Lipid Signals from Plasma Membrane

Abstract

Plasma membrane is a more and more appreciated topic in life sciences research for the specific roles of this lipid asset for cell functions. In particular, fatty acids, which are the principal constituents of membrane phospholipids, are known for their crucial contributions to the membrane organisation, biophysical properties and molecular signalling. An interdisciplinary vision of lipid signaling from plasma membrane is necessary, combining interdisciplinary vision of lipid signalling from plasma membrane, combining the intrinsic significance of saturated and unsaturated lipid structures, the interplay between metabolism and diet creating healthy signalling and the perspectives of fatty acid‐based membrane lipidomics to obtain molecular information that can predict the signalling, in particular for inflammatory conditions. From this scenario, several issues emerge for future research, pointing to the full integration of the plasma membrane analysis in molecular biology studies and to calibrated and automated protocols for gathering big data on membrane lipidome.

Key Concepts

  • Fatty acid‐containing phospholipids provide structural, functional and signalling properties to cell membranes.
  • Each tissue has its own membrane fatty acid composition which regulates the structure and functions.
  • Plasma membrane needs unsaturated fatty acids as cis isomers, prepared both endogenously by desaturase enzymes and by taking the precursors of polyunsaturated fatty acids from diet.
  • The presence of trans fatty acids in plasma membrane can be marker of free radical stress causing an endogenous isomerisation of the naturally occurring cis lipids.
  • The position and geometry of double bonds are crucial for the organisation given by fatty acids to cell membranes and must be recognised by appropriate analytical methodologies.
  • The balance between saturated and unsaturated fatty acids regulates plasma membrane organisation and responses, thus influencing the entire cell fate.
  • Fatty acids in membranes are epigenetic molecular factors, showing how nutritional and metabolic factors control the release of important signalling molecules in inflammatory conditions and other metabolic processes.
  • The balance between omega‐6 and omega‐3 components in membranes creates the predisposition of cell membrane to signalling responses in the inflammatory process.

Keywords: membrane lipidomics; fatty acid signalling; cis–trans isomerisation; peroxidation index; membrane unsaturation index; PUFA balance; geometrical isomers; positional isomers

Figure 1. The main saturated, monounsaturated and polyunsaturated fatty acid residues of the cell membrane phospholipids.
Figure 2. Arachidonic acid and cis–trans isomerisation of double bonds in the membrane bilayer by sulfur‐centred radicals.
Figure 3. The membrane remodelling process called Lands's cycle.
close

References

Abbott SK, Else PA, Atkins TA and Hulbert AJ (2012) Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochimica Biophysica Acta 1818: 1309–1317.

Alvheim AR, Malde MK, Osei‐Hyiaman D, et al. (2012) Dietary linoleic acid elevates endogenous 2‐AG and anandamide and induces obesity. Obesity 20: 1984–1994.

Ayala A, Muñoz MF and Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4‐hydroxy‐2‐nonenal. Oxidative Medicine and Cellular Longevity 2014: 360438. DOI: 10.1155/2014/360438.

Baleztena J, Ruiz‐Canela M, Sayon‐Orea C, et al. (2018) Association between cognitive function and supplementation with omega‐3 PUFAs and other nutrients in > 75 years old patients: a randomized multicenter study. PLoS ONE 13 (3): e0193568. DOI: 10.1371/journal.pone.0193568.

Chatgilialoglu C, Ferreri C, Melchiorre M, Sansone A and Torreggiani A (2014) Lipid geometrical isomerism: from chemistry to biology and diagnostics. Chemical Reviews 114: 255–284.

Chawla A, Repa JJ, Evans RM and Mangelsdorf DJ (2001) Nuclear receptors and lipid physiology: opening the X‐files. Science 294: 1866–1870.

Cortie CH, Hulbert AJ, Hancock SE, et al. (2015) Of mice, pigs and humans: an analysis of mitochondrial phospholipids from mammals with very different maximal lifespans. Experimental Gerontology 70: 135–143.

Cotran RS, Kumar V and Collins T (1999) Robbins Pathologic Basis of Disease, 6th edn. W.B. Saunders Company: Philadelphia, PA.

Covino R, Ballweg S, Stordeur C, et al. (2016) A eukaryotic sensor for membrane lipid saturation. Molecular Cell 63: 49–59.

De Carvalho CCCR and Caramujo MC (2018) The various roles of fatty acids. Molecules 23: 2583. DOI: 10.3390/molecules23102583.

Eberlein C, Baumgarten T, Starke S and Heipieper HJ (2018) Immediate response mechanisms of Gram‐negative solvent‐tolerant bacteria to cope with environmental stress: cis‐trans isomerization of unsaturated fatty acids and outer membrane vesicle secretion. Applied Microbiology and Biotechnology 102: 2583–2593.

