A deleted prion protein that is neurotoxic in vivo is localized normally in cultured cells

Journal of Neurochemistry

Volumn 108, Issue 1, 2009, Pages 44-56

  Christensen, Heather M ^a   Harris, David A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Neurodegeneration; Neurotoxic; Polarized sorting; Prion

Indexed keywords

AMINO ACID; PRION PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL SURFACE; CONTROLLED STUDY; EPITHELIUM CELL; GENE DELETION; HUMAN; HUMAN CELL; LIPID RAFT; MOUSE; NERVE CELL; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; CELL LINE, TRANSFORMED; CRICETINAE; DOGS; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; NEUROBLASTOMA; PRIONS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; TRANSFECTION;

ANIMALIA; MUS;

EID: 57249111813     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05719.x     Document Type: Article

References (63)

1. Barmada S., Piccardo P., Yamaguchi K., Ghetti B. Harris D. A. (2004) GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice. Neurobiol. Dis. 16, 527 537.
2. Baumann F., Tolnay M., Brabeck C. et al. (2007) Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J. 26, 538 547.
3. Bolton D. C., Seligman S. J., Bablanian G., Windsor D., Scala L. J., Kim K. S., Chen C. M., Kascsak R. J. Bendheim P. E. (1991) Molecular location of a species-specific epitope on the hamster scrapie agent protein. J. Virol. 65, 3667 3675.
4. Bradke F. Dotti C. G. (1998) Membrane traffic in polarized neurons. Biochim. Biophys. Acta 1404, 245 258.
5. Brandner S., Isenmann S., Raeber A., Fischer M., Sailer A., Kobayashi Y., Marino S., Weissmann C. Aguzzi A. (1996) Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379, 339 343.
6. Büeler H., Fischer M., Lang Y., Fluethmann H., Lipp H.-P., DeArmond S. J., Prusiner S. B., Aguet M. Weissmann C. (1992) Normal development and behavior of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577 582.
7. Büeler H., Aguzzi A., Sailer A., Greiner R. A., Autenried P., Aguet M. Weissmann C. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339 1347.
8. Chen S., Mange A., Dong L., Lehmann S. Schachner M. (2003) Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol. Cell. Neurosci. 22, 227 233.
9. Chesebro B., Trifilo M., Race R. et al. (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308, 1435 1439.
10. Chiesa R. Harris D. A. (2001) Prion diseases: what is the neurotoxic molecule? Neurobiol. Dis. 8, 743 763.
11. Chiesa R., Piccardo P., Ghetti B. Harris D. A. (1998) Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21, 1339 1351.
12. De Keukeleire B., Donadio S., Micoud J., Lechardeur D. Benharouga M. (2007) Human cellular prion protein hPrPC is sorted to the apical membrane of epithelial cells. Biochem. Biophys. Res. Commun. 354, 949 954.
13. C offset pro-apoptotic activity of the Doppel helix B/B′ region. J. Biol. Chem. 279, 55443 55454.
14. Fivaz M., Vilbois F., Thurnheer S., Pasquali C., Abrami L., Bickel P. E., Parton R. G. van der Goot F. G. (2002) Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21, 3989 4000.
15. C depends on cholesterol- sphingomyelin-enriched membrane domains and is developmentally regulated in hippocampal neurons. Mol. Cell. Neurosci. 30, 304 315.
16. Gorodinsky A. Harris D. A. (1995) Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129, 619 627.
17. Goslin K. Banker G. (1991) Rat hippocampal neurons in low-density culture, in Culturing Nerve Cells (Banker G. Goslin K., eds pp. 251 281. MIT Press, Cambridge.
18. Harris D. A. (2003) Trafficking, turnover and membrane topology of PrP. Br. Med. Bull. 66, 71 85.
19. Harris D. A. True H. L. (2006) New insights into prion structure and toxicity. Neuron 50, 353 357.
