Lipid bilayer stress in obesity-linked inflammatory and metabolic disorders.

[en] The maintenance of the characteristic lipid compositions and physicochemical properties of biological membranes is essential for their proper function. Mechanisms allowing to sense and restore membrane homeostasis have been identified in prokaryotes for a long time and more recently in eukaryotes. A membrane remodeling can result from aberrant metabolism as seen in obesity. In this review, we describe how such lipid bilayer stress can account for the modulation of membrane proteins involved in the pathogenesis of obesity-linked inflammatory and metabolic disorders. We address the case of the Toll-like receptor 4 that is implicated in the obesity-related low grade inflammation and insulin resistance. The lipid raft-mediated TLR4 activation is promoted by an enrichment of the plasma membrane with saturated lipids or cholesterol increasing the lipid phase order. We discuss of the plasma membrane Na, K-ATPase that illustrates a new concept according to which direct interactions between specific residues and particular lipids determine both stability and activity of the pump in parallel with indirect effects of the lipid bilayer. The closely related sarco(endo)-plasmic Ca-ATPase embedded in the more fluid ER membrane seems to be more sensitive to a lipid bilayer stress as demonstrated by its inactivation in cholesterol-loaded macrophages or its inhibition mediated by an increased PtdCho/PtdEtn ratio in obese mice hepatocytes. Finally, we describe the model recently proposed for the activation of the conserved IRE-1 protein through alterations in the ER membrane lipid packing and thickness. Such IRE-1 activation could occur in response to abnormal lipid synthesis and membrane remodeling as observed in hepatocytes exposed to excess nutrients. Since the IRE-1/XBP1 branch also stimulates the lipid synthesis, this pathway could create a vicious cycle "lipogenesis-ER lipid bilayer stress-lipogenesis" amplifying hepatic ER pathology and the obesity-linked systemic metabolic defects.

Disciplines :

Endocrinology, metabolism & nutrition

Author, co-author :

Gianfrancesco, Marco ; Université de Liège - ULiège > Département des sciences de la santé publique > Diabétologie, nutrition et maladies métaboliques

Paquot, Nicolas ; Université de Liège - ULiège > Département des sciences de la santé publique > Diabétologie, nutrition et maladies métaboliques

Piette, Jacques ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie et immunologie

Legrand, Sylvie ; Université de Liège - ULiège > GIGA-R : Virologie - Immunologie

Language :

English

Title :

Lipid bilayer stress in obesity-linked inflammatory and metabolic disorders.

Publication date :

17 February 2018

Journal title :

Biochemical Pharmacology

ISSN :

0006-2952

eISSN :

1873-2968

Publisher :

