Detection of bovine spongiform encephalopathy, ovine scrapie prion-related protein (PrPSc) and normal PrPc by monoclonal antibodies raised to copper-refolded prion protein

Biochemical Journal

Volumn 370, Issue 1, 2003, Pages 81-90

  Thackray, Alana M ^a   Madec, Jean Yves ^b   Wong, Edmond ^a   Morgan Warren, Robert ^a   Brown, David R ^c   Baron, Thierry ^b   Bujdoso, Raymond ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Healthy Pigs Production and Experimentation Section   (France)

^c University of Bath   (United Kingdom)

Author keywords

Conformational; Epitope; Metal ion; Neurodegenerative

Indexed keywords

BLOOD; CELLS; ELECTROPHORESIS; IMMUNOLOGY; MONOCLONAL ANTIBODIES; NEUROLOGY; TISSUE;

IMMUNE SYSTEM;

PROTEINS;

COPPER; MANGANESE; MONOCLONAL ANTIBODY; PRION PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOVINE SPONGIFORM ENCEPHALOPATHY; ELECTROPHORETIC MOBILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; LYMPHOCYTE; LYMPHOID CELL; MOUSE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; SCRAPIE; SHEEP; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CATTLE; COPPER; CROSS REACTIONS; ENCEPHALOPATHY, BOVINE SPONGIFORM; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; FLOW CYTOMETRY; GLYCOSYLATION; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PRPC PROTEINS; PRPSC PROTEINS; SHEEP;

ANIMALIA; BOVINAE; MURINAE; OVIS; OVIS ARIES; SCRAPIE PRION;

EID: 0037442530     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021280     Document Type: Article

