Soluble dimeric prion protein binds PrPSc in vivo and antagonizes prion disease

Cell

Volumn 113, Issue 1, 2003, Pages 49-60

  Meier, Philipp ^a,c,d   Genoud, Nicolas ^a   Prinz, Marco ^a,e   Maissen, Manuela ^a   Rülicke, Thomas ^b   Zurbriggen, Andreas ^c   Raeber, Alex J ^a,f   Aguzzi, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f Prionics AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; ISOPROTEIN; PRION PROTEIN; PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; CONTROLLED STUDY; DISEASE COURSE; IMMUNOPRECIPITATION; IN VIVO STUDY; INOCULATION; MOUSE; NONHUMAN; PATHOGENESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SCRAPIE; TRANSGENIC MOUSE; WILD TYPE;

ANIMALIA; MUS MUSCULUS;

EID: 0037418828     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00201-0     Document Type: Article

References (46)

1. Aguzzi A. Prions and the immune system. a journey through gut, spleen, and nerves Adv. Immunol. in press:2003.
2. Aguzzi A., Glatzel M., Montrasio F., Prinz M., Heppner F.L. Interventional strategies against prion diseases. Nat. Rev. Neurosci. 2:2001;745-749. a.
3. Aguzzi A., Montrasio F., Kaeser P.S. Prions. health scare and biological challenge Nat. Rev. Mol. Cell Biol. 2:2001;118-126. b.
4. Behrens A., Aguzzi A. Small is not beautiful. antagonizing functions for the prion protein PrP(C) and its homologue Dpl Trends Neurosci. 25:2002;150-154.
5. Bessen R.A., Kocisko D.A., Raymond G.J., Nandan S., Lansbury P.T., Caughey B. Non-genetic propagation of strain-specific properties of scrapie prion protein. Nature. 375:1995;698-700.
6. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. Charmm. a program for macromolecular energy, minimization, and dynamics calculations J. Comp. Chem. 4:1983;187-217.
7. Bueler H., Raeber A., Sailer A., Fischer M., Aguzzi A., Weissmann C. High prion and PrPSc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol. Med. 1:1994;19-30.
8. Büeler H.R., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell. 73:1993;1339-1347.
9. Canfield S.M., Morrison S.L. The binding affinity of human IgG for its high affinity Fc receptor is determined by multiple amino acids in the CH2 domain and is modulated by the hinge region. J. Exp. Med. 173:1991;1483-1491.
10. Carlson G.A., Ebeling C., Yang S.L., Telling G., Torchia M., Groth D., Westaway D., DeArmond S.J., Prusiner S.B. Prion isolate specified allotypic interactions between the cellular and scrapie prion proteins in congenic and transgenic mice. Proc. Natl. Acad. Sci. USA. 91:1994;5690-5694.
11. Doherty P., Williams E., Walsh F.S. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron. 14:1995;57-66.
12. Ettinger R., Browning J.L., Michie S.A., van Ewijk W., McDevitt H.O. Disrupted splenic architecture, but normal lymph node development in mice expressing a soluble lymphotoxin-beta receptor-IgG1 fusion protein. Proc. Natl. Acad. Sci. USA. 93:1996;13102-13107.
13. 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.
14. Fischer M.B., Roeckl C., Parizek P., Schwarz H.P., Aguzzi A. Binding of disease-associated prion protein to plasminogen. Nature. 408:2000;479-483.
15. Gatti J.L., Metayer S., Moudjou M., Andreoletti O., Lantier F., Dacheux J.L., Sarradin P. Prion protein is secreted in soluble forms in the epididymal fluid and proteolytically processed and transported in seminal plasma. Biol. Reprod. 67:2002;393-400.
16. Heppner F.L., Musahl C., Arrighi I., Klein M.A., Rulicke T., Oesch B., Zinkernagel R.M., Kalinke U., Aguzzi A. Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science. 294:2001;178-182.
17. Horiuchi M., Caughey B. Specific binding of normal prion protein to the scrapie form via a localized domain initiates its conversion to the protease-resistant state. EMBO J. 18:1999;3193-3203.
18. Hsiao K., Baker H.F., Crow T.J., Poulter M., Owen F., Terwilliger J.D., Westaway D., Ott J., Prusiner S.B. Linkage of a prion protein missense variant to Gerstmann-Straussler syndrome. Nature. 338:1989;342-345.
19. Kaeser P.S., Klein M.A., Schwarz P., Aguzzi A. Efficient lymphoreticular prion propagation requires prp(c) in stromal and hematopoietic cells. J. Virol. 75:2001;7097-7106.
20. Klein M.A., Frigg R., Flechsig E., Raeber A.J., Kalinke U., Bluethmann H., Bootz F., Suter M., Zinkernagel R.M., Aguzzi A. A crucial role for B cells in neuroinvasive scrapie. Nature. 390:1997;687-690.
