Hydration water mobility is enhanced around tau amyloid fibers

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 20, 2015, Pages 6365-6370

  Fichoua, Yann ^a,b   Schirò, Giorgio ^a,b   Gallat, François Xavier ^a,b   Laguri, Cedric ^a,b   Moulin, Martine ^c   Combet, Jérôme ^c,d   Zamponi, Michaela ^e   Härtlein, Michael ^c   Picart, Catherine ^a,f   Mossou, Estelle ^c,g   Lortat Jacob, Hugues ^a,b   Colletier, Jacques Philippe ^a,b   Tobias, Douglas J ^h   Weik, Martin ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c INSTITUT LAUE LANGEVIN   (France)

^d INSTITUT CHARLES SADRON   (France)

^e FORSCHUNGSZENTRUM JÜLICH   (Germany)

^f LABORATOIRE DES MATÉRIAUX ET DU GÉNIE PHYSIQUE   (France)

^g KEELE UNIVERSITY   (United Kingdom)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid fibers; Hydration water; Intrinsically disordered proteins; Neutron scattering; Tau protein

Indexed keywords

AMYLOID; HEXAPEPTIDE; HYDROGEN; TAU PROTEIN; WATER; MEMBRANE PROTEIN; TAU 40 PROTEIN, HUMAN;

ARTICLE; DIFFUSION WEIGHTED IMAGING; HUMAN; HYDRATION; HYDRATION WATER MOBILITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; NEUTRON SCATTERING; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; WATER ANALYSIS; WATER FLOW; ALZHEIMER DISEASE; BIOSYNTHESIS; CHEMICAL MODEL; CHEMISTRY; ELECTRON MICROSCOPY; METABOLISM; PROTEINOSIS;

ALZHEIMER DISEASE; AMYLOID; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MODELS, CHEMICAL; MOLECULAR DYNAMICS SIMULATION; PROTEIN AGGREGATION, PATHOLOGICAL; WATER;

EID: 84929587507     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422824112     Document Type: Article

