Glycan-controlled epitopes of prion protein include a major determinant of susceptibility to sheep scrapie

Journal of Virology

Volumn 78, Issue 17, 2004, Pages 9270-9276

  Moudjou, Mohammed ^a   Treguer, Eric ^a   Rezaei, Human ^a   Sabuncu, Elifsu ^a   Neuendorf, Erdi ^b   Groschup, Martin H ^b   Grosclaude, Jeanne ^a   Laude, Hubert ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b FRCVDA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; EPITOPE; GLYCOPROTEIN P; PRION PROTEIN;

ALLOTYPE; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; BINDING SITE; BIODIVERSITY; BRAIN DISEASE; CARBOHYDRATE ANALYSIS; CELL CULTURE; CELL FREE SYSTEM; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITOPE MAPPING; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DETERMINATION; PROTEIN FOLDING; SCRAPIE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BRAIN; EPITOPES; GLYCOSYLATION; MICE; POLYSACCHARIDES; PROTEIN ISOFORMS; PRPC PROTEINS; SCRAPIE; SHEEP;

EID: 4143137548     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.17.9270-9276.2004     Document Type: Article

References (49)

1. Baylis, M., F. Houston, R. R. Kao, A. R. McLean, N. Hunter, and M. B. Gravenor. 2002. BSE - a wolf in sheep's clothing? Trends Microbiol. 10:563-570.
2. Beringue, V., G. Mallinson, M. Kaisar, M. Tayebi, Z. Sattar, G. Jackson, D. Anstee, J. Collinge, and S. Hawke. 2003. Regional heterogeneity of cellular priori protein isoforms in the mouse brain. Brain 126:1-9.
3. Bossers, A., P. B. G. M. Belt, G. J. Raymond, B. Caughey, R. De Vries, and M. A. Smits. 1997. Scrapie susceptibility-linked polymorphisms modulate the in vitro conversion of sheep prion protein to protease-resistant forms. Proc. Natl. Acad. Sci. USA 94:4931-4936.
4. Bruce, M. E. 2003. TSE strain variation. Br. Med. Bull. 66:99-108.
5. Bueler, H., A. Aguzzi, A. Sailer, R. A. Greiner, P. Autenried, M. Aguet, and C. Weissmann. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
6. Caughey, B. 2001. Interaction between prion protein isoforms: the kiss of death. Trends Biochem. Sci. 4:235-242.
7. Caughey, B., R. E. Race, D. Ernst, M. J. Buchmeier, and B. Chesebro. 1989. Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells. J. Virol. 63:175-181.
8. Collinge, J. 2001. Prion diseases of human and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24:519-550.
9. Collinge, J., K. C. Sidle, J. Meads, J. Ironside, and A. F. Hill. 1996. Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 383:685-690.
10. DeArmond, S. J., Y. Qiu, H. Sanchez, P. R. Spilman, A. Ninchak-Casey, D. Alonso, and V. Daggett. 1999. PrPc glycoform heterogeneity as a function of brain region: implications for selective targeting of neurons by prion strains. J. Neuropathol. Exp. Neurol. 58:1000-1009.
11. Elsen, J. M., Y. Amigues, F. Schelcher, V. Ducrocq, O. Andréoletti, F. Eychenne, J. V. Tien Khang, J. P. Poivey, F. Lantier, and J. L. Laplanche. 1999. Genetic susceptibility and transmission factors in scrapie: detailed analysis of an epidemic in a closed flock of Romanov. Arch. Virol. 144:431-445.
12. Endo, T., D. Groth, S. B. Prusiner, and A. Kobata. 1989. Diversity of oligosaccharide structures linked to asparagines of the scrapie prion protein. Biochemistry 28:8380-8388.
13. Goldman, W., N. Hunter, G. Smith, J. Foster, and J. Hope. 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.
14. Harris, D. A. 2003. Trafficking, turnover and membrane topology of PrP. Br. Med. Bull. 66:71-85.
15. Houston, F., W. Goldman, A. Chong, M. Jeffery, L. Gonzalez, J. Foster, D. Parnham, and N. Hunter. 2003. Prion diseases: BSE in sheep bred for resistance to infection. Nature 423:498.
