Residues surrounding the glycosylphosphatidylinositol anchor attachment site of PrP modulate prion infection: Insight from the resistance of rabbits to prion disease

Journal of Virology

Volumn 84, Issue 13, 2010, Pages 6678-6686

  Nisbet, Rebecca M ^a,b   Harrison, Christopher F ^a,b   Lawson, Victoria A ^b   Masters, Colin L ^b   Cappai, Roberto ^a,b   Hill, Andrew F ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GLYCOSYLPHOSPHATIDYLINOSITOL; PRION PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONFORMATIONAL TRANSITION; DISEASE RESISTANCE; MOUSE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RABBIT; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; GLYCOSYLPHOSPHATIDYLINOSITOLS; IMMUNITY, INNATE; MICE; MOLECULAR SEQUENCE DATA; PREGNANCY PROTEINS; PRION DISEASES; PROTEIN BINDING; RABBITS; SEQUENCE ALIGNMENT;

ANIMALIA; MAMMALIA; ORYCTOLAGUS CUNICULUS; PRIONS (INFECTIVE AGENTS);

EID: 77953315370     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02709-09     Document Type: Article

References (46)

1. Barboni, E., B. P. Rivero, A. J. George, S. R. Martin, D. V. Renoup, E. F. Hounsell, P. C. Barber, and R. J. Morris. 1995. The glycophosphatidylinositol anchor affects the conformation of Thy-1 protein. J. Cell Sci. 108:487-497.
2. Bate, C., S. Reid, and A. Williams. 2004. Phospholipase A2 inhibitors or platelet-activating factor antagonists prevent prion replication. J. Biol. Chem. 279:36405-36411.
3. Borchelt, D. R., M. Scott, A. Taraboulos, N. Stahl, and S. B. Prusiner. 1990. Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells. J. Cell Biol. 110:743-752. (Pubitemid 20088941)
4. Borchelt, D. R., A. Taraboulos, and S. B. Prusiner. 1992. Evidence for synthesis of scrapie prion proteins in the endocytic pathway. J. Biol. Chem. 267:16188-16199.
5. Brugger, B., C. Graham, I. Leibrecht, E. Mombelli, A. Jen, F. Wieland, and R. Morris. 2004. The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279:7530-7536.
6. Courageot, M. P., N. Daude, R. Nonno, S. Paquet, M. A. Di Bari, A. Le Dur, J. Chapuis, A. F. Hill, U. Agrimi, H. Laude, and D. Vilette. 2008. A cell line infectible by prion strains from different species. J. Gen. Virol. 89:341-347.
7. Doh-Ura, K., T. Iwaki, and B. Caughey. 2000. Lysosomotropic agents and cysteine protease inhibitors inhibit scrapie-associated prion protein accumulation. J. Virol. 74:4894-4897.
8. Eisenhaber, B., P. Bork, and F. Eisenhaber. 1999. Prediction of potential GPI-modification sites in proprotein sequences. J. Mol. Biol. 292:741-758.
9. Eisenhaber, B., P. Bork, and F. Eisenhaber. 1998. Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng. 11:1155-1161. (Pubitemid 29012126)
10. Fischer, M., T. Rulicke, A. Raeber, A. Sailer, M. Moser, B. Oesch, S. Brandner, A. Aguzzi, and C. Weissmann. 1996. Prion protein (PrP) with aminoproximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15:1255-1264. (Pubitemid 26093461)
11. Frieman, M. B., and B. P. Cormack. 2003. The omega-site sequence of glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall. Mol. Microbiol. 50:883-896.
12. Gibbs, C. J., Jr., and D. C. Gajdusek. 1973. Experimental subacute spongiform virus encephalopathies in primates and other laboratory animals. Science 182:67-68.