References (59)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75(1):333-366.
2. Lednev IK (2014) Amyloid fibrils: The eighth wonder of the world in protein folding and aggregation. Biophys J 106(7):1433-1435.
3. Uversky VN, Oldfield CJ, Dunker AK (2008) Intrinsically disordered proteins in human diseases: Introducing the D2 concept. Annu Rev Biophys 37(1):215-246.
4. Brion JP, Couck AM, Passareiro E, Flament-Durand J (1985) Neurofibrillary tangles of Alzheimer's disease: An immunohistochemical study. J Submicrosc Cytol 17(1):89-96.
5. Kosik KS, Joachim CL, Selkoe DJ (1986) Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci USA 83(11):4044-4048.
6. Mandelkow EM, Mandelkow E (2012) Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med 2(7):a006247.
7. Amos LA (2004) Microtubule structure and its stabilisation. Org Biomol Chem 2(15):2153-2160.
8. von Bergen M, et al. (2000) Assembly of τ protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQIVYK(311)) forming β structure. Proc Natl Acad Sci USA 97(10):5129-5134.
9. Wischik CM, et al. (1988) Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA 85(12):4506-4510.
10. Crowther T, Goedert M, Wischik CM (1989) The repeat region of microtubule-associated protein tau forms part of the core of the paired helical filament of Alzheimer's disease. Ann Med 21(2):127-132.
11. Bibow S, et al. (2011) The dynamic structure of filamentous tau. Angew Chem Int Ed Engl 50(48):11520-11524.
12. Ball P (2008) Water as an active constituent in cell biology. Chem Rev 108(1):74-108.
13. Gallat F-X, et al. (2012) Dynamical coupling of intrinsically disordered proteins and their hydration water: Comparison with folded soluble and membrane proteins. Biophys J 103(1):129-136.
14. Thirumalai D, Reddy G, Straub JE (2012) Role of water in protein aggregation and amyloid polymorphism. Acc Chem Res 45(1):83-92.
15. Chong S-H, Ham S (2014) Interaction with the surrounding water plays a key role in determining the aggregation propensity of proteins. Angew Chem Int Ed Engl 53(15):3961-3964.
16. Bellissent-Funel M, Chen SH, Zanotti J (1995) Single-particle dynamics of water molecules in confined space. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 51(5):4558-4569.
17. Russo D, Hura G, Head-Gordon T (2004) Hydration dynamics near a model protein surface. Biophys J 86(3):1852-1862.
18. Bellissent-Funel M-C, Teixeira J, Bradley K-F, Chen SH (1992) Dynamics of hydration water in protein. J Phys I 2(6):995-1001.
19. Doster W, et al. (2010) Dynamical transition of protein-hydration water. Phys Rev Lett 104(9):098101.
20. Achterhold K, et al. (2011) Dynamical properties of the hydration shell of fully deuterated myoglobin. Phys Rev E Stat Nonlin Soft Matter Phys 84(4 Pt 1):041930.
21. Nickels JD, et al. (2012) Dynamics of protein and its hydration water: Neutron scattering studies on fully deuterated GFP. Biophys J 103(7):1566-1575.
22. Frolich A, et al. (2009) From shell to cell: Neutron scattering studies of biological water dynamics and coupling to activity. Faraday Discuss 141:117-30, and discussion (2009) 141:175-207.
23. Gabel F, et al. (2002) Protein dynamics studied by neutron scattering. Q Rev Biophys 35(4):327-367.
24. Bizzarri AR (2004) Neutron scattering and molecular dynamics simulation: A conjugate approach to investigate the dynamics of electron transfer proteins. J Phys Condens Matter 16(6):R83-R110.
25. Goedert M, et al. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383(6600):550-553.
26. Astbury WT, Dickinson S, Bailey K (1935) The X-ray interpretation of denaturation and the structure of the seed globulins. Biochem J 29(10):2351-2360-1.
27. Sunde M, et al. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 273(3):729-739.
28. Wood K, et al. (2008) Coincidence of dynamical transitions in a soluble protein and its hydration water: Direct measurements by neutron scattering and MD simulations. J Am Chem Soc 130(14):4586-4587.
29. Schiró G, et al. (2015) Translational diffusion of hydration water correlates with functional motions in folded and intrinsically disordered proteins, Nat Commun 6:6490.
30. Becker T, Smith JC (2003) Energy resolution and dynamical heterogeneity effects on elastic incoherent neutron scattering from molecular systems. Phys Rev E Stat Nonlin Soft Matter Phys 67(2 Pt 1):021904.
31. Yi Z, Miao Y, Baudry J, Jain N, Smith JC (2012) Derivation of mean-square displacements for protein dynamics from elastic incoherent neutron scattering. J Phys Chem B 116(16):5028-5036.
32. Sievers SA, et al. (2011) Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation. Nature 475(7354):96-100.
33. Berhanu WM, Masunov AE (2011) Can molecular dynamics simulations assist in design of specific inhibitors and imaging agents of amyloid aggregation? Structure, stability and free energy predictions for amyloid oligomers of VQIVYK, MVGGVV and LYQLEN. J Mol Model 17(10):2423-2442.
34. Sawaya MR, et al. (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447(7143):453-457.
35. Zhao J-H, et al. (2010) Molecular dynamics simulations to investigate the stability and aggregation behaviour of the amyloid-forming peptide VQIVYK from tau protein. Mol Simul 36(13):1013-1024.
36. Tarek M, Tobias DJ (2002) Role of protein-water hydrogen bond dynamics in the protein dynamical transition. Phys Rev Lett 88(13):138101.
37. Jana B, Pal S, Bagchi B (2008) Hydrogen bond breaking mechanism and water reorientational dynamics in the hydration layer of lysozyme. J Phys Chem B 112(30):9112-9117.
38. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105-132.
39. Pavlova A, et al. (2009) Site-specific dynamic nuclear polarization of hydration water as a generally applicable approach to monitor protein aggregation. Phys Chem Chem Phys 11(31):6833-6839.
40. Zhang L, et al. (2007) Mapping hydration dynamics around a protein surface. Proc Natl Acad Sci USA 104(47):18461-18466.
41. Luise A, Falconi M, Desideri A (2000) Molecular dynamics simulation of solvated azurin: correlation between surface solvent accessibility and water residence times. Proteins 39(1):56-67.
42. Makarov VA, Andrews BK, Smith PE, Pettitt BM (2000) Residence times of water molecules in the hydration sites of myoglobin. Biophys J 79(6):2966-2974.
43. Sterpone F, Stirnemann G, Laage D (2012) Magnitude and molecular origin of water slowdown next to a protein. J Am Chem Soc 134(9):4116-4119.
44. Bagchi K, Roy S (2014) Sensitivity of water dynamics to biologically significant surfaces of monomeric insulin: Role of topology and electrostatic interactions. J Phys Chem B 118(14):3805-3813.
45. Wegmann S, Medalsy ID, Mandelkow E, Müller DJ (2013) The fuzzy coat of pathological human Tau fibrils is a two-layered polyelectrolyte brush. Proc Natl Acad Sci USA 110(4):E313-E321.
46. Swenson J, Bergman R, Longeville S, Howells WS (2001) Dynamics of 2D-water as studied by quasi-elastic neutron scattering and neutron resonance spin-echo. Physica B 301(1-2):28-34.
47. Hummer G, Rasaiah JC, Noworyta JP (2001) Water conduction through the hydrophobic channel of a carbon nanotube. Nature 414(6860):188-190.
48. Harano Y, Kinoshita M (2004) Large gain in translational entropy of water is a major driving force in protein folding. Chem Phys Lett 399(4-6):342-348.
49. Breiten B, et al. (2013) Water networks contribute to enthalpy/entropy compensation in protein-ligand binding. J Am Chem Soc 135(41):15579-15584.
50. Brovchenko I, Oleinikova A (2008) Which properties of a spanning network of hydration water enable biological functions? ChemPhysChem 9(18):2695-2702.
51. Nelson R, et al. (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435(7043):773-778.
52. Sasikala WD, Mukherjee A (2014) Single water entropy: Hydrophobic crossover and application to drug binding. J Phys Chem B 118(36):10553-10564.
53. Kantarci K, et al. (2005) DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology 64(5):902-904.
54. Nir TM, et al.; Alzheimer's Disease Neuroimaging Initiative (2013) Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging. Neuroimage Clin 3:180-195.
55. Le Bihan D, Johansen-Berg H (2012) Diffusion MRI at 25: Exploring brain tissue structure and function. Neuroimage 61(2):324-341.
56. Itoh Y, Amano N, Inoue M, Yagishita S (1997) Scanning electron microscopical study of the neurofibrillary tangles of Alzheimer's disease. Acta Neuropathol 94(1):78-86.
57. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239-259.
58. Wuttke J, et al. (2012) SPHERES, Jülich's high-flux neutron backscattering spectrometer at FRM II. Rev Sci Instrum 83(7):075109.
59. Frick B, Gonzalez M (2001) Five years operation of the second generation backscattering spectrometer IN16 - A retrospective, recent developments and plans. Physica B 301(1-2):8-19.