Abstract
The effect of moderate and deeper hypothermia on the phospholipid (PL) and fatty acid (FA) composition of synaptic membranes (synaptosomes) in the rat brain was investigated. As hypothermia deepened, phosphatidylcholine (PC) and phosphatidylserine (PS) levels decreased while those of phosphatidylethanolamine (PEA) remained intact. We attribute the differences both to a peculiar localization of these PL in the synaptic membrane and to a specificity of their function. Under hypothermal exposure, the saturated FA (SFA) level in the FA repertoire of total synaptosomal PL slightly decreased (by 9%) while that of polyunsaturated FA (PUFA) considerably increased, leading to a rise in the lipid unsaturation index (LUI) (by 47%) and promoting the maintenance of synaptic membrane fluidity. For three basic PL (PC, PS and PEA), the tendency was opposite: the SFA level increased while that of PUFA decreased, leading to a fall in the LUI and promoting a higher packing order of PL within the synaptic membrane. In the FA repertoire of the plasmalogen form of PEA (p-PEA), enforced hypothermia led to elevated levels both of SFA and PUFA as well as to a particularly high LUI, typical for this PL. These changes are supposed to be aimed at maintaining optimal membrane fluidity. We consider all the observed changes in lipid characteristics as adaptive, allowing the synaptic function in homeotherms to be supported as body temperature falls.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Dowhan, W., Bogdanov, M., and Mileykovskaya, E., Functional roles of lipids in membranes, Biochemistry of Lipids, Lipoproteins and Membranes, Vance, D.E. and Vance, J.E., Eds., Elsevier, 2008, chapter 1, pp. 1–39.
Berridge, M.J., The inositol trisphosphate/calcium signaling pathway in health and disease, Physiol. Rev., 2016, vol. 96, pp. 1261–1296.
Vance, J.E., Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids, J. Lipid Res., 2008, vol. 49, pp. 1377–1387.
Fajardo, V.A., McMeekin, L., and LeBlanc, P.J., Influence of phospholipid species on membrane fluidity: a meta-analysis for a novel phospholipid fluidity index, J. Membrane Biol., 2011, vol. 244, pp. 97–103.
Kreps, E.M., Lipidy kletochnykh membran: Evolyutsiya lipidov mozga. Adaptatsionnaya funktsiya lipidov (Lipids of Cell Membranes: Evolution of Cerebral Lipids. Adaptational Function of Lipids), Leningrad, 1981.
Hazel, J.R., Thermal adaptation in biological membrane: is homeoviscous adaptation the explanation? Annu. Rev. Physiol., 1995, vol. 57, pp. 19–24.
Logue, J.A., De Vries, A.L., Fodor, E., and Cossins, A.R., Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure, J. Exp. Biol., 2000, vol. 203, pp. 2105–2115.
Shepelev, A.P., Dependence of lipid composition and phase transitions in myocardial mitochondria of white rats and dogs on the depth of hypothermia, Biofiz., 1977, vol. XXII, iss. 3, pp. 465–467.
Rabadanova, Z.G., Abdurakhmanov, R.G., Klichkhanov, N.K., and Pinyaskina, E.V., Effect of intraperitoneal infusion of sucrose on electrical activity of the rat brain under hypothermic conditions, Fundament. Issled., 2014, vol. 12, pp. 141–144.
Kufel, D.S. and Wojcik, G.M., Analytical modelling of temperature effects on synapses, Neurons and Cognition, arXiv:1610.00611 [q-bio.NC], 2016.
Lapetina, E.G., Soto, E.F., and De Robertis, E., Gangliosides and acetylcholinesterase in isolated membranes of the rat-brain cortex, Biochem. Biophis. Acta, 1967, vol. 135, pp. 33–43.
Rouser, G., Siakotos, A.N., and Fleischer, S., Quantitative analysis of phospholipids by thinlayer chromatography and phosphorus analysis of spots, Lipids, 1966, vol. 1, pp. 85–86.
Zabelinskii, S.A., Chebotareva, M.A., Shukolyukova, E.P., and Krivchenko, A.I., The fatty acid composition of phospholipids and absorption spectra of lipid extracts from lamprey, frog, and rat erythrocytes, J. Evol. Biochem. Physiol., 2014, vol. 50, iss. 4, pp. 303–309.
