Orchestration of membrane receptor signaling by membrane lipids

Biochimie

Volumn 113, Issue , 2015, Pages 111-124

  Arish, Mohd ^a   Husein, Atahar ^a   Kashif, Mohammad ^a   Sandhu, Padmani ^b   Hasnain, Seyed E ^c   Akhter, Yusuf ^b   Rub, Abdur ^a  

^a JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

^b CENTRAL UNIVERSITY OF HIMACHAL PRADESH   (India)

^c INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

Author keywords

Host pathogen; Lipid; Membrane; Membrane properties; Receptor; Signaling

Indexed keywords

CHOLINERGIC RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MEMBRANE LIPID; MEMBRANE RECEPTOR; OPIATE RECEPTOR; SEROTONIN 1A RECEPTOR; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; CELL SURFACE RECEPTOR;

AMINO ACID SEQUENCE; AUTOPHOSPHORYLATION; BACTERIAL INFECTION; BIOLOGICAL FUNCTIONS; CELL MEMBRANE; CONFORMATIONAL TRANSITION; HOST PATHOGEN INTERACTION; HUMAN; INTERNALIZATION; MEMBRANE FLUIDITY; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; NONHUMAN; PROTOZOAL INFECTION; REGULATORY MECHANISM; REVIEW; RIGIDITY; SECOND MESSENGER; SIGNAL TRANSDUCTION; SURFACE TENSION; VIRUS INFECTION; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL MEMBRANE; HUMANS; MEMBRANE LIPIDS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84928471907     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.04.005     Document Type: Review

References (194)

1. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
2. A. Rub, R. Dey, M. Jadhav, R. Kamat, S. Chakkaramakkil, S. Majumdar, R. Mukhopadhyaya, and B. Saha Cholesterol depletion associated with leishmania major infection alters macrophage CD40 signalosome composition and effector function Nat. Immunol. 10 2009 273 280
3. T. Shimamura, S. Weyand, O. Beckstein, N.G. Rutherford, J.M. Hadden, D. Sharples, M.S. Sansom, S. Iwata, P.J. Henderson, and A.D. Cameron Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1 Science 328 2010 470 473
4. K.G. Harikumar, V. Puri, R.D. Singh, K. Hanada, R.E. Pagano, and L.J. Miller Differential effects of modification of membrane cholesterol and sphingolipids on the conformation, function, and trafficking of the G protein-coupled cholecystokinin receptor J. Biol. Chem. 280 2005 2176 2185
5. A. Laganowsky, E. Reading, T.M. Allison, M.B. Ulmschneider, M.T. Degiacomi, A.J. Baldwin, and C.V. Robinson Membrane proteins bind lipids selectively to modulate their structure and function Nature 510 2014 172 175
6. H. Sprong, P. van der Sluijs, and G. van Meer How proteins move lipids and lipids move proteins Nat. Rev. Mol. Cell Biol. 2 2001 504 513
7. J. Fantini, and F.J. Barrantes Sphingolipid/cholesterol regulation of neurotransmitter receptor conformation and function Biochim. Biophys. Acta 1788 2009 2345 2361
8. A.P. Demchenko, Y. Mely, G. Duportail, and A.S. Klymchenko Monitoring biophysical properties of lipid membranes by environment-sensitive fluorescent probes Biophys. J. 96 2009 3461 3470
9. M.T. Stockl, and A. Herrmann Detection of lipid domains in model and cell membranes by fluorescence lifetime imaging microscopy Biochim. Biophys. Acta 1798 2010 1444 1456
10. D.M. Owen, C. Rentero, A. Magenau, A. Abu-Siniyeh, and K. Gaus Quantitative imaging of membrane lipid order in cells and organisms Nat. Protoc. 7 2012 24 35
11. P.A. Janmey, and P.K. Kinnunen Biophysical properties of lipids and dynamic membranes Trends Cell Biol. 16 2006 538 546
12. H. Cho, M. Wu, B. Bilgin, S.P. Walton, and C. Chan Latest developments in experimental and computational approaches to characterize protein-lipid interactions Proteomics 12 2012 3273 3285
13. K.A. Scott, P.J. Bond, A. Ivetac, A.P. Chetwynd, S. Khalid, and M.S. Sansom Coarse-grained MD simulations of membrane protein-bilayer self-assembly Structure 16 2008 621 630
14. G. Khelashvili, and D. Harries How sterol tilt regulates properties and organization of lipid membranes and membrane insertions Chem. Phys. Lipids 169 2013 113 123
15. R. Rusinova, E.A. Hobart, R.E. Koeppe 2nd, and O.S. Andersen Phosphoinositides alter lipid bilayer properties J. Gen. Physiol. 141 2013 673 690
16. A.G. Lee Lipid-protein interactions in biological membranes: a structural perspective Biochim. Biophys. Acta 1612 2003 1 40
17. B.P. Head, H.H. Patel, and P.A. Insel Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling Biochim. Biophys. Acta 1838 2014 532 545
18. T. Rog, and M. Pasenkiewicz-Gierula Cholesterol effects on the phospholipid condensation and packing in the bilayer: a molecular simulation study FEBS Lett. 502 2001 68 71
