A mirror code for protein-cholesterol interactions in the two leaflets of biological membranes

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Fantini, Jacques ^a   Di Scala, Coralie ^a   Evans, Luke S ^b   Williamson, Philip T F ^b   Barrantes, Francisco J ^c  

^a Aix Marseille University   (France)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c PONTIFICIA UNIVERSIDAD CATÓLICA ARGENTINA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CHOLESTEROL; CHOLINERGIC RECEPTOR; PROTEIN BINDING;

CELL MEMBRANE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN MOTIF;

AMINO ACID MOTIFS; ATP-BINDING CASSETTE TRANSPORTERS; CELL MEMBRANE; CHOLESTEROL; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; RECEPTORS, CHOLINERGIC;

EID: 84959377636     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21907     Document Type: Article

References (53)

1. Maguire, P. A. & Druse, M. J. The influence of cholesterol on synaptic fluidity, dopamine D1 binding and dopamine-stimulated adenylate cyclase. Brain Res. Bull. 23, 69-74 (1989).
2. el Battari, A., Ah-Kye, E., Muller, J. M., Sari, H. & Marvaldi, J. Modification of HT 29 cell response to the vasoactive intestinal peptide (VIP) by membrane fluidization. Biochimie 67, 1217-1223 (1985).
3. Lazar, D. F. & Medzihradsky, F. Altered microviscosity at brain membrane surface induces distinct and reversible inhibition of opioid receptor binding. J. Neurochem. 59, 1233-1240 (1992).
4. Yesylevskyy, S. O., Demchenko, A. P., Kraszewski, S. & Ramseyer, C. Cholesterol induces uneven curvature of asymmetric lipid bilayers. The Scientific World Journal 2013, 965230 (2013).
5. Lee, A. G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666, 62-87 (2004).
6. Popot, J. L., Demel, R. A., Sobel, A., van Deenen, L. L. & Changeux, J. P. Preferential affinity of acetylcholine receptor protein for certain lipids studied using monolayer cultures. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D. 285, 1005-1008 (1977).
7. Barrantes, F. J. Structural basis for lipid modulation of nicotinic acetylcholine receptor function. Brain Res. Brain Res. Rev. 47, 71-95 (2004).
8. Baier, C. J., Fantini, J. & Barrantes, F. J. Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor. Sci. Rep. 1, 69 (2011).
9. Fantini, J. & Barrantes, F. J. How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front. Physiol. 4, 31 (2013).
10. Posada, I. M. et al. A cholesterol recognition motif in human phospholipid scramblase 1. Biophys. J. 107, 1383-1392 (2014).
11. Hanson, M. A. et al. A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16, 897-905 (2008).
12. Fantini, J. & Barrantes, F. J. Sphingolipid/cholesterol regulation of neurotransmitter receptor conformation and function. Biochim. Biophys. Acta 1788, 2345-2361 (2009).
13. Jamin, N. et al. Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor. Mol. Endocrinol. 19, 588-594 (2005).
14. Epand, R. F. et al. Juxtamembrane protein segments that contribute to recruitment of cholesterol into domains. Biochemistry 45, 6105-6114 (2006).
15. Epand, R. M. Proteins and cholesterol-rich domains. Biochim. Biophys. Acta 1778, 1576-1582 (2008).
16. Epand, R. M., Thomas, A., Brasseur, R. & Epand, R. F. Cholesterol interaction with proteins that partition into membrane domains: an overview. Subcell. Biochem. 51, 253-278 (2010).
17. Strandberg, E. & Killian, J. A. Snorkeling of lysine side chains in transmembrane helices: how easy can it get? FEBS Lett. 544, 69-73 (2003).
18. Hamouda, A. K., Chiara, D. C., Sauls, D., Cohen, J. B. & Blanton, M. P. Cholesterol interacts with transmembrane alpha-helices M1, M3, and M4 of the Torpedo nicotinic acetylcholine receptor: photolabeling studies using [3H]Azicholesterol. Biochemistry 45, 976-986 (2006).
19. Di Scala, C., Chahinian, H., Yahi, N., Garmy, N. & Fantini, J. Interaction of Alzheimer's beta-Amyloid Peptides with Cholesterol: Mechanistic Insights into Amyloid Pore Formation. Biochemistry 53, 4489-4502 (2014).
20. Thakur, G., Pao, C., Micic, M., Johnson, S. & Leblanc, R. M. Surface chemistry of lipid raft and amyloid Abeta (1-40) Langmuir monolayer. Colloids Surf. B Biointerfaces 87, 369-377 (2011).
21. Yahi, N. & Fantini, J. Deciphering the glycolipid code of Alzheimer's and Parkinson's amyloid proteins allowed the creation of a universal ganglioside-binding Peptide. PloS One 9, e104751 (2014).
22. Seelig, A. Local anesthetics and pressure: a comparison of dibucaine binding to lipid monolayers and bilayers. Biochim. Biophys. Acta 899, 196-204 (1987).
23. Fantini, J., Carlus, D. & Yahi, N. The fusogenic tilted peptide (67-78) of alpha-synuclein is a cholesterol binding domain. Biochim. Biophys. Acta 1808, 2343-2351 (2011).
24. Williamson, P. T. F., Zandomeneghi, G., Barrantes, F. J., Watts, A. & Meier, B. H. Structural and dynamic studies of the gamma-M4 trans-membrane domain of the nicotinic acetylcholine receptor. Mol. Membr. Biol. 22, 485-496 (2005).
