GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice

Neurobiology of Disease

Volumn 16, Issue 3, 2004, Pages 527-537

  Barmada, Sami ^a   Piccardo, Pedro ^b,c   Yamaguchi, Keiji ^b   Ghetti, Bernardino ^b   Harris, David A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

Brain; Golgi apparatus; Prion

Indexed keywords

GLYCOLIPID; GLYCOSYLATED PROTEIN; GREEN FLUORESCENT PROTEIN; PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; GOLGI COMPLEX; MOUSE; NERVE CELL; NERVE DEGENERATION; NERVE FIBER; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE; TRANSGENIC MOUSE;

ANIMALS; AXONS; BRAIN; CEREBELLUM; DISEASE MODELS, ANIMAL; GLYCOSYLATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MUTAGENESIS, INSERTIONAL; NEOCORTEX; NERVE DEGENERATION; PHENOTYPE; PRESYNAPTIC TERMINALS; PRION DISEASES; PRIONS;

EID: 3242661985     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.05.005     Document Type: Article

References (56)

1. Beringue V., Mallinson G., Kaisar M., Tayebi M., Sattar Z., Jackson G., Anstee D., Collinge J., Hawke S. Regional heterogeneity of cellular prion protein isoforms in the mouse brain. Brain. 126:2003;2065-2073
2. 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. Molecular location of a species-specific epitope on the hamster scrapie agent protein. J. Virol. 65:1991;3667-3675
3. 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. 269:1994;14711-14714
4. Borchelt D.R., Davis J., Fischer M., Lee M.K., Slunt H.H., Ratovitsky T., Regard J., Copeland N.G., Jenkins N.A., Sisodia S.S., Price D.L. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal.: Biomol. Eng. 13:1996;159-163
5. Büeler H., Fischer M., Lang Y., Fluethmann H., Lipp H.-P., DeArmond S.J., Prusiner S.B., Aguet M., Weissmann C. Normal development and behavior of mice lacking the neuronal cell-surface PrP protein. Nature. 356:1992;577-582
6. Chiarini L.B., Freitas A.R., Zanata S.M., Brentani R.R., Martins V.R., Linden R. Cellular prion protein transduces neuroprotective signals. EMBO J. 21:2002;3317-3326
7. Chiesa R., Piccardo P., Ghetti B., Harris D.A. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron. 21:1998;1339-1351
8. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24:2001;519-550
9. Courtoy P.J., Picton D.H., Farquhar M.G. Resolution and limitations of the immunoperoxidase procedure in the localization of extracellular matrix antigens. J. Histochem. Cytochem. 31:1983;945-951
10. Dotti C.G., Parton R.G., Simons S. Polarized sorting of glypiated proteins in hippocampal neurons. Nature. 349:1991;158-161
11. Drisaldi B., Stewart R.S., Adles C., Stewart L.R., Quaglio E., Biasini E., Fioriti L., Chiesa R., Harris D.A. 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. 278:2003;21732-21743
12. Fischer M., Rülicke T., Raeber A., Sailer A., Moser M., Oesch B., Brandner S., Aguzzi A., Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15:1996;1255-1264
13. Ford M.J., Burton L.J., Li H., Graham C.H., Frobert Y., Grassi J., Hall S.M., Morris R.J. A marked disparity between the expression of prion protein and its message by neurones of the CNS. Neuroscience. 111:2002;533-551
14. C) in synaptic boutons of normal hamster hippocampus. C. R. Acad. Sci. Paris, Life Sci. 318:1995;339-344
15. Fournier J.G., Escaig-Haye F., Grigoriev V. Ultrastructural localization of prion proteins: physiological and pathological implications. Microsc. Res. Tech. 50:2000;76-88
16. Gorodinsky A., Harris D.A. Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129:1995;619-627
17. 2-terminal cellular prion protein fragment. Biochem. Biophys. Res. Commun. 313:2004;818-823
18. Haeberlé A.-M., Ribaut-Barassin C., Bombarde G., Mariani J., Hunsmann G., Grassi J., Bailly Y. Synaptic prion protein immuno-reactivity in the rodent cerebellum. Microsc. Res. Tech. 50:2000;66-75
19. Harris D.A. Cellular biology of prion diseases. Clin. Microbiol. Rev. 12:1999;429-444
20. Harris D.A., Lele P., Snider W.D. Localization of the mRNA for a chicken prion protein by in situ hybridization. Proc. Natl. Acad. Sci. U. S. A. 90:1993;4309-4313
21. Harris D.A., Peters P.J., Taraboulos A., Lingappa V., DeArmond S.J., Prusiner S.B. Cell biology of prions. Prusiner S.B. Prion Biology and Diseases. second edition:2004;483-544 Cold Spring Harbor Laboratory Press, Cold Spring Harbor
22. 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. 19:1999;8866-8875
23. Huber G., Matus A. Differences in the cellular distributions of two microtubule-associated proteins, MAP1 and MAP2, in rat brain. J. Neurosci. 4:1984;151-160
24. Ivanova L., Barmada S., Kummer T., Harris D.A. Mutant prion proteins are partially retained in the endoplasmic reticulum. J. Biol. Chem. 276:2001;42409-42421