19. R.M. Potter, K.G. Harikumar, S.V. Wu, and L.J. Miller Differential sensitivity of types 1 and 2 cholecystokinin receptors to membrane cholesterol J. Lipid Res. 53 2012 137 148
20. S. Majumder, R. Dey, S. Bhattacharjee, A. Rub, G. Gupta, S. Bhattacharyya Majumdar, B. Saha, and S. Majumdar Leishmania-induced biphasic ceramide generation in macrophages is crucial for uptake and survival of the parasite J. Infect. Dis. 205 2012 1607 1616
21. D. Ramel, F. Lagarrigue, V. Pons, J. Mounier, S. Dupuis-Coronas, G. Chicanne, P.J. Sansonetti, F. Gaits-Iacovoni, H. Tronchere, and B. Payrastre Shigella flexneri infection generates the lipid PI5P to alter endocytosis and prevent termination of EGFR signaling Sci. Signal 4 2011 ra61
22. E.A. Miljan, and E.G. Bremer Regulation of growth factor receptors by gangliosides Sci. STKE 2002 2002 re15
23. A.J. Yates, and A. Rampersaud Sphingolipids as receptor modulators. An overview Ann. N. Y. Acad. Sci. 845 1998 57 71
24. M.R. Wenk The emerging field of lipidomics Nat. Rev. Drug Discov. 4 2005 594 610
25. A.A. Farooqui, L.A. Horrocks, and T. Farooqui Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions, and involvement in neurological disorders Chem. Phys. Lipids 106 2000 1 29
26. B. Fadeel, and D. Xue The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease Crit. Rev. Biochem. Mol. Biol. 44 2009 264 277
27. S. Chiantia, and E. London Sphingolipids and membrane domains: recent advances Handb. Exp. Pharmacol. 2013 33 55
28. D.E. Lee, M.G. Lew, and D.J. Woodbury Vesicle fusion to planar membranes is enhanced by cholesterol and low temperature Chem. Phys. Lipids 166 2013 45 54
29. Y. Barenholz Cholesterol and other membrane active sterols: from membrane evolution to "rafts Prog. Lipid Res. 41 2002 1 5
30. E.J. Dufourc Sterols and membrane dynamics J. Chem. Biol. 1 2008 63 77
31. M.Y. Sun, A.J. Linsenbardt, C.M. Emnett, L.N. Eisenman, Y. Izumi, C.F. Zorumski, and S. Mennerick 24(S)-hydroxycholesterol as a modulator of neuronal signaling and survival Neuroscientist 2015 10.1177/1073858414568122 [Epub ahead of print]
32. Y. Wang, S. Muneton, J. Sjovall, J.N. Jovanovic, and W.J. Griffiths The effect of 24S-hydroxycholesterol on cholesterol homeostasis in neurons: quantitative changes to the cortical neuron proteome J. Proteome Res. 7 2008 1606 1614
33. M.O. Jensen, and O.G. Mouritsen Lipids do influence protein function-the hydrophobic matching hypothesis revisited Biochim. Biophys. Acta 1666 2004 205 226
34. I. Lopez-Montero, M. Velez, and P.F. Devaux Surface tension induced by sphingomyelin to ceramide conversion in lipid membranes Biochim. Biophys. Acta 1768 2007 553 561
35. K.J. Seu, L.R. Cambrea, R.M. Everly, and J.S. Hovis Influence of lipid chemistry on membrane fluidity: tail and headgroup interactions Biophys. J. 91 2006 3727 3735
36. J.C. Mathai, S. Tristram-Nagle, J.F. Nagle, and M.L. Zeidel Structural determinants of water permeability through the lipid membrane J. Gen. Physiol. 131 2008 69 76
37. C.J. Hsieh, Y.W. Chen, and D.W. Hwang Effects of cholesterol on membrane molecular dynamics studied by fast field cycling NMR relaxometry Phys. Chem. Chem. Phys. 15 2013 16634 16640
38. M. Weik, H. Patzelt, G. Zaccai, and D. Oesterhelt Localization of glycolipids in membranes by in vivo labeling and neutron diffraction Mol. Cell 1 1998 411 419
39. J. Zhang, R. Xue, W.Y. Ong, and P. Chen Roles of cholesterol in vesicle fusion and motion Biophys. J. 97 2009 1371 1380
40. M.M. Gleason, M.S. Medow, and T.N. Tulenko Excess membrane cholesterol alters calcium movements, cytosolic calcium levels, and membrane fluidity in arterial smooth muscle cells Circ. Res. 69 1991 216 227
41. J.G. Kay, M. Koivusalo, X. Ma, T. Wohland, and S. Grinstein Phosphatidylserine dynamics in cellular membranes Mol. Biol. Cell 23 2012 2198 2212
42. P. Xu, R.D. Baldridge, R.J. Chi, C.G. Burd, and T.R. Graham Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport J. Cell Biol. 202 2013 875 886
43. J.I. Elliott, A. Surprenant, F.M. Marelli-Berg, J.C. Cooper, R.L. Cassady-Cain, C. Wooding, K. Linton, D.R. Alexander, and C.F. Higgins Membrane phosphatidylserine distribution as a non-apoptotic signalling mechanism in lymphocytes Nat. Cell Biol. 7 2005 808 816
44. T. Yeung, G.E. Gilbert, J. Shi, J. Silvius, A. Kapus, and S. Grinstein Membrane phosphatidylserine regulates surface charge and protein localization Science 319 2008 210 213
45. T. Yeung, B. Heit, J.F. Dubuisson, G.D. Fairn, B. Chiu, R. Inman, A. Kapus, M. Swanson, and S. Grinstein Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation J. Cell Biol. 185 2009 917 928
46. P.F. Devaux Static and dynamic lipid asymmetry in cell membranes Biochemistry 30 1991 1163 1173
