Novel single chain antibodies to the prion protein identified by phage display

Virology

Volumn 358, Issue 1, 2007, Pages 166-177

  Adamson, Catherine S ^a   Yao, Yongxiu ^a   Vasiljevic, Snezana ^a   Sy, Man Sun ^b   Ren, Junyuan ^a   Jones, Ian M ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Antibody; Conformation; Epitope; Phage display; Prion; scFv; Truncation

Indexed keywords

ANTIBODY; EPITOPE; MONOCLONAL ANTIBODY; POLYPEPTIDE; PRION PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; NONHUMAN; PHAGE DISPLAY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TARGETING; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANTIBODIES; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; BINDING SITES, ANTIBODY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; IMMUNOGLOBULIN FRAGMENTS; IMMUNOGLOBULIN VARIABLE REGION; PEPTIDE LIBRARY; PROTEIN STRUCTURE, TERTIARY; PRPC PROTEINS; SEQUENCE ALIGNMENT;

EID: 33845971450     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.08.023     Document Type: Article

References (50)

1. Arbel M., Lavie V., and Solomon B. Generation of antibodies against prion protein in wild-type mice via helix 1 peptide immunization. J. Neuroimmunol. 144 (2003) 38-45
2. 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., and Kretzschmar H. The cellular prion protein binds copper in vivo. Nature 390 (1997) 684-687
3. Brown D.R., Hafiz F., Glasssmith L.L., Wong B.S., Jones I.M., Clive C., and Haswell S.J. Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19 (2000) 1180-1186
4. Calzolai L., Lysek D.A., Guntert P., von Schroetter C., Riek R., Zahn R., and Wuthrich K. NMR structures of three single-residue variants of the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 8340-8345
5. Chan D.C., Fass D., Berger J.M., and Kim P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89 (1997) 263-273
6. Demart S., Fournier J.G., Creminon C., Frobert Y., Lamoury F., Marce D., Lasmezas C., Dormont D., Grassi J., and Deslys J.P. New insight into abnormal prion protein using monoclonal antibodies. Biochem. Biophys. Res. Commun. 265 (1999) 652-657
7. Donne D.G., Viles J.H., Groth D., Mehlhorn I., James T.L., Cohen F.E., Prusiner S.B., Wright P.E., and Dyson H.J. Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 13452-13457
8. Donofrio G., Heppner F.L., Polymenidou M., Musahl C., and Aguzzi A. Paracrine inhibition of prion propagation by anti-PrP single-chain Fv miniantibodies. J. Virol. 79 (2005) 8330-8338
9. Flechsig E., Shmerling D., Hegyi I., Raeber A.J., Fischer M., Cozzio A., von Mering C., Aguzzi A., and Weissmann C. Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice. Neuron 27 (2000) 399-408
10. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., and Tagliavini F. Neurotoxicity of a prion protein fragment. Nature 362 (1993) 543-546
11. Gavin R., Braun N., Nicolas O., Parra B., Urena J.M., Mingorance A., Soriano E., Torres J.M., Aguzzi A., and del Rio J.A. PrP(106-126) activates neuronal intracellular kinases and Egr1 synthesis through activation of NADPH-oxidase independently of PrPc. FEBS Lett. 579 (2005) 4099-4106
12. Griffiths A.D., Williams S.C., Hartley O., Tomlinson I.M., Waterhouse P., Crosby W.L., Kontermann R.E., Jones P.T., Low N.M., Allison T.J., et al. Isolation of high affinity human antibodies directly from large synthetic repertoires. EMBO J. 13 (1994) 3245-3260
13. Hoogenboom H.R., Griffiths A.D., Johnson K.S., Chiswell D.J., Hudson P., and Winter G. Multi-subunit proteins on the surface of filamentous phage: methodologies for displaying antibody (Fab) heavy and light chains. Nucleic Acids Res. 19 (1991) 4133-4137
14. Horwich A.L., and Weissman J.S. Deadly conformations-Protein misfolding in prion disease. Cell 89 (1997) 499-510
