Mammalian phospholipid homeostasis: evidence that membrane curvature elastic stress drives homeoviscous adaptation in vivo

Abstract

Several theories of phospholipid homeostasis have postulated that cells regulate the molecular composition of their bilayer membranes, such that a common biophysical membrane parameter is under homeostatic control. Two commonly cited theories are the intrinsic curvature hypothesis, which states that cells control membrane curvature elastic stress, and the theory of homeoviscous adaptation, which postulates cells control acyl chain packing order (membrane order). In this paper, we present evidence from datadriven modelling studies that these two theories correlate in vivo. We estimate the curvature elastic stress of mammalian cells to be 4-7 Â 10 212 N, a value high enough to suggest that in mammalian cells the preservation of membrane order arises through a mechanism where membrane curvature elastic stress is controlled. These results emerge from analysing the molecular contribution of individual phospholipids to both membrane order and curvature elastic stress in nearly 500 cellular compositionally diverse lipidomes. Our model suggests that the de novo synthesis of lipids is the dominant mechanism by which cells control curvature elastic stress and hence membrane order in vivo. These results also suggest that cells can increase membrane curvature elastic stress disproportionately to membrane order by incorporating polyunsaturated fatty acids into lipids.

Lipid Spontaneous Curvatures Estimated from Temperature-Dependent Changes in Inverse Hexagonal Phase Lattice Parameters: Effects of Metal Cations

“…For example, curvature elastic stress, which arises from a system being forced to adopt a curvature that is different from c 0 , has been shown to modulate the activity of many membrane interacting proteins 3,4 and drives the folding of other membrane bound proteins 5,6 . These observations underpin the intrinsic curvature hypothesis, which postulates that cells regulate the composition of their biological membranes so that the net curvature elastic stress is under homeostatic control [7][8][9][10] .…”

Fatty Acid Composition and Contents of Seven Commercial Fish Species of Genus Coregonus from Russian Subarctic Water Bodies

“…However, other authors did not find any significant effect of water temperature on the PUFA levels in fish in a laboratory or in natural waters [18,[57][58][59][60][61]. Moreover, in many works the putative peculiar role of EPA or DHA in the temperature adaptations of the cell membrane properties (fluidity, order, curvature and elastic stress) was not confirmed [53,58,[62][63][64]. In any case, in our study water temperature in the subarctic water bodies was below 16 °C and hardly contributed considerably to the observed differences in EPA and DHA contents between the studied species.…”

“…For instance, Arts et al [54] found that under a laboratory conditions an increase of water temperature from 12 to 19 °C caused a decrease of DHA content in juvenile Atlantic salmon (Salmo salar) from 4.6 to 3.3 mg g −1 wet weight (recalculated from dry weight using mean moisture content in Salmoniformes 72.5%). Moreover, in many works the putative peculiar role of EPA or DHA in the temperature adaptations of the cell membrane properties (fluidity, order, curvature and elastic stress) was not confirmed [53,58,[62][63][64]. However, other authors did not find any significant effect of water temperature on the PUFA levels in fish in a laboratory or in natural waters [18,[57][58][59][60][61].…”

Meta-analysis of factors associated with omega-3 fatty acid contents of wild fish

“…Moreover, membrane fluidity or membrane viscosity, in addition to the degree of unsaturation, strongly depends on the type of lipid head-groups as well as the presence of another lipid species, cholesterol (Arts and Kohler 2009;Dymond 2016). Therefore, the notion that the differences in DHA contents between species are dictated by temperature-dependent membrane fluidity needs is simplistic (Infanteet al 2001).…”