16. Kaneko, K., L. Zulianello, M. Scott, C. M. Cooper, A. C. Wallace, T. L. James, F. E. Cohen, and S. B. Prusiner. 1997. Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc. Natl. Acad. Sci. USA 94:10069-10074.
17. Kascsak, R. J., R. Rubenstein, P. A. Merz, R. I. Carp, N. K. Robakis, H. M. Wisniewski, and H. Diringer. 1986. Immunological comparison of scrapie-associated fibrils isolated from animals infected with four different scrapie strains. J. Virol. 59:676-683.
18. Kocisko, D. A., J. H. Come, S. A. Priola, B. Chesebro, G. J. Raymond, P. T. Lansbury, and B. Caughey. 1994. Cell-free formation of protease-resistant prion protein. Nature 370:471-474.
19. Korth, C., K. Kaneko, and S. B. Prusiner. 2000. Expression of unglycosylated mutated prion protein facilitates PrP(Sc) formation in neuroblastoma cells infected with different prion strains. J. Gen. Virol. 81:2555-2563.
20. Kuczius, T., I. Haist, and M. H. Groschup. 1998. Molecular analysis of bovine spongiform encephalopathy and scrapie strain variation. J. Infect. Dis. 178:693-699.
21. Lawson, V. A., S. A. Priola, K. Wehrly, and B. Chesebro. 2001. N-terminal truncation of prion protein affects both formation and conformation of abnormal protease-resistant prion protein generated in vitro. J. Biol. Chem. 21:35265-35271.
22. Lehmann, S., and D. A. Harris. 1997. Blockade of glycosylation promotes acquisition of scrapie-like properties by the prion protein in cultured cells. J. Biol. Chem. 272:21479-21487.
23. Liu, T., T. Zwinman, R. Li, T. Pan, B. S. Wong, R. B. Petersen, P. Gambetti, K. Herrup, and M. S. Sy. 2001. Differential expression of cellular prion protein in mouse brain as detected with multiple anti-PrP monoclonal antibodies. Brain Res. 896:118-129.
24. Moudjou, M., Y. Frobert, J. Grassi, and C. Labonnardière. 2001. Cellular prion protein status in sheep: tissue-specific biochemical signatures. J. Gen. Virol. 82:2017-2024.
25. Nonno, R., E. Esposito, G. Vaccari, M. Conte, S. Marcon, M. Di Bari, C. Ligios, G. Di Guardo, and U. Agrimi. 2003. Molecular analysis of cases of Italian sheep scrapie and comparison with cases of bovine spongiform encephalopathy (BSE) and experimental BSE in sheep. J. Clin. Microbiol. 41:4127-4133.
26. Pan, T., M. Colucci, B.-S. Wong, R. Li, T. Liu, R. B. Petersen, S. Chen, P. Gambetti, and M.-S. Sy. 2001. Novel differences between two human prion strains revealed by two-dimensional gel electrophoresis. J. Biol. Chem. 276:37284-37288.
27. Parchi, P., R. Castellani, S. Capellari, B. Ghetti, K. Young, S. G. Chen, M. Farlow, D. W. Dickson, A. A. Sima, J. Q. Trojanowski, R. B. Petersen, and P. Gambetti. 1996. Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 39:767-778.
28. Perrier, V., A. C. Wallace, K. Kaneko, J. Safar, S. B. Prusiner, and F. E. Cohen. 2000. Mimicking dominant negative inhibition of prion replication through structure-based drug design. Proc. Natl. Acad. Sci. USA 97:6073-6078.
29. Petersen, R. B., P. Parchi, S. L. Richardson, C. B. Urig, and P. Gambetti. 1996. Effect of the D178N mutation and the codon 129 polymorphism on the metabolism of the prion protein. J. Biol. Chem. 271:12661-12668.
30. Priola, S. A., and V. A. Lawson. 2001. Glycosylation influences cross-species formation of protease-resistant prion protein. EMBO J. 20:6692-6699.
31. Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. USA 95:13363-13383.
32. Rezaei, H., Y. Choiset, F. Eghiaian, E. Treguer, P. Mentre, P. Debey, J. Grosclaude, and T. Haertle. 2002. Amyloidogenic unfolding intermediates differentiate sheep prion protein variants. J. Mol. Biol. 322:799-814.