15. Jobling M.F., Huang X., Stewart L.R., Barnham K.J., Curtain C., Volitakis I., Perugini M., White A.R., Cherny R.A., Masters C.L., Barrow C.J., Collins S.J., Bush A.I., and Cappai R. Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126. Biochemistry 40 (2001) 8073-8084
16. Kim C.L., Umetani A., Matsui T., Ishiguro N., Shinagawa M., and Horiuchi M. Antigenic characterization of an abnormal isoform of prion protein using a new diverse panel of monoclonal antibodies. Virology 320 (2004) 40-51
17. Korth C., Stierli B., Streit P., Moser M., Schaller O., Fischer R., Schulz-Schaeffer W., Kretzschmar H., Raeber A., Braun U., Ehrensperger F., Hornemann S., Glockshuber R., Riek R., Billeter M., Wuthrich K., and Oesch B. Prion (PrPSc)-specific epitope defined by a monoclonal antibody. Nature 390 (1997) 74-77
18. Korth C., Streit P., and Oesch B. Monoclonal antibodies specific for the native, disease-associated isoform of the prion protein. Methods Enzymol. 309 (1999) 106-122
19. Kramer M.L., Kratzin H.D., Schmidt B., Romer A., Windl O., Liemann S., Hornemann S., and Kretzschmar H. Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276 (2001) 16711-16719
20. Leclerc E., Peretz D., Ball H., Sakurai H., Legname G., Serban A., Prusiner S.B., Burton D.R., and Williamson R.A. Immobilized prion protein undergoes spontaneous rearrangement to a conformation having features in common with the infectious form. Embo J. 20 (2001) 1547-1554
21. Leclerc E., Peretz D., Ball H., Solforosi L., Legname G., Safar J., Serban A., Prusiner S.B., Burton D.R., and Williamson R.A. Conformation of PrP(C) on the cell surface as probed by antibodies. J. Mol. Biol. 326 (2003) 475-483
22. Li R., Liu T., Wong B.S., Pan T., Morillas M., Swietnicki W., O'Rourke K., Gambetti P., Surewicz W.K., and Sy M.S. Identification of an epitope in the C terminus of normal prion protein whose expression is modulated by binding events in the N terminus. J. Mol. Biol. 301 (2000) 567-573
23. Liemann S., and Glockshuber R. Transmissible spongiform encephalopathies. Biochem. Biophys. Res. Commun. 250 (1998) 187-193
24. Moroncini G., Kanu N., Solforosi L., Abalos G., Telling G.C., Head M., Ironside J., Brockes J.P., Burton D.R., and Williamson R.A. Motif-grafted antibodies containing the replicative interface of cellular PrP are specific for PrPSc. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 10404-10409
25. Novitskaya V., Makarava N., Bellon A., Bocharova O.V., Bronstein I.B., Williamson R.A., and Baskakov I.V. Probing the conformation of the prion protein within a single amyloid fibril using a novel immunoconformational assay. J. Biol. Chem. 281 (2006) 15536-15545
26. Pan T., Wong B.S., Liu T., Li R., Petersen R.B., and Sy M.S. Cell surface prion protein interacts with glycosaminoglycans. Biochem. J. 368 (2002) 81-90
27. Paramithiotis E., Pinard M., Lawton T., LaBoissiere S., Leathers V.L., Zou W.Q., Estey L.A., Lamontagne J., Lehto M.T., Kondejewski L.H., Francoeur G.P., Papadopoulos M., Haghighat A., Spatz S.J., Head M., Will R., Ironside J., O'Rourke K., Tonelli Q., Ledebur H.C., Chakrabartty A., and Cashman N.R. A prion protein epitope selective for the pathologically misfolded conformation. Nat. Med. (2003) 893-899
28. Perera W.S., and Hooper N.M. Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr. Biol. 11 (2001) 519-523
29. Peretz D., Williamson R.A., Matsunaga Y., Serban H., Pinilla C., Bastidas R.B., Rozenshteyn R., James T.L., Houghten R.A., Cohen F.E., Prusiner S.B., and Burton D.R. A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J. Mol. Biol. 273 (1997) 614-622
30. Peretz D., Williamson R.A., Kaneko K., Vergara J., Leclerc E., Schmitt-Ulms G., Mehlhorn I.R., Legname G., Wormald M.R., Rudd P.M., Dwek R.A., Burton D.R., and Prusiner S.B. Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412 (2001) 739-743
