Membrane Lipid Microenvironment Modulates Thermodynamic Properties of the Na+-K+-ATPase in Branchial and Intestinal Epithelia in Euryhaline Fish In vivo

Abstract

We have analyzed the effects of different native membrane lipid composition on the thermodynamic properties of the Na+-K+-ATPase in different epithelia from the gilthead seabream Sparus aurata. Thermodynamic parameters of activation for the Na+-K+-ATPase, as well as contents of lipid classes and fatty acids from polar lipids were determined for gill epithelia and enterocytes isolated from pyloric caeca, anterior intestine and posterior intestine. Arrhenius analyses of control animals revealed differences in thermal discontinuity values (Td) and activation energies determined at both sides of Td between intestinal and gill epithelia. Eyring plots disclosed important differences in enthalpy of activation (ΔH‡) and entropy of activation (ΔS‡) between enterocytes and branchial cells. Induction of n-3 LCPUFA deficiency dramatically altered membrane lipid composition in enterocytes, being the most dramatic changes the increase in 18:1n-9 (oleic acid) and the reduction of n-3 LCPUFA (mainly DHA, docosahexaenoic acid). Strikingly, branchial cells were much more resistant to diet-induced lipid alterations than enterocytes, indicating the existence of potent lipostatic mechanisms preserving membrane lipid matrix in gill epithelia. Paralleling lipid alterations, values of Ea1, ΔH‡ and ΔS‡ for the Na+-K+-ATPase were all increased, while Td values vanished, in LCPUFA deficient enterocytes. In turn, Differences in thermodynamic parameters were highly correlated with specific changes in fatty acids, but not with individual lipid classes including cholesterol in vivo. Thus, Td was positively related to 18:1n-9 and negatively to DHA. Td, Ea1 and ΔH‡ were exponentially related to DHA/18:1n-9 ratio. The exponential nature of these relationships highlights the strong impact of subtle changes in the contents of oleic acid and DHA in setting the thermodynamic properties of epithelial Na+-K+-ATPase in vivo. The effects are consistent with physical effects on the lipid membrane surrounding the enzyme as well as with direct interactions with the Na+-K+-ATPase.

Diet, Immunity, and Microbiota Interactions: An Integrative Analysis of the Intestine Transcriptional Response and Microbiota Modulation in Gilthead Seabream (Sparus aurata) Fed an Essential Oils-Based Functional Diet

“…For instance, the ATPase Na + /K + transporting subunit alpha 1 ( atp1a1 ) was significantly upregulated in the intestine of fish fed the EOs-supplemented diet. In other studies, diet-induced lipid alterations dramatically affected enterocytes lipid profile in gilthead seabream, reducing significantly Na + /K + ATPase specific activity, suggesting a regulatory role of the lipid microenvironment on the enzyme activity ( 47 ). Additionally, tribbles pseudokinase 1 ( trib1 ) gene expression was upregulated in the gilthead seabream fed the EOs-supplemented diet.…”

Effects of the defattedSchizochytriumsp. on growth performance, fatty acid composition, histomorphology and antioxidant status of juvenile mirror carp (Cyprinus carpiovar.specularis)

“…Also, Oxley et al (2005) and Pérez et al (1999) found that enterocytes could actively take up LC‐PUFA from lipid digestion. Intestinal epithelial cells have many phospholipids rich in n‐3 LC‐PUFA, including DHA, which play an important role in the physical properties of intestinal epithelial cell membranes, fish physiological processes and adaptive responses (Díaz et al, 2016). The whole body of fish fed with 3% and 6% DS were detected to be richer in DHA than the control group (Table 6).…”

Lipid classes and fatty acid composition in two parasitic copepods Peroderma cylindricum and Lernaeocera lusci and their respective fish hosts Sardina pilchardus and Merluccius merluccius from the Tunisian waters

“…In the other hand, the high proportions of WE/CE recorded in the host's tissues (i.e. gills and kidney) could be explained by the essential role played by cholesterol in the physiological regulation of the physical properties of cell membranes (Díaz et al, 2016). Differences in the proportion of polar lipid classes were herein observed between the two studied parasites and their respective hosts.…”