Dynamics of Biomembranes and Rheological Properties of Living Cells

Doctoral thesis, 2011

An ingenious assembly of biomolecules and water constitute what we call biological tissue. The presence of water in this assembly is fundamental for the physiological processes and can make the difference between life and death. One of the hallmark features of cellular life is the presence of membranes that separates the cell from the rest of the world and its compartments from each other. There is, however, some fluidity through the membranes. This fluid environment is possible due to the presence of water. The close association and dynamical interplay between lipid membranes and the surrounding water is investigated in the first part of this work. Membranes and water constitute important parts in the macromolecular assemblies and architecture that builds the whole living cell. Cells are highly dynamic with internal structures that constantly remodels and respond to external forces like a viscoelastic material. In many critical biological processes, cells both exert and respond to forces in their surroundings; the mechanical and rheological properties of cells are intimately related to their viscoelastic character which is the topic of the second part of this work. At biological temperatures there is a mix of many types of motions occurring on similar time scales which makes it difficult to separate different motions and elucidate interrelations. However, at low temperatures the different dynamical processes occur on considerably more separated time scales, which simplifies the analysis. Starting at low temperatures the onset of different motions of the water and the lipids were probed at successively higher temperatures by using broadband dielectric spectroscopy, differential scanning calorimetry and quasielastic neutron scattering. We found that the molecular motions of the lipids are similar to the molecular motions of glass forming liquids at low temperatures and the exact dynamical behavior was strongly dependent on the amount of water in the lipid system. The hydration water in lipid membranes modulates the motions of the lipid head groups and vice-versa there are also local lipid motions that influence the water dynamics at low hydration levels. Thus, in lipid membranes there is a strong interplay between water and lipid dynamics. The rheological properties of living cells were probed with optical magnetic twisting cytometry. The results show that the cellular mechanical function is susceptible to particulate exposure, and that the structural relaxation time is faster by nearly a factor 10, but also less temperature dependent close to the membrane compared to in the interior cytoskeletal structures. Moreover, for ATP depleted cells the relaxation dynamics slows down around physiological temperatures, which indicates the importance of ATP hydrolysis for the cellular relaxation dynamics.