Elsevier, Netherlands

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 28 May 2018

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Bibliography

Singer, S.J., Nicolson, G.L., The fluid mosaic model of the structure of cell membranes. Science 175 (1972), 720–731, 10.1126/science.175.4023.720.
Chandler, D., Interfaces and the driving force of hydrophobic assembly. Nature, 437, 2005, 10.1038/nature04162 nature04162.
Ray, S., Kassan, A., Busija, A.R., Rangamani, P., Patel, H.H., The plasma membrane as a capacitor for energy and metabolism. Am. J. Physiol. – Cell Physiol. 310 (2016), C181–C192, 10.1152/ajpcell.00087.2015.
Ladha, S., The lipid organisation of the cell membrane. Grasas Aceites 51 (2000), 56–65.
Meyer zu Heringdorf, D., Jakobs, K.H., Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim. Biophys. Acta 1768 (2007), 923–940, 10.1016/j.bbamem.2006.09.026.
Vance, J.E., Phospholipid synthesis and transport in mammalian cells. Traffic 16 (2015), 1–18, 10.1111/tra.12230.
Frolov, V.A., Shnyrova, A.V., Zimmerberg, J., Lipid polymorphisms and membrane shape. Cold Spring Harb. Perspect. Biol., 3, 2011, 10.1101/cshperspect.a004747.
Marsh, D., Lateral pressure profile, spontaneous curvature frustration, and the incorporation and conformation of proteins in membranes. Biophys. J. 93 (2007), 3884–3899, 10.1529/biophysj.107.107938.
Holthuis, J.C.M., Menon, A.K., Lipid landscapes and pipelines in membrane homeostasis. Nature, 510, 2014, 10.1038/nature13474 nature13474.
Magalhaes, M.A.O., Glogauer, M., Pivotal advance: phospholipids determine net membrane surface charge resulting in differential localization of active Rac1 and Rac2. J. Leukoc. Biol. 87 (2010), 545–555, 10.1189/jlb.0609390.
Fuller, N., Rand, R.P., The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophys. J. 81 (2001), 243–254, 10.1016/S0006-3495(01)75695-0.
Fahy, E., Subramaniam, S., Brown, H.A., Glass, C.K., Merrill, A.H., Murphy, R.C., Raetz, C.R.H., Russell, D.W., Seyama, Y., Shaw, W., Shimizu, T., Spener, F., van Meer, G., VanNieuwenhze, M.S., White, S.H., Witztum, J.L., Dennis, E.A., A comprehensive classification system for lipids. J. Lipid Res. 46 (2005), 839–862, 10.1194/jlr.E400004-JLR200.
Fahy, E., Subramaniam, S., Murphy, R.C., Nishijima, M., Raetz, C.R.H., Shimizu, T., Spener, F., van Meer, G., Wakelam, M.J.O., Dennis, E.A., Update of the LIPID MAPS comprehensive classification system for lipids. J. Lipid Res. 50 (2009), S9–S14, 10.1194/jlr.R800095-JLR200.
Řezanka, T., Sigler, K., Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog. Lipid Res. 48 (2009), 206–238, 10.1016/j.plipres.2009.03.003.
Rustan, A.C., Drevon, C.A., Fatty acids: structures and properties. John Wiley & Sons, Ltd., 2005, John Wiley & Sons, Ltd., Chichester, 10.1038/npg.els.0003894.
Slotte, J.P., Biological functions of sphingomyelins. Prog. Lipid Res. 52 (2013), 424–437, 10.1016/j.plipres.2013.05.001.
Aittoniemi, J., Niemelä P.S., Hyvönen, M.T., Karttunen, M., Vattulainen, I., Insight into the putative specific interactions between cholesterol, sphingomyelin, and palmitoyl-oleoyl phosphatidylcholine. Biophys. J. 92 (2007), 1125–1137, 10.1529/biophysj.106.088427.
Hofsäß C., Lindahl, E., Edholm, O., Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 84 (2003), 2192–2206.
Schwarz, D.S., Blower, M.D., The endoplasmic reticulum: structure, function and response to cellular signaling. Cell. Mol. Life Sci. 73 (2016), 79–94, 10.1007/s00018-015-2052-6.
Gulati, S., Liu, Y., Munkacsi, A.B., Wilcox, L., Sturley, S.L., Sterols and sphingolipids: dynamic duo or partners in crime?. Prog. Lipid Res. 49 (2010), 353–365, 10.1016/j.plipres.2010.03.003.
van Meer, G., de Kroon, A.I.P.M., Lipid map of the mammalian cell. J. Cell Sci. 124 (2011), 5–8, 10.1242/jcs.071233.
Holthuis, J.C.M., Pomorski, T., Raggers, R.J., Sprong, H., Meer, G.V., The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81 (2001), 1689–1723.
van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 (2008), 112–124, 10.1038/nrm2330.
Strauss, J.F., Kishida, T., Christenson, L.K., Fujimoto, T., Hiroi, H., START domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells. Mol. Cell. Endocrinol. 202 (2003), 59–65, 10.1016/S0303-7207(03)00063-7.
Wilfling, F., Haas, J.T., Walther, T.C., Farese, R.V., Lipid droplet biogenesis. Curr. Opin. Cell Biol. 29 (2014), 39–45, 10.1016/j.ceb.2014.03.008.
Thiam, A.R., Farese, R.V., Walther, T.C., The biophysics and cell biology of lipid droplets. Nat. Rev. Mol. Cell Biol. 14 (2013), 775–786, 10.1038/nrm3699.
Cambridge Advanced Learner's Dictionary, Cambridge University Press, 2008.
Veatch, S.L., Keller, S.L., Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85 (2003), 3074–3083.
Kaiser, H.-J., Lingwood, D., Levental, I., Sampaio, J.L., Kalvodova, L., Rajendran, L., Simons, K., Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 16645–16650, 10.1073/pnas.0908987106.
Wang, T.-Y., Silvius, J.R., Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane. Biophys. J. 81 (2001), 2762–2773, 10.1016/S0006-3495(01)75919-X.
Weber, G., Farris, F.J., Synthesis and spectral properties of a hydrophobic fluorescent probe: 6-propionyl-2-(dimethylamino)naphthalene. Biochemistry (Moscow) 18 (1979), 3075–3078, 10.1021/bi00581a025.
Bagatolli, L.A., To see or not to see: lateral organization of biological membranes and fluorescence microscopy. Biochim. Biophys. Acta 1758 (2006), 1541–1556, 10.1016/j.bbamem.2006.05.019.
Harris, F.M., Best, K.B., Bell, J.D., Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim. Biophys. Acta 1565 (2002), 123–128, 10.1016/S0005-2736(02)00514-X.
Sanchez, S.A., Tricerri, M.A., Gratton, E., Laurdan generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 7314–7319, 10.1073/pnas.1118288109.
Pike, L.J., Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J. Lipid Res. 47 (2006), 1597–1598, 10.1194/jlr.E600002-JLR200.
Guan, X.L., Souza, C.M., Pichler, H., Dewhurst, G., Schaad, O., Kajiwara, K., Wakabayashi, H., Ivanova, T., Castillon, G.A., Piccolis, M., Abe, F., Loewith, R., Funato, K., Wenk, M.R., Riezman, H., Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol. Biol. Cell. 20 (2009), 2083–2095, 10.1091/mbc.E08-11-1126.
Ramstedt, B., Slotte, J.P., Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length. Biophys. J. 76 (1999), 908–915.
Levental, I., Grzybek, M., Simons, K., Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry (Moscow) 49 (2010), 6305–6316, 10.1021/bi100882y.
Surma, M.A., Klose, C., Peng, D., Shales, M., Mrejen, C., Stefanko, A., Braberg, H., Gordon, D.E., Vorkel, D., Ejsing, C.S., Farese, R., Simons, K., Krogan, N.J., Ernst, R., A lipid E-MAP identifies Ubx2 as a critical regulator of lipid saturation and lipid bilayer stress. Mol. Cell. 51 (2013), 519–530, 10.1016/j.molcel.2013.06.014.
Diaz-Rohrer, B.B., Levental, K.R., Simons, K., Levental, I., Membrane raft association is a determinant of plasma membrane localization. Proc. Natl. Acad. Sci. 111 (2014), 8500–8505, 10.1073/pnas.1404582111.
