G protein-membrane interactions II: Effect of G protein-linked lipids on membrane structure and G protein-membrane interactions

Biochimica et Biophysica Acta - Biomembranes

Volumn 1859, Issue 9, 2017, Pages 1526-1535

  Casas, Jesús ^a   Ibarguren, Maitane ^a,b   Álvarez, Rafael ^a   Terés, Silvia ^a,b   Lladó, Victoria ^a   Piotto, Stefano P ^c   Concilio, Simona ^c   Busquets, Xavier ^a   López, David J ^a,b   Escribá, Pablo V ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b Lipopharma Therapeutics SL   (Spain)

^c UNIVERSITY OF SALERNO   (Italy)

Author keywords

Cell signaling; G proteins; Isoprenoids; Membranes; Myristoylation; Palmitoylation

Indexed keywords

DIMER; GERANYLGERANIOL; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA BETA GAMMA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA GAMMA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; LIPID; MYRISTIC ACID; PALMITIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG; DITERPENE; LIPID BILAYER; MEMBRANE LIPID; MEMBRANE PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; LAMELLAR BODY; MEMBRANE MODEL; MEMBRANE STRUCTURE; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PHYSICAL CHEMISTRY; PLASMA PROTEIN BINDING; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; PROTEIN MEMBRANE INTERACTION; PROTEIN PROCESSING; CHEMISTRY; LIPID BILAYER; PROTEIN MULTIMERIZATION;

DITERPENES; GTP-BINDING PROTEINS; LIPID BILAYERS; MEMBRANE LIPIDS; MEMBRANE PROTEINS; PROTEIN MULTIMERIZATION;

EID: 85017571337     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2017.04.005     Document Type: Article

References (57)