47. K. Kanno, M.K. Wu, E.F. Scapa, S.L. Roderick, and D.E. Cohen Structure and function of phosphatidylcholine transfer protein (PC-TP)/StarD2 Biochim. Biophys. Acta 1771 2007 654 662
48. R.M. Epand, R.F. Epand, A. Decicco, and D. Schwarz Curvature properties of novel forms of phosphatidylcholine with branched acyl chains Eur. J. Biochem. 267 2000 2909 2915
49. M.E. Haque, T.J. McIntosh, and B.R. Lentz Influence of lipid composition on physical properties and peg-mediated fusion of curved and uncurved model membrane vesicles: "nature's own" fusogenic lipid bilayer Biochemistry 40 2001 4340 4348
50. K. Emoto, and M. Umeda An essential role for a membrane lipid in cytokinesis. Regulation of contractile ring disassembly by redistribution of phosphatidylethanolamine J. Cell Biol. 149 2000 1215 1224
51. S.N. Pinto, L.C. Silva, A.H. Futerman, and M. Prieto Effect of ceramide structure on membrane biophysical properties: the role of acyl chain length and unsaturation Biochim. Biophys. Acta 1808 2011 2753 2760
52. B. Westerlund, P.M. Grandell, Y.J. Isaksson, and J.P. Slotte Ceramide acyl chain length markedly influences miscibility with palmitoyl sphingomyelin in bilayer membranes Eur. Biophys. J. 39 2010 1117 1128
53. A.R. Varela, A.M. Goncalves da Silva, A. Fedorov, A.H. Futerman, M. Prieto, and L.C. Silva Effect of glucosylceramide on the biophysical properties of fluid membranes Biochim. Biophys. Acta 1828 2013 1122 1130
54. P.S. Niemela, M.T. Hyvonen, and I. Vattulainen Influence of chain length and unsaturation on sphingomyelin bilayers Biophys. J. 90 2006 851 863
55. A. Magarkar, V. Dhawan, P. Kallinteri, T. Viitala, M. Elmowafy, T. Rog, and A. Bunker Cholesterol level affects surface charge of lipid membranes in saline solution Sci. Rep. 4 2014 5005
56. J.E. Hale, and F. Schroeder Asymmetric transbilayer distribution of sterol across plasma membranes determined by fluorescence quenching of dehydroergosterol Eur. J. Biochem. 122 1982 649 661
57. M.A. Soto-Arriaza, C. Olivares-Ortega, F.H. Quina, L.F. Aguilar, and C.P. Sotomayor Effect of cholesterol content on the structural and dynamic membrane properties of DMPC/DSPC large unilamellar bilayers Biochim. Biophys. Acta 1828 2013 2763 2769
58. D.A. Brown, and E. London Structure and function of sphingolipid- and cholesterol-rich membrane rafts J. Biol. Chem. 275 2000 17221 17224
59. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
60. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell. Biol. 1 2000 31 39
61. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
62. A. Choubey, R.K. Kalia, N. Malmstadt, A. Nakano, and P. Vashishta Cholesterol translocation in a phospholipid membrane Biophys. J. 104 2013 2429 2436
63. W.F. Bennett, J.L. MacCallum, M.J. Hinner, S.J. Marrink, and D.P. Tieleman Molecular view of cholesterol flip-flop and chemical potential in different membrane environments J. Am. Chem. Soc. 131 2009 12714 12720
64. P.L. Yeagle Modulation of membrane function by cholesterol Biochimie 73 1991 1303 1310
65. K.G. Ormerod, T.P. Rogasevskaia, J.R. Coorssen, and A.J. Mercier Cholesterol-independent effects of methyl-beta-cyclodextrin on chemical synapses PLoS One 7 2012 e36395
66. D.W. Hilgemann, S. Feng, and C. Nasuhoglu The complex and intriguing lives of PIP2 with ion channels and transporters Sci. STKE 2001 2001 re19
67. G. Di Paolo, and P. De Camilli Phosphoinositides in cell regulation and membrane dynamics Nature 443 2006 651 657
68. I.E. Michailidis, T.D. Helton, V.I. Petrou, T. Mirshahi, M.D. Ehlers, and D.E. Logothetis Phosphatidylinositol-4,5-bisphosphate regulates NMDA receptor activity through alpha-actinin J. Neurosci. 27 2007 5523 5532
69. L.C. Silva, O. Ben David, Y. Pewzner-Jung, E.L. Laviad, J. Stiban, S. Bandyopadhyay, A.H. Merrill Jr., M. Prieto, and A.H. Futerman Ablation of ceramide synthase 2 strongly affects biophysical properties of membranes J. Lipid Res. 53 2012 430 436
70. Megha, P. Sawatzki, T. Kolter, R. Bittman, and E. London Effect of ceramide N-acyl chain and polar headgroup structure on the properties of ordered lipid domains (lipid rafts) Biochim. Biophys. Acta 1768 2007 2205 2212
71. Y. Zhang, X. Li, K.A. Becker, and E. Gulbins Ceramide-enriched membrane domains-structure and function Biochim. Biophys. Acta 1788 2009 178 183
72. J.M. Holopainen, M.I. Angelova, and P.K. Kinnunen Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes Biophys. J. 78 2000 830 838
73. Y. Taniguchi, T. Ohba, H. Miyata, and K. Ohki Rapid phase change of lipid microdomains in giant vesicles induced by conversion of sphingomyelin to ceramide Biochim. Biophys. Acta 1758 2006 145 153
