Cubic Cell Membrane Architectures. Taking another look at membrane bound cell spaces

Sammanfattning: A systematic study of cell membrane morphologies whose structure is governed by cubic symmetries has been performed. It is suggested that they are described by periodic cubic surfaces for which space filling surface foliations given by truncated Fourier series defined by the space groups is used as structural representations. Using this a method is developed which enables a direct ultrastructural comparison between calculated projected electron density maps of a given periodic cubic surface and transmission electron micrographs of biological specimens displaying cubic membrane morphologies. Convincing results are given for the existence of three families of periodic cubic structures based on the surfaces known as the gyroid, double-diamond, and primitive. In each family balanced, unbalanced, and morphologies with a set of multiple membrane foliations are perceived. The accuracy to which these morphologies are described as periodic cubic surfaces, and the ease with which parameters such as surface area and volume ratios can be calculated, suggest their utility as a stereologic tool. A manifold of membrane morphologies with hitherto unknown cubic symmetries is identified and classified to form in conjunction with endoplasmic reticulum, inner nuclear envelope, mitochondria, trans-Golgi apparatus, chloroplasts, plasma membrane and lysosomes. Their occurrence is concluded to be of general nature and representative examples are given in cells ranging from protozoa to man in a large variety of species and tissue types thereof. In all cases studied, formation of cubic membrane morphologies can be explained by an intersection-free membrane folding model. From analysis of a vast number of electron micrographs of particular cases of cubic membranes the existence of structurally invariant morphologies is conjectured. Examples include the prolamellar body and the t-tubular honeycomb networks of skeletal muscles, which are invariantly described in reference to a double diamond and a gyroid surface, respectively. Plausible structure-function relations for these are discussed. Several theories regarding the function of cubic membranes as subcellular space-partitioners are put forward. Noticeably, the cubic membrane morphologies described by a set of n multiple membrane foliations defines n + 1 subspaces inherent to the organelle. It is postulated to be of global validity in cell space partitioning and its possible significance is addressed.