13. Gilch, S., K. F. Winklhofer, M. H. Groschup, M. Nunziante, R. Lucassen, C. Spielhaupter, W. Muranyi, D. Riesner, J. Tatzelt, and H. M. Schatzl. 2001. Intracellular re-routing of prion protein prevents propagation of PrP(Sc) and delays onset of prion disease. EMBO J. 20:3957-3966.
14. Gu, Y., A. Singh, S. Bose, and N. Singh. 2008. Pathogenic mutations in the glycosylphosphatidylinositol signal peptide of PrP modulate its topology in neuroblastoma cells. Mol. Cell. Neurosci. 37:647-656.
15. Hamada, K., H. Terashima, M. Arisawa, and K. Kitada. 1998. Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J. Biol. Chem. 273:26946-26953.
16. Hamada, K., H. Terashima, M. Arisawa, N. Yabuki, and K. Kitada. 1999. Amino acid residues in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J. Bacteriol. 181:3886-3889. (Pubitemid 29295903)
17. Hizume, M., A. Kobayashi, H. Mizusawa, and T. Kitamoto. 2009. Amino acid conditions near the GPI anchor attachment site of prion protein for the conversion and the GPI anchoring. Biochem. Biophys. Res. Commun. 391:1681-1686.
18. Horiuchi, M., and B. Caughey. 1999. Specific binding of normal prion protein to the scrapie form via a localized domain initiates its conversion to the protease-resistant state. EMBO J. 18:3193-3203.
19. Kaneko, K., M. Vey, M. Scott, S. Pilkuhn, F. E. Cohen, and S. B. Prusiner. 1997. COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scrapie isoform. Proc. Natl. Acad. Sci. U. S. A. 94:2333-2338.
20. Kiachopoulos, S., A. Bracher, K. F. Winklhofer, and J. Tatzelt. 2005. Pathogenic mutations located in the hydrophobic core of the prion protein interfere with folding and attachment of the glycosylphosphatidylinositol anchor. J. Biol. Chem. 280:9320-9329.
21. Kim, C. L., A. Karino, N. Ishiguro, M. Shinagawa, M. Sato, and M. Horiuchi. 2004. Cell-surface retention of PrPC by anti-PrP antibody prevents protease-resistant PrP formation. J. Gen. Virol. 85:3473-3482.
22. Klingeborn, M., L. Wik, M. Simonsson, L. H. Renstrom, T. Ottinger, and T. Linne. 2006. Characterization of proteinase K-resistant N- and C-terminally truncated PrP in Nor98 atypical scrapie. J. Gen. Virol. 87:1751-1760.
23. Klöhn, P. C., L. Stoltze, E. Flechsig, M. Enari, and C. Weissmann. 2003. A quantitative, highly sensitive cell-based infectivity assay for mouse scrapie prions. Proc. Natl. Acad. Sci. U. S. A. 100:11666-11671.
24. Korth, C., B. C. May, F. E. Cohen, and S. B. Prusiner. 2001. Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease. Proc. Natl. Acad. Sci. U. S. A. 98:9836-9841.
25. Lau, A. L., A. Y. Yam, M. M. Michelitsch, X. Wang, C. Gao, R. J. Goodson, R. Shimizu, G. Timoteo, J. Hall, A. Medina-Selby, D. Coit, C. McCoin, B. Phelps, P. Wu, C. Hu, D. Chien, and D. Peretz. 2007. Characterization of prion protein (PrP)-derived peptides that discriminate full-length PrPSc from PrPC. Proc. Natl. Acad. Sci. U. S. A. 104:11551-11556.
26. Lawson, V. A., L. J. Vella, J. D. Stewart, R. A. Sharples, H. Klemm, D. M. Machalek, C. L. Masters, R. Cappai, S. J. Collins, and A. F. Hill. 2008. Mouse-adapted sporadic human Creutzfeldt-Jakob disease prions propagate in cell culture. Int. J. Biochem. Cell Biol. 40:2793-2801.
27. Loftus, B., and M. Rogers. 1997. Characterization of a prion protein (PrP) gene from rabbit - a species with apparent resistance to infection by prions. Gene 184:215-219.