74. M. Colombini Membrane channels formed by ceramide Handb. Exp. Pharmacol. 2013 109 126
75. M.N. Perera, V. Ganesan, L.J. Siskind, Z.M. Szulc, J. Bielawski, A. Bielawska, R. Bittman, and M. Colombini Ceramide channels: influence of molecular structure on channel formation in membranes Biochim. Biophys. Acta 1818 2012 1291 1301
76. L.J. Siskind, S. Fluss, M. Bui, and M. Colombini Sphingosine forms channels in membranes that differ greatly from those formed by ceramide J. Bioenerg. Biomembr. 37 2005 227 236
77. F.X. Contreras, J. Sot, A. Alonso, and F.M. Goni Sphingosine increases the permeability of model and cell membranes Biophys. J. 90 2006 4085 4092
78. E.E. Kooijman, V. Chupin, B. de Kruijff, and K.N. Burger Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid Traffic 4 2003 162 174
79. X. Yang, W. Sheng, G.Y. Sun, and J.C. Lee Effects of fatty acid unsaturation numbers on membrane fluidity and alpha-secretase-dependent amyloid precursor protein processing Neurochem. Int. 58 2011 321 329
80. J.E. Baenziger, M.L. Morris, T.E. Darsaut, and S.E. Ryan Effect of membrane lipid composition on the conformational equilibria of the nicotinic acetylcholine receptor J. Biol. Chem. 275 2000 777 784
81. K. Krauss, and P. Altevogt Integrin leukocyte function-associated antigen-1-mediated cell binding can be activated by clustering of membrane rafts J. Biol. Chem. 274 1999 36921 36927
82. R. Saxena, and A. Chattopadhyay Membrane cholesterol stabilizes the human serotonin(1A) receptor Biochim. Biophys. Acta 1818 2012 2936 2942
83. F.J. Barrantes Cholesterol effects on nicotinic acetylcholine receptor: cellular aspects Subcell. Biochem. 51 2010 467 487
84. E.S. Levitt, M.J. Clark, P.M. Jenkins, J.R. Martens, and J.R. Traynor Differential effect of membrane cholesterol removal on mu- and delta-opioid receptors: a parallel comparison of acute and chronic signaling to adenylyl cyclase J. Biol. Chem. 284 2009 22108 22122
85. U. Coskun, M. Grzybek, D. Drechsel, and K. Simons Regulation of human EGF receptor by lipids Proc. Natl. Acad. Sci. U. S. A. 108 2011 9044 9048
86. E. Molnar, M. Swamy, M. Holzer, K. Beck-Garcia, R. Worch, C. Thiele, G. Guigas, K. Boye, I.F. Luescher, P. Schwille, R. Schubert, and W.W. Schamel Cholesterol and sphingomyelin drive ligand-independent T-cell antigen receptor nanoclustering J. Biol. Chem. 287 2012 42664 42674
87. T. Furuchi, and R.G. Anderson Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK) J. Biol. Chem. 273 1998 21099 21104
88. A. Balbis, and B.I. Posner Compartmentalization of EGFR in cellular membranes: role of membrane rafts J. Cell. Biochem. 109 2010 1103 1108
89. N. Ariotti, H. Liang, Y. Xu, Y. Zhang, Y. Yonekubo, K. Inder, G. Du, R.G. Parton, J.F. Hancock, and S.J. Plowman Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation Mol. Cell Biol. 30 2010 3795 3804
90. T. Ringerike, F.D. Blystad, F.O. Levy, I.H. Madshus, and E. Stang Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae J. Cell Sci. 115 2002 1331 1340
91. E.J. Westover, D.F. Covey, H.L. Brockman, R.E. Brown, and L.J. Pike Cholesterol depletion results in site-specific increases in epidermal growth factor receptor phosphorylation due to membrane level effects. Studies with cholesterol enantiomers J. Biol. Chem. 278 2003 51125 51133
92. Y. Liu, R. Li, and S. Ladisch Exogenous ganglioside GD1a enhances epidermal growth factor receptor binding and dimerization J. Biol. Chem. 279 2004 36481 36489
93. S. Julien, M. Bobowski, A. Steenackers, X. Le Bourhis, and P. Delannoy How do gangliosides regulate RTKs signaling? Cells 2 2013 751 767
94. E.G. Bremer, J. Schlessinger, and S. Hakomori Ganglioside-mediated modulation of cell growth. Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor J. Biol. Chem. 261 1986 2434 2440
95. E.A. Miljan, E.J. Meuillet, B. Mania-Farnell, D. George, H. Yamamoto, H.G. Simon, and E.G. Bremer Interaction of the extracellular domain of the epidermal growth factor receptor with gangliosides J. Biol. Chem. 277 2002 10108 10113
96. X. Wang, Z. Rahman, P. Sun, E. Meuillet, D. George, E.G. Bremer, A. Al-Qamari, and A.S. Paller Ganglioside modulates ligand binding to the epidermal growth factor receptor J. Invest Dermatol 116 2001 69 76
97. E.J. Meuillet, B. Mania-Farnell, D. George, J.I. Inokuchi, and E.G. Bremer Modulation of EGF receptor activity by changes in the GM3 content in a human epidermoid carcinoma cell line, A431 Exp. Cell Res. 256 2000 74 82
98. N. Kawashima, S.J. Yoon, K. Itoh, and K. Nakayama Tyrosine kinase activity of epidermal growth factor receptor is regulated by GM3 binding through carbohydrate to carbohydrate interactions J. Biol. Chem. 284 2009 6147 6155
