Basic Equations in Statics and Kinetics of Protein Polymerization and the Mechanism of the Formation and Dissociation of Amyloid Fibrils Revealed by Pressure Perturbation

Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 72)

Abstract

Studies of the pressure-dissociation of several amyloid or amyloid-like fibrils have shown that the fibril state is considerably voluminous. Quantitative characterization of the protein fibrillation reaction with respect to volumetric parameters is necessary to elucidate mechanisms of amyloid fibrillation in molecular terms such as protein cavity and hydration. Here we discuss, firstly, basic equations in statics and kinetics of protein polymerization as employed to obtain thermodynamic, volumetric, and kinetic parameters. Equilibrium treatment of the reactions with the scheme such as one-step polymerization, linear-association polymerization, or nucleation-dependent polymerization, and kinetic treatment of seeded linear-polymerization or spontaneous nucleation-elongation polymerization are described. In particular we will detail kinetics of the dissociation of fibrils which have been produced under the linear-association mechanism and therefore the length-distribution of which conforms to a geometric sequence in the degree of polymerization with a common ratio r, which is less than, and usually very close to, unity. In this case, an observed macroscopic rate of dissociation is shown to be a product of the microscopic elementary dissociation rate constant and a factor (1–r), extremely reduced compared with the intrinsic elementary rate. Secondly, we discuss protein conformational states in fibrillogenesis with molecular and volumetric observations reported, such as the unfolded state responsible for the association with seeds and the extension of amyloid fibrils, the transition state in which protein cavity formation and dehydration occur to intermediate levels, and the fibril state in which they occur to final respective levels which, in some cases, depend on the maturity of the fibril.

Keywords

Amyloid fibril β2-microglobulin Cavity and hydration Lysozyme Partial specific volume Unfolded state 
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Notes

Acknowledgements

The author thanks Dr K Sakurai for valuable discussions about β2-m studies, and Prof K Akasaka for inspiring general discussions.

