Cross-strand pairing and amyloid assembly.

Amino acid cross-strand pairing interactions along a beta-sheet surface have been implicated in protein beta-structural assembly and stability, yet the relative contributions have been difficult to evaluate directly. Here we develop the central core sequence of the Abeta peptide associated with Alzheimer's disease, Abeta(16-22), as an experimental system for evaluating these interactions. The peptide allows for internal comparisons between electrostatic and steric interactions within the beta-sheet and an evaluation of these cross-strand pair contributions to beta-sheet registry. A morphological transition from fibers to hollow nanotubes arises from changes in beta-sheet surface complementarity and provides a convenient indicator of the beta-strand strand registry. The intrinsic beta-sequence and pair correlations are critical to regulate secondary assembly. These studies provide evidence for a critical desolvation step that is not present in most models of the nucleation-dependent pathway for amyloid assembly.

[1]  J. Snyder,et al.  Facial symmetry in protein self-assembly. , 2008, Journal of the American Chemical Society.

[2]  Seokmin Shin,et al.  Computational study on the structural diversity of amyloid Beta Peptide (abeta(10-35)) oligomers. , 2008, The journal of physical chemistry. B.

[3]  K. Makabe,et al.  Beta-strand flipping and slipping triggered by turn replacement reveal the opportunistic nature of beta-strand pairing. , 2007, Journal of the American Chemical Society.

[4]  Elizabeth Head,et al.  Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers , 2007, Molecular Neurodegeneration.

[5]  Junichi Higo,et al.  Simulation study on the disordered state of an Alzheimer's β amyloid peptide Aβ(12–36) in water consisting of random‐structural, β‐structural, and helical clusters , 2007, Protein science : a publication of the Protein Society.

[6]  K. Makabe,et al.  Hydrophobic surface burial is the major stability determinant of a flat, single-layer beta-sheet. , 2007, Journal of molecular biology.

[7]  R. Kayed,et al.  Small Molecule Inhibitors of Aggregation Indicate That Amyloid β Oligomerization and Fibrillization Pathways Are Independent and Distinct* , 2007, Journal of Biological Chemistry.

[8]  Shohei Koide,et al.  Atomic structures of peptide self-assembly mimics , 2006, Proceedings of the National Academy of Sciences.

[9]  David Rodriguez-Larrea,et al.  Energetic and structural consequences of desolvation/solvation barriers to protein folding/unfolding assessed from experimental unfolding rates. , 2006, Biophysical journal.

[10]  R. Wetzel.  Kinetics and thermodynamics of amyloid fibril assembly. , 2006, Accounts of chemical research.

[11]  S. Decatur.  Elucidation of Residue-Level Structure and Dynamics of Polypeptides via Isotope-Edited Infrared Spectroscopy , 2006 .

[12]  T. Funck,et al.  Protein amyloidogenesis in the context of volume fluctuations: a case study on insulin. , 2006, Chemphyschem : a European journal of chemical physics and physical chemistry.

[13]  A. Mehta,et al.  Controlling amyloid growth in multiple dimensions , 2006, Amyloid : the international journal of experimental and clinical investigation : the official journal of the International Society of Amyloidosis.

[14]  P. Westermark.  Aspects on human amyloid forms and their fibril polypeptides , 2005, The FEBS journal.

[15]  T. Kitagawa,et al.  FT-IR approaches on amyloid fibril structure. , 2005, Biochimica et biophysica acta.

[16]  R. Jansen,et al.  Ethanol-perturbed amyloidogenic self-assembly of insulin: looking for origins of amyloid strains. , 2005, Biochemistry.

[17]  P. Axelsen,et al.  β Sheet Structure in Amyloid β Fibrils and Vibrational Dipolar Coupling , 2005 .

[18]  C. Hall,et al.  Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Dobson.  Experimental investigation of protein folding and misfolding. , 2004, Methods.

[20]  Roger D Kamm,et al.  Kinetic control of dimer structure formation in amyloid fibrillogenesis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  V. Uversky,et al.  Conformational constraints for amyloid fibrillation: the importance of being unfolded. , 2004, Biochimica et biophysica acta.

[22]  Roland Winter,et al.  Hydration and structure?the two sides of the insulin aggregation process , 2004 .

[23]  H. Stanley,et al.  Molecular Dynamics Simulation of Amyloid β Dimer Formation , 2004, physics/0403040.

[24]  C. Dobson.  Protein folding and misfolding , 2003, Nature.

[25]  L. Serpell,et al.  Structure and texture of fibrous crystals formed by Alzheimer's abeta(11-25) peptide fragment. , 2003, Structure.

[26]  V. Conticello,et al.  Exploiting amyloid fibril lamination for nanotube self-assembly. , 2003, Journal of the American Chemical Society.