99. F. Guan, K. Handa, and S.I. Hakomori Regulation of epidermal growth factor receptor through interaction of ganglioside GM3 with GlcNAc of N-linked glycan of the receptor: demonstration in ldlD cells Neurochem. Res. 36 2011 1645 1653
100. X. Huang, Y. Li, J. Zhang, Y. Xu, Y. Tian, and K. Ma Ganglioside GM3 inhibits hepatoma cell motility via down-regulating activity of EGFR and PI3K/AKT signaling pathway J. Cell Biochem. 114 2013 1616 1624
101. R. Li, Y. Liu, and S. Ladisch Enhancement of epidermal growth factor signaling and activation of SRC kinase by gangliosides J. Biol. Chem. 276 2001 42782 42792
102. H.J. Yang, K.Y. Jung, D.H. Kwak, S.H. Lee, J.S. Ryu, J.S. Kim, K.T. Chang, J.W. Lee, and Y.K. Choo Inhibition of ganglioside GD1a synthesis suppresses the differentiation of human mesenchymal stem cells into osteoblasts Dev. Growth Differ. 53 2011 323 332
103. S.Y. Park, C.Y. Kwak, J.A. Shayman, and J.H. Kim Globoside promotes activation of ERK by interaction with the epidermal growth factor receptor Biochim. Biophys. Acta 1820 2012 1141 1148
104. T. Goldkorn, K.A. Dressler, J. Muindi, N.S. Radin, J. Mendelsohn, D. Menaldino, D. Liotta, and R.N. Kolesnick Ceramide stimulates epidermal growth factor receptor phosphorylation in A431 human epidermoid carcinoma cells. Evidence that ceramide may mediate sphingosine action J. Biol. Chem. 266 1991 16092 16097
105. L.D. Alexander, Y. Ding, S. Alagarsamy, X.L. Cui, and J.G. Douglas Arachidonic acid induces ERK activation via Src SH2 domain association with the epidermal growth factor receptor Kidney Int. 69 2006 1823 1832
106. A. Petiot, J. Faure, H. Stenmark, and J. Gruenberg PI3P signaling regulates receptor sorting but not transport in the endosomal pathway J. Cell Biol. 162 2003 971 979
107. Y. Sun, A.C. Hedman, X. Tan, N.J. Schill, and R.A. Anderson Endosomal type Igamma PIP 5-kinase controls EGF receptor lysosomal sorting Dev. Cell. 25 2013 144 155
108. A. Norambuena, C. Metz, J.E. Jung, A. Silva, C. Otero, J. Cancino, C. Retamal, J.C. Valenzuela, A. Soza, and A. Gonzalez Phosphatidic acid induces ligand-independent epidermal growth factor receptor endocytic traffic through PDE4 activation Mol. Biol. Cell 21 2010 2916 2929
109. E. Gellynck, K. Heyninck, K.W. Andressen, G. Haegeman, F.O. Levy, P. Vanhoenacker, and K. Van Craenenbroeck The serotonin 5-HT7 receptors: two decades of research Exp. Brain Res. 230 2013 555 568
110. R. Prasad, Y.D. Paila, and A. Chattopadhyay Membrane cholesterol depletion enhances ligand binding function of human serotonin1A receptors in neuronal cells Biochem. Biophys. Res. Commun. 390 2009 93 96
111. S.L. Lin, S. Setya, N.N. Johnson-Farley, and D.S. Cowen Differential coupling of 5-HT(1) receptors to G proteins of the G(i) family Br. J. Pharmacol. 136 2002 1072 1078
112. T.J. Pucadyil, and A. Chattopadhyay Cholesterol modulates ligand binding and G-protein coupling to serotonin(1A) receptors from bovine hippocampus Biochim. Biophys. Acta 1663 2004 188 200
113. R. Prasad, Y.D. Paila, M. Jafurulla, and A. Chattopadhyay Membrane cholesterol depletion from live cells enhances the function of human serotonin(1A) receptors Biochem. Biophys. Res. Commun. 389 2009 333 337
114. Y.D. Paila, and A. Chattopadhyay The function of G-protein coupled receptors and membrane cholesterol: specific or general interaction? Glycoconj J. 26 2009 711 720
115. R.M. Epand Cholesterol and the interaction of proteins with membrane domains Prog. Lipid Res. 45 2006 279 294
116. G. Gimpl Cholesterol-protein interaction: methods and cholesterol reporter molecules Subcell. Biochem. 51 2010 1 45
117. D. Sengupta, and A. Chattopadhyay Identification of cholesterol binding sites in the serotonin1A receptor J. Phys. Chem. B 116 2012 12991 12996
118. M. Jafurulla, S. Tiwari, and A. Chattopadhyay Identification of cholesterol recognition amino acid consensus (CRAC) motif in G-protein coupled receptors Biochem. Biophys. Res. Commun. 404 2011 569 573
119. Y.D. Paila, S. Ganguly, and A. Chattopadhyay Metabolic depletion of sphingolipids impairs ligand binding and signaling of human serotonin1A receptors Biochemistry 49 2010 2389 2397
120. P. Singh, Y.D. Paila, and A. Chattopadhyay Role of glycosphingolipids in the function of human serotonin(1)A receptors J. Neurochem. 123 2012 716 724
121. B. Sjogren, and P. Svenningsson Depletion of the lipid raft constituents, sphingomyelin and ganglioside, decreases serotonin binding at human 5-HT7(a) receptors in HeLa cells Acta Physiol. (Oxf) 190 2007 47 53
