Phospholipid composition of membranes directs prions down alternative aggregation pathways

Biophysical Journal

Volumn 98, Issue 8, 2010, Pages 1520-1528

  Robinson, Philip J ^a   Pinheiro, Teresa J T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77951650561     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.12.4304     Document Type: Article

References (49)

1. Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. USA. 95: 13363-13383.
2. Caughey, B. W., A. Dong, ..., W. S. Caughey. 1991. Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry. 30:7672-7680.
3. Oesch, B., D. Westaway, ..., C. Weissmann. 1985. A cellular gene encodes scrapie PrP 27-30 protein. Cell. 40:735-746. (Pubitemid 15240279)
4. Bell, J. E., and J. W. Ironside. 1993. Neuropathology of spongiform encephalopathies in humans. Br. Med. Bull. 49:738-777.
5. Giaccone, G., L. Verga, ..., F. Tagliavini. 1992. Prion protein preamyloid and amyloid deposits in Gerstmann-Sträussler-Scheinker disease, Indiana kindred. Proc. Natl. Acad. Sci. USA. 89:9349-9353.
6. Jeffrey, M., I. A. Goodbrand, and C. M. Goodsir. 1995. Pathology of the transmissible spongiform encephalopathies with special emphasis on ultrastructure. Micron. 26:277-298.
7. Brandner, S., S. Isenmann, ..., A, Aguzzi. 1996. Normal host prion protein, necessary for scrapie-induced neurotoxicity. Nature. 379: 339-343.
8. Büeler, H., A. Aguzzi, ..., C. Weissmann. 1993. Mice devoid of PrP are resistant to scrapie. Cell. 73:1339-1347. (Pubitemid 23201147)
9. Collinge, J., M. S. Palmer, ..., P. Lantos. 1995. Transmission of fatal familial, insomnia to laboratory animals. Lancet. 346:569-570.
10. Lasmézas, C. I., J. P. Deslys, ..., D. Dormont. 1997. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein, Science. 275:402-405.
11. Swietnicki, W., M. Morillas, ..., W. K. Surewicz. 2000. Aggregation and fibrlllization of the recombinant human prion protein huPrP90231. Biochemistry. 39:424-431. (Pubitemid 30056478)
12. Baskakov, I. V., G. Legname, ..., F. E. Cohen. 2002. Pathway complexity of prion protein assembly into amyloid. J. Biol. Chem. 277:21140-21148. (Pubitemid 34952249)
13. sc). J. Mol. Biol. 346:645-659.
14. Baskakov, I. V., and O. V. Bocharova. 2005. In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry. 44:2339-2348. (Pubitemid 40279538)
15. Stahl, N., D. R. Borchelt, ..., S. B. Prusiner. 1987. Scrapie prion, protein. contains a phosphatidylinositol glycolipid. Cell. 51:229-240.
16. Baskakov, I. V., G. Legname, ..., F. E. Cohen. 2001. Folding of prion protein to its native a-helicál conformation is under kinetic control. J. Biol. Chem. 276:19687-19690. (Pubitemid 37411025)
17. Zhao, H., E. K. Tuominen, and P. K. Kinnunen. 2004. Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry. 43:10302-10307. (Pubitemid 39079303)
18. Sanghera, N., and T. J. Pinheiro. 2002. Binding of prion protein to lipid membranes and implications for prion conversion. J. Mol. Biol. 315:1241-1256. (Pubitemid 34729301)
19. van Meer, G. 1989. Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5:247-275.
20. Sackmann, E. 1996. Supported membranes: scientific and practical applications. Science. 271:43-48.
21. Zhang, L., J. Zhong, ...,Y. Sha. 2008. Parallel-oriented fibrogenesis of a β-sheet forming peptide on supported lipid bilayers. J. Phys. Chem. B. 112:8950-8954.
22. Zhong, J., W. Zheng, Y. Sha. 2007. PrP.106-126 amide causes the semi-penetrated poration in the supported lipid bilayers. Biochim. Biophys. Acta. 1768:1420-1429. (Pubitemid 46795477)
23. Domanov, Y. A., and P. K. Kinnunen. 2008. Islet amyloid polypeptide forms rigid lipid-protein amyloid fibrils on supported phospholipid bilayers. J. Mol. Biol. 376:42-54.
24. Re, F., S. Sesana, ..., M. Masserini. 2008. Prion protein structure is affected by pH-dependent interaction with membranes: a study in a model system. FEBS Lett. 582:215-220.