[27]  Ariel Fernández,et al.  Protein folding: could hydrophobic collapse be coupled with hydrogen‐bond formation? , 2003, FEBS letters.

[28]  R. Leapman,et al.  Supramolecular structural constraints on Alzheimer's beta-amyloid fibrils from electron microscopy and solid-state nuclear magnetic resonance. , 2002, Biochemistry.

[29]  D. M. Morgan,et al.  Dynamics and fluidity of amyloid fibrils: a model of fibrous protein aggregates. , 2002, Journal of the American Chemical Society.

[30]  D. M. Morgan,et al.  Metal switch for amyloid formation: insight into the structure of the nucleus. , 2002, Journal of the American Chemical Society.

[31]  Ariel Fernández,et al.  Dynamics of hydrogen bond desolvation in protein folding. , 2002, Journal of molecular biology.

[32]  Ruth Nussinov,et al.  Close‐Range Electrostatic Interactions in Proteins , 2002, Chembiochem : a European journal of chemical biology.

[33]  R. L. Baldwin,et al.  Role of backbone solvation in determining thermodynamic β propensities of the amino acids , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Neysa Nevins,et al.  Calculated conformer energies for organic molecules with multiple polar functionalities are method dependent: Taxol (case study) , 2001, BMC chemical biology.

[35]  T. Keiderling,et al.  The Anomalous Infrared Amide I Intensity Distribution in 13C Isotopically Labeled Peptide β-Sheets Comes from Extended, Multiple-Stranded Structures. An ab Initio Study [J. Am. Chem. Soc. 2001, 123, 6142−6150]. , 2001 .

[36]  J. Thornton,et al.  Determinants of strand register in antiparallel β‐sheets of proteins , 1998, Protein science : a publication of the Protein Society.

[37]  L. Serpell,et al.  Common core structure of amyloid fibrils by synchrotron X-ray diffraction. , 1997, Journal of molecular biology.

[38]  Louise C. Serpell,et al.  Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix , 1996 .

[39]  L. Regan,et al.  Guidelines for Protein Design: The Energetics of β Sheet Side Chain Interactions , 1995, Science.

[40]  M. A. Wouters,et al.  An analysis of side chain interactions and pair correlations within antiparallel β‐sheets: The differences between backbone hydrogen‐bonded and non‐hydrogen‐bonded residue pairs , 1995, Proteins.

[41]  B. Honig,et al.  Classical electrostatics in biology and chemistry. , 1995, Science.

[42]  P. S. Kim,et al.  Context is a major determinant of β-sheet propensity , 1994, Nature.

[43]  P. S. Kim,et al.  Measurement of the β-sheet-forming propensities of amino acids , 1994, Nature.

[44]  B. Tidor,et al.  Do salt bridges stabilize proteins? A continuum electrostatic analysis , 1994, Protein science : a publication of the Protein Society.

[45]  B. Matthews,et al.  Structural basis of amino acid alpha helix propensity. , 1993, Science.

[46]  Jeremy M. Berg,et al.  Thermodynamic β -sheet propensities measured using a zinc-finger host peptide , 1993, Nature.

[47]  A. Fersht,et al.  Alpha-helix stability in proteins. II. Factors that influence stability at an internal position. , 1992, Journal of molecular biology.

[48]  P. Lansbury,et al.  Location of .beta.-sheet-forming sequences in amyloid proteins by FTIR , 1991 .

[49]  W. DeGrado,et al.  A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. , 1990, Science.

[50]  N R Kallenbach,et al.  Side chain contributions to the stability of alpha-helical structure in peptides. , 1990, Science.

[51]  Robert L. Baldwin,et al.  Relative helix-forming tendencies of nonpolar amino acids , 1990, Nature.

[52]  E. J. Ambrose,et al.  Chain Configurations in Natured and Denatured Insulin: Evidence from infra-red Spectra , 1950, Nature.

[53]  S. Decatur,et al.  Experimental evidence for the reorganization of beta-strands within aggregates of the Abeta(16-22) peptide. , 2005, Journal of the American Chemical Society.

[54]  L. Gregoret,et al.  Context-dependence of amino acid residue pairing in antiparallel beta-sheets. , 1999, Journal of molecular biology.

[55]  P. Lansbury,et al.  Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. , 1997, Annual review of biochemistry.

[56]  G. Rose,et al.  Hydrophobicity of amino acid subgroups in proteins , 1990, Proteins.

[57]  H. Scheraga,et al.  Helix‐coil stability constants for the naturally occurring amino acids in water. XXIII. Proline parameters from random poly(hydroxybutylglutamine‐CO‐L‐proline) , 1990, Biopolymers.