Hitzemann, R.J. and Johnson, D.A., Developmental changes in synaptic membrane lipid composition and fluidity, Neurochem. Res., 1983, vol. 8, no. 2, pp. 121–131.
Davletov, B. and Montecucco, C., Lipid function at synapses, Curr. Opin. Neurobiol., 2010, vol. 20, pp. 543–549.
Puchkov, D. and Haucke, V., Greasing the synaptic vesicle cycle by membrane lipids, Trends Cell Biol., 2013, vol. 23, pp. 493–503.
Marquardt, D., Geier, B., and Pabst, G., Asymmetric lipid membranes: towards more realistic model systems, Membranes, 2015, vol. 5, pp. 180–196.
Lauwers, E., Goodchild, R., and Verstreken, P., Membrane lipids in presynaptic function and disease, Neuron, 2016, vol. 90, pp. 11–25.
Williams, D., Vicôgne, J., Zaitseva, I., McLaughlin, S., and Pessin, J.E., Evidence that electrostatic interactions between vesicle-associated membrane protein 2 and acidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane, Mol. Biol. Cell., 2009, vol. 20, pp. 4910–4919.
Moyes, C.D. and Ballantyne, J.S., Membranes and temperature: homeoviscous adaptation, Encyclopedia of Fish Physiology: From Genome to Environment, Farrell, A., Ed., Academic, Elsevier Inc., 2011, pp. 1725–1731.
Emirbekov, E.Z. and Klichkhanov, N.K., Svobodnoradikal’nye protsessy i sostoyanie membran pri gipotermii (Free Radical Processes and Membrane Status in Hypothermia), Rostov-on-Don, 2011.
Braverman, N.E. and Mose, A.B., Functions of plasmalogen lipids in health and disease, Biochim. Biophys. Acta–Mol. Basis of Disease, 2012, vol. 1822, pp. 1442–1452.
Kuczynski, B. and Reo, N.V., Evidence that plasmalogen is protective against oxidative stress in the rat brain, Neurochem. Res., 2006, vol. 31, pp. 639–656.
Broniec, A., Klosinski, R., Pawlak, A., Wrona-Krol, M., Thompson, D., and Sarna, T., Interactions of plasmalogens and their diacyl analogs with singlet oxygen in selected model systems, Free Radic. Biol. Med., 2011, vol. 50, pp. 892–898.
Brennan, A.M., Suh, S.W., Won, S.J., Narasimhan, P., Kauppinen, T.M., Lee, H., Edling, Y., Chan, P.H., and Swanson, R.A., NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation, Nat. Neurosci., 2009, vol. 12, pp. 857–863.
Shelat, P.B., Chalimoniuk, M., Wang, J.-H., Strosznajder, J.B., Lee, J.C., Sun, A.Y., Simonyi, A., and Sun, G.Y., Amyloid beta peptide and NMDA induce ROS from NADPH oxidase and AA release from cytosolic phospholipase A2 in cortical neurons, J. Neurochem., 2008, vol. 106, pp. 45–55.
Magomedov, K.G., Shikhamirova, Z.M., and Klichkhanov, N.K., Effect of hypothermia on Na, K-ATPase activity in synaptic membranes of the rat brain, Vestn Dag. Nauch. Tsentra RAN, 2011, no. 42, p. 5357.
Paradies, G., Paradies, V., De Benedictis, V., Ruggiero, F.M., and Petrosillo, G., Functional role of cardiolipin in mitochondrial bioenergetics, Biochem. Biophys. Acta, 2014, vol. 1837, pp. 408–417.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © A.M. Kalandarov, Z. Radzhabova, S.A. Zabelinskii, B. A. Feizulaev, N.K. Klichkhanov, M.A. Chebotareva, A.M. Krivchenko, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 2, pp. 81–90.
Rights and permissions
About this article
Cite this article
Kalandarov, A.M., Radzhabova, Z., Zabelinskii, S.A. et al. The Effect of Hypothermia on Phospholipid and Fatty Acid Composition of Synaptic Membranes in the Rat Brain. J Evol Biochem Phys 54, 91–102 (2018). https://doi.org/10.1134/S0022093018020011
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0022093018020011