Fritzsche, M., Erlenkämper, C., Moeendarbary, E., Charras, G., Kruse, K., Actin kinetics shapes cortical network structure and mechanics. Sci. Adv., 2, 2016, e1501337, 10.1126/sciadv.1501337.
Köster, D.V., Mayor, S., Cortical actin and the plasma membrane: inextricably intertwined. Curr. Opin. Cell Biol. 38 (2016), 81–89, 10.1016/j.ceb.2016.02.021.
Lingwood, D., Binnington, B., Róg, T., Vattulainen, I., Grzybek, M., Coskun, Ü., Lingwood, C.A., Simons, K., Cholesterol modulates glycolipid conformation and receptor activity. Nat. Chem. Biol., 7, 2011, 10.1038/nchembio.551 nchembio.51.
Laganowsky, A., Reading, E., Allison, T.M., Ulmschneider, M.B., Degiacomi, M.T., Baldwin, A.J., Robinson, C.V., Membrane proteins bind lipids selectively to modulate their structure and function. Nature, 510, 2014, 10.1038/nature13419 nature13419.
Varshney, P., Yadav, V., Saini, N., Lipid rafts in immune signalling: current progress and future perspective. Immunology 149 (2016), 13–24, 10.1111/imm.12617.
Beissert, S., He, H.-T., Hueber, A.-O., Lellouch, A.C., Metze, D., Mehling, A., Luger, T.A., Schwarz, T., Grabbe, S., Impaired cutaneous immune responses in Thy-1-deficient mice. J. Immunol. 161 (1998), 5296–5302.
Ameer, F., Scandiuzzi, L., Hasnain, S., Kalbacher, H., Zaidi, N., De novo lipogenesis in health and disease. Metab. Clin. Exp. 63 (2014), 895–902, 10.1016/j.metabol.2014.04.003.
Diraison, F., Yankah, V., Letexier, D., Dusserre, E., Jones, P., Beylot, M., Differences in the regulation of adipose tissue and liver lipogenesis by carbohydrates in humans. J. Lipid Res. 44 (2003), 846–853, 10.1194/jlr.M200461-JLR200.
Lodhi, I.J., Wei, X., Semenkovich, C.F., Lipoexpediency: de novo lipogenesis as a metabolic signal transmitter. Trends Endocrinol. Metab. 22 (2011), 1–8, 10.1016/j.tem.2010.09.002.
Strable, M.S., Ntambi, J.M., Genetic control of de novo lipogenesis: role in diet-induced obesity. Crit. Rev. Biochem. Mol. Biol. 45 (2010), 199–214, 10.3109/10409231003667500.
Shao, W., Espenshade, P.J., Expanding roles for SREBP in metabolism. Cell Metab. 16 (2012), 414–419, 10.1016/j.cmet.2012.09.002.
Herman, M.A., Peroni, O.D., Villoria, J., Schön, M.R., Abumrad, N.A., Blüher, M., Klein, S., Kahn, B.B., A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism. Nature 484 (2012), 333–338, 10.1038/nature10986.
Guillou, H., Zadravec, D., Martin, P.G.P., Jacobsson, A., The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog. Lipid Res. 49 (2010), 186–199, 10.1016/j.plipres.2009.12.002.
Jakobsson, A., Westerberg, R., Jacobsson, A., Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45 (2006), 237–249, 10.1016/j.plipres.2006.01.004.
Ye, J., DeBose-Boyd, R.A., Regulation of cholesterol and fatty acid synthesis. Cold Spring Harb. Perspect. Biol., 3, 2011, a004754, 10.1101/cshperspect.a004754.
Brown, M.S., Goldstein, J.L., The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89 (1997), 331–340, 10.1016/S0092-8674(00)80213-5.
Sun, L.-P., Li, L., Goldstein, J.L., Brown, M.S., Insig required for sterol-mediated inhibition of scap/SREBP binding to COPII proteins in vitro. J. Biol. Chem. 280 (2005), 26483–26490, 10.1074/jbc.M504041200.
DeBose-Boyd, R.A., Brown, M.S., Li, W.-P., Nohturfft, A., Goldstein, J.L., Espenshade, P.J., Transport-dependent proteolysis of SREBP: relocation of site-1 protease from golgi to ER obviates the need for SREBP transport to golgi. Cell 99 (1999), 703–712, 10.1016/S0092-8674(00)81668-2.
Nohturfft, A., Yabe, D., Goldstein, J.L., Brown, M.S., Espenshade, P.J., Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102 (2000), 315–323, 10.1016/S0092-8674(00)00037-4.
Horton, J.D., Shah, N.A., Warrington, J.A., Anderson, N.N., Park, S.W., Brown, M.S., Goldstein, J.L., Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. 100 (2003), 12027–12032, 10.1073/pnas.1534923100.
Hua, X., Nohturfft, A., Goldstein, J.L., Brown, M.S., Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell 87 (1996), 415–426, 10.1016/S0092-8674(00)81362-8.
Pai, J., Guryev, O., Brown, M.S., Goldstein, J.L., Differential stimulation of cholesterol and unsaturated fatty acid biosynthesis in cells expressing individual nuclear sterol regulatory element-binding proteins. J. Biol. Chem. 273 (1998), 26138–26148, 10.1074/jbc.273.40.26138.
DeBose-Boyd, R.A., Ou, J., Goldstein, J.L., Brown, M.S., Expression of sterol regulatory element-binding protein 1c (SREBP-1c) mRNA in rat hepatoma cells requires endogenous LXR ligands. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 1477–1482.
Ou, J., Tu, H., Shan, B., Luk, A., DeBose-Boyd, R.A., Bashmakov, Y., Goldstein, J.L., Brown, M.S., Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 6027–6032, 10.1073/pnas.111138698.
Repa, J.J., Liang, G., Ou, J., Bashmakov, Y., Lobaccaro, J.-M.A., Shimomura, I., Shan, B., Brown, M.S., Goldstein, J.L., Mangelsdorf, D.J., Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRα and LXRβ. Genes Dev. 14 (2000), 2819–2830, 10.1101/gad.844900.
Hannah, V.C., Ou, J., Luong, A., Goldstein, J.L., Brown, M.S., Unsaturated fatty acids down-regulate SREBP isoforms 1a and 1c by two mechanisms in HEK-293 cells. J. Biol. Chem. 276 (2001), 4365–4372, 10.1074/jbc.M007273200.
Ikeda, Y., DeMartino, G.N., Brown, M.S., Lee, J.N., Goldstein, J.L., Ye, J., Regulated endoplasmic reticulum-associated degradation of a polytopic protein. J. Biol. Chem. 284 (2009), 34889–34900, 10.1074/jbc.M109.044875.
Lee, J.N., Song, B., DeBose-Boyd, R.A., Ye, J., Sterol-regulated degradation of Insig-1 mediated by the membrane-bound ubiquitin ligase gp78. J. Biol. Chem. 281 (2006), 39308–39315, 10.1074/jbc.M608999200.
Lee, J.N., Zhang, X., Feramisco, J.D., Gong, Y., Ye, J., Unsaturated fatty acids inhibit proteasomal degradation of Insig-1 at a postubiquitination step. J. Biol. Chem. 283 (2008), 33772–33783, 10.1074/jbc.M806108200.
Yamashita, A., Hayashi, Y., Matsumoto, N., Nemoto-Sasaki, Y., Oka, S., Tanikawa, T., Sugiura, T., Glycerophosphate/acylglycerophosphate acyltransferases. Biology 3 (2014), 801–830, 10.3390/biology3040801.
Reue, K., The lipin family: mutations and metabolism. Curr. Opin. Lipidol. 20 (2009), 165–170, 10.1097/MOL.0b013e32832adee5.
Yen, C.-L.E., Stone, S.J., Koliwad, S., Harris, C., Farese, R.V., Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J. Lipid Res. 49 (2008), 2283–2301, 10.1194/jlr.R800018-JLR200.
Fagone, P., Jackowski, S., Phosphatidylcholine and the CDP-Choline Cycle. Biochim. Biophys. Acta 2013 (1831), 523–532, 10.1016/j.bbalip.2012.09.009.
Vance, D.E., Phospholipid methylation in mammals: from biochemistry to physiological function. Biochim. Biophys. Acta 2014 (1838), 1477–1487, 10.1016/j.bbamem.2013.10.018.
Shindou, H., Hishikawa, D., Harayama, T., Eto, M., Shimizu, T., Generation of membrane diversity by lysophospholipid acyltransferases. J. Biochem. (Tokyo) 154 (2013), 21–28, 10.1093/jb/mvt048.
Lands, W.E.M., Metabolism of glycerolipides: a comparison of lecithin and triglyceride synthesis. J. Biol. Chem. 231 (1958), 883–888.
Lands, W.E.M., Stories about acyl chains. Biochim. Biophys. Acta 1483 (2000), 1–14, 10.1016/S1388-1981(99)00177-8.