31. Peretz D., Williamson R.A., Legname G., Matsunaga Y., Vergara J., Burton D.R., DeArmond S.J., Prusiner S.B., and Scott M.R. A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34 (2002) 921-932
32. Perrier V., Solassol J., Crozet C., Frobert Y., Mourton-Gilles C., Grassi J., and Lehmann S. Anti-PrP antibodies block PrP replication in prion-infected cell cultures by accelerating PrP degradation. J. Neurochem. 89 (2004) 454-463
33. Polymenidou M., Heppner F.L., Pellicioli E.C., Urich E., Miele G., Braun N., Wopfner F., Schatzl H.M., Becher B., and Aguzzi A. Humoral immune response to native eukaryotic prion protein correlates with anti-prion protection. Proc. Natl. Acad. Sci. U.S.A. 101 Suppl 2 (2004) 14670-14676
34. Prusiner S.B., and Scott M.R. Genetics of prions. Annu. Rev. Genet. 31 (1997) 139-175
35. Reid B.G., and Flynn G.C. Chromophore formation in green fluorescent protein. Biochemistry 36 (1997) 6786-6791
36. Riek R., Hornemann S., Wider G., Billeter M., Glockshuber R., and Wuthrich K. NMR structure of the mouse prion protein domain PrP(121-321). Nature 382 (1996) 180-182
37. Rivera-Milla E., Stuermer C.A., and Malaga-Trillo E. An evolutionary basis for scrapie disease: identification of a fish prion mRNA. Trends Genet. 19 (2003) 72-75
38. Rubenstein R., Kascsak R.J., Papini M., Kascsak R., Carp R.I., and Langeveld J. Identification of a highly immunogenic site on the murine prion protein. Alzheimer's Disease Rev. 4 (1999) 13-18
39. Sachsamanoglou M., Paspaltsis I., Petrakis S., Verghese-Nikolakaki S., Panagiotidis C.H., Voigtlander T., Budka H., Langeveld J.P., and Sklaviadis T. Antigenic profile of human recombinant PrP: generation and characterization of a versatile polyclonal antiserum. J. Neuroimmunol. 146 (2004) 22-32
40. 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., and Williamson R.A. Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303 (2004) 1514-1516
41. Stockel J., Safar J., Wallace A.C., Cohen F.E., and Prusiner S.B. Prion protein selectively binds copper(II) ions. Biochemistry 37 (1998) 7185-7193
42. van Rheede T., Smolenaars M.M., Madsen O., and de Jong W.W. Molecular evolution of the mammalian prion protein. Mol. Biol. Evol. 20 (2003) 111-121
43. White A.R., Enever P., Tayebi M., Mushens R., Linehan J., Brandner S., Anstee D., Collinge J., and Hawke S. Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature 422 (2003) 80-83
44. Williamson R.A., Peretz D., Smorodinsky N., Bastidas R., Serban H., Mehlhorn I., DeArmond S.J., Prusiner S.B., and Burton D.R. Circumventing tolerance to generate autologous monoclonal antibodies to the prion protein. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 7279-7282
45. Williamson R.A., Peretz D., Pinilla C., Ball H., Bastidas R.B., Rozenshteyn R., Houghten R.A., Prusiner S.B., and Burton D.R. Mapping the prion protein using recombinant antibodies. J. Virol. 72 (1998) 9413-9418
46. Wong B.S., Venien-Bryan C., Williamson R.A., Burton D.R., Gambetti P., Sy M.S., Brown D.R., and Jones I.M. Copper refolding of prion protein. Biochem. Biophys. Res. Commun. 276 (2000) 1217-1224
47. Wopfner F., Weidenhofer G., Schneider R., von Brunn A., Gilch S., Schwarz T.F., Werner T., and Schatzl H.M. Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. J. Mol. Biol. 289 (1999) 1163-1178
48. Yao Y., Ren J., and Jones I.M. Amino terminal interaction in the prion protein identified using fusion to green fluorescent protein. J. Neurochem. 87 (2003) 1057-1065
49. Zahn R., Liu A., Luhrs T., Riek R., von Schroetter C., Lopez Garcia F., Billeter M., Calzolai L., Wider G., and Wuthrich K. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 145-150
50. 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., and 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