1. Kim, G.D., Adie, E.J., Milligan, G., Quantitative stoichiometry of the proteins of the stimulatory arm of the adenylyl cyclase cascade in neuroblastoma × glioma hybrid, NG108-15 cells. Eur. J. Biochem. 219 (1994), 135–143.
2. Lagnado, L., Signal amplification: let's turn down the lights. Curr. Biol. 12 (2002), R215–R217.
3. Rudajev, V., Novotny, J., Hejnova, L., Milligan, G., Svoboda, P., Dominant portion of thyrotropin-releasing hormone receptor is excluded from lipid domains. Detergent-resistant and detergent-sensitive pools of TRH receptor and Gqalpha/G11alpha protein. J. Biochem. 138 (2005), 111–125.
4. Vögler, O., Casas, J., Capo, D., Nagy, T., Borchert, G., Martorell, G., Escribá, P.V., The Gbetagamma dimer drives the interaction of heterotrimeric Gi proteins with nonlamellar membrane structures. J. Biol. Chem. 279 (2004), 36540–36545.
5. Lefkowitz, R.J., Seven transmembrane receptors: a brief personal retrospective. Biochim. Biophys. Acta 1768 (2007), 748–755.
6. Nair, K.S., Balasubramanian, N., Slepak, V.Z., Signal-dependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr. Biol. 12 (2002), 421–425.
7. Hur, E.M., Park, Y.S., Lee, B.D., Jang, I.H., Kim, H.S., Kim, T.D., Suh, P.G., Ryu, S.H., Kim, K.T., Sensitization of epidermal growth factor-induced signaling by bradykinin is mediated by c-Src. Implications for a role of lipid microdomains. J. Biol. Chem. 279 (2004), 5852–5860.
8. Álvarez, R., López, D.J., Casas, J., Lladó, V., Higuera, M., Nagy, T., Barceló, M., Busquets, X., Escribá, P.V., G protein-membrane interactions I: Gαi1 myristoyl and palmitoyl modifications in protein-lipid interactions and its implications in membrane microdomain localization. Biochim. Biophys. Acta 1851:11 (2015), 1511–1520.
9. Prades, J., Encinar, J.A., Funari, S.S., González-Ros, J.M., Escribá, P.V., Barceló, F., Interaction of transmembrane-spanning segments of the alpha2-adrenergic receptor with model membranes. Mol. Membr. Biol. 26 (2009), 265–278.
10. Drmota, T., Novotny, J., Gould, G.W., Svoboda, P., Milligan, G., Visualization of distinct patterns of subcellular redistribution of the thyrotropin-releasing hormone receptor-1 and gqalpha/G11alpha induced by agonist stimulation. Biochem. J. 340:Pt 2 (1999), 529–538.
11. Escribá, P.V., Wedegaertner, P.B., Goñi, F.M., Vögler, O., Lipid-protein interactions in GPCR-associated signaling. Biochim. Biophys. Acta 1768 (2007), 836–852.
12. Moffett, S., Brown, D.A., Linder, M.E., Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275 (2000), 2191–2198.
13. Escribá, P.V., Sastre, M., García-Sevilla, J.A., Disruption of cellular signaling pathways by daunomycin through destabilization of nonlamellar membrane structures. Proc. Natl. Acad. Sci. 92 (1995), 7595–7599.
14. Funari, S.S., Barceló, F., Escribá, P.V., Effects of oleic acid and its congeners, elaidic and stearic acids, on the structural properties of phosphatidylethanolamine membranes. J. Lipid Res. 44 (2003), 567–575.
15. Krieger, E., Darden, T., Nabuurs, S., Finkelstein, A., Vriend, G., Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57 (2004), 678–683.
16. Berendsen, H.J.C., Postma, J.P.M., van Gunsteren, W.F., Di Nola, A., Haak, J.R., Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984), 3684–3698.
17. Klamt, A., Conductor-like screening model for real solvents. A new approach to the quantitative calculation of solvatation phenomena. J. Phys. Chem. 99 (1995), 2224–2235.
18. Stewart, J.J., MOPAC: a semiempirical molecular orbital program. J. Comput. Aided Mol. Des. 4 (1990), 1–105.
19. Essmann, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H., Pedersen, L.G., A sooth particle mesh Ewald method. J. Chem. Phys. 103 (1995), 193–202.
20. Kucerka, N., Tristram-Nagle, S., Nagle, J.F., Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J. Membr. Biol. 208 (2005), 193–202.
21. Crul, T., Toth, N., Piotto, S., Literati-Nagy, P., Tory, K., Haldimann, P., Kalmar, B., Greensmith, L., Torok, Z., Balogh, G., Gombos, I., Campana, F., Concilio, S., Gallyas, F., Nagy, G., Berente, Z., Gungor, B., Peter, M., Glatz, A., Hunya, A., Literati-Nagy, Z., Vigh, L. Jr., Hoogstra-Berends, F., Heeres, A., Kuipers, I., Loen, L., Seerden, J.P., Zhang, D., Meijering, R.A., Henning, R.H., Brundel, B.J., Kampinga, H.H., Koranyi, L., Szilvassy, Z., Mandl, J., Sumegi, B., Febbraio, M.A., Horvath, I., Hooper, P.L., Vigh, L., Hydroximic acid derivatives: pleiotropic HSP co-inducers restoring homeostasis and robustness. Curr. Pharm. Des. 19 (2013), 309–346.
22. Piotto, S., Di Biasi, L., Concilio, S., Castiglione, A., Cattaneo, G., GRIMD: Distributed Computing for Chemists and Biologists. 2014.
23. Cantor, R.S., Lateral pressures in cell membranes: a mechanism for modulation of protein function. J. Phys. Chem. 101 (1997), 1723–1725.
24. Piotto, S., Concilio, S., Bianchino, E., Iannelli, P., López, D.J., Terés, S., Ibarguren, M., Barceló-Coblijn, G., Martin, M.L., Guardiola-Serrano, F., Alonso-Sande, M., Funari, S.S., Busquets, X., Escribá, P.V., Differential effect of 2-hydroxyoleic acid enantiomers on protein (sphingomyelin synthase) and lipid (membrane) targets. Biochim. Biophys. Acta 1838 (2014), 1628–1637.
25. Piotto, S., Trapani, A., Bianchino, E., Ibarguren, M., López, D.J., Busquets, X., Concilio, S., The effect of hydroxylated fatty acid-containing phospholipids in the remodeling of lipid membranes. Biochim. Biophys. Acta 1838 (2014), 1509–1517.
26. Laio, A., Parrinello, M., Escaping free-energy minima. Proc. Natl. Acad. Sci. 99 (2002), 12562–12566.
27. Bowers, K.J., Chow, E., Xu, H., Dror, R.O., Eastwood, M.P., Gregersen, B.A., Klepeis, J.L., Kolossvary, I., Moraes, M.A., Sacerdoti, F.D., Scalable algorithms for molecular dynamics simulations on commodity clusters. SC 2006 Conference, Proceedings of the ACM/IEEE, IEEE, 2006, 43.
28. Escribá, P.V., Sastre, M., García-Sevilla, J.A., Increased density of guanine nucleotide-binding proteins in the postmortem brains of heroin addicts. Arch. Gen. Psychiatry 51 (1994), 494–501.
29. Angelova, I.M., Dimitrov, D.S., Liposome electroformation. Faraday Discuss. Chem. Soc. 81 (1986), 303–311.
30. Ibarguren, M., López, D.J., Montes, L.R., Sot, J., Vasil, A.I., Vasil, M.L., Goñi, F.M., Alonