Quantitative determination of size and shape of surface-bound DNA using an acoustic wave sensor.

DNA bending plays a significant role in many biological processes, such as gene regulation, DNA replication, and chromosomal packing. Understanding how such processes take place and how they can, in turn, be regulated by artificial agents for individual oriented therapies is of importance to both biology and medicine. In this work, we describe the application of an acoustic wave device for characterizing the conformation of DNA molecules tethered to the device surface via a biotin-neutravidin interaction. The acoustic energy dissipation per unit mass observed upon DNA binding is directly related to DNA intrinsic viscosity, providing quantitative information on the size and shape of the tethered molecules. The validity of the above approach was verified by showing that the predesigned geometries of model double-stranded and triple-helix DNA molecules could be quantitatively distinguished: the resolution of the acoustic measurements is sufficient to allow discrimination between same size DNA carrying a bent at different positions along the chain. Furthermore, the significance of this analysis to the study of biologically relevant systems is shown during the evaluation of DNA conformational change upon protein (histone) binding.

[1]  Stephen J. Martin,et al.  Effect of surface roughness on the response of thickness-shear mode resonators in liquids , 1993 .

[2]  S. Satija,et al.  Using Self-Assembly To Control the Structure of DNA Monolayers on Gold: A Neutron Reflectivity Study , 1998 .

[3]  DNA Structure Changes Coupled to Protein Binding , 2001 .

[4]  Fabien Josse,et al.  Analysis of shear horizontal surface waves at the boundary between a piezoelectric crystal and a viscous fluid medium , 1988 .

[5]  J. Thornton,et al.  An overview of the structures of protein-DNA complexes , 2000, Genome Biology.

[6]  E. M. White,et al.  Sequence and properties of the message encoding Tetrahymena hv1, a highly evolutionarily conserved histone H2A variant that is associated with active genes , 1988, Nucleic Acids Res..

[7]  C. Cantor,et al.  DNA conformation on surfaces measured by fluorescence self-interference. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Jay W. Grate,et al.  Acoustic Wave Sensors , 1996 .

[9]  Electra Gizeli,et al.  Design considerations for the acoustic waveguide biosensor , 1997 .

[10]  W. R. Moore.  Viscosities of dilute polymer solutions , 1967 .

[11]  H. Hansma,et al.  Atomic force microscopy of long and short double-stranded, single-stranded and triple-stranded nucleic acids. , 1996, Nucleic acids research.

[12]  L. Maher.  Mechanisms of DNA bending. , 1998, Current opinion in chemical biology.

[13]  Stokes flow through a rectangular array of circular cylinders , 2001 .

[14]  C. Cantor,et al.  Biophysical chemistry. Part III, The behavior of biologicalmacromolecules , 1980 .

[15]  G. Maret,et al.  Segment distributions of end-tethered polymers in a good solvent. , 2006, Physical review letters.

[16]  D M Crothers,et al.  Intrinsically bent DNA. , 1990, The Journal of biological chemistry.

[17]  R Balhorn,et al.  AFM analysis of DNA-protamine complexes bound to mica. , 1997, Nucleic acids research.

[18]  K. Luger,et al.  Crystal structure of a nucleosome core particle containing the variant histone H2A.Z , 2000, Nature Structural Biology.

[19]  N. Düzgüneş,et al.  The shape parameter of liposomes and DNA-lipid complexes determined by viscometry utilizing small sample volumes. , 2003, Biophysical journal.

[20]  Electra Gizeli,et al.  Probing the Viscoelasticity and Mass of a Surface-Bound Protein Layer with an Acoustic Waveguide Device , 2003 .

[21]  Charles Tanford,et al.  Physical Chemistry of Macromolecules , 1961 .

[22]  V. Bloomfield,et al.  Hydrodynamic properties of macromolecular complexes. IV. Intrinsic viscosity theory, with applications to once‐broken rods and multisubunit proteins , 1978 .

[23]  Antonio J. Ricco,et al.  Characterization of SH acoustic plate mode liquid sensors , 1989 .

[24]  A. Ricco,et al.  Acoustic wave viscosity sensor , 1987 .

[25]  Antonio Carcaterra,et al.  Energy sinks: Vibration absorption by an optimal set of undamped oscillators , 2005 .

[26]  D. Liberles,et al.  Design of artificial sequence-specific DNA bending ligands. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Lowen.  The Biophysical Journal , 1960, Nature.

[28]  W. Knoll,et al.  Comparison of surface plasmon resonance spectroscopy and quartz crystal microbalance techniques for studying DNA assembly and hybridization. , 2005, Biosensors & bioelectronics.

[29]  A. Philipse,et al.  LOW-SHEAR VISCOSITY OF ISOTROPIC DISPERSIONS OF (BROWNIAN) RODS AND FIBRES; A REVIEW OF THEORY AND EXPERIMENTS , 1998 .

[30]  Erik Reimhult,et al.  Understanding ligand binding effects on the conformation of estrogen receptor alpha-DNA complexes: a combinational quartz crystal microbalance with dissipation and surface plasmon resonance study. , 2007, Biophysical journal.

[31]  R. Pecora,et al.  Rotational and translational diffusion of short rodlike molecules in solution: Oligonucleotides , 1991 .

[32]  A. Wolffe,et al.  Review: chromatin structural features and targets that regulate transcription. , 2000, Journal of structural biology.

[33]  R. Netz,et al.  Hydrodynamic effects in driven soft matter. , 2006, Soft matter.

[34]  M. Thompson,et al.  Kinetics of interfacial nucleic acid hybridization studied by acoustic network analysis , 1995 .

[35]  Fredrik Höök,et al.  Characterization of DNA immobilization and subsequent hybridization on a 2D arrangement of streptavidin on a biotin-modified lipid bilayer supported on SiO2. , 2003, Analytical chemistry.

[36]  J. García de la Torre,et al.  Hydrodynamic properties of complex, rigid, biological macromolecules: theory and applications , 1981, Quarterly Reviews of Biophysics.

[37]  D. Crothers,et al.  Detection of localized DNA flexibility , 1994, Nature.

[38]  Jean-Michel Friedt,et al.  Combined atomic force microscope and acoustic wave devices: Application to electrodeposition , 2003 .

[39]  M. Bolognesi,et al.  The X-ray three-dimensional structure of avidin. , 1999, Biomolecular engineering.