Shimizu, T., Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 49 (2009), 123–150, 10.1146/annurev.pharmtox.011008.145616.
Shindou, H., Shimizu, T., Acyl-CoA: lysophospholipid acyltransferases. J. Biol. Chem. 284 (2009), 1–5, 10.1074/jbc.R800046200.
Hishikawa, D., Hashidate, T., Shimizu, T., Shindou, H., Diversity and function of membrane glycerophospholipids generated by the remodeling pathway in mammalian cells. J. Lipid Res. 55 (2014), 799–807, 10.1194/jlr.R046094.
Shindou, H., Hishikawa, D., Nakanishi, H., Harayama, T., Ishii, S., Taguchi, R., Shimizu, T., A single enzyme catalyzes both platelet-activating factor production and membrane biogenesis of inflammatory cells cloning and characterization of acetyl-CoA:LYSO-PAF acetyltransferase. J. Biol. Chem. 282 (2007), 6532–6539, 10.1074/jbc.M609641200.
Demeure, O., Lecerf, F., Duby, C., Desert, C., Ducheix, S., Guillou, H., Lagarrigue, S., Regulation of LPCAT3 by LXR. Gene 470 (2011), 7–11, 10.1016/j.gene.2010.09.002.
Eto, M., Shindou, H., Koeberle, A., Harayama, T., Yanagida, K., Shimizu, T., Lysophosphatidylcholine acyltransferase 3 Is the key enzyme for incorporating arachidonic acid into glycerophospholipids during adipocyte differentiation. Int. J. Mol. Sci. 13 (2012), 16267–16280, 10.3390/ijms131216267.
Hishikawa, D., Shindou, H., Kobayashi, S., Nakanishi, H., Taguchi, R., Shimizu, T., Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 2830–2835, 10.1073/pnas.0712245105.
Zhao, Y., Chen, Y.-Q., Bonacci, T.M., Bredt, D.S., Li, S., Bensch, W.R., Moller, D.E., Kowala, M., Konrad, R.J., Cao, G., Identification and characterization of a major liver lysophosphatidylcholine acyltransferase. J. Biol. Chem. 283 (2008), 8258–8265, 10.1074/jbc.M710422200.
Matsuda, S., Inoue, T., Lee, H.-C., Kono, N., Tanaka, F., Gengyo-Ando, K., Mitani, S., Arai, H., Member of the membrane-bound O-acyltransferase (MBOAT) family encodes a lysophospholipid acyltransferase with broad substrate specificity. Genes Cells Devoted Mol. Cell. Mech. 13 (2008), 879–888, 10.1111/j.1365-2443.2008.01212.x.
Rong, X., Albert, C.J., Hong, C., Duerr, M.A., Chamberlain, B.T., Tarling, E.J., Ito, A., Gao, J., Wang, B., Edwards, P.A., Jung, M.E., Ford, D.A., Tontonoz, P., LXRs regulate ER stress and inflammation through dynamic modulation of membrane phospholipid composition. Cell Metab. 18 (2013), 685–697, 10.1016/j.cmet.2013.10.002.
Dawaliby, R., Trubbia, C., Delporte, C., Noyon, C., Ruysschaert, J.-M., Antwerpen, P.V., Govaerts, C., Phosphatidylethanolamine is a key regulator of membrane fluidity in eukaryotic cells. J. Biol. Chem. 291 (2016), 3658–3667, 10.1074/jbc.M115.706523.
Jensen, M.D., Fate of fatty acids at rest and during exercise: regulatory mechanisms. Acta Physiol. Scand. 178 (2003), 385–390, 10.1046/j.1365-201X.2003.01167.x.
Li, Y., Ge, M., Ciani, L., Kuriakose, G., Westover, E.J., Dura, M., Covey, D.F., Freed, J.H., Maxfield, F.R., Lytton, J., Tabas, I., Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages. J. Biol. Chem. 279 (2004), 37030–37039, 10.1074/jbc.M405195200.
Cornelius, F., Habeck, M., Kanai, R., Toyoshima, C., Karlish, S.J.D., General and specific lipid-protein interactions in Na, K-ATPase. Biochim. Biophys. Acta 2015 (1848), 1729–1743, 10.1016/j.bbamem.2015.03.012.
Abbott, S.K., Else, P.L., Atkins, T.A., Hulbert, A.J., Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochim. Biophys. Acta 2012 (1818), 1309–1317, 10.1016/j.bbamem.2012.01.011.
Lund, E.K., Harvey, L.J., Ladha, S., Clark, D.C., Johnson, I.T., Effects of dietary fish oil supplementation on the phospholipid composition and fluidity of cell membranes from human volunteers. Ann. Nutr. Metab. 43 (1999), 290–300.
Andersson, A., Nälsén, C., Tengblad, S., Vessby, B., Fatty acid composition of skeletal muscle reflects dietary fat composition in humans. Am. J. Clin. Nutr. 76 (2002), 1222–1229.
Kersten, S., Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep. 2 (2001), 282–286, 10.1093/embo-reports/kve071.
Rysman, E., Brusselmans, K., Scheys, K., Timmermans, L., Derua, R., Munck, S., Van Veldhoven, P.P., Waltregny, D., Daniëls, V.W., Machiels, J., Vanderhoydonc, F., Smans, K., Waelkens, E., Verhoeven, G., Swinnen, J.V., De novo lipogenesis protects cancer cells from free radicals and chemotherapeutics by promoting membrane lipid saturation. Cancer Res. 70 (2010), 8117–8126, 10.1158/0008-5472.CAN-09-3871.
Fu, S., Yang, L., Li, P., Hofmann, O., Dicker, L., Hide, W., Lin, X., Watkins, S.M., Ivanov, A.R., Hotamisligil, G.S., Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473 (2011), 528–531, 10.1038/nature09968.
Alberti, K.G.M.M., Eckel, R.H., Grundy, S.M., Zimmet, P.Z., Cleeman, J.I., Donato, K.A., Fruchart, J.-C., James, W.P.T., Loria, C.M., Smith, S.C., International Diabetes Federation Task Force on Epidemiology and Prevention, Hational Heart, Lung, and Blood Institute, American Heart Association, World Heart Federation, International Atherosclerosis Society, International Association for the Study of Obesity, Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120 (2009), 1640–1645, 10.1161/CIRCULATIONAHA.109.192644.
Soriguer, F., García-Serrano, S., García-Almeida, J.M., Garrido-Sánchez, L., García-Arnés, J., Tinahones, F.J., Cardona, I., Rivas-Marín, J., Gallego-Perales, J.L., García-Fuentes, E., Changes in the serum composition of free-fatty acids during an intravenous glucose tolerance test. Obes. Silver Spring MD 17 (2009), 10–15, 10.1038/oby.2008.475.
Pilon, M., Revisiting the membrane-centric view of diabetes. Lipids Health Dis., 15, 2016, 10.1186/s12944-016-0342-0.
Clifton, P.M., Nestel, P.J., Relationship between plasma insulin and erythrocyte fatty acid composition. Prostaglandins Leukot. Essent. Fatty Acids 59 (1998), 191–194.
Borkman, M., Storlien, L.H., Pan, D.A., Jenkins, A.B., Chisholm, D.J., Campbell, L.V., The relation between insulin sensitivity and the fatty-acid composition of skeletal-muscle phospholipids. N. Engl. J. Med. 328 (1993), 238–244, 10.1056/NEJM199301283280404.
Bakan, E., Yildirim, A., Kurtul, N., Polat, M.F., Dursun, H., Cayir, K., Effects of type 2 diabetes mellitus on plasma fatty acid composition and cholesterol content of erythrocyte and leukocyte membranes. Acta Diabetol. 43 (2006), 109–113, 10.1007/s00592-007-0224-4.
Forouhi, N.G., Koulman, A., Sharp, S.J., Imamura, F., Kröger, J., Schulze, M.B., Crowe, F.L., Huerta, J.M., Guevara, M., Beulens, J.W.J., van Woudenbergh, G.J., Wang, L., Summerhill, K., Griffin, J.L., Feskens, E.J.M., Amiano, P., Boeing, H., Clavel-Chapelon, F., Dartois, L., Fagherazzi, G., Franks, P.W., Gonzalez, C., Jakobsen, M.U., Kaaks, R., Key, T.J., Khaw, K.-T., Kühn, T., Mattiello, A., Nilsson, P.M., Overvad, K., Pala, V., Palli, D., Quirós, J.R., Rolandsson, O., Roswall, N., Sacerdote, C., Sánchez, M.-J., Slimani, N., Spijkerman, A.M.W., Tjonneland, A., Tormo, M.-J., Tumino, R., van der A, D.L., van der Schouw, Y.T., Langenberg, C., Riboli, E., Wareham, N.J., Differences in the prospective association between individual plasma phospholipid saturated fatty acids and incident type 2 diabetes: the EPIC-InterAct case-cohort study. Lancet Diabetes Endocrinol. 2 (2014), 810–818, 10.1016/S2213-8587(14)70146-9.