25. Sanghera, N., M. J. Swann, ..., T. J. Pinheiro. 2009. Insight into early events in the aggregation of the prion protein on lipid membranes. Biochim. Biophys. Acta. 1788:2245-2251.
26. Knight, J. D., J. A. Hebda, and A. D. Miranker. 2006. Conserved and cooperative assembly of membrane-bound α-helical states of islet amyloid polypeptide. Biochemistry. 45:9496-9508.
27. James, T. L., H. Liu, ..., F. E. Cohen. 1997. Solution structure of a 142-residue recombinant prion protein, corresponding to the infectious fragment of the scrapie isoform. Proc Natl. Acad. Sci. USA. 94: 10086-10091. (Pubitemid 27406998)
28. Richter, R. P., R. Bérat, and A. R. Brisson. 2006. Formation of solidsupported lipid bilayers: an integrated view. Langmuir. 22:3497-3505. (Pubitemid 43672517)
29. Caughey, B., and G. J. Raymond. 1991. The scrapie-associated form of PrP is made from a cell surface precursor that is both protease- and phospholipase-sensitive. J. Biol. Chem. 266:18217-18223. (Pubitemid 21908068)
30. Kazlauskaite, J., N. Sanghera, ..., T. J. Pinheiro. 2003. Structural. changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry. 42:3295-3304. (Pubitemid 36348638)
31. Morillas, M., W. Swietnicki, ..., W. K. Surewicz. 1999. Membrane environment alters the conformational structure of the recombinant human, prion protein. J. Biol. Chem. 274:36859-36865. (Pubitemid 30016751)
32. Forloni, G., N. Angeretti, ..., F. Tagliavini. 1993. Neurotoxicity of a prion protein fragment. Nature. 362:543-546.
33. Paulick, M. G., and C. R. Bertozzi. 2008. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry. 47:6991-7000.
34. Miura, T., M. Yoda, ..., H. Takeuchi. 2007. Clustered negative charges on the lipid membrane surface induce β-sheet formation of prion protein fragment 106-126. Biochemistry. 46:11589-11597. (Pubitemid 47585504)
35. Henriques, S. T., L. K. Pattenden, ..., M. A. Castanho. 2008. PrP(106- 126) does not interact with membranes under physiological conditions. Biophys. J. 95:1877-1889.
36. Shaked, G. M., Z. Meiner, ..., R. Gabizon. 2001. Reconstitution of prion infectivity from solubilized protease-resistant PrP and nonprotein components of prion rods. J. Biol. Chem. 276:14324-14328.
37. Ben-Zaken, O., S. Tzaban, ..., A. Taraboulos. 2003. Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278: 40041-40049.
38. Caughey, B., and R. E. Race. 1994. Scrapie-associated PrP accumulation and its inhibition: revisiting the amyloid-glycosaminoglycan connection. Ann. N. Y. Acad. Sci. 724:290-295.
39. Nandi, P. K., E. Leclerc, ..., M. Takahashi. 2002. DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J. Mol. Biol. 322:153-161.
40. Deleault, N. R., R. W. Lucassen, and S. Supattapone. 2003. RNA molecules stimulate prion protein conversion. Nature. 425:717-720.
41. Res) in vitro. J. Mol. Biol. 332:47-57.
42. Deleault, N. R., B. T. Harris, ..., S. Supattapone. 2007. Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. USA. 104:9741-9746.
43. Quist, A., I. Doudevski, ..., R. Lal, 2005. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl. Acad. Sci. USA. 102:10427-10432.
44. Sanghera, N., M. Wall, ..., T. J. Pinheiro. 2008. Globular and pre- fibrillar prion, aggregates are toxic to neuronal cells and perturb their electrophysiology. Biochim. Biophys. Acta. 1784:873-881.
45. Wang, X., F. Wang, ..., J. Ma. 2006. The interaction between cytoplasmic prion protein and the hydrophobic lipid core of membrane correlates with neurotoxicity. J. Biol. Chem. 281:13559-13565.
46. Boon, J. M., and B. D. Smith, 2002. Chemical control of phospholipid distribution across bilayer membranes. Med. Res. Rev. 22:251-281.
47. Zachowski, A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294:1-14.
48. Martin, S. J., C. P. Reutelingsperger,..., D. R. Green. 1995. Early redistribution of plasma membrane phosphatidy lserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bc.1-2 and Abl. J. Exp. Med. 182:1545-1556.
49. Eden, M. 1960. A two-dimensional growth, process. Proc Berkeley Symp. Math. Stat. Prob., 4th, Berkeley. 223-239.