67-kDa laminin receptor in mouse brain by transgenic expression of specific antisense LRP RNA. Transgenic Res. 13, 81-85 (2004).
62. Kuczius, T. et al. Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding. Biol. Chem. 385, 739-747 (2004).
63. Quaglio, E., Chiesa, R. & Harris, D. A. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 276, 11432-11438 (2001).
64. Hijazi, N., Shaked, Y., Rosenmann, H., Ben-Hur, T. & Gabizon, R. Copper binding to PrPC may inhibit prion disease propagation. Brain Res. 993, 192-200 (2003).
65. Kiachopoulos, S., Heske, J., Tatzelt, J. & Winklhofer, K. F. Misfolding of the prion protein at the plasma membrane induces endocytosis, intracellular retention and degradation. Traffic. 5, 426-436 (2004).
66. Sigurdsson, E. M. et al. Copper chelation delays the onset of prion disease. J. Biol. Chem. 278, 46199-46202 (2003).
67. McKenzie, D. et al. Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273, 25545-25547 (1998).
68. Sc protease resistance and conversion-inducing activity. J. Biol. Chem. 279, 40788-40794 (2004).
69. Orem, N. R., Geoghegan, J. C., Deleault, N. R., Kascsak, R. & Supattapone, S. Copper (II) ions potently inhibit purified PrPres amplification. J. Neurochem. 96, 1409-1415 (2006).
70. Bocharova, O. V., Breydo, L., Salnikov, V. V. & Baskakov, I. V. Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787 (2005).
71. Ben-Zaken, O. et al. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278, 40041-40049 (2003).
72. Magalhaes, A. C. et al. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J. Neurosci. 25, 5207-5216 (2005).
73. Sc) into contiguous membranes. EMBO J. 21, 1031-1040 (2002).
74. Graner, E. et al. Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76, 85-92 (2000).
75. Chen, S., Mange, A., Dong, L., Lehmann, S. & Schachner, M. Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol. Cell. Neurosci. 22, 227-233 (2003).
76. Solforosi, L. et al. Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303, 1514-1516 (2004).
77. Taylor, D. R., Watt, N. T., Perera, W. S. & Hooper, N. M. Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis. J. Cell Sci. 118, 5141-5153 (2005).
78. Schneider, B. et al. NADPH oxidase and extracellular regulated kinases 1/2 are targets of prion protein signaling in neuronal and nonneuronal cells. Proc. Natl Acad. Sci. USA 100, 13326-13331 (2003).
79. Cashman, N. R. et al. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 61, 185-192 (1990).
80. Jouvin-Marche, E. et al. Overexpression of cellular prion protein induces an antioxidant environment altering T cell development in the thymus. J. Immunol. 176, 3490-3497 (2006).
81. Dodelet, V. C. & Cashman, N. R. Prion protein expression in human leukocyte differentiation. Blood 91, 1556-1561 (1998).
82. Caughey, B. & Raymond, G. J. The scrapie-associated form of PrP is made from a cell surface precursor that is both protease- and phospholipase-sensitive. J. Biol. Chem. 266, 18217-18223 (1991).
83. Borchelt, D. R., Taraboulos, A. & Prusiner, S. B. Evidence for synthesis of scrapie prion protein in the endocytic pathway. J. Biol. Chem. 267, 16188-16199 (1992).
84. Campana, V., Sarnataro, D. & Zurzolo, C. The highways and byways of prion protein trafficking. Trends Cell Biol. 15, 102-111 (2005).
85. 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. 65, 6597-6603 (1991).
86. Uehara, T. et al. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441, 513-517 (2006).
87. Fevrier, B. et al. Cells release prions in association with exosomes. Proc. Natl Acad. Sci. USA 101, 9683-9688 (2004).
88. Kocisko, D. A. et al. A porphyrin increases survival time of mice after intracerebral prion infection. Antimicrob. Agents Chemother. 50, 759-761 (2006).
89. Raymond, G. J. et al. Inhibition of protease-resistant prion protein formation in a transformed deer cell line infected with chronic wasting disease. J. Virol. 80, 596-604 (2006).
90. Cashman, N. R. & Caughey, B. Prion diseases - close to effective therapy? Nature Rev. Drug Discov. 3, 874-884 (2004).
91. Doh-ura, K. et al. Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. J. Virol. 78, 4999-5006 (2004).
92. Caughey, B. et al. Prions and spongiform encephalopathy (TSE) chemotherapeutics: a common mechanism for anti-TSE compounds? Acc. Chem. Res. 39, 646-653 (2006).
93. Caughey, B., Brown, K., Raymond, G. J., Katzenstien, G. E. & Thresher, W. Binding of the protease-sensitive form of PrP (prion protein) to sulfated glycosaminoglycan and Congo red. J. Virol. 68, 2135-2141 (1994).
94. 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. 277, 18421-18430 (2002).
95. C, in cultured cells. J. Biol. Chem. 270, 30221-30229 (1995).
96. Yin, S. et al. Prion proteins with insertion mutations have altered N-terminal conformation and increased ligand binding activity and are more susceptible to oxidative attack. J. Biol. Chem. 281, 10698-10705 (2006).