Kröger, J., Jacobs, S., Jansen, E.H.J.M., Fritsche, A., Boeing, H., Schulze, M.B., Erythrocyte membrane fatty acid fluidity and risk of type 2 diabetes in the EPIC-Potsdam study. Diabetologia 58 (2015), 282–289, 10.1007/s00125-014-3421-7.
Elmendorf, J.S., Fluidity of insulin action. Mol. Biotechnol. 27 (2004), 127–138, 10.1385/MB:27:2:127.
Ginsberg, B.H., Brown, T.J., Simon, I., Spector, A.A., Effect of the membrane lipid environment on the properties of insulin receptors. Diabetes 30 (1981), 773–780.
Weijers, R.N.M., Lipid composition of cell membranes and its relevance in type 2 diabetes mellitus. Curr. Diabetes Rev. 8 (2012), 390–400.
Vidya, M.K., Kumar, V.G., Sejian, V., Bagath, M., Krishnan, G., Bhatta, R., Toll-like receptors: significance, ligands, signaling pathways, and functions in mammals. Int. Rev. Immunol., 2017, 1–17, 10.1080/08830185.2017.1380200.
Steimle, A., Autenrieth, I.B., Frick, J.-S., Structure and function: lipid A modifications in commensals and pathogens. Int. J. Med. Microbiol. IJMM 306 (2016), 290–301, 10.1016/j.ijmm.2016.03.001.
Mertins, P., Przybylski, D., Yosef, N., Qiao, J., Clauser, K., Raychowdhury, R., Eisenhaure, T.M., Maritzen, T., Haucke, V., Satoh, T., Akira, S., Carr, S.A., Regev, A., Hacohen, N., Chevrier, N., An integrative framework reveals signaling-to-transcription events in toll-like receptor signaling. Cell Rep. 19 (2017), 2853–2866, 10.1016/j.celrep.2017.06.016.
Kuzmich, N.N., Sivak, K.V., Chubarev, V.N., Porozov, Y.B., Savateeva-Lyubimova, T.N., Peri, F., TLR4 signaling pathway modulators as potential therapeutics in inflammation and sepsis. Vaccines, 5, 2017, 10.3390/vaccines5040034.
Shi, H., Kokoeva, M.V., Inouye, K., Tzameli, I., Yin, H., Flier, J.S., TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116 (2006), 3015–3025, 10.1172/JCI28898.
Manolakis, A.C., Kapsoritakis, A.N., Tiaka, E.K., Sidiropoulos, A., Gerovassili, A., Satra, M., Vamvakopoulou, D., Tsiopoulos, F., Papanas, N., Skoularigis, I., Potamianos, S.P., Vamvakopoulos, N., TLR4 gene polymorphisms: evidence for protection against type 2 diabetes but not for diabetes-associated ischaemic heart disease. Eur. J. Endocrinol. 165 (2011), 261–267, 10.1530/EJE-11-0280.
Park, B.S., Song, D.H., Kim, H.M., Choi, B.-S., Lee, H., Lee, J.-O., The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458 (2009), 1191–1195, 10.1038/nature07830.
Akira, S., Uematsu, S., Takeuchi, O., Pathogen recognition and innate immunity. Cell 124 (2006), 783–801, 10.1016/j.cell.2006.02.015.
Haziot, A., Ferrero, E., Köntgen, F., Hijiya, N., Yamamoto, S., Silver, J., Stewart, C.L., Goyert, S.M., Resistance to endotoxin shock and reduced dissemination of gram-negative bacteria in CD14-deficient mice. Immunity 4 (1996), 407–414.
Ferrero, E., Jiao, D., Tsuberi, B.Z., Tesio, L., Rong, G.W., Haziot, A., Goyert, S.M., Transgenic mice expressing human CD14 are hypersensitive to lipopolysaccharide. Proc. Natl. Acad. Sci. U.S.A. 90 (1993), 2380–2384.
Jiang, Z., Georgel, P., Du, X., Shamel, L., Sovath, S., Mudd, S., Huber, M., Kalis, C., Keck, S., Galanos, C., Freudenberg, M., Beutler, B., CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6 (2005), 565–570, 10.1038/ni1207.
da Silva Correia, J., Soldau, K., Christen, U., Tobias, P.S., Ulevitch, R.J., Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex. Transfer from CD14 to TLR4 and MD-2. J. Biol. Chem. 276 (2001), 21129–21135, 10.1074/jbc.M009164200.
Fitzgerald, K.A., Rowe, D.C., Golenbock, D.T., Endotoxin recognition and signal transduction by the TLR4/MD2-complex. Microbes Infect. 6 (2004), 1361–1367, 10.1016/j.micinf.2004.08.015.
Triantafilou, M., Miyake, K., Golenbock, D.T., Triantafilou, K., Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115 (2002), 2603–2611.
Triantafilou, M., Morath, S., Mackie, A., Hartung, T., Triantafilou, K., Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane. J. Cell Sci. 117 (2004), 4007–4014, 10.1242/jcs.01270.
Dhungana, S., Merrick, B.A., Tomer, K.B., Fessler, M.B., Quantitative proteomics analysis of macrophage rafts reveals compartmentalized activation of the proteasome and of proteasome-mediated ERK activation in response to lipopolysaccharide. Mol. Cell. Proteomics MCP 8 (2009), 201–213, 10.1074/mcp.M800286-MCP200.
Płóciennikowska, A., Hromada-Judycka, A., Borzęcka, K., Kwiatkowska, K., Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell. Mol. Life Sci. CMLS 72 (2015), 557–581, 10.1007/s00018-014-1762-5.
Koseki, M., Hirano, K.-I., Masuda, D., Ikegami, C., Tanaka, M., Ota, A., Sandoval, J.C., Nakagawa-Toyama, Y., Sato, S.B., Kobayashi, T., Shimada, Y., Ohno-Iwashita, Y., Matsuura, F., Shimomura, I., Yamashita, S., Increased lipid rafts and accelerated lipopolysaccharide-induced tumor necrosis factor-alpha secretion in Abca1-deficient macrophages. J. Lipid Res. 48 (2007), 299–306, 10.1194/jlr.M600428-JLR200.
Yvan-Charvet, L., Welch, C., Pagler, T.A., Ranalletta, M., Lamkanfi, M., Han, S., Ishibashi, M., Li, R., Wang, N., Tall, A.R., Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118 (2008), 1837–1847, 10.1161/CIRCULATIONAHA.108.793869.
Lee, J.Y., Sohn, K.H., Rhee, S.H., Hwang, D., Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276 (2001), 16683–16689, 10.1074/jbc.M011695200.
Wong, S.W., Kwon, M.-J., Choi, A.M.K., Kim, H.-P., Nakahira, K., Hwang, D.H., Fatty acids modulate Toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner. J. Biol. Chem. 284 (2009), 27384–27392, 10.1074/jbc.M109.044065.
Brandl, K., Glück, T., Hartmann, P., Salzberger, B., Falk, W., A designed TLR4/MD-2 complex to capture LPS. J. Endotoxin Res. 11 (2005), 197–206, 10.1179/096805105X58670.
Erridge, C., Samani, N.J., Saturated fatty acids do not directly stimulate Toll-like receptor signaling. Arterioscler. Thromb. Vasc. Biol. 29 (2009), 1944–1949, 10.1161/ATVBAHA.109.194050.
Pal, D., Dasgupta, S., Kundu, R., Maitra, S., Das, G., Mukhopadhyay, S., Ray, S., Majumdar, S.S., Bhattacharya, S., Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat. Med. 18 (2012), 1279–1285, 10.1038/nm.2851.
Velloso, L.A., Folli, F., Saad, M.J., TLR4 at the crossroads of nutrients, gut microbiota, and metabolic inflammation. Endocr. Rev. 36 (2015), 245–271, 10.1210/er.2014-1100.
Hwang, D.H., Kim, J.-A., Lee, J.Y., Mechanisms for the activation of Toll-like receptor 2/4 by saturated fatty acids and inhibition by docosahexaenoic acid. Eur. J. Pharmacol. 785 (2016), 24–35, 10.1016/j.ejphar.2016.04.024.
Snodgrass, R.G., Huang, S., Choi, I.-W., Rutledge, J.C., Hwang, D.H., Inflammasome-mediated secretion of IL-1β in human monocytes through TLR2 activation; modulation by dietary fatty acids. J. Immunol. 191 (2013), 4337–4347, 10.4049/jimmunol.1300298.
Stulnig, T.M., Huber, J., Leitinger, N., Imre, E.-M., Angelisová P., Nowotny, P., Waldhäusl, W., Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J. Biol. Chem. 276 (2001), 37335–37340, 10.1074/jbc.M106193200.
