Why size and speed matter: frequency dependence and the mechanical properties of biomolecules

Abstract

Biomolecules, cells and the cellular environment have characteristic mechanical properties that determine a range of biological responses. The affected responses include the differentiation and phenotypic expression of cells, an area that has gained prominence due to the current interest in the control of stem cell development. Recent research on biomaterials includes many measurements that have been made on a micro or nano-scale and which are not well described by continuum models. The focus of this review is on the integration and comparison of information obtained from different experimental techniques: mechanical properties are discussed in terms of the wide range of molecular motions and relaxation times that are characteristic of biological materials. Starting at the smaller end of the scale, one component which will be almost universally present in biomolecular samples is water; although bulk water has a relaxation time that would make it fluid in typical experiments, interfacial water and water in confined films will exhibit much slower motions and may therefore show an elastic response, depending on the experimental technique used for the measurements. Water at the surface of hydrophilic solids may thus appear elastic when characterised using high-frequency acoustic devices such as the quartz crystal microbalance (QCM), although the layer will still be fluid in AFM measurements at typical load rates. Likewise, lipid bilayers are viscous at low shear but would be elastic at a sufficiently high frequency. Supported lipid bilayers (SLB) are effectively elastic in acoustic experiments; this could be due to the relaxation time with respect to shear displacements in the bilayer. At the larger end of the size scale, whole cells can also show a frequency-dependent transition to elastic behaviour, at frequencies as low as 0.1 Hz. Other examples mentioned here include proteins and the protein networks of cells.