References

  1. Abdul Latif QR, Kono R, Tachibana H, Akasaka K (2007) Kinetic analysis of amyloid protofibril dissociation and volumetric properties of the transition state. Biophys J 92:323–329PubMedCentralCrossRefPubMedGoogle Scholar
  2. Akasaka K (2006) Probing conformational fluctuation of proteins by pressure perturbation. Chem Rev 106:1814–1835CrossRefPubMedGoogle Scholar
  3. Akasaka K, Abdul Latif AR, Nakamura A, Matsuo K, Tachibana H, Gekko K (2007) Amyloid protofibril is highly voluminous and compressible. Biochemistry 46:10444–10450CrossRefPubMedGoogle Scholar
  4. Akasaka K, Nagahata H, Maeno A, Sasaki K (2008) Pressure acceleration of proteolysis: a general mechanism. Biophysics 4:29–32CrossRefGoogle Scholar
  5. Akasaka K, Maeno A, Murayama T, Tachibana H, Fujita Y, Yamanaka H, Nishida N, Atarashi R (2014) Pressure-assisted dissociation and degradation of “proteinase K-resistant” fibrils prepared by seeding with scrapie-infected hamster prion protein. Prion 8:314–318CrossRefPubMedGoogle Scholar
  6. Ban T, Yamaguchi K, Goto Y (2006) Direct observation of amyloid fibril growth, propagation, and adaptation. Acc Chem Res 39:663–670CrossRefPubMedGoogle Scholar
  7. Booth DR, Sunde M, Belloti V, Robinson CV, Hutchinson WL, Fraser PE, Hawkins PN, Dobson CM, Radford SE, Blake CC, Pepys MB (1997) Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385:787–793CrossRefPubMedGoogle Scholar
  8. Cantor CR, Schimmel PR (1980) Biophysical chemistry, Part I. WH Freeman & Company, New YorkGoogle Scholar
  9. Cordeiro Y, Kraineva J, Ravindra R, Mauricio L, Lima TR, Gomes MPB, Foguel D, Winter R, Silva JL (2004) Hydration and packing effects on prion folding and beta-sheet conversion. J Biol Chem 279:32354–32359CrossRefPubMedGoogle Scholar
  10. Dirix C, Meersman F, MacPhee CE, Dobson CM, Heremans K (2005) High hydrostatic pressure dissociates early aggregates of TTR105-115, but not the mature amyloid fibrils. J Mol Biol 347:903–909CrossRefPubMedGoogle Scholar
  11. Fink AL (1998) Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des 3:R9–R23CrossRefPubMedGoogle Scholar
  12. Foguel D, Silva JL (2004) New insights into the mechanism of protein misfolding and aggregation in amyloidogenic disease derived from pressure studies. Biochemistry 43:11361–11370CrossRefPubMedGoogle Scholar
  13. Ikkai T, Ooi T, Noguchi H (1965) Actin: volume change on transformation of G-form to F-form. Science 152:1756–1757CrossRefGoogle Scholar
  14. Jansen R, Grudzielanek S, Dzwolak W, Winter R (2004) High pressure promotes circularly shaped insulin amyloid. J Mol Biol 338:203–206CrossRefPubMedGoogle Scholar
  15. Josephs R, Harrington WF (1967) An unusual pressure dependence for a reversibly associated protein system; sedimentation studies on myosin. Proc Natl Acad Sci U S A 58:1587–1594PubMedCentralCrossRefPubMedGoogle Scholar
  16. Kelly JW (1998) The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr Opin Struct Biol 8:101–106CrossRefPubMedGoogle Scholar
  17. Klein-Seetharaman J, Oikawa M, Grimshaw SB, Wirmer J, Duchardt E, Ueda T, Imoto T, Smith LJ, Dobson CM, Schwalbe H (2002) Long-range interactions within a non-native protein. Science 295:1719–1722CrossRefPubMedGoogle Scholar
  18. Knowles TJ, Waudby CA, Devlin GL, Cohen SA, Aguzzi A, Vendruscolo M, Terenjev EM, Welland ME, Dobson CM (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326:1533–1537CrossRefPubMedGoogle Scholar
  19. Kodaka M (2004) Interpretation of concentration-dependence in aggregation kinetics. Biophys Chem 109:325–332CrossRefPubMedGoogle Scholar
  20. Kono R, Fujisawa T, Akasaka K, Tachibana H (2009) Amyloid fibrillation rate differs greatly among single-disulfide variants of hen lysozyme. J Biol Macromol 9:23–30Google Scholar
  21. Lansbury PT Jr (1999) Evolution of amyloid: what normal protein folding may tell us about fibrillogenesis and disease. Proc Natl Acad Sci U S A 96:3342–3344PubMedCentralCrossRefPubMedGoogle Scholar
  22. Lee YH, Chatani E, Sasahahara K, Naiki H, Goto Y (2009) A comprehensive model for packing and hydration for amyloid fibrils of beta2-microglobulin. J Biol Chem 284:2169–2175CrossRefPubMedGoogle Scholar
  23. Matsuo K, Watanabe H, Tate S, Tachibana H, Gekko K (2009) Comprehensive secondary-structure analysis of disulfide variants of lysozyme by synchrotron-radiation vacuum-ultraviolet circular dichroism. Proteins 77:191–201CrossRefPubMedGoogle Scholar
