Membrane Adhesion via Glycolipids Occurs for Abundant Saccharide Chemistries

Abstract

Membrane-bound oligosaccharides with specific chemistries are known to promote tight adhesion between adjacent membranes via the formation of weak saccharide bonds. However, in the literature, one can find scattered evidence that other, more abundant saccharide chemistries exhibit similar behavior. Here, the influence of various glycolipids on the interaction between adjacent membranes is systematically investigated with the help of small-and wide-angle x-ray scattering and complementary neutron diffraction experiments. Added electrostatic repulsion between the membrane surfaces is used to identify the formation of saccharide bonds and to challenge their stability against tensile stress. Some of the saccharide headgroup types investigated are able to bind adjacent membranes together, but this ability has no significant influence on the membrane bending rigidity. Our results indicate that glycolipid-mediated membrane adhesion is a highly abundant phenomenon and therefore potentially of great biological relevance.

Weak carbohydrate–carbohydrate interactions in membrane adhesion are fuzzy and generic

“…[4][5][6][7][8] About three decades ago, homophilic carbohydratecarbohydrate interactions of the trisaccharide Lewis X (Le X ) have been reported to be involved in embryonal cell compaction and aggregation, [9][10][11] and interactions between long carbohydrate chains have been linked to the species-specific aggregation of marine sponges. 12 In the following decades, carbohydrate-carbohydrate interactions in adhesion have been investigated in a variety of reconstituted or synthetic systems including nanoparticles and surfaces functionalized with carbohydrates, [13][14][15] atomic force microscopy setups, [16][17][18][19] and reconstituted vesicles 20,21 or membranes [22][23][24] containing glycolipids. While some carbohydrate-carbohydrate interactions have been reported to be strong, 17,25,26 interactions of small, neutral carbohydrates are typically considered to be weak.…”

Myelin sheath and cyanobacterial thylakoids as concentric multilamellar structures with similar bioenergetic properties

“…Apart from that, in silico simulation of the dispersion of lipids shows the spontaneous formation of multilamellar lipid vesicles [ 60 ], supporting the idea that the multilayer structure is generically stable. It is interesting that glycolipids contribute to the stability of the multilamellar structures by creating non-covalent saccharide bonds with the glucidic residues that protrude from the membrane [ 52 ]. Consideration should also be given to the fact that galactose is the predominant residue and that galactolipids are present in significant quantities in the thylakoids of cyanobacteria, in the cyanelles of unicellular algae and in myelin.…”

“…As pointed out by Latza et al . [ 52 ], galactolipids that counteract the repulsive electrostatic force depend on the glucidic residues of galactolipids, which protrude towards the aqueous phase adhering to both the membrane and form the non-covalent saccharide bonds between the two galactoside residues. Latza et al .…”

“…Latza et al . [ 52 ] highlighted that their results ‘indicate that glycolipid-mediated membrane adhesion is a highly abundant phenomenon and therefore potentially of great biological relevance’.…”

Interplay of Trans- and Cis-Interactions of Glycolipids in Membrane Adhesion

“…Glycolipids are abundant components of biological membranes and play important roles in cell-cell interactions (Schnaar, 2004;Day et al, 2015;Varki, 2017;Poole et al, 2018) and the interactions of stacked membranes in cellular organelles (Stoffel and Bosio, 1997;Boudiere et al, 2014). Besides glycolipid recognition by proteins (Liu and Rabinovich, 2005;Arnaud et al, 2013), glycolipid-glycolipid interactions have been investigated in a variety of reconstituted or synthetic systems including nanoparticles and surfaces functionalized with carbohydrate tips of glycolipids (de la Hernáiz and de la Fuente, 2002;de la Fuente et al, 2005), atomic force microscopy setups (Tromas et al, 2001;Bucior et al, 2004;Lorenz et al, 2012;Witt et al, 2016), reconstituted vesicles (Pincet et al, 2001;Gourier et al, 2005;Kunze et al, 2013), as well as supported membranes (Yu et al, 1998), and stacks of membranes (Schneck et al, 2011;Latza et al, 2020) containing glycolipids. Experiments with giant vesicles and stacks of membranes indicate that glycolipids can mediate stable membrane adhesion (Gourier et al, 2005;Schneck et al, 2011;Latza et al, 2020), but a molecular view and quantification of the glycolipid-glycolipid interactions that lead to membrane adhesion is still largely missing.…”