Defining the pathway of worm-like amyloid fibril formation by the mouse prion protein by delineation of the productive and unproductive oligomerization reactions

Biochemistry

Volumn 50, Issue 7, 2011, Pages 1153-1161

  Jain, Shweta ^a   Udgaonkar, Jayant B ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; AMYLOID FIBRIL; AMYLOID FIBRIL FORMATION; APPARENT RATE CONSTANT; FIBRIL FORMATION; HETEROGENEOUS POPULATIONS; INTERNAL STRUCTURE; PRION PROTEIN; PROTEIN VARIANTS;

AMINO ACIDS; CONCENTRATION (PROCESS); GLYCOPROTEINS; OLIGOMERIZATION; PROTEINS; RATE CONSTANTS; SODIUM CHLORIDE;

OLIGOMERS;

AMYLOID; MUTANT PROTEIN; OLIGOMER; PRION PROTEIN; SODIUM CHLORIDE;

ARTICLE; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STRUCTURE; PROTEIN VARIANT; WILD TYPE;

AMYLOID; ANIMALS; CATALYSIS; EFFICIENCY; HYDROGEN-ION CONCENTRATION; KINETICS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTANT PROTEINS; OSMOLAR CONCENTRATION; PRIONS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

EID: 79951607134     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101757x     Document Type: Article

References (51)

1. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie Science 216, 136-144 (Pubitemid 12089840)
2. Prusiner, S. B. (1998) Prions Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383 (Pubitemid 28525623)
3. Chiesa, R. and Harris, D. A. (2009) Fishing for Prion Protein Function PLoS Biol. 7, 439-443
4. Bremer, J., Baumann, F., Tiberi, C., Wessig, C., Fischer, H., Schwarz, P., Steele, A. D., Toyka, K. V., Nave, K., Weis, J., and Aguzzi, A. (2010) Axonal prion protein is required for peripheral myelin maintenance Nat. Neurosci. 13, 310-320
5. Collinge, J. (2001) Prion diseases of humans and animals: Their causes and molecular basis Annu. Rev. Neurosci. 24, 519-550 (Pubitemid 32695238)
6. Aguzzi, A. and Polymenidou, M. (2004) Mammalian prion biology: One century of evolving concepts Cell 116, 313-327
7. Caughey, B., Baron, G. S., Chesebro, B., and Jeffrey, M. (2009) Getting a grip on prions: Oligomers, amyloids, and pathological membrane interactions Annu. Rev. Biochem. 78, 177-204
8. Wille, H., Michelitsch, M. D., Guénebaut, V., Supattapone, S., Serban, A., Cohen, F. E., Agard, D. A., and Prusiner, S. B. (2002) Structural studies of the scrapie prion protein by electron crystallography Proc. Natl. Acad. Sci. U.S.A. 99, 3563-3568
9. Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed β-helices into trimmers Proc. Natl. Acad. Sci. U.S.A. 101, 8342-8347
10. Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions Science 305, 673-676
11. Hornemann, S. and Glockshuber, R. (1998) A scrapie like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH Proc. Natl. Acad. Sci. U.S.A. 95, 6010-6014
12. Baskakov, I. V., Legname, G., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2002) Pathway complexity of prion protein assembly into amyloid J. Biol. Chem. 277, 21140-21148
13. Sc J. Mol. Biol. 346, 645-659
14. Baskakov, I. V. (2004) Autocatalytic conversion of recombinant prion proteins displays a species barrier J. Biol. Chem. 279, 7671-7677 (Pubitemid 38294648)
15. Cobb, N. J. and Surewicz, W. K. (2009) Prion Diseases and Their Biochemical Mechanisms Biochemistry 48, 2574-2585
16. Jain, S. and Udgaonkar, J. B. (2008) Evidence for stepwise formation of amyloid fibrils by the mouse prion protein J. Mol. Biol. 382, 1228-1241
17. Jain, S. and Udgaonkar, J. B. (2010) Salt-induced modulation of the pathway of amyloid fibril formation by the mouse prion protein Biochemistry 49, 7615-7624
18. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein Science 327, 1132-1135
19. Parchi, P., Gambetti, P., Picardo, P., and Ghetti, B. (1998) Human prion diseases. In Progress in Pathology IV (Haddock, G. M., Ed.) pp 39 - 77, Churchill Livingstone, Edinburgh, U.K.
20. 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 356, 577-582
21. 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 73, 1339-1347
22. Brandner, S., Isenmann, S., Raeber, A., Fischer, M., Sailer, A., Kobayashi, Y., Marino, S., Weissmann, C., and Aguzzi, A. (1996) Normal host prion protein necessary for scrapie-induced neurotoxicity Nature 379, 339-343
23. Lasmezas, C. I., Deslys, J. P., Robain, O., Jaegly, A., Beringue, V., and Peyrin, J. M. 1997, Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein Science 275, 402-405
24. Mallucci, G., Dickinson, A., Linehan, J., Klohn, P. C., Brandner, S., and Collinge, J. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis Science 302, 871-874
25. Mallucci, G. R., White, M. D., Farmer, M., Dickinson, A., Khatun, H., Powell, A. D., Brandner, S., Jefferys, J. G., and Collinge, J. (2007) Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice Neuron 53, 325-335
26. Caughey, B. and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26, 267-298
27. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300, 486-489
28. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T. M., Milton, S. C., Hall, J. E., and Glabe, C. G. (2004) Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279, 46363-46366
29. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
30. Kodali, R. and Wetzel, R. (2007) Polymorphism in the intermediates and products of amyloid assembly Curr. Opin. Struct. Biol. 17, 48-57
31. Kumar, S. and Udgaonkar, J. B. (2010) Mechanisms of amyloid fibril formation by proteins Curr. Sci. 98, 639-656
32. Seshadri, S., Khurana, R., and Fink, A. L. (1999) Fourier transform infrared spectroscopy in analysis of protein deposits Methods Enzymol. 309, 559-576
33. Zandomeneghi, G., Krebs, M. R., McCammon, M. G., and Fandrich, M. (2004) FTIR reveals structural differences between native β-sheet proteins and amyloid fibrils Protein Sci. 13, 3314-3321
34. Susi, H. (1972) Infrared spectroscopy: Conformation Methods Enzymol. 26 (Part C) 455-472
35. Prusiner, S. B. (2004) Prion biology and diseases, Cold Spring Harbor Monograph Series, Cold Spring Harbor Laboratory Press, Plainview, NY.
36. Apetri, A. C., Vanik, D. L., and Surewicz, W. K. (2005) Polymorphism at Residue 129 Modulates the Conformational Conversion of the D178N Variant of Human Prion Protein 90-231 Biochemistry 44, 15880-15888
37. Jones, E. M., Surewicz, K., and Surewicz, W. K. (2006) Role of N-terminal Familial Mutations in Prion Protein Fibrillization and Prion Amyloid Propagation in Vitro J. Biol. Chem. 281, 8190-8196
38. Mukhopadhyay, S., Nayak, P. K., Udgaonkar, J. B., and Krishnamoorthy, G. (2006) Characterization of the formation of amyloid protofibrils from barstar by mapping residue-specific fluorescence dynamics J. Mol. Biol. 358, 935-942
39. Apetri, M. M., Maiti, N. C., Zagorski, M. G., Carey, P. R., and Anderson, V. E. (2006) Secondary structure of α-synuclein oligomers: Characterization by Raman and atomic force microscopy J. Mol. Biol. 355, 63-71
40. Kheterpal, I., Chen, M., Cook, K. D., and Wetzel, R. (2006) Structural differences in Aβ amyloid protofibrils and fibrils mapped by hydrogen exchange: Mass spectrometry with on-line proteolytic fragmentation J. Mol. Biol. 361, 785-795
41. Gosal, W. S., Morten, I. J., Hewitt, E. W., Smith, D. A., Thomson, N. H., and Radford, S. E. (2005) Competing pathways determine fibril morphology in the self-assembly of β2-microglobulin into amyloid J. Mol. Biol. 351, 850-864
42. Chen, Y. R. and Glabe, C. G. (2006) Distinct early folding and aggregation properties of Alzheimer amyloid-β peptides Aβ40 and Aβ42: Stable trimer or tetramer formation by Aβ42 J. Biol. Chem. 281, 24414-24422
43. Hong, D. P., Ahmad, A., and Fink, A. L. (2006) Fibrillation of human insulin A and B chains Biochemistry 45, 9342-9353
44. Chien, P., Weissman, J. S., and DePace, A. H. (2004) Emerging principles of conformation-based prion inheritance Annu. Rev. Biochem. 73, 617-656
45. Rezaei, H., Eghiaian, F., Perez, J., Doublet, B., Choiset, Y., Haertle, T., and Grosclaude, J. (2005) Sequential generation of two structurally distinct ovine prion protein soluble oligomers displaying different biochemical reactivities J. Mol. Biol. 347, 665-679
46. Vendrely, C., Valadie, H., Bednarova, L., Cardin, L., Pasdeloup, M., Cappadoro, J., Bednar, J., Rinaudo, M., and Jamin, M. (2005) Assembly of the full-length recombinant mouse prion protein I. Formation of soluble oligomers Biochim. Biophys. Acta 1724, 355-366
47. Eghiaian, F., Daubenfeld, T., Quenet, Y., van Audenhaege, M., Bouin, A. P., van der Rest, G., Grosclaude, J., and Rezaei, H. (2007) Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage Proc. Natl. Acad. Sci. U.S.A. 104, 7414-7419
48. Bader, R., Bamford, R., Zurdo, J., Luisi, B. F., and Dobson, C. M. (2006) Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation J. Mol. Biol. 356, 189-208
49. Modler, A. J., Gast, K., Lutsch, G., and Damaschun, G. (2003) Assembly of amyloid protofibrils via critical oligomers: A novel pathway of amyloid formation J. Mol. Biol. 325, 135-148
50. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F., and Caughey, B. (2005) The most infectious prion protein particles Nature 437, 257-261
51. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.