28. Mayor, S., and H. Riezman. 2004. Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell. Biol. 5:110-120.
29. Paladino, S., S. Lebreton, S. Tivodar, V. Campana, R. Tempre, and C. Zurzolo. 2008. Different GPI-attachment signals affect the oligomerisation of GPI-anchored proteins and their apical sorting. J. Cell Sci. 121:4001-4007.
30. Pan, T., R. Li, S. C. Kang, B. S. Wong, T. Wisniewski, and M. S. Sy. 2004. Epitope scanning reveals gain and loss of strain specific antibody binding epitopes associated with the conversion of normal cellular prion to scrapie prion. J. Neurochem. 90:1205-1217.
31. Paquet, S., E. Sabuncu, J. L. Delaunay, H. Laude, and D. Vilette. 2004. Prion infection of epithelial Rov cells is a polarized event. J. Virol. 78:7148-7152.
32. Paulick, M. G., and C. R. Bertozzi. 2008. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47:6991-7000.
33. Pierleoni, A., P. L. Martelli, and R. Casadio. 2008. PredGPI: a GPI-anchor predictor. BMC Bioinformatics 9:392.
34. Prusiner, S. B. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144.
35. Stahl, N., M. A. Baldwin, A. L. Burlingame, and S. B. Prusiner. 1990. Identification of glycoinositol phospholipid linked and truncated forms of the scrapie prion protein. Biochemistry 29:8879-8884. (Pubitemid 20311960)
36. Stahl, N., M. A. Baldwin, R. Hecker, K. Pan, A. L. Burlingame, and S. B. Prusiner. 1992. Glycosylinositol phospholipid anchors of the scrapie and cellular prion protein contain sialic acid. Biochemistry 31:5043-5053.
37. Stahl, N., D. R. Borchelt, K. Hsiao, and S. B. Prusiner. 1987. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51:229-240.
38. Taraboulos, A., A. J. Raeber, D. R. Borchelt, D. Serban, and S. B. Prusiner. 1992. Synthesis and trafficking of prion proteins in cultured cells. Mol. Biol. Cell 3:851-863.
39. Taraboulos, A., M. Scott, A. Semenov, D. Avraham, L. Laszlo, and S. B. Prusiner. 1995. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129:121-132.
40. Udenfriend, S., and K. Kodukula. 1995. How glycosylphosphatidylinositolanchored membrane proteins are made. Annu. Rev. Biochem. 64:563-591.
41. Uelhoff, A., J. Tatzelt, A. Aguzzi, K. F. Winklhofer, and C. Haass. 2005. A pathogenic PrP mutation and doppel interfere with polarized sorting of the prion protein. J. Biol. Chem. 280:5137-5140.
42. Vella, L. J., R. A. Sharples, V. A. Lawson, C. L. Masters, R. Cappai, and A. F. Hill. 2007. Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J. Pathol. 211:582-590.
43. Vey, M., S. Pilkuhn, H. Wille, R. Nixon, S. J. DeArmond, E. J. Smart, R. G. Anderson, A. Taraboulos, and S. B. Prusiner. 1996. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl. Acad. Sci. U. S. A. 93:14945-14949.
44. Vilette, D., O. Andreoletti, F. Archer, M. F. Madelaine, J. L. Vilotte, S. Lehmann, and H. Laude. 2001. Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein. Proc. Natl. Acad. Sci. U. S. A. 98:4055-4059.
45. Vogtherr, M., S. Grimme, B. Elshorst, D. M. Jacobs, K. Fiebig, C. Griesinger, and R. Zahn. 2003. Antimalarial drug quinacrine binds to Cterminal helix of cellular prion protein. J. Med. Chem. 46:3563-3564.
46. Vorberg, I., M. H. Groschup, E. Pfaff, and S. A. Priola. 2003. Multiple amino acid residues within the rabbit prion protein inhibit formation of its abnormal isoform. J. Virol. 77:2003-2009.