References (56)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
2. Collinge, J. (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550
3. Prusiner, S. B., McKinley, M. P., Bowman, K. A., Bolton, D. C., Bendheim, P. E., Groth, D. F. and Glenner, G. G. (1983) Scrapie prions aggregate to form amyloid-like birefringent rods. Cell (Cambridge, Mass.) 35, 349-358
4. Safar, J., Wang, W., Padgett, M. P., Ceroni, M., Piccardo, P., Zopf, D., Gajdusek, D. C. and Gibbs, Jr, C. J. (1990) Molecular mass, biochemical composition, and physicochemical behavior of the infectious form of the scrapie precursor protein monomer. Proc. Natl. Acad. Sci. U.S.A. 87, 6373-6377
5. Gasset, M., Baldwin, M. A., Fletterick, R. J. and Prusiner, S. B. (1993) Perturbation of the secondary structure of the scrapie priori protein under conditions that alter infectivity. Proc. Natl. Acad. Sci. U.S.A. 90, 1-5
6. Pan, K. M., Baldwin, M., Nguyen, J., Gasser, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E. et al. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
7. DeArmond, S. J., Mobley, W. C., DeMott, D. L., Barry, R. A., Beckstead, J. H. and Prusiner, S. B. (1987) Changes in the localization of brain prion proteins during scrapie infection. Neurology 37, 1271-1280
8. Jendroska, K., Heinzel, F. P., Torchia, M., Stowring, L., Kretzschmar, H. A., Kon, A., Stern, A., Prusiner, S. B. and DeArmond, S. J. (1991) Proteinase-resistant prion protein accumulation in Syrian hamster brain correlates with regional pathology and scrapie infectivity. Neurology 41, 1482-1490
9. Williams, A., Lucassen, P. J., Ritchie, D. and Bruce, M. (1997) PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Exp. Neurol. 144, 433-438
10. Jeffrey, M., Martin, S., Barr, J., Chong, A. and Fraser, J. R. (2001) Onset of accumulation of PrPres in murine ME7 scrapie in relation to pathological and PrP immunohistochemical changes. J. Comp. Pathol. 124, 20-28
11. Hill, A. F., Zeidler, M., Ironside, J. and Collinge, J. (1997) Diagnosis of new variant Creutzfeldt-Jakob disease by tonsil biopsy. Lancet 349, 99-100
12. Wadsworth, J. D., Joiner, S., Hill, A. F., Campbell, T. A., Desbruslais, M., Luthert, P. J. and Collinge, J. (2001) Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358, 171-180
13. Chiesa, R. and Harris, D. A. (2001) Prion diseases: what is the neurotoxic molecule? Neurobiol. Dis. 8, 743-763
14. Bueler, H., Aguzzi, A., Sailer, A., Greiner, R. A., Autenried, P., Aguet, M. and Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie. Cell (Cambridge, Mass.) 73, 1339-1347
15. Hornshaw, M. P., McDermott, J. R., Candy, J. M. and Lakey, J. H. (1995) Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem. Biophys. Res. Commun. 214, 993-999
16. 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. et al. (1997) The cellular prion protein binds copper in vivo. Nature (London) 390, 684-687
17. Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E. and Dyson, H. J. (1999) Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. U.S.A. 96, 2042-2047
18. Jackson, G. S., Murray, I., Hosszu, L. L., Gibbs, N., Waltho, J. P., Clarke, A. R. and Collinge, J. (2001) Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. U.S.A 98, 8531-8535
19. Kramer, M. L., Kratzin, H. D., Schmidt, B., Romer, A., Windl, O., Liemann, S., Hornemann, S. and Kretzschmar, H. (2001) Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276, 16711-16719
20. Stockel, J., Safar, J., Wallace, A. C., Cohen, F. E. and Prusiner, S. B. (1998) Prion protein selectively binds copper(II) ions. Biochemistry 37, 7185-7193
21. Gustiananda, M., Haris, P. I., Milburn, P. J. and Gready, J. E. (2002) Copper-induced conformational change in a marsupial prion protein repeat peptide probed using FTIR spectroscopy. FEBS Lett 512, 38-42
22. Pauly, P. C. and Harris, D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem 273, 33107-33110
23. McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R. and Aiken, J. (1998) Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273, 25545-25547
24. Quaglio, E., Chiesa, R. and Harris, D. A. (2001) Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 276, 11432-11438
25. Wadsworth, J. D., Hill, A. F., Joiner, S., Jackson, G. S., Clarke, A. R. and Collinge, J. (1999) Strain-specific prion-protein conformation determined by metal ions. Nat. Cell Biol. 1, 55-59
26. Bueler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M. and Weissmann, C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature (London) 356, 577-582
27. Fischer, M., Rulicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A. and Weissmann, C. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15, 1255-1264
28. Brown, D. R., Hafiz, F., Glasssmith, L. L., Wong, B. S., Jones, I. M., Clive, C. and Haswell, S. J. (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19, 1180-1186
29. Galfre, G., Howe, S. C., Milstein, C., Butcher, G. W. and Howard, J. C. (1977) Antibodies to major histocompatibility antigens produced by hybrid cell lines. Nature (London) 266, 550-552
30. Montrasio, F., Frigg, R., Glatzel, M., Klein, M. A., Mackay, F., Aguzzi, A. and Weissmann, C. (2000) Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science (Washington, D.C.) 288, 1257-1259