Fan, Y.-Y., Ly, L.H., Barhoumi, R., McMurray, D.N., Chapkin, R.S., Dietary docosahexaenoic acid suppresses T cell protein kinase Cθ lipid raft recruitment and IL-2 production. J. Immunol. 173 (2004), 6151–6160, 10.4049/jimmunol.173.10.6151.
Rivera, C.A., Gaskin, L., Singer, G., Houghton, J., Allman, M., Western diet enhances hepatic inflammation in mice exposed to cecal ligation and puncture. BMC Physiol., 10, 2010, 20, 10.1186/1472-6793-10-20.
Ciesielska, A., Kwiatkowska, K., Modification of pro-inflammatory signaling by dietary components: the plasma membrane as a target. BioEssays News Rev. Mol. Cell. Dev. Biol. 37 (2015), 789–801, 10.1002/bies.201500017.
Sakr, Y., Madl, C., Filipescu, D., Moreno, R., Groeneveld, J., Artigas, A., Reinhart, K., Vincent, J.-L., Obesity is associated with increased morbidity but not mortality in critically ill patients. Intensive Care Med. 34 (2008), 1999–2009, 10.1007/s00134-008-1243-0.
Cani, P.D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A.M., Delzenne, N.M., Burcelin, R., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 57 (2008), 1470–1481, 10.2337/db07-1403.
Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J.P., Druart, C., Bindels, L.B., Guiot, Y., Derrien, M., Muccioli, G.G., Delzenne, N.M., de Vos, W.M., Cani, P.D., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 9066–9071, 10.1073/pnas.1219451110.
Plovier, H., Everard, A., Druart, C., Depommier, C., Van Hul, M., Geurts, L., Chilloux, J., Ottman, N., Duparc, T., Lichtenstein, L., Myridakis, A., Delzenne, N.M., Klievink, J., Bhattacharjee, A., van der Ark, K.C.H., Aalvink, S., Martinez, L.O., Dumas, M.-E., Maiter, D., Loumaye, A., Hermans, M.P., Thissen, J.-P., Belzer, C., de Vos, W.M., Cani, P.D., A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat. Med. 23 (2017), 107–113, 10.1038/nm.4236.
Skou, J.C., The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 23 (1957), 394–401, 10.1016/0006-3002(57)90343-8.
Blanco, G., Mercer, R.W., Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am. J. Physiol. 275 (1998), F633–650.
Post, R.L., Kume, S., Tobin, T., Orcutt, B., Sen, A.K., Flexibility of an active center in sodium-plus-potassium adenosine triphosphatase. J. Gen. Physiol. 54 (1969), 306–326.
Shull, G.E., Greeb, J., Lingrel, J.B., Molecular cloning of three distinct forms of the Na+, K+-ATPase alpha-subunit from rat brain. Biochemistry (Moscow) 25 (1986), 8125–8132.
Shamraj, O.I., Lingrel, J.B., A putative fourth Na+, K(+)-ATPase alpha-subunit gene is expressed in testis. Proc. Natl. Acad. Sci. U.S.A. 91 (1994), 12952–12956.
Morth, J.P., Pedersen, B.P., Toustrup-Jensen, M.S., Sørensen, T.L.-M., Petersen, J., Andersen, J.P., Vilsen, B., Nissen, P., Crystal structure of the sodium-potassium pump. Nature 450 (2007), 1043–1049, 10.1038/nature06419.
Morth, J.P., Pedersen, B.P., Buch-Pedersen, M.J., Andersen, J.P., Vilsen, B., Palmgren, M.G., Nissen, P., A structural overview of the plasma membrane Na+, K+-ATPase and H+-ATPase ion pumps. Nat. Rev. Mol. Cell Biol. 12 (2011), 60–70, 10.1038/nrm3031.
Clausen, M.V., Hilbers, F., Poulsen, H., The structure and function of the Na, K-ATPase isoforms in health and disease. Front. Physiol., 8, 2017, 10.3389/fphys.2017.00371.
Bagrov, A.Y., Shapiro, J.I., Fedorova, O.V., Endogenous cardiotonic steroids: physiology, pharmacology, and novel therapeutic targets. Pharmacol. Rev. 61 (2009), 9–38, 10.1124/pr.108.000711.
Schoner, W., Scheiner-Bobis, G., Endogenous and exogenous cardiac glycosides and their mechanisms of action. Am. J. Cardiovasc. Drugs 7 (2007), 173–189.
Laursen, M., Yatime, L., Nissen, P., Fedosova, N.U., Crystal structure of the high-affinity Na+, K+-ATPase–ouabain complex with Mg2+ bound in the cation binding site. Proc. Natl. Acad. Sci. 110 (2013), 10958–10963, 10.1073/pnas.1222308110.
McMahon, W.S., Holzgrefe, H.H., Walker, J.D., Mukherjee, R., Arthur, S.R., Cavallo, M.J., Child, M.J., Spinale, F.G., Cellular basis for improved left ventricular pump function after digoxin therapy in experimental left ventricular failure. J. Am. Coll. Cardiol. 28 (1996), 495–505, 10.1016/0735-1097(96)00151-9.
Cui, X., Xie, Z., Protein interaction and Na/K-ATPase-mediated signal transduction. Molecules (Basel Switzerland), 22, 2017, 10.3390/molecules22060990.
Nezil, F.A., Bloom, M., Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes. Biophys. J. 61 (1992), 1176–1183, 10.1016/S0006-3495(92)81926-4.
Cornelius, F., Modulation of Na,K-ATPase and Na-ATPase activity by phospholipids and cholesterol. I. Steady-state kinetics. Biochemistry (Moscow) 40 (2001), 8842–8851.
Shinoda, T., Ogawa, H., Cornelius, F., Toyoshima, C., Crystal structure of the sodium-potassium pump at 2.4 A resolution. Nature 459 (2009), 446–450, 10.1038/nature07939.
Kanai, R., Ogawa, H., Vilsen, B., Cornelius, F., Toyoshima, C., Crystal structure of a Na+-bound Na+, K+-ATPase preceding the E1P state. Nature 502 (2013), 201–206, 10.1038/nature12578.
Cohen, E., Goldshleger, R., Shainskaya, A., Tal, D.M., Ebel, C., le Maire, M., Karlish, S.J.D., Purification of Na+, K+-ATPase expressed in Pichia pastoris reveals an essential role of phospholipid-protein interactions. J. Biol. Chem. 280 (2005), 16610–16618, 10.1074/jbc.M414290200.
Kapri-Pardes, E., Katz, A., Haviv, H., Mahmmoud, Y., Ilan, M., Khalfin-Penigel, I., Carmeli, S., Yarden, O., Karlish, S.J.D., Stabilization of the α2 isoform of Na, K-ATPase by mutations in a phospholipid binding pocket. J. Biol. Chem. 286 (2011), 42888–42899, 10.1074/jbc.M111.293852.
Haviv, H., Habeck, M., Kanai, R., Toyoshima, C., Karlish, S.J.D., Neutral phospholipids stimulate Na, K-ATPase activity: a specific lipid-protein interaction. J. Biol. Chem. 288 (2013), 10073–10081, 10.1074/jbc.M112.446997.
Habeck, M., Haviv, H., Katz, A., Kapri-Pardes, E., Ayciriex, S., Shevchenko, A., Ogawa, H., Toyoshima, C., Karlish, S.J.D., Stimulation, inhibition, or stabilization of Na, K-ATPase caused by specific lipid interactions at distinct sites. J. Biol. Chem. 290 (2015), 4829–4842, 10.1074/jbc.M114.611384.
Habeck, M., Kapri-Pardes, E., Sharon, M., Karlish, S.J.D., Specific phospholipid binding to Na, K-ATPase at two distinct sites. Proc. Natl. Acad. Sci. U.S.A. 114 (2017), 2904–2909, 10.1073/pnas.1620799114.
Rodrigo, R., Bächler, J.P., Araya, J., Prat, H., Passalacqua, W., Relationship between (Na + K)-ATPase activity, lipid peroxidation and fatty acid profile in erythrocytes of hypertensive and normotensive subjects. Mol. Cell. Biochem. 303 (2007), 73–81, 10.1007/s11010-007-9457-y.
Rodrigo, R., Miranda-Merchak, A., Valenzuela Grau, R., Bachler, J.P., Vergara, L., Modulation of (Na, K)-ATPase activity by membrane fatty acid composition: therapeutic implications in human hypertension. Clin. Exp. Hypertens. 1993:36 (2014), 17–26, 10.3109/10641963.2013.783048.
Iannello, S., Milazzo, P., Belfiore, F., Animal and human tissue Na,K-ATPase in normal and insulin-resistant states: regulation, behaviour and interpretative hypothesis on NEFA effects. Obes. Rev. Off. J. Int. Assoc. Study Obes. 8 (2007), 231–251, 10.1111/j.1467-789X.2006.00276.x.