25. Lainé J., Marc M.E., Sy M.S., Axelrad H. Cellular and subcellular morphological localization of normal prion protein in rodent cerebellum. Eur. J. Neurosci. 14:2001;47-56
26. Liu T., Zwingman T., Li R., Pan T., Wong B.S., Petersen R.B., Gambetti P., Herrup K., Sy M.S. Differential expression of cellular prion protein in mouse brain as detected with multiple anti-PrP monoclonal antibodies. Brain Res. 896:2001;118-129
27. Lorenz H., Windl O., Kretzschmar H.A. Cellular phenotyping of secretory and nuclear prion proteins associated with inherited prion diseases. J. Biol. Chem. 277:2002;8508-8516
28. Ma J., Lindquist S. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. Proc. Natl. Acad. Sci. U. S. A. 98:2001;14955-14960
29. Sc-like conformation in the cytosol. Science. 298:2002;1785-1788
30. Ma J., Wollmann R., Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science. 298:2002;1781-1785
31. Magalhães A.C., Silva J.A., Lee K.S., Martins V.R., Prado V.F., Ferguson S.S., Gomez M.V., Brentani R.R., Prado M.A. Endocytic intermediates involved with the intracellular trafficking of a fluorescent cellular prion protein. J. Biol. Chem. 277:2002;33311-33318
32. Mange A., Milhavet O., Umlauf D., Harris D., Lehmann S. PrP-dependent cell adhesion in N2a neuroblastoma cells. FEBS Lett. 514:2002;159-162
33. Manson J., West J.D., Thomson V., McBride P., Kaufman M.H., Hope J. The prion protein gene: a role in mouse embryogenesis? Development. 115:1992;117-122
34. 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. 8:1994;121-127
35. Mayor S., Maxfield F.R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell. 6:1995;929-944
36. Mayor S., Rothberg K.G., Maxfield F.R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264:1994;1948-1951
37. 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. 23:2003;7183-7193
38. Mishra R.S., Bose S., Gu Y., Li R., Singh N. Aggresome formation by mutant prion proteins: the unfolding role of proteasomes in familial prion disorders. J. Alzheimer's Dis. 5:2003;15-23
39. 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. 50:2000;58-65
40. C in peripheral nerve. J. Neurochem. 88:2004;155-160
41. 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. 17:2001;521-538
42. Palay S.L., Chan-Palay V. Cerebellar Cortex. 1974;Springer-Verlag, Berlin
43. Pauly P.C., Harris D.A. Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273:1998;33107-33110
44. Piccardo P., Safar J., Ceroni M., Gajdusek D.C., Gibbs C.J. Jr. Immunohistochemical localization of prion protein in spongiform encephalopathies and normal brain tissue. Neurology. 40:1990;518-522
45. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. U. S. A. 95:1998;13363-13383
46. Salès N., Rodolfo K., Hässig R., Faucheux B., Di Giamberardino L., Moya K.L. Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10:1998;2464-2471
47. Salès N., Hassig R., Rodolfo K., Di Giamberardino L., Traiffort E., Ruat M., Fretier P., Moya K.L. Developmental expression of the cellular prion protein in elongating axons. Eur. J. Neurosci. 15:2002;1163-1177
48. Shmerling D., Hegyi I., Fischer M., Blättler T., Brandner S., Götz J., Rülicke 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. 93:1998;203-214
49. Shyng S.L., Heuser J.E., Harris D.A. A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J. Cell Biol. 125:1994;1239-1250
50. Shyng S.L., Moulder K.L., Lesko A., Harris D.A. The N-terminal domain of a glycolipid-anchored prion protein is essential for its endocytosis via clathrin-coated pits. J. Biol. Chem. 270:1995;14793-14800
51. 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. 22:2003;3591-3601
52. Vey M., Pilkuhn S., Wille H., Nixon R., DeArmond S.J., Smart E.J., Anderson R.G.W., Taraboulos A., Prusiner S.B. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl. Acad. Sci. U. S. A. 93:1996;14945-14949
53. Wiedenmann B., Franke W.W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 41:1985;1017-1028
54. Wong B.S., Pan T., Liu T., Li R., Petersen R.B., Jones I.M., Gambetti P., Brown D.R., Sy M.S. Prion disease: a loss of antioxidant function? Biochem. Biophys. Res. Commun. 275:2000;249-252
55. Yedidia Y., Horonchik L., Tzaban S., Yanai A., Taraboulos A. Proteasomes and ubiquitin are involved in the turnover of the wild-type prion protein. EMBO J. 20:2001;5383-5391
56. Zanusso G., Liu D., Ferrari S., Hegyi I., Yin X., Aguzzi A., Hornemann S., Liemann S., Glockshuber R., Manson J.C., Brown P., Petersen R.B., Gambetti P., Sy M.S. Prion protein expression in different species: analysis with a panel of new mAbs. Proc. Natl. Acad. Sci. U. S. A. 95:1998;8812-8816