21. Klein M.A., Kaeser P.S., Schwarz P., Weyd H., Xenarios I., Zinkernagel R.M., Carroll M.C., Verbeek J.S., Botto M., Walport M.J.et al. Complement facilitates early prion pathogenesis. Nat. Med. 7:2001;488-492.
22. Kocisko D.A., Come J.H., Priola S.A., Chesebro B., Raymond G.J., Lansbury P.T., Caughey B. Cell-free formation of protease-resistant prion protein. Nature. 370:1994;471-474.
23. Kocisko D.A., Priola S.A., Raymond G.J., Chesebro B., Lansbury P.T. Jr., Caughey B. Species specificity in the cell-free conversion of prion protein to protease-resistant forms. a model for the scrapie species barrier Proc. Natl. Acad. Sci. USA. 92:1995;3923-3927.
24. Lansbury P.T. Mechanism of scrapie replication. Science. 265:1994;1510.
25. Lopez C.D., Yost C.S., Prusiner S.B., Myers R.M., Lingappa V.R. Unusual topogenic sequence directs prion protein biogenesis. Science. 248:1990;226-229.
26. Lund J., Winter G., Jones P.T., Pound J.D., Tanaka T., Walker M.R., Artymiuk P.J., Arata Y., Burton D.R., Jefferis R.et al. Human Fc gamma RI and Fc gamma RII interact with distinct but overlapping sites on human IgG. J. Immunol. 147:1991;2657-2662.
27. Mabbott N.A., Mackay F., Minns F., Bruce M.E. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat. Med. 6:2000;719-720.
28. Mabbott N.A., Bruce M.E., Botto M., Walport M.J., Pepys M.B. Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat. Med. 7:2001;485-487.
29. Maissen M., Roeckl C., Glatzel M., Goldmann W., Aguzzi A. Plasminogen binds to disease-associated prion protein of multiple species. Lancet. 357:2001;2026-2028.
30. Montrasio F., Frigg R., Glatzel M., Klein M.A., Mackay F., Aguzzi A., Weissmann C. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science. 288:2000;1257-1259.
31. Naslavsky N., Stein R., Yanai A., Friedlander G., Taraboulos A. Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272:1997;6324-6331.
32. Parizek P., Roeckl C., Weber J., Flechsig E., Aguzzi A., Raeber A.J. Similar turnover and shedding of the cellular prion protein in primary lymphoid and neuronal cells. J. Biol. Chem. 276:2001;44627-44632.
33. Perini F., Vidal R., Ghetti B., Tagliavini F., Frangione B., Prelli F. Prp(27-30) is a normal soluble prion protein fragment released by human platelets. Biochem. Biophys. Res. Commun. 223:1996;572-577.
34. Perrier V., Kaneko K., Safar J., Vergara J., Tremblay P., DeArmond S.J., Cohen F.E., Prusiner S.B., Wallace A.C. Dominant-negative inhibition of prion replication in transgenic mice. Proc. Natl. Acad. Sci. USA. 99:2002;13079-13084.
35. Prusiner S.B. Molecular biology of prion diseases. Science. 252:1991;1515-1522.
36. Prusiner S.B., Cochran S.P., Groth D.F., Downey D.E., Bowman K.A., Martinez H.M. Measurement of the scrapie agent using an incubation time interval assay. Ann. Neurol. 11:1982;353-358.
37. Prusiner S.B., Groth D., Serban A., Stahl N., Gabizon R. Attempts to restore scrapie prion infectivity after exposure to protein denaturants. Proc. Natl. Acad. Sci. USA. 90:1993;2793-2797.
38. Safar J., Wille H., Itri V., Groth D., Serban H., Torchia M., Cohen F.E., Prusiner S.B. Eight prion strains have PrP(Sc) molecules with different conformations. Nat. Med. 4:1998;1157-1165.
39. Sailer A., Büeler H., Fischer M., Aguzzi A., Weissmann C. No propagation of prions in mice devoid of PrP. Cell. 77:1994;967-968.
40. Schwenk F., Baron U., Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23:1995;5080-5081.
41. Scott M., Foster D., Mirenda C., Serban D., Coufal F., Waelchli M., Torchia M., Groth D., Carlson G., DeArmond S.J.et al. Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell. 59:1989;847-857.
42. Tagliavini F., Prelli F., Porro M., Salmona M., Bugiani O., Frangione B. A soluble form of prion protein in human cerebrospinal fluid. implications for prion-related encephalopathies Biochem. Biophys. Res. Commun. 184:1992;1398-1404.
43. Tao M.H., Smith R.I., Morrison S.L. Structural features of human immunoglobulin G that determine isotype-specific differences in complement activation. J. Exp. Med. 178:1993;661-667.
44. 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. 93:1996;14945-14949.
45. Wadsworth J.D.F., Joiner S., Hill A.F., Campbell T.A., Desbruslais M., Luthert P.J., Collinge J. Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immuno-blotting assay. Lancet. 358:2001;171-180.
46. Weissmann C. Spongiform encephalopathies. The prion's progress. Nature. 349:1991;569-571.