33. Rezaei, H., D. Marc, Y. Choiset, M. Takahashi, G. Hui Hon Boa, T. Haertlé, J. Grosclaude, and P. Deby. 2000. High yield purification and physicochemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility. Eur. J. Biochem. 267:2833-2839.
34. Riek, R., S. Hornemann, G. Wider, M. Billeter, R. Glockshuber, and K. Wuthrich. 1996. NMR structure of the mouse prion protein domain PrP (121-321). Nature 382:180-182.
35. Rogers, M., A. Taraboulos, M. Scott, D. Groth, and S. B. Prusiner. 1990. Intracellular accumulation of the cellular prion protein after mutagenesis of its Asn-linked glycosylation sites. Glycobiology 1:101-109.
36. Rudd, M. P., M. R. Wormald, D. R. Wing, S. B. Prusiner, and R. A. Dwek. 2001. Prion glycoprotein: structure, dynamics and roles for the sugars. Biochemistry 40:3759-3766.
37. Rudd, P. M., T. Endo, C. Colominas, D. Groth, S. F. Wheeler, D. J. Harvey, M. R. Wormald, H. Serban, S. B. Prusiner, A. Kobata, and R. A. Dweck. 1999. Glycosylation differences between the normal and pathologic prion protein isoforms. Proc. Natl. Acad. Sci. USA 96:13044-13049.
38. Sabuncu, E., S. Petit, A. Le Dur, T. Lan Lai, J. L. Vilotte, H. Laude, and D. Vilette. 2003. PrP polymorphisms tightly control sheep prion replication in cultured cells. J. Virol. 77:2696-2700.
39. Somerville, R. A. 1999. Host and transmissible spongiform encephalopathy agent strain control glycosylation of PrP. J. Gen. Virol. 80:1865-1872.
40. Stimson, E., J. Hope, A. Chong, and A. L. Burlingame. 1999. Site-specific characterization of the N-linked glycans of murine prion protein by high-performance liquid chromatography/electrospray mass spectrometry and exoglycosidase digestions. Biochemistry 38:4885-4895.
41. Taraboulos, A., M. Rogers, D. R. Borchelt, M. P. McKinley, M. Scott, D. Serban, and S. B. Prusiner. 1990. Acquisition of protease resistance by prion proteins in scrapie-infected cells does not require asparagine-linked glycosylation. Proc. Natl. Acad. Sci. USA 87:8262-8266.
42. Thackray, A. M., J. Y. Madec, E. Wong, R. Morgan-Warren, D. R. Brown, T. Baron, and R. Bujdoso. 2003. Detection of bovine spongiform encephalopathy, ovine scrapie prion-related protein (PrPSc) and normal PrPc by monoclonal antibodies raised to copper-refolded prion protein. Biochem. J. 370:81-90.
43. Vilotte, J. L., S. Soulier, R. Essalmani, M. G. Stinnakre, D. Vaiman, L. Lepourry, J. C. Da Silva, N. Besnard, M. Dawson, A. Buschmann, M. Groschup, S. Petit, M. F. Madelaine, S. Rakatobe, A. Le Dur, D. Vilette, and H. Laude. 2002. Markedly increased susceptibility to natural sheep scrapie of transgenic mice expressing ovine PrP. J. Virol. 75:5977-5984.
44. Vorberg, I., and S. A. Priola. 2002. Molecular basis of scrapie strain glycoform variation. J. Biol. Chem. 277:36775-36781.
45. Wadsworth, J. D., A. F. Hill, J. A. Beck, and J. Collinge. 2003. Molecular and clinical classification of human prion disease. Br. Med. Bull. 66:241-254.
46. Westaway, D., V. Zuliani, C. M. Cooper, M. Da Costa, S. Neuman, A. L. Jenny, L. Detwiler, and S. B. Prusiner. 1994. Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev. 8:959-969.
47. Winklhofer, K. F., U. Heller, A. Reintjes, and J. Tatzlet. 2003. Inhibition of complex glycosylation increases the formation of PrPsc. Traffic 4:312-322.
48. Zanusso, G., D. Liu, S. Ferrari, I. Heigyi, X. Yin, A. Aguzzi, S. Hornemann, S. Liemann, R. Glockshuber, J. C. Manson, P. Brown, R. B. Petersen, P. Gambetti, and M.-S. Sy. 1998. Prion protein expression in different species: analysis with a panel of new MAbs. Proc. Natl. Acad. Sci. USA 95:8812-8816.
49. Zuegg, J., and J. E. Gready. 2000. Molecular dynamics simulation of human prion protein including both N-linked oligosaccharides and the GPI anchor. Glycobiology 10:959-974.