Iannello, S., Milazzo, P., Belfiore, F., Animal and human tissue Na, K-ATPase in obesity and diabetes: a new proposed enzyme regulation. Am. J. Med. Sci. 333 (2007), 1–9.
Chemaly, E.R., Troncone, L., Lebeche, D., SERCA control of cell death and survival. Cell Calcium, 2017, 10.1016/j.ceca.2017.07.001.
Toyoshima, C., Structural aspects of ion pumping by Ca2+-ATPase of sarcoplasmic reticulum. Arch. Biochem. Biophys. 476 (2008), 3–11, 10.1016/j.abb.2008.04.017.
Norimatsu, Y., Hasegawa, K., Shimizu, N., Toyoshima, C., Protein-phospholipid interplay revealed with crystals of a calcium pump. Nature 545 (2017), 193–198, 10.1038/nature22357.
Drachmann, N.D., Olesen, C., Møller, J.V., Guo, Z., Nissen, P., Bublitz, M., Comparing crystal structures of Ca(2+)-ATPase in the presence of different lipids. FEBS J. 281 (2014), 4249–4262, 10.1111/febs.12957.
Cheng, K.H., Lepock, J.R., Hui, S.W., Yeagle, P.L., The role of cholesterol in the activity of reconstituted Ca-ATPase vesicles containing unsaturated phosphatidylethanolamine. J. Biol. Chem. 261 (1986), 5081–5087.
Los, D.A., Murata, N., Membrane fluidity and its roles in the perception of environmental signals. Biochim. Biophys. Acta 1666 (2004), 142–157, 10.1016/j.bbamem.2004.08.002.
Martin, C.E., Oh, C.-S., Jiang, Y., Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochim. Biophys. Acta 1771 (2007), 271–285, 10.1016/j.bbalip.2006.06.010.
Saita, E., Albanesi, D., de Mendoza, D., Sensing membrane thickness: lessons learned from cold stress. Biochim. Biophys. Acta 2016 (1861), 837–846, 10.1016/j.bbalip.2016.01.003.
Ernst, R., Ejsing, C.S., Antonny, B., Homeoviscous adaptation and the regulation of membrane lipids. J. Mol. Biol. 428 (2016), 4776–4791, 10.1016/j.jmb.2016.08.013.
de Mendoza, D., Temperature sensing by membranes. Annu. Rev. Microbiol. 68 (2014), 101–116, 10.1146/annurev-micro-091313-103612.
Sengupta, P., Garrity, P., Sensing temperature. Curr. Biol. 23 (2013), R304–R307, 10.1016/j.cub.2013.03.009.
Ejsing, C.S., Sampaio, J.L., Surendranath, V., Duchoslav, E., Ekroos, K., Klemm, R.W., Simons, K., Shevchenko, A., Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc. Natl. Acad. Sci. 106 (2009), 2136–2141, 10.1073/pnas.0811700106.
Klose, C., Surma, M.A., Gerl, M.J., Meyenhofer, F., Shevchenko, A., Simons, K., Flexibility of a eukaryotic lipidome – insights from yeast lipidomics. PLoS One, 7, 2012, e35063, 10.1371/journal.pone.0035063.
Ballweg, S., Ernst, R., Control of membrane fluidity: the OLE pathway in focus. Biol. Chem. 398 (2016), 215–228, 10.1515/hsz-2016-0277.
Albanesi, D., Mansilla, M.C., de Mendoza, D., The membrane fluidity sensor DesK of Bacillus subtilis controls the signal decay of its cognate response regulator. J. Bacteriol. 186 (2004), 2655–2663, 10.1128/JB.186.9.2655-2663.2004.
Cybulski, L.E., del Solar, G., Craig, P.O., Espinosa, M., de Mendoza, D., Bacillus subtilis DesR functions as a phosphorylation-activated switch to control membrane lipid fluidity. J. Biol. Chem. 279 (2004), 39340–39347, 10.1074/jbc.M405150200.
Aguilar, P.S., Lopez, P., de Mendoza, D., Transcriptional control of the low-temperature-inducible des Gene, encoding the Δ5 desaturase of Bacillus subtilis. J. Bacteriol. 181 (1999), 7028–7033.
Altabe, S.G., Aguilar, P., Caballero, G.M., de Mendoza, D., The Bacillus subtilis acyl lipid desaturase is a Δ5 desaturase. J. Bacteriol. 185 (2003), 3228–3231, 10.1128/JB.185.10.3228-3231.2003.
Diaz, A.R., Mansilla, M.C., Vila, A.J., de Mendoza, D., Membrane topology of the acyl-lipid desaturase from Bacillus subtilis. J. Biol. Chem. 277 (2002), 48099–48106, 10.1074/jbc.M208960200.
Sharpe, H.J., Stevens, T.J., Munro, S., A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142 (2010), 158–169, 10.1016/j.cell.2010.05.037.
Covino, R., Ballweg, S., Stordeur, C., Michaelis, J.B., Puth, K., Wernig, F., Bahrami, A., Ernst, A.M., Hummer, G., Ernst, R., A eukaryotic sensor for membrane lipid saturation. Mol. Cell. 63 (2016), 49–59, 10.1016/j.molcel.2016.05.015.
Hoppe, T., Matuschewski, K., Rape, M., Schlenker, S., Ulrich, H.D., Jentsch, S., Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102 (2000), 577–586, 10.1016/S0092-8674(00)00080-5.
Svensk, E., Devkota, R., Ståhlman, M., Ranji, P., Rauthan, M., Magnusson, F., Hammarsten, S., Johansson, M., Borén, J., Pilon, M., Caenorhabditis elegans PAQR-2 and IGLR-2 protect against glucose toxicity by modulating membrane lipid composition. PLoS Genet., 12, 2016, e1005982, 10.1371/journal.pgen.1005982.
Gilst, M.R.V., Hadjivassiliou, H., Jolly, A., Yamamoto, K.R., Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol., 3, 2005, e53, 10.1371/journal.pbio.0030053.
Pathare, P.P., Lin, A., Bornfeldt, K.E., Taubert, S., Gilst, M.R.V., Coordinate regulation of lipid metabolism by novel nuclear receptor partnerships. PLoS Genet., 8, 2012, e1002645, 10.1371/journal.pgen.1002645.
Walker, A.K., Jacobs, R.L., Watts, J.L., Rottiers, V., Jiang, K., Finnegan, D.M., Shioda, T., Hansen, M., Yang, F., Niebergall, L.J., Vance, D.E., Tzoneva, M., Hart, A.C., Näär, A.M., A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell 147 (2011), 840–852, 10.1016/j.cell.2011.09.045.
Holland, W.L., Miller, R.A., Wang, Z.V., Sun, K., Barth, B.M., Bui, H.H., Davis, K.E., Bikman, B.T., Halberg, N., Rutkowski, J.M., Wade, M.R., Tenorio, V.M., Kuo, M.-S., Brozinick, J.T., Zhang, B.B., Birnbaum, M.J., Summers, S.A., Scherer, P.E., Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med., 17, 2010, nm.2277, 10.1038/nm.2277.
Tanabe, H., Fujii, Y., Okada-Iwabu, M., Iwabu, M., Nakamura, Y., Hosaka, T., Motoyama, K., Ikeda, M., Wakiyama, M., Terada, T., Ohsawa, N., Hato, M., Ogasawara, S., Hino, T., Murata, T., Iwata, S., Hirata, K., Kawano, Y., Yamamoto, M., Kimura-Someya, T., Shirouzu, M., Yamauchi, T., Kadowaki, T., Yokoyama, S., Crystal structures of the human adiponectin receptors. Nature, 520, 2015, 10.1038/nature14301 nature14301.
Yamauchi, T., Kamon, J., Ito, Y., Tsuchida, A., Yokomizo, T., Kita, S., Sugiyama, T., Miyagishi, M., Hara, K., Tsunoda, M., Murakami, K., Ohteki, T., Uchida, S., Takekawa, S., Waki, H., Tsuno, N.H., Shibata, Y., Terauchi, Y., Froguel, P., Tobe, K., Koyasu, S., Taira, K., Kitamura, T., Shimizu, T., Nagai, R., Kadowaki, T., Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature, 423, 2003, 10.1038/nature01705 nature01705.
Bernales, S., Papa, F.R., Walter, P., Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol. 22 (2006), 487–508, 10.1146/annurev.cellbio.21.122303.120200.
Jonikas, M.C., Collins, S.R., Denic, V., Oh, E., Quan, E.M., Schmid, V., Weibezahn, J., Schwappach, B., Walter, P., Weissman, J.S., Schuldiner, M., Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323 (2009), 1693–1697, 10.1126/science.1167983.
Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., Walter, P., Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000), 249–258, 10.1016/S0092-8674(00)80835-1.
Walter, P., Ron, D., The unfolded protein response: from stress pathway to homeostatic regulation. Science 334 (2011), 1081–1086, 10.1126/science.1209038.
