Secondary structure and rigidity in model proteins.

There is tremendous interest in understanding the role that secondary structure plays in the rigidity and dynamics of proteins. In this work we analyze nanomechanical properties of proteins chosen to represent different secondary structures: α-helices (myoglobin and bovine serum albumin), β-barrels (green fluorescent protein), and α + β + loop structures (lysozyme). Our experimental results show that in these model proteins, the β motif is a stiffer structural unit than the α-helix in both dry and hydrated states. This difference appears not only in the rigidity of the protein, but also in the amplitude of fast picosecond fluctuations. Moreover, we show that for these examples the secondary structure correlates with the temperature- and hydration-induced changes in the protein dynamics and rigidity. Analysis also suggests a connection between the length of the secondary structure (α-helices) and the low-frequency vibrational mode, the so-called boson peak. The presented results suggest an intimate connection of dynamics and rigidity with the protein secondary structure.

[1]  John R. D. Copley,et al.  DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data , 2009, Journal of research of the National Institute of Standards and Technology.

[2]  Jeremy C. Smith,et al.  Elastic and conformational softness of a globular protein. , 2013, Physical review letters.

[3]  K. Chou,et al.  Low-frequency vibrations of helical structures in protein molecules. , 1983, The Biochemical journal.

[4]  A. Kisliuk,et al.  A broad glass transition in hydrated proteins. , 2010, Biochimica et biophysica acta.

[5]  Robert Fredriksson,et al.  Mapping the human membrane proteome : a majority of the human membrane proteins can be classified according to function and evolutionary origin , 2015 .

[6]  Markus J. Buehler,et al.  Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of α-helical and β-sheet protein domains , 2007, Proceedings of the National Academy of Sciences.

[7]  D. Engelman,et al.  A dimerization motif for transmembrane α–helices , 1994, Nature Structural Biology.

[8]  O. Nielsen.  Chapter 2. Low-frequency spetroscopic studies of interactions in liquids , 1993 .

[9]  J. L. Lippert,et al.  RAMAN SCATTERING FROM LONGITUDINAL ACOUSTICAL VIBRATIONS OF SINGLE CRYSTALS OF POLYETHYLENE , 1971 .

[10]  A. Paciaroni,et al.  Broadband depolarized light scattering study of diluted protein aqueous solutions. , 2010, The journal of physical chemistry. B.

[11]  S Kriminski,et al.  Sound velocity and elasticity of tetragonal lysozyme crystals by Brillouin spectroscopy. , 2003, Biophysical journal.

[12]  D. Tobias,et al.  Effects of solvent damping on side chain and backbone contributions to the protein boson peak , 2001 .

[13]  K. Chou,et al.  Biological functions of low-frequency vibrations (phonons). III. Helical structures and microenvironment. , 1984, Biophysical journal.

[14]  Markus J Buehler,et al.  Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. , 2008, Nano letters.

[15]  W. Doster,et al.  Dynamics of well-folded and natively disordered proteins in solution: a time-of-flight neutron scattering study , 2008, European Biophysics Journal.

[16]  V. Urban,et al.  Characterization of sol-gel-encapsulated proteins using small-angle neutron scattering. , 2009, ACS applied materials & interfaces.

[17]  G. Schirò,et al.  The “Protein Dynamical Transition” Does Not Require the Protein Polypeptide Chain , 2011 .

[18]  G. Schirò,et al.  Direct evidence of the amino acid side chain and backbone contributions to protein anharmonicity. , 2010, Journal of the American Chemical Society.

[19]  C. Petrillo,et al.  Vibrational collective dynamics of dry proteins in the terahertz region. , 2012, The journal of physical chemistry. B.

[20]  G. Onori,et al.  Comparative study of protein dynamics in hydrated powders and in solutions: A neutron scattering investigation , 2008 .

[21]  Jeremy C. Smith,et al.  Low-temperature protein dynamics: a simulation analysis of interprotein vibrations and the boson peak at 150 k. , 2006, Journal of the American Chemical Society.

[22]  Dumas,et al.  Low-frequency Raman scattering from fractal vibrational modes in a silica gel. , 1986, Physical review letters.

[23]  N Go,et al.  Breathing mode of conformational fluctuations in globular proteins. , 2009, International journal of peptide and protein research.