122. S. Ganguly, Y.D. Paila, and A. Chattopadhyay Metabolic depletion of sphingolipids enhances the mobility of the human serotonin1A receptor Biochem. Biophys. Res. Commun. 411 2011 180 184
123. M. Jafurulla, T.J. Pucadyil, and A. Chattopadhyay Effect of sphingomyelinase treatment on ligand binding activity of human serotonin1A receptors Biochim. Biophys. Acta 1778 2008 2022 2025
124. P. Singh, and A. Chattopadhyay Removal of sphingomyelin headgroup inhibits the ligand binding function of hippocampal serotonin1A receptors Biochem. Biophys. Res. Commun. 419 2012 321 325
125. R.L. Thomas, R. Mistry, C.J. Langmead, M.D. Wood, and R.A. Challiss G protein coupling and signaling pathway activation by m1 muscarinic acetylcholine receptor orthosteric and allosteric agonists J. Pharmacol. Exp. Ther. 327 2008 365 374
126. V. Itier, and D. Bertrand Neuronal nicotinic receptors: from protein structure to function FEBS Lett. 504 2001 118 125
127. C.J. daCosta, L. Dey, J.P. Therien, and J.E. Baenziger A distinct mechanism for activating uncoupled nicotinic acetylcholine receptors Nat. Chem. Biol. 9 2013 701 707
128. C.J. daCosta, and J.E. Baenziger A lipid-dependent uncoupled conformation of the acetylcholine receptor J. Biol. Chem. 284 2009 17819 17825
129. D. Zhu, W.C. Xiong, and L. Mei Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering J. Neurosci. 26 2006 4841 4851
130. C. Weston, B. Yee, E. Hod, and J. Prives Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42 J. Cell Biol. 150 2000 205 212
131. Z.G. Luo, H.S. Je, Q. Wang, F. Yang, G.C. Dobbins, Z.H. Yang, W.C. Xiong, B. Lu, and L. Mei Implication of geranylgeranyltransferase I in synapse formation Neuron 40 2003 703 717
132. Z.G. Luo, Q. Wang, J.Z. Zhou, J. Wang, Z. Luo, M. Liu, X. He, A. Wynshaw-Boris, W.C. Xiong, B. Lu, and L. Mei Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1 Neuron 35 2002 489 505
133. J. Oshikawa, Y. Toya, T. Fujita, M. Egawa, J. Kawabe, S. Umemura, and Y. Ishikawa Nicotinic acetylcholine receptor alpha 7 regulates cAMP signal within lipid rafts Am. J. Physiol. Cell Physiol. 285 2003 C567 C574
134. V. Bermudez, S.S. Antollini, G.A. Fernandez Nievas, M.I. Aveldano, and F.J. Barrantes Partition profile of the nicotinic acetylcholine receptor in lipid domains upon reconstitution J. Lipid Res. 51 2010 2629 2641
135. K. Niimi, C. Nishioka, T. Miyamoto, E. Takahashi, I. Miyoshi, C. Itakura, and T. Yamashita Improvement of spontaneous alternation behavior deficit by activation of alpha4beta2 nicotinic acetylcholine receptor signaling in the ganglioside GM3-deficient mice Biomed. Res. 34 2013 189 195
136. C.J. daCosta, A.A. Ogrel, E.A. McCardy, M.P. Blanton, and J.E. Baenziger Lipid-protein interactions at the nicotinic acetylcholine receptor. A functional coupling between nicotinic receptors and phosphatidic acid-containing lipid bilayers J. Biol. Chem. 277 2002 201 208
137. C.E. Gallegos, M.F. Pediconi, and F.J. Barrantes Ceramides modulate cell-surface acetylcholine receptor levels Biochim. Biophys. Acta 1778 2008 917 930
138. T. Nishizaki, T. Matsuoka, T. Nomura, and K. Sumikawa Modulation of ACh receptor currents by arachidonic acid Brain Res. Mol. Brain Res. 57 1998 173 179
139. T. Andoh, H. Itoh, T. Higashi, Y. Saito, D. Ishiwa, Y. Kamiya, and Y. Yamada PKC-independent inhibition of neuronal nicotinic acetylcholine receptors by diacylglycerol Brain Res. 1013 2004 125 133
140. A.V. Solin, and Y.D. Lyashev Effect of opioid peptides on the content of LPO products and antioxidant enzyme activity in the liver of rats after restraint stress Bull. Exp. Biol. Med. 153 2012 827 829
141. R. Al-Hasani, and M.R. Bruchas Molecular mechanisms of opioid receptor-dependent signaling and behavior Anesthesiology 115 2011 1363 1381
142. Y. Feng, X. He, Y. Yang, D. Chao, L.H. Lazarus, and Y. Xia Current research on opioid receptor function Curr. Drug Targets 13 2012 230 246
143. C. Duraffourd, F. De Vadder, D. Goncalves, F. Delaere, A. Penhoat, B. Brusset, F. Rajas, D. Chassard, A. Duchampt, A. Stefanutti, A. Gautier-Stein, and G. Mithieux Mu-opioid receptors and dietary protein stimulate a gut-brain neural circuitry limiting food intake Cell 150 2012 377 388
144. B.N. Dhawan, F. Cesselin, R. Raghubir, T. Reisine, P.B. Bradley, P.S. Portoghese, and M. Hamon International Union of Pharmacology. XII. Classification of opioid receptors Pharmacol. Rev. 48 1996 567 592
145. E.W. Ong, and C.M. Cahill Molecular perspectives for mu/delta opioid receptor heteromers as distinct, functional receptors Cells 3 2014 152 179