Ernst R, Ballweg S and Levental I (2018) Cellular mechanisms of physicochemical membrane homeostasis. Current Opinion in Cell Biology 53: 44–51.

Ferreri C, Angelini F, Chatgilialoglu C, et al. (2005) Trans fatty acids and atopic eczema/dermatitis syndrome: the relationship with a free radical cis‐trans isomerization of membrane lipids. Lipids 40: 661–667.

Ferreri C, Pierotti S, Barbieri A, et al. (2006a) Comparison of phosphatidylcholine vesicle properties related to geometrical isomerism. Photochemistry Photobiology 82: 274–280.

Ferreri C, Pierotti S, Chatgilialoglu C, Barbieri A and Barigelletti F (2006b) Probing the influence of cis‐trans isomers on model lipid membrane fluidity using cis‐parinaric acid and stop‐flow technique. Chemical Communications 5: 529–531.

Ferreri C and Chatgilialoglu C (2015) Membrane Lipidomics for Personalized Health. John Wiley & Sons: Chichester.

Ferreri C, Masi A, Sansone A, et al. (2017) Fatty acids in membranes as homeostatic, metabolic and nutritional biomarkers: recent advancements in analytics and diagnostics. Diagnostics 7: 1. DOI: 10.3390/diagnostics7010001.

Fratini F, Raggi C, Sferra G, et al. (2017) An integrated approach to explore composition and dynamics of cholesterol‐rich membrane microdomains in sexual stages of malaria parasite. Molecular & Cellular Proteomics 16: 1801–1814.

Harman D (1956) Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology 11: 298–300.

Hong S, Gronert K, Devchand PR, Moussignac RL and Serhan CN (2003) Novel docosatrienes and 17S‐ resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti‐inflammation. Journal of Biological Chemistry 278: 14677–14687.

Hulbert AJ (2007) Membrane fatty acids as pacemakers of animal metabolism. Lipids 42: 811–819.

Hulbert AJ (2008) Explaining longevity of different animals: is membrane fatty acid composition the missing link? Age (Dordr). 30: 89–97.

Kadhum AA and Shamma MN (2017) Edible lipids modification processes: a review. Critical Review Food Science Nutrition 57: 48–58.

Kimura I, Ichimura A, Ohue‐Kitano R and Igarashi M (2020) Free fatty acid receptors in health and disease. Physiology Reviews 100: 171–210.

Lands WE (1958) Metabolism of glycerolipids: a comparison of lecithin and triglyceride synthesis. Journal of Biological Chemistry 231: 883–888.

Lauritzen L, Hansen HS, Jørgensen MH and Michaelsen KF (2001) The essentiality of long chain n‐3 fatty acids in relation to development and function of the brain and retina. Progress in Lipid Research 40: 1–94.

Law SH, Chan ML, Marathe GK, et al. (2019) An updated review of lysophosphatidylcholine metabolism in human diseases. International Journal Molecular Sciences 20: 1149. DOI: 10.3390/ijms20051149.

Levy BD, Clish CB, Schmidt B, Gronert K and Serhan CN (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nature Immunology 2: 612–619.

Lockshon D, Olsen CP, Brett CL, et al. (2012) Rho signaling participates in membrane fluidity homeostasis. PLoS ONE 7 (10): e45049. DOI: 10.1371/journal.pone.0045049.

Los DA and Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochimica Biophysica Acta 1666: 142–157.

Mansilla MC and de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Archives Microbiology 183: 229–235.

van Meer G, Voelker DR and Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nature Review Molecular Cell Biology 9: 112–124.

Nicolson GL and Ash ME (2017) Membrane lipid replacement for chronic illnesses, aging and cancer using oral glycerophospholipid formulations with fructooligosaccharides to restore phospholipid function in cellular membranes, organelles, cells and tissues. Biochimica Biophysica Acta 1859: 1704–1724.

Otengo A‐B and Kersten S (2019) Mechanisms of action of trans fatty acids. Advances in Nutrition: 1–12. DOI: 10.1093/advances/nmz125.

Puca AA, Andrew P, Novelli V, et al. (2008) Rejuvenation Research 11: 63–72.

Rabini RA, Moretti N, Staffolani R, et al. (2002) Reduced susceptibility to peroxidation of erythrocyte plasma membranes from centenarians. Experimental Gerontology 37: 657–663.

Rausch V and Hansen CG (2019) The hippo pathway, YAP/TAZ, and the plasma membrane. Trends in Cell Biology. DOI: 10.1016/j.tcb.2019.10.005.

Ruysschaert JM and Lonez C (2015) Role of lipid microdomains in TLR‐mediated signalling. Biochimica Biophysica Acta 1848: 1860–1867. DOI: 10.1016/j.bbamem.2015.03.014.

Sansone A, Tolika E, Louka M, et al. (2016) Hexadecenoic fatty acid isomers in human blood lipids and their relevance for interpretation of lipidomic profiles. PLoS ONE 11: e0152378.

Sauvat A, Chen G, Müller K et al. (2018) Trans‐Fats Inhibit Autophagy Induced by Saturated Fatty Acids. EBioMedicine 30: 261–272.

Scanferlato R, Bortolotti M, Sansone A, et al. (2019) Hexadecenoic fatty acid positional isomers and de novo PUFA synthesis in colon cancer cells. International Journal of Molecular Sciences 20: 832. DOI: 10.3390/ijms20040832.

Serhan CN, Hong S, Gronert K, et al. (2002) Resolvins: a family of bioactive products of omega‐3 fatty acid transformation circuits initiated by aspirin treatment that counter pro‐inflammation signals. Journal Experimental Medicine 196: 1025–1037.

Serhan CN (2014) Pro‐resolving lipid mediators are leads for resolution physiology. Nature 510: 92–101.

Simons K and Toomre D (2000) Lipid rafts and signal transduction. Nature Review Molecular Cell Biology 1: 31–39.

Simopoulos AP (2016) An increase in the omega‐6/omega‐3 fatty acid ratio increases the risk for obesity. Nutrients 8: 128. DOI: 10.3390/nu80300128.

Snezhkina AV, Kudryavtseva AV, Kardymon OL, et al. (2019) ROS generation and antioxidant defense systems in normal and malignant cells. Cells 2019: 6175804. DOI: 10.1155/2019/6175804.

Souabni H, Thoma V, Bizouarn T, et al. (2012) trans‐Arachidonic acid isomers inhibit NADPH‐oxidase activity by direct interaction with enzyme components. Biochimica Biophysica Acta Biomembranes 1818: 2314–2324.

Stark KD, Van Elswyk ME, Higgins MR, Weatherford CA and Salem N (2016) Global survey of the omega‐3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the blood stream of healthy adults. Progress in Lipid Research 63: 132–152.

Tyler AII, Greenfield JL, Seddon JM, Brooks NJ and Purushothaman S (2019) Coupling phase behavior of fatty acid containing membranes to membrane bio‐mechanics. Frontiers in Cell Developmental Biology 7: 187. DOI: 10.3389/fcell.2019.00187.

Vane JR and Botting RM (eds) (2001) Therapeutic Roles of Selective COX‐2 Inhibitors. William Harvey Press: London, United Kingdom.

Xu Z, You W, Zhou Y, et al. (2019) Cold‐induced lipid dynamics and transcriptional programs in white adipose tissue. BMC Biology 17: 74. DOI: 10.1186/s12915‐019‐0693‐x.

Yokomizo T and Murakami M (2015) Bioactive Lipid Mediators. Current Reviews and Protocols. Springer: Tokyo.

Zambonin L, Ferreri C, Cabrini L, et al. (2006) Occurrence of trans fatty acids in rats fed a trans‐free diet: a free radical mediated formation? Free Radicals Biology and Medicine 40: 2595–2598.

Further Reading

Baenke F, Peck B, Meiss H and Schulze A (2013) Hooked on fat: the role of lipid synthesis in cancer metabolism and tumour development. Disease Models & Mechanism 6: 1353–1363.

Barba‐bon A, Nilam M and Hennig A (2019) Supramolecular chemistry in the biomembrane. ChemBioChem. DOI: 10.1002/cbic.201900646.

Chatgilialoglu C and Studer A (2012) Encyclopedia of Radicals in Chemistry, Biology and Materials. John Wiley & Sons: New York.

Focus on Inflammation (2017) A current view on inflammation. Nature Immunology 18: 825–869.

Friedman D, French JA and Maccarrone M (2019) Safety, efficacy, and mechanisms of action of cannabinoids in neurological disorders. Lancet Neurology 18: 504–512.

Holthuis JCM and Menon AK (2014) Lipid landscapes and pipelines in membrane homeostasis. Nature 510: 48–57.

Maccarrone M, Guzmán M, Mackie K, Doherty P and Harkany T (2014) Programming of neural cells by (endo)cannabinoids: from physiological rules to emerging therapies. Nature Review Neurosciences 15: 786–801.

Van Meer G and de Kroon AIPM (2011) Lipid map of the mammalian cell. Journal of Cell Science 124: 5–8.

Nicolson GL (2014) The Fluid—Mosaic Model of Membrane Structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochimica et Biophysica Acta (BBA) – Biomembranes 1838: 1451–1466.

Yin H, Xu L and Porter NA (2011) Free radical lipid peroxidation: mechanisms and analysis. Chemical Reviews 111: 5944–5972.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Ferreri, Carla(May 2020) Lipid Signals from Plasma Membrane. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028843]