Lipids and Membrane Lateral Organization

Abstract

Shortly after the elucidation of the very basic structure and properties of cellular membranes, it became evident that cellular membranes are highly organized structures with multiple and multi-dimensional levels of order. Very early observations suggested that the lipid components of biological membranes might be active players in the creation of these levels of order. In the late 1980s, several different and diverse experimental pieces of evidence coalesced together giving rise to the lipid raft hypothesis. Lipid rafts became enormously (and, in the opinion of these authors, sometimes acritically) popular, surprisingly not just within the lipidologist community (who is supposed to be naturally sensitive to the fascination of lipid rafts). Today, a PubMed search using the key word “lipid rafts” returned a list of 3767 papers, including 690 reviews (as a term of comparison, searching over the same time span for a very hot lipid-related key word, “ceramide” returned 6187 hits with 799 reviews), and a tremendous number of different cellular functions have been described as “lipid raft-dependent.” However, a clear consensus definition of lipid raft has been proposed only in recent times, and the basic properties, the ruling forces, and even the existence of lipid rafts in living cells has been recently matter of intense debate. The scenario that is gradually emerging from the controversies elicited by the lipid raft hypothesis emphasizes multiple roles for membrane lipids in determining membrane order, that encompass their tendency to phase separation but are clearly not limited to this. In this review, we would like to re-focus the attention of the readers on the importance of lipids in organizing the fine structure of cellular membranes.

Differential Effect of Plant Lipids on Membrane Organization

“…Animal glycosphingolipid with a monosaccharide headgroup is much bulkier than phospholipid ones and occupies a larger volume, as proposed by theoretical calculations of the minimum energy conformation, which results in spontaneous membrane curvature (25). According to these predictions, ganglioside phase separation in model membrane depends on the surface area occupied by the oligosaccharide chain that is usually directly correlated with the number of sugar residues (121)(122)(123).…”

“…Multiple roles for lipids in determining membrane order were thus emphasized and encompassed their tendency to phase separation and organization of biological membranes (25). However, all of these studies were performed on model and animal systems, where the lipid diversity is considerably lower than in plants.…”

Specific Membrane Lipid Composition Is Important for Plasmodesmata Function in Arabidopsis

“…However, to date, the lipid constituents of PD have not been identified, although research on biological membranes has unequivocally demonstrated that lipids can form functional units capable of modulating membrane organization, protein partitioning, and cellular functions (Lingwood and Simons, 2010;Sonnino and Prinetti, 2010;Munnik and Nielsen, 2011;Bigay and Antonny, 2012;Barrera et al, 2013;Li et al, 2014). Furthermore, the potential for membrane lipids to contribute to the regulation of intercellular communication in plants has never been investigated.…”

“…Not only proteins but also lipids are laterally organized within the plane of the membrane and contribute to the formation, dynamics, and function of microdomains (Lingwood and Simons, 2010;Sonnino and Prinetti, 2010;Schäfer et al, 2011;van den Bogaart et al, 2011;Contreras et al, 2012). In plants, a compelling example of membrane functional subcompartmentalization is illustrated by the specialization of the endoplasmic reticulum (ER) and the plasma membrane (PM) at sites of cell-to-cell junctions, called plasmodesmata (PD) (Maule, 2008;Tilsner et al, 2011).…”

Shiga toxin glycosphingolipid receptors of Vero-B4 kidney epithelial cells and their membrane microdomain lipid environment

“…GSLs participate as driving forces in the formation of membrane microdomains and exert specifi c functions related to their physicochemical characteristics through GSL-protein interactions in those domains (87)(88)(89)(90)(91). GSLs preferentially distribute to phase-separated microdomains in the outer leafl et of the plasma membrane, which are suggested to operate as attachment platforms for host pathogens and their toxins on epithelial cells ( 57,92,93 ) to gain entry into cells and retrograde routing to intracellular targets in the cytosol ( 35,56,94 ).…”