20. Ivanova L., Barmada S., Kummer T. Harris D. A. (2001) Mutant prion proteins are partially retained in the endoplasmic reticulum. J. Biol. Chem. 276, 42409 42421.
21. Sc)-specific epitope defined by a monoclonal antibody. Nature 390, 74 77.
22. Kwiatkowska K., Frey J. Sobota A. (2003) Phosphorylation of FcgammaRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J. Cell Sci. 116, 537 550.
23. Lehmann S. Harris D. A. (1995) A mutant prion protein displays an aberrant membrane association when expressed in cultured cells. J. Biol. Chem. 270, 24589 24597.
24. Li A., Sakaguchi S., Atarashi R., Roy B. C., Nakaoke R., Arima K., Okimura N., Kopacek J. Shigematsu K. (2000) Identification of a novel gene encoding a PrP-like protein expressed as chimeric transcripts fused to PrP exon 1/2 in ataxic mouse line with a disrupted PrP gene. Cell. Mol. Neurobiol. 20, 553 567.
25. Li A., Christensen H. M., Stewart L. R., Roth K. A., Chiesa R. Harris D. A. (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J. 26, 548 558.
26. 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. (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25, 11330 11339.
27. Mallucci G., Dickinson A., Linehan J., Klohn P. C., Brandner S. Collinge J. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302, 871 874.
28. Matucci A., Zanusso G., Gelati M. et al. (2005) Analysis of mammalian scrapie protein by novel monoclonal antibodies recognizing distinct prion protein glycoforms: an immunoblot and immunohistochemical study at the light and electron microscopic levels. Brain Res. Bull. 65, 155 162.
29. Moore R. C., Lee I. Y., Silverman G. L. et al. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein Doppel. J. Mol. Biol. 292, 797 817.
30. Morel E., Fouquet S., Chateau D., Yvernault L., Frobert Y., Pincon-Raymond M., Chambaz J., Pillot T. Rousset M. (2004) The cellular prion protein PrPc is expressed in human enterocytes in cell-cell junctional domains. J. Biol. Chem. 279, 1499 1505.
31. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J. L., Lehmann S., Launay J. M. Kellermann O. (2000) Signal transduction through prion protein. Science 289, 1925 1928.
32. Mouillet-Richard S., Pietri M., Schneider B., Vidal C., Mutel V., Launay J. M. Kellermann O. (2005) Modulation of serotonergic receptor signaling and cross-talk by prion protein. J. Biol. Chem. 280, 4592 4601.
33. Naslavsky N., Stein R., Yanai A., Friedlander G. Taraboulos A. (1996) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272, 6324 6331.
34. Nishida N., Tremblay P., Sugimoto T. et al. (1999) A mouse prion protein transgene rescues mice deficient for the prion protein gene from Purkinje cell degeneration and demyelination. Lab. Invest. 79, 689 697.
35. Ojakian G. K. Schwimmer R. (1988) The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells. J. Cell Biol. 107, 2377 2387.
36. Paladino S., Pocard T., Catino M. A. Zurzolo C. (2006) GPI-anchored proteins are directly targeted to the apical surface in fully polarized MDCK cells. J. Cell Biol. 172, 1023 1034.
37. Paladino S., Sarnataro D., Tivodar S. Zurzolo C. (2007) Oligomerization is a specific requirement for apical sorting of glycosyl-phosphatidylinositol- anchored proteins but not for non-raft-associated apical proteins. Traffic 8, 251 258.
38. Pang S., Urquhart P. Hooper N. M. (2004) N-glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI-anchored protein in polarised epithelial cells. J. Cell Sci. 117, 5079 5086.
39. Pankiewicz J., Prelli F., Sy M. S. et al. (2006) Clearance and prevention of prion infection in cell culture by anti-PrP antibodies. Eur. J. Neurosci. 23, 2635 2647.
40. Paquet S., Sabuncu E., Delaunay J. L., Laude H. Vilette D. (2004) Prion infection of epithelial Rov cells is a polarized event. J. Virol. 78, 7148 7152.