146. H. Zhao, H.H. Loh, and P.Y. Law Adenylyl cyclase superactivation induced by long-term treatment with opioid agonist is dependent on receptor localized within lipid rafts and is independent of receptor internalization Mol. Pharmacol. 69 2006 1421 1432
147. W. Xu, S.I. Yoon, P. Huang, Y. Wang, C. Chen, P.L. Chong, and L.Y. Liu-Chen Localization of the kappa opioid receptor in lipid rafts J. Pharmacol. Exp. Ther. 317 2006 1295 1306
148. H. Zheng, E.A. Pearsall, D.P. Hurst, Y. Zhang, J. Chu, Y. Zhou, P.H. Reggio, H.H. Loh, and P.Y. Law Palmitoylation and membrane cholesterol stabilize mu-opioid receptor homodimerization and G protein coupling BMC Cell Biol. 13 2012 6
149. A.D. Goddard, and A. Watts Regulation of G protein-coupled receptors by palmitoylation and cholesterol BMC Biol. 10 2012 27
150. S.M. Crain, and K.F. Shen GM1 ganglioside-induced modulation of opioid receptor-mediated functions Ann. N. Y. Acad. Sci. 845 1998 106 125
151. G. Wu, Z.H. Lu, T.J. Wei, R.D. Howells, K. Christoffers, and R.W. Ledeen The role of GM1 ganglioside in regulating excitatory opioid effects Ann. N. Y. Acad. Sci. 845 1998 126 138
152. S. Apaydin, and H.A. Oktem Effect of arachidonic acid on specific binding of [3H]naloxone to opioid receptors Acta Neurobiol. Exp. (Wars) 60 2000 361 363
153. H.A. Oktem, and S. Apaydin Arachidonic acid modulation of [3H]naloxone specific binding to rat brain opioid receptors Neurobiol. (Bp) 6 1998 323 332
154. L.C. Sullivan, K.A. Berg, and W.P. Clarke Dual regulation of delta-opioid receptor function by arachidonic acid metabolites in rat peripheral sensory neurons J. Pharmacol. Exp. Ther. 353 2015 44 51
155. L. Yang, A. Seifert, D. Wu, X. Wang, V. Rankovic, H. Schroder, L.O. Brandenburg, V. Hollt, and T. Koch Role of phospholipase D2/phosphatidic acid signal transduction in micro- and delta-opioid receptor endocytosis Mol. Pharmacol. 78 2010 105 113
156. C. van Kooten, and J. Banchereau CD40-CD40 ligand J. Leukoc. Biol. 67 2000 2 17
157. R. Elgueta, M.J. Benson, V.C. de Vries, A. Wasiuk, Y. Guo, and R.J. Noelle Molecular mechanism and function of CD40/CD40L engagement in the immune system Immunol. Rev. 229 2009 152 172
158. S.S. Pullen, H.G. Miller, D.S. Everdeen, T.T. Dang, J.J. Crute, and M.R. Kehry CD40-tumor necrosis factor receptor-associated factor (TRAF) interactions: regulation of CD40 signaling through multiple TRAF binding sites and TRAF hetero-oligomerization Biochemistry 37 1998 11836 11845
159. C. van Kooten, and J. Banchereau Functional role of CD40 and its ligand Int. Arch. Allergy Immunol. 113 1997 393 399
160. J. Suttles, D.M. Milhorn, R.W. Miller, J.C. Poe, L.M. Wahl, and R.D. Stout CD40 signaling of monocyte inflammatory cytokine synthesis through an ERK1/2-dependent pathway. A target of interleukin (il)-4 and il-10 anti-inflammatory action J. Biol. Chem. 274 1999 5835 5842
161. P.O. Vidalain, O. Azocar, C. Servet-Delprat, C. Rabourdin-Combe, D. Gerlier, and S. Manie CD40 signaling in human dendritic cells is initiated within membrane rafts EMBO J. 19 2000 3304 3313
162. C. Reyes-Moreno, E. Sharif-Askari, J. Girouard, C. Leveille, M. Jundi, A. Akoum, R. Lapointe, A. Darveau, and W. Mourad Requirement of oxidation-dependent CD40 homodimers for CD154/CD40 bidirectional signaling J. Biol. Chem. 282 2007 19473 19480
163. A. Nadiri, M.J. Polyak, M. Jundi, H. Alturaihi, C. Reyes-Moreno, G.S. Hassan, and W. Mourad CD40 translocation to lipid rafts: signaling requirements and downstream biological events Eur. J. Immunol. 41 2011 2358 2367
164. H. Grassme, V. Jendrossek, J. Bock, A. Riehle, and E. Gulbins Ceramide-rich membrane rafts mediate CD40 clustering J. Immunol. 168 2002 298 307
165. R.K. Mathur, A. Awasthi, P. Wadhone, B. Ramanamurthy, and B. Saha Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses Nat. Med. 10 2004 540 544
166. E.Y. Kim, J.L. Sturgill, N.C. Hait, D. Avni, E.C. Valencia, M. Maceyka, S. Lima, J. Allegood, W.C. Huang, S. Zhang, S. Milstien, D. Conrad, and S. Spiegel Role of sphingosine kinase 1 and sphingosine-1-phosphate in CD40 signaling and IgE class switching FASEB J. 28 2014 4347 4358
167. B. Alarcon, D. Gil, P. Delgado, and W.W. Schamel Initiation of TCR signaling: regulation within CD3 dimers Immunol. Rev. 191 2003 38 46
168. R.J. Brownlie, and R. Zamoyska T cell receptor signalling networks: branched, diversified and bounded Nat. Rev. Immunol. 13 2013 257 269
169. P.W. Janes, S.C. Ley, A.I. Magee, and P.S. Kabouridis The role of lipid rafts in T cell antigen receptor (TCR) signalling Semin. Immunol. 12 2000 23 34
170. M. Nix, and W. Stoffel Perturbation of membrane microdomains reduces mitogenic signaling and increases susceptibility to apoptosis after T cell receptor stimulation Cell Death Differ. 7 2000 413 424