  24. Meersman F, Dobson CM (2006) Probing the pressure-temperature stability of amyloid fibrils provides new insights into their molecular properties. Biochim Biophys Acta 1764:452–460CrossRefPubMedGoogle Scholar
  25. Morris AM, Watzky MA, Finke RG (2009) Protein aggregation kinetics, mechanism, and curve-fitting: A review of the literature. Biochim Biophys Acta 1794:375–397CrossRefPubMedGoogle Scholar
  26. Niraula TN, Konno T, Li H, Yamada H, Akasaka K, Tachibana H (2004) Pressure-dissociable reversible assembly of intrinsically denatured lysozyme is a precursor for amyloid fibrils. Proc Natl Acad Sci U S A 101:4089–4093PubMedCentralCrossRefPubMedGoogle Scholar
  27. Noda Y, Narama K, Kasai K, Tachibana H, Segawa S (2012) Glycerol-enhanced detection of a preferential structure latent in unstructured 1SS-variants of lysozyme. Biopolymers 97:539–549CrossRefPubMedGoogle Scholar
  28. Oosawa F, Asakura S (1975) Thermodynamics of the polymerization of protein. Academic, LondonGoogle Scholar
  29. Oosawa F, Asakura S, Hotta K, Nobuhisa I, Ooi T (1959) G-F transformation of actin as a fibrous condensation. J Polym Sci 37:323–336CrossRefGoogle Scholar
  30. Royer CA (1995) Application of pressure to biochemical equilibria: the other thermodynamic variable. Methods Enzymol 259:357–377CrossRefPubMedGoogle Scholar
  31. Royer CA (2002) Revisiting volume changes in pressure-induced protein unfolding. Biochim Biophys Acta 1595:201–209CrossRefPubMedGoogle Scholar
  32. Sasaki K, Nakatsuka K, Hayashi I, Shah BR, Morimoto K, Akasaka K (2008) Efficient conversion of intact hen lysozyme into amyloid fibrils by seeding. J Biol Macromol 8:11–18CrossRefGoogle Scholar
  33. Shah BR, Maeno A, Matsuo H, Tachibana H, Akasaka K (2012) Pressure-dissociation of amyloid fibrils in wild-type hen lysozyme. Biophys J 102:121–126PubMedCentralCrossRefPubMedGoogle Scholar
  34. Silva JL, Weber G (1993) Pressure stability of proteins. Annu Rev Phys Chem 44:89–113CrossRefPubMedGoogle Scholar
  35. Silva JL, Foguel D, Royer CA (2001) Pressure provides new insights into protein folding, dynamics and structure. Trends Biochem Sci 26:612–618CrossRefPubMedGoogle Scholar
  36. Silva JL, Cordeiro Y, Foguel D (2006) Protein folding and aggregation: two sides of the same coin in the condensation of proteins revealed by pressure studies. Biochim Biophys Acta 1764:443–451CrossRefPubMedGoogle Scholar
  37. Silva JL, de Oliveira AC, Vieira TCR, de Oliveira GAP, Suarez MC, Foguel D (2014) High-pressure chemical biology and biotechnology. Chem Rev 114:7239–7267CrossRefPubMedGoogle Scholar
  38. Smirnovas V, Winter R (2008) Revealing different aggregation pathways of amyloidogenic proteins by ultrasound velocimetry. Biophys J 94:3241–3246PubMedCentralCrossRefPubMedGoogle Scholar
  39. Smirnovas V, Winter R, Funk T, Dzwolak W (2006) Protein amyloidogenesis in the context of volume fluctuations: a case study of insulin. Chem Phys Chem 7:1046–1049PubMedGoogle Scholar
  40. Tachibana H (2000) Propensities for the formation of individual disulfide bonds in hen lysozyme and the size and stability of disulfide-associated submolecular structures. FEBS Lett 480:175–178CrossRefPubMedGoogle Scholar
  41. Tachibana H, Segawa S (2004) Disulfide-bond associated protein folding. In: Nalwa HS (ed) Encyclopedia of nanoscience and nanotechnology, vol 2. American Scientific Publishers, Los Angeles, pp 443–473Google Scholar
  42. Watzky MA, Finke RG (1997) Transition metal nanocluster formation kinetic and mechanistic studies. A new mechanism when hydrogen is the reductant: slow, continuous nucleation and fast autocatalytic surface growth. J Am Chem Soc 119:10382–10400CrossRefGoogle Scholar
  43. Yanagi K, Sakurai K, Yoshimura Y, Konuma T, Lee YH, Sugase K, Ikegami T, Naiki H, Goto Y (2012) The monomer-seed interaction mechanism in the formation of the beta2-microglobulin amyloid fibril clarified by solution NMR techniques. J Mol Biol 422:390–402CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of Biotechnological Science, School of Biology-Oriented Science and Technology, and High Pressure Protein Research Center, Institute of Advanced TechnologyKinki UniversityKinokawaJapan

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