41. Pignatelli M., Cortes-Canteli M., Santos A. Perez-Castillo A. (1999) Involvement of the NGFI-A gene in the differentiation of neuroblastoma cells. FEBS Lett. 461, 37 42.
42. Potter B. A., Hughey R. P. Weisz O. A. (2006) Role of N- and O-glycans in polarized biosynthetic sorting. Am. J. Physiol. Cell Physiol. 290, C1 C10.
43. Prusiner S. B. (2004) Prion Biology and Diseases, pp. 1050. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Rossi D., Cozzio A., Flechsig E., Klein M. A., Rülicke T., Aguzzi A. Weissmann C. (2001) Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J. 20, 694 702.
45. Sakaguchi S., Katamine S., Nishida N. et al. (1996) Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380, 528 531.
46. C is sorted to the basolateral membrane of epithelial cells independently of its association with rafts. Traffic 3, 810 821.
47. Schubert D., Humphreys S., Baroni C. Cohn M. (1969) In vitro differentiation of a mouse neuroblastoma. Proc. Natl Acad. Sci. USA 64, 316 323.
48. Schubert D., Humphreys S., Jacob F. De Vitry F. (1971) Induced differentiation of a neuroblastoma. Dev. Biol. 25, 514 546.
49. Shmerling D., Hegyi I., Fischer M. et al. (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93, 203 214.
50. Solforosi L., Criado J. R., McGavern D. B. et al. (2004) Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303, 1514 1516.
51. Stewart R. S. Harris D. A. (2003) Mutational analysis of topological determinants in prion protein (PrP) and measurement of transmembrane and cytosolic PrP during prion infection. J. Biol. Chem. 278, 45960 45968.
52. Stewart R. S. Harris D. A. (2005) A transmembrane form of the prion protein is localized in the Golgi apparatus of neurons. J. Biol. Chem. 280, 15855 15864.
53. Stewart R. S., Drisaldi B. Harris D. A. (2001) A transmembrane form of the prion protein contains an uncleaved signal peptide and is retained in the endoplasmic reticulum. Mol. Biol. Cell 12, 881 889.
54. Stewart R. S., Piccardo P., Ghetti B. Harris D. A. (2005) Neurodegenerative illness in transgenic mice expressing a transmembrane form of the prion protein. J. Neurosci. 25, 3469 3477.
55. Taraboulos A., Raeber A. J., Borchelt D. R., Serban D. Prusiner S. B. (1992) Synthesis and trafficking of prion proteins in cultured cells. Mol. Biol. Cell 3, 851 863.
56. Taylor D. R., Watt N. T., Perera W. S. Hooper N. M. (2005) 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.
57. Uelhoff A., Tatzelt J., Aguzzi A., Winklhofer K. F. Haass C. (2005) A pathogenic PrP mutation and Doppel interfere with polarized sorting of the prion protein. J. Biol. Chem. 280, 5137 5140.
58. Vassallo N., Herms J., Behrens C., Krebs B., Saeki K., Onodera T., Windl O. Kretzschmar H. A. (2005) Activation of phosphatidylinositol 3-kinase by cellular prion protein and its role in cell survival. Biochem. Biophys. Res. Commun. 332, 75 82.
59. Viegas P., Chaverot N., Enslen H., Perriere N., Couraud P. O. Cazaubon S. (2006) Junctional expression of the prion protein PrPC by brain endothelial cells: a role in trans-endothelial migration of human monocytes. J. Cell Sci. 119, 4634 4643.
60. Wang Y. P., Wang Z. F., Zhang Y. C., Tian Q. Wang J. Z. (2004) Effect of amyloid peptides on serum withdrawal-induced cell differentiation and cell viability. Cell Res. 14, 467 472.
61. Watts J. C., Drisaldi B., Ng V. et al. (2007) The CNS glycoprotein Shadoo has PrP(C)-like protective properties and displays reduced levels in prion infections. EMBO J. 26, 4038 4050.
62. Weise J., Sandau R., Schwarting S., Crome O., Wrede A., Schulz-Schaeffer W., Zerr I. Bahr M. (2006) Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury. Stroke 37, 1296 1300.
63. Zanata S. M., Lopes M. H., Mercadante A. F. et al. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307 3316.