171. D. Schieffer, S. Naware, W. Bakun, and A.K. Bamezai Lipid raft-based membrane order is important for antigen-specific clonal expansion of CD4 + T lymphocytes BMC Immunol. 15 2014 58
172. K.Y. Chyu, W.M. Lio, P.C. Dimayuga, J. Zhou, X. Zhao, J. Yano, P. Trinidad, T. Honjo, B. Cercek, and P.K. Shah Cholesterol lowering modulates T cell function in vivo and in vitro PLoS One 9 2014 e92095
173. D.A. Cantrell T-cell antigen receptor signal transduction Immunology 105 2002 369 374
174. M. Almena, E. Andrada, R. Liebana, and I. Merida Diacylglycerol metabolism attenuates T-cell receptor signaling and alters thymocyte differentiation Cell Death Dis. 4 2013 e912
175. C. Menne, J.P. Lauritsen, J. Dietrich, J. Kastrup, A.M. Wegener, N. Odum, and C. Geisler Ceramide-induced TCR up-regulation J. Immunol. 165 2000 3065 3072
176. C. Menne, J.P. Lauritsen, J. Dietrich, J. Kastrup, A.K. Wegener, P.S. Andersen, N. Odum, and C. Geisler T-cell receptor downregulation by ceramide-induced caspase activation and cleavage of the zeta chain Scand. J. Immunol. 53 2001 176 183
177. A. Rub, M. Arish, S.A. Husain, N. Ahmed, and Y. Akhter Host-lipidome as a potential target of protozoan parasites Microbes Infect. 15 2013 649 660
178. Y.P. van der Meer-Janssen, J. van Galen, J.J. Batenburg, and J.B. Helms Lipids in host-pathogen interactions: pathogens exploit the complexity of the host cell lipidome Prog. Lipid Res. 49 2010 1 26
179. A. Hartlova, L. Cerveny, M. Hubalek, Z. Krocova, and J. Stulik Membrane rafts: a potential gateway for bacterial entry into host cells Microbiol. Immunol. 54 2010 237 245
180. F.S. Vieira, G. Correa, M. Einicker-Lamas, and R. Coutinho-Silva Host-cell lipid rafts: a safe door for micro-organisms? Biol. Cell 102 2010 391 407
181. A.M. Goldston, R.R. Powell, and L.A. Temesvari Sink or swim: lipid rafts in parasite pathogenesis Trends Parasitol. 28 2012 417 426
182. D.W. Zaas, M. Duncan, J. Rae Wright, and S.N. Abraham The role of lipid rafts in the pathogenesis of bacterial infections Biochim. Biophys. Acta 1746 2005 305 313
183. N.S. Heaton, and G. Randall Multifaceted roles for lipids in viral infection Trends Microbiol. 19 2011 368 375
184. O. Silvie, S. Charrin, M. Billard, J.F. Franetich, K.L. Clark, G.J. van Gemert, R.W. Sauerwein, F. Dautry, C. Boucheix, D. Mazier, and E. Rubinstein Cholesterol contributes to the organization of tetraspanin-enriched microdomains and to CD81-dependent infection by malaria sporozoites J. Cell Sci. 119 2006 1992 2002
185. S.B. Kapadia, H. Barth, T. Baumert, J.A. McKeating, and F.V. Chisari Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I J. Virol. 81 2007 374 383
186. C. Voisset, M. Lavie, F. Helle, A. Op De Beeck, A. Bilheu, J. Bertrand-Michel, F. Terce, L. Cocquerel, C. Wychowski, N. Vu-Dac, and J. Dubuisson Ceramide enrichment of the plasma membrane induces CD81 internalization and inhibits hepatitis C virus entry Cell Microbiol. 10 2008 606 617
187. P. Goluszko, and B. Nowicki Membrane cholesterol: a crucial molecule affecting interactions of microbial pathogens with mammalian cells Infect. Immun. 73 2005 7791 7796
188. J.M. Mackenzie, A.A. Khromykh, and R.G. Parton Cholesterol manipulation by West Nile virus perturbs the cellular immune response Cell Host Microbe 2 2007 229 239
189. M.M. Monick, K. Cameron, L.S. Powers, N.S. Butler, D. McCoy, R.K. Mallampalli, and G.W. Hunninghake Sphingosine kinase mediates activation of extracellular signal-related kinase and akt by respiratory syncytial virus Am. J. Respir. Cell. Mol. Biol. 30 2004 844 852
190. J. Gatfield, and J. Pieters Essential role for cholesterol in entry of mycobacteria into macrophages Science 288 2000 1647 1650
191. N. Khan, K. Alam, S.C. Mande, V.L. Valluri, S.E. Hasnain, and S. Mukhopadhyay Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages Cell Microbiol. 10 2008 1711 1722
192. M. Klink, M. Brzezinska, I. Szulc, A. Brzostek, M. Kielbik, Z. Sulowska, and J. Dziadek Cholesterol oxidase is indispensable in the pathogenesis of Mycobacterium tuberculosis PLoS One 8 2013 e73333
193. A. Oizumi, H. Nakayama, N. Okino, C. Iwahara, K. Kina, R. Matsumoto, H. Ogawa, K. Takamori, M. Ito, Y. Suga, and K. Iwabuchi Pseudomonas-derived ceramidase induces production of inflammatory mediators from human keratinocytes via sphingosine-1-phosphate PLoS One 9 2014 e89402
194. T.J. Pucadyil, P. Tewary, R. Madhubala, and A. Chattopadhyay Cholesterol is required for Leishmania donovani infection: implications in leishmaniasis Mol. Biochem. Parasitol. 133 2004 145 152