25. Burnett, L. J. & Muller, B. H. Deuteron quadrupole coupling constants in 3 solid deuterated paraffin hydrocarbons-C2d6, C4d10, C6d14. J. Chem. Phys. 55, 5829-5831 (1971).
26. Mehring, M. Principles of high-resolution NMR in solids, (Springer-Verlag, 1983).
27. de Almeida, R. F. M. et al. Cholesterol modulates the organization of the gamma M4 transmembrane domain of the muscle nicotinic acetylcholine receptor. Biophys. J. 86, 2261-2272 (2004).
28. Jaremko, L., Jaremko, M., Giller, K., Becker, S. & Zweckstetter, M. Structure of the mitochondrial translocator protein in complex with a diagnostic ligand. Science 343, 1363-1366 (2014).
29. Lacapere, J. J. et al. Structural and functional study of reconstituted peripheral benzodiazepine receptor. Biochem. Biophys. Res. Commun. 284, 536-541 (2001).
30. Papadopoulos, V. et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 27, 402-409 (2006).
31. Harris, J. S., Epps, D. E., Davio, S. R. & Kezdy, F. J. Evidence for transbilayer, tail-to-tail cholesterol dimers in dipalmitoylglycerophosphocholine liposomes. Biochemistry 34, 3851-3857 (1995).
32. Rukmini, R., Rawat, S. S., Biswas, S. C. & Chattopadhyay, A. Cholesterol organization in membranes at low concentrations: effects of curvature stress and membrane thickness. Biophys. J. 81, 2122-2134, (2001).
33. Nishio, M., Umezawa, Y., Fantini, J., Weiss, M. S. & Chakrabarti, P. CH-π hydrogen bonds in biological macromolecules. Phys. Chem. Chem. Phys. 16, 12648-12683 (2014).
34. Opekarova, M. & Tanner, W. Specific lipid requirements of membrane proteins-a putative bottleneck in heterologous expression. Biochim. Biophys. Acta 1610, 11-22 (2003).
35. Lagane, B. et al. Role of sterols in modulating the human mu-opioid receptor function in Saccharomyces cerevisiae. J. Biol. Chem. 275, 33197-33200 (2000).
36. Czub, J. & Baginski, M. Comparative molecular dynamics study of lipid membranes containing cholesterol and ergosterol. Biophys. J. 90, 2368-2382 (2006).
37. Baginski, M., Tempczyk, A. & Borowski, E. Comparative conformational analysis of cholesterol and ergosterol by molecular mechanics. Eur. Biophys. J. 17, 159-166 (1989).
38. Gál, Z. et al. Mutations of the central tyrosines of putative cholesterol recognition amino acid consensus (CRAC) sequences modify folding, activity, and sterol-sensing of the human ABCG2 multidrug transporter. Biochim. Biophys. Acta 1848, 477-487 (2015).
39. Telbisz, A., Hegedüs, C., Váradi, A., Sarkadi, B. & Özvegy-Laczka, C. Regulation of the function of the human ABCG2 multidrug transporter by cholesterol and bile acids: effects of mutations in potential substrate and steroid binding sites. Drug Metab. Dispos. 42, 575-585 (2014).
40. Clay, A. T., Lu, P. & Sharom, F. J. Interaction of the P-Glycoprotein Multidrug Transporter with Sterols. Biochemistry 54, 6586-6597 (2015).
41. Aller, S. G. et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722 (2009).
42. Fantini, J. & Yahi, N. Brain lipids in synaptic function and neurological disease. Clues to innovative therapeutic strategies for brain disorders, (Elsevier Academic Press, 2015).
43. Fantini, J. et al. Bexarotene blocks calcium-permeable ion channels formed by neurotoxic Alzheimer's b-amyloid peptides. ACS Chem. Neurosci. 5, 216-224 (2014).
44. Di Scala, C. et al. Broad neutralization of calcium-permeable amyloid pore channels with a chimeric Alzheimer/Parkinson peptide targeting brain gangliosides. Biochim. Biophys. Acta 1862, 213-222 (2016).
45. Partridge, A. W., Therien, A. G. & Deber, C. M. Missense mutations in transmembrane domains of proteins: phenotypic propensity of polar residues for human disease. Proteins 54, 648-656 (2004).
46. Brooks, B. R. et al. CHARMM: the biomolecular simulation program. J. Comput. Chem. 30, 1545-1614 (2009).
47. Di Scala, C. et al. Mechanism of cholesterol-assisted oligomeric channel formation by a short Alzheimer beta-amyloid peptide. J. Neurochem. 128, 186-195 (2014).
48. Di Scala, C. et al. Biochemical identification of a linear cholesterol-binding domain within Alzheimer's beta amyloid peptide. ACS Chem. Neurosci. 4, 509-517 (2013).
49. Thomsen, R. & Christensen, M. H. MolDock: a new technique for high-accuracy molecular docking. J. Med. Chem. 49, 3315-3321 (2006).
50. Guex, N. & Peitsch, M. C. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (1997).
51. Hibino, M. & Tsuchiya, H. Self-assembled monolayers of cholesterol and cholesteryl esters on graphite. Langmuir 30, 6852-6857 (2014).
52. Sabatini, K., Mattila, J. P. & Kinnunen, P. K. Interfacial behavior of cholesterol, ergosterol, and lanosterol in mixtures with DPPC and DMPC. Biophys. J. 95, 2340-2355 (2008).
53. van Beek, J. D. matNMR: a flexible toolbox for processing, analyzing and visualizing magnetic resonance data in Matlab. J. Magnet. Res. 187, 19-26 (2007).