Halbleib, K., Pesek, K., Covino, R., Hofbauer, H.F., Wunnicke, D., Hänelt, I., Hummer, G., Ernst, R., Activation of the unfolded protein response by lipid bilayer stress. Mol. Cell., 67, 2017, 10.1016/j.molcel.2017.06.012 673–684.e8.
Mori, K., Signalling pathways in the unfolded protein response: development from yeast to mammals. J. Biochem. (Tokyo) 146 (2009), 743–750, 10.1093/jb/mvp166.
Fagone, P., Sriburi, R., Ward-Chapman, C., Frank, M., Wang, J., Gunter, C., Brewer, J.W., Jackowski, S., Phospholipid biosynthesis program underlying membrane expansion during B-lymphocyte differentiation. J. Biol. Chem. 282 (2007), 7591–7605, 10.1074/jbc.M608175200.
Sriburi, R., Jackowski, S., Mori, K., Brewer, J.W., XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167 (2004), 35–41, 10.1083/jcb.200406136.
Sriburi, R., Bommiasamy, H., Buldak, G.L., Robbins, G.R., Frank, M., Jackowski, S., Brewer, J.W., Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem. 282 (2007), 7024–7034, 10.1074/jbc.M609490200.
Lee, A.-H., Chu, G.C., Iwakoshi, N.N., Glimcher, L.H., XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24 (2005), 4368–4380, 10.1038/sj.emboj.7600903.
Schuck, S., Prinz, W.A., Thorn, K.S., Voss, C., Walter, P., Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J. Cell Biol. 187 (2009), 525–536, 10.1083/jcb.200907074.
Volmer, R., van der Ploeg, K., Ron, D., Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc. Natl. Acad. Sci. 110 (2013), 4628–4633, 10.1073/pnas.1217611110.
Han, S., Lone, M.A., Schneiter, R., Chang, A., Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control. Proc. Natl. Acad. Sci. 107 (2010), 5851–5856, 10.1073/pnas.0911617107.
Lajoie, P., Moir, R.D., Willis, I.M., Snapp, E.L., Kar2p availability defines distinct forms of endoplasmic reticulum stress in living cells. Mol. Biol. Cell 23 (2012), 955–964, 10.1091/mbc.E11-12-0995.
Pineau, L., Colas, J., Dupont, S., Beney, L., Fleurat-Lessard, P., Berjeaud, J.-M., Bergès, T., Ferreira, T., Lipid-induced ER stress: synergistic effects of sterols and saturated fatty acids. Traffic 10 (2009), 673–690, 10.1111/j.1600-0854.2009.00903.x.
Promlek, T., Ishiwata-Kimata, Y., Shido, M., Sakuramoto, M., Kohno, K., Kimata, Y., Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways. Mol. Biol. Cell 22 (2011), 3520–3532, 10.1091/mbc.E11-04-0295.
Thibault, G., Shui, G., Kim, W., McAlister, G.C., Ismail, N., Gygi, S.P., Wenk, M.R., Ng, D.T.W., The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network. Mol. Cell 48 (2012), 16–27, 10.1016/j.molcel.2012.08.016.
Gregor, M.F., Yang, L., Fabbrini, E., Mohammed, B.S., Eagon, J.C., Hotamisligil, G.S., Klein, S., Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 58 (2009), 693–700, 10.2337/db08-1220.
Pietiläinen, K.H., Róg, T., Seppänen-Laakso, T., Virtue, S., Gopalacharyulu, P., Tang, J., Rodriguez-Cuenca, S., Maciejewski, A., Naukkarinen, J., Ruskeepää A.-L., Niemelä P.S., Yetukuri, L., Tan, C.Y., Velagapudi, V., Castillo, S., Nygren, H., Hyötyläinen, T., Rissanen, A., Kaprio, J., Yki-Järvinen, H., Vattulainen, I., Vidal-Puig, A., Orešič M., Association of lipidome remodeling in the adipocyte membrane with acquired obesity in humans. PLoS Biol., 9, 2011, 10.1371/journal.pbio.1000623.
Herbert, T.P., Laybutt, D.R., A Reevaluation of the role of the unfolded protein response in islet dysfunction: maladaptation or a failure to adapt?. Diabetes 65 (2016), 1472–1480, 10.2337/db15-1633.
Rocha, M., Diaz-Morales, N., Rovira-Llopis, S., Escribano-Lopez, I., Bañuls, C., Hernandez-Mijares, A., Diamanti-Kandarakis, E., Victor, V.M., Mitochondrial dysfunction and endoplasmic reticulum stress in diabetes. Curr. Pharm. Des. 22 (2016), 2640–2649.
Eizirik, D.L., Cardozo, A.K., Cnop, M., The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 29 (2008), 42–61, 10.1210/er.2007-0015.
Fonseca, S.G., Gromada, J., Urano, F., Endoplasmic reticulum stress and pancreatic β-cell death. Trends Endocrinol. Metab. 22 (2011), 266–274, 10.1016/j.tem.2011.02.008.
Scheuner, D., Kaufman, R.J., The Unfolded protein response: a pathway that links insulin demand with β-cell failure and diabetes. Endocr. Rev. 29 (2008), 317–333, 10.1210/er.2007-0039.
Soubias, O., Teague, W.E., Hines, K.G., Gawrisch, K., The role of membrane curvature elastic stress for function of rhodopsin-like G protein-coupled receptors. Biochimie 107:Pt A (2014), 28–32, 10.1016/j.biochi.2014.10.011.
Arish, M., Husein, A., Kashif, M., Sandhu, P., Hasnain, S.E., Akhter, Y., Rub, A., Orchestration of membrane receptor signaling by membrane lipids. Biochimie 113 (2015), 111–124, 10.1016/j.biochi.2015.04.005.
Savage, D.B., Choi, C.S., Samuel, V.T., Liu, Z.-X., Zhang, D., Wang, A., Zhang, X.-M., Cline, G.W., Yu, X.X., Geisler, J.G., Bhanot, S., Monia, B.P., Shulman, G.I., Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J. Clin. Invest. 116 (2006), 817–824, 10.1172/JCI27300.
Ntambi, J.M., Miyazaki, M., Stoehr, J.P., Lan, H., Kendziorski, C.M., Yandell, B.S., Song, Y., Cohen, P., Friedman, J.M., Attie, A.D., Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. U.S.A. 99 (2002), 11482–11486, 10.1073/pnas.132384699.
Jacquemyn, J., Cascalho, A., Goodchild, R.E., The ins and outs of endoplasmic reticulum-controlled lipid biosynthesis. EMBO Rep. 18 (2017), 1905–1921, 10.15252/embr.201643426.
Cassel, S.L., Joly, S., Sutterwala, F.S., The NLRP3 inflammasome: a sensor of immune danger signals. Semin. Immunol. 21 (2009), 194–198, 10.1016/j.smim.2009.05.002.
Vandanmagsar, B., Youm, Y.-H., Ravussin, A., Galgani, J.E., Stadler, K., Mynatt, R.L., Ravussin, E., Stephens, J.M., Dixit, V.D., The NALP3/NLRP3 inflammasome instigates obesity-induced autoinflammation and insulin resistance. Nat. Med. 17 (2011), 179–188, 10.1038/nm.2279.
L'homme, L., Esser, N., Riva, L., Scheen, A., Paquot, N., Piette, J., Legrand-Poels, S., Unsaturated fatty acids prevent activation of NLRP3 inflammasome in human monocytes/macrophages. J. Lipid Res. 54 (2013), 2998–3008, 10.1194/jlr.M037861.
Esser, N., L'homme, L., Roover, A.D., Kohnen, L., Scheen, A.J., Moutschen, M., Piette, J., Legrand-Poels, S., Paquot, N., Obesity phenotype is related to NLRP3 inflammasome activity and immunological profile of visceral adipose tissue. Diabetologia 56 (2013), 2487–2497, 10.1007/s00125-013-3023-9.
Legrand-Poels, S., Esser, N., L'Homme, L., Scheen, A., Paquot, N., Piette, J., Free fatty acids as modulators of the NLRP3 inflammasome in obesity/type 2 diabetes. Biochem. Pharmacol., 2014, 10.1016/j.bcp.2014.08.013.
Esser, N., Legrand-Poels, S., Piette, J., Scheen, A.J., Paquot, N., Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract. 105 (2014), 141–150, 10.1016/j.diabres.2014.04.006.
Robblee, M.M., Kim, C.C., Abate, J.P., Valdearcos, M., Sandlund, K.L.M., Shenoy, M.K., Volmer, R., Iwawaki, T., Koliwad, S.K., Saturated fatty acids engage an IRE1α-dependent pathway to activate the NLRP3 inflammasome in myeloid cells. Cell Rep. 14 (2016), 2611–2623, 10.1016/j.celrep.2016.02.053.