[24]  A. Sokolov,et al.  Influence of hydration on the dynamics of lysozyme. , 2006, Biophysical journal.

[25]  G. Ehlers,et al.  The new cold neutron chopper spectrometer at the Spallation Neutron Source: design and performance. , 2011, The Review of scientific instruments.

[26]  Alasdair C. Steven,et al.  β‐Rolls, β‐Helices, and Other β‐Solenoid Proteins , 2006 .

[27]  Zhiping Xu,et al.  Mechanical energy transfer and dissipation in fibrous beta-sheet-rich proteins. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  K. Chou,et al.  Low-frequency motions in protein molecules. Beta-sheet and beta-barrel. , 1985, Biophysical journal.

[29]  J. Smith,et al.  Protein dynamics: comparison of simulations with inelastic neutron scattering experiments , 1991, Quarterly Reviews of Biophysics.

[30]  K. G. Brown,et al.  Conformationally dependent low-frequency motions of proteins by laser Raman spectroscopy. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Fritz Vollrath,et al.  Materials: Surprising strength of silkworm silk , 2002, Nature.

[32]  Jeremy C. Smith,et al.  Dynamics of protein and its hydration water: neutron scattering studies on fully deuterated GFP. , 2012, Biophysical journal.

[33]  Michele Vendruscolo,et al.  Role of Intermolecular Forces in Defining Material Properties of Protein Nanofibrils , 2007, Science.

[34]  Markus J Buehler,et al.  Deformation and failure of protein materials in physiologically extreme conditions and disease. , 2009, Nature materials.

[35]  Roger Y. Tsien,et al.  Crystal Structure of the Aequorea victoria Green Fluorescent Protein , 1996, Science.

[36]  T. Straatsma,et al.  Internal Dynamics of Green Fluorescent Protein , 1999 .

[37]  Sokolov,et al.  Comparison of Raman- and neutron-scattering data for glass-forming systems. , 1995, Physical review. B, Condensed matter.

[38]  Markus J Buehler,et al.  Nanomechanics of functional and pathological amyloid materials. , 2011, Nature nanotechnology.

[39]  H. Cummins,et al.  Low-frequency light-scattering spectroscopy of powders , 1996 .

[40]  W. Doster,et al.  Water-coupled low-frequency modes of myoglobin and lysozyme observed by inelastic neutron scattering. , 1997, Biophysical journal.

[41]  A. Boukenter,et al.  Vibrational dynamics and the structure of glasses , 1990 .

[42]  Zha,et al.  Elasticity of hydrogen to 24 GPa from single-crystal Brillouin scattering and synchrotron x-ray diffraction. , 1993, Physical review. B, Condensed matter.

[43]  Alberto Redaelli,et al.  Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. , 2010, Nano letters.

[44]  Markus J. Buehler,et al.  Nature designs tough collagen: Explaining the nanostructure of collagen fibrils , 2006, Proceedings of the National Academy of Sciences.

[45]  S. Mizushima,et al.  Raman frequencies of n-paraffin molecules. , 1949, Journal of the American Chemical Society.

[46]  Markus J. Buehler,et al.  Elasticity, strength and resilience: A comparative study on mechanical signatures of α-Helix, β-sheet and tropocollagen domains , 2008 .

[47]  Parshin.  Interactions of soft atomic potentials and universality of low-temperature properties of glasses. , 1994, Physical review. B, Condensed matter.

[48]  Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor , 2000, The EMBO journal.

[49]  L. Clifton,et al.  Lyophilised protein dynamics: more than just methyls? , 2012 .

[50]  K. Kojima,et al.  Sound velocity and dynamic elastic constants of lysozyme single crystals , 2000 .

[51]  T. Shimanouchi,et al.  Longitudinal Acoustical Vibrations of Finite Polymethylene Chains , 1967 .

[52]  Christopher M Dobson,et al.  Characterization of the nanoscale properties of individual amyloid fibrils , 2006, Proceedings of the National Academy of Sciences.

[53]  Zhiping Xu,et al.  Nanoconfinement Controls Stiffness, Strength and Mechanical Toughness of Β-sheet Crystals in Silk , 2010 .

[54]  A. Oberhauser,et al.  The study of protein mechanics with the atomic force microscope. , 1999, Trends in biochemical sciences.