31. Baron, T. G., Madec, J. Y., Calavas, D., Richard, Y. and Barillet, F. (2000) Comparison of French natural scrapie isolates with bovine spongiform encephalopathy and experimental scrapie infected sheep. Neurosci. Lett. 284, 175-178
32. Baron, T. G. and Biacabe, A. G. (2001) Molecular analysis of the abnormal prion protein during coinfection of mice by bovine spongiform encephalopathy and a scrapie agent. J. Virol. 75, 107-114
33. Baron, T. G., Betemps, D., Groschup, M. H. and Madec, J. Y. (1999) Immunological characterization of the sheep prion protein expressed as fusion proteins in Escherichia coli. FEMS Immunol. Med. Microbiol. 25, 379-384
34. Goldmann, W., Hunter, N., Smith, G., Foster, J. and Hope, J. (1994) PrP genotype and agent effects in scrapie: change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. J. Gen. Virol. 75, 989-995
35. Goldmann, W., Hunter, N., Benson, G., Foster, J. D. and Hope, J. (1991) Different scrapie-associated fibril proteins (PrP) are encoded by lines of sheep selected for different alleles of the Sip gene. J. Gen. Virol. 72, 2411-2417
36. Miura, T., Hori-i, A., Mototani, H. and Takeuchi, H. (1999) Raman spectroscopic study on the copper(II) binding mode of prion octapeptide and its pH dependence. Biochemistry 38, 11560-11569
37. Bonomo, R. P., Imperllizzeri, G., Pappalardo, G., Rizzarelli, E. and Tabbi, G. (2000) Copper(II) binding modes in the prion octapeptide PHGGGWGQ: a spectroscopic and voltammetric study. Chemistry 6, 4195-4202
38. Burns, C. S., Aronoff-Spencer, E., Dunham, C. M., Lario, P., Avdievich, N. I., Antholine, W. E., Olmstead, M. M., Vrielink, A., Gerfen, G. J., Peizach, J. et al. (2002) Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41, 3991-4001
39. 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. (2000) 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, 567-573
40. Matsunaga, Y., Peretz, D., Williamson, A., Burton, D., Mehlhorn, I., Groth, D., Cohen, F. E., Prusiner, S. B. and Baldwin, M. A. (2001) Cryptic epitopes in N-terminally truncated prion protein are exposed in the full-length molecule: dependence of conformation on pH. Proteins: Struct. Funct. Genet. 44, 110-118
41. Endo, T., Groth, D., Prusiner, S. B. and Kobata, A. (1989) Diversity of oligosaccharide structures linked to asparagines of the scrapie prion protein. Biochemistry 28, 8380-8388
42. Haraguchi, T., Fisher, S., Olofsson, S., Endo, T., Groth, D., Tarentino, A., Borchelt, D. R., Teplow, D., Hood, L., Burlingame, A. et al. (1989) Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Arch. Biochem. Biophys. 274, 1-13
43. Zanusso, G., Liu, D., Ferrari, S., Hegyi, I., Yin, X., Aguzzi, A., Hornemann, S., Liemann, S., Glockshuber, R., Manson, J. C. et al. (1998) Prion protein expression in different species: analysis with a panel of new mAbs. Proc. Natl. Acad. Sci. U.S.A. 95, 8812-8816
44. Collinge, J., Sidle, K. C., Meads, J., Ironside, J. and Hill, A. F. (1996) Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature (London) 383, 685-690
45. Somerville, R. A., Chong, A., Mulqueen, O, U., Birkett, C. R., Wood, S. C. and Hope, J. (1997) Biochemical typing of scrapie strains. Nature (London) 386, 564
46. Parchi, P., Capellari, S., Chen, S. G., Petersen, R. B., Gambetti, P., Kopp, N., Brown, P., Kitamoto, T., Tateishi, J., Giese, A. and Kretzschmar, H. (1997) Typing prion isoforms, Nature (London) 386, 232-234
47. Kuczius, T., Haist, I. and Groschup, M. H. (1998) Molecular analysis of bovine spongiform encephalopathy and scrapie strain variation. J. Infect Dis. 178, 693-699
48. Hill, A. F., Sidle, K. C., Joiner, S., Keyes, P., Martin, T. C., Dawson, M. and Collinge, J. (1998) Molecular screening of sheep for bovine spongiform encephalopathy. Neurosci. Lett. 255, 159-162
49. Bruce, M. E., McConnell, I., Fraser, H. and Dickinson, A. G. (1991) The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J. Gen. Virol. 72, 595-603
50. Fraser, H. and Dickinson, A. G. (1973) Scrapie in mice. Agent-strain differences in the distribution and intensity of grey matter vacuolation. J. Comp. Pathol. 83, 29-40
51. Thackray, A. M., Knight, R., Haswell, S. J., Bujdoso, R. and Brown, D. R. (2002) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253-258
52. Wong, B. S., Chen, S. G., Colucci, M., Xie, Z., Pan, T., Liu, T., Li, R., Gambetti, P., Sy, M. S. and Brown, D. R. (2001) Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78, 1400-1408
53. Wong, B. S., Brown, D. R., Pan, T., Whiteman, M., Liu, T., Bu, X., Li, R., Gambetti, P., Olesik, J., Rubenstein, R. and Sy, M. S. (2001) Oxidative impairment in scrapie-infected mice is associated with brain metals perturbations and altered antioxidant activities. J. Neurochem. 79, 689-698
54. Dodelet, V. C. and Cashman, N. R. (1998) Prion protein expression in human leukocyte differentiation. Blood 91, 1556-1561
55. Bendheim, P. E., Brown, H. R., Rudelli, R. D., Scala, L. J., Goller, N. L., Wen, G. Y., Kascsak, R. J., Cashman, N. R. and Bolton, D. C. (1992) Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology 42, 149-156
56. Houston, F., Foster, J. D., Chong, A., Hunter, N. and Bostock, C. J. (2000) Transmission of BSE by blood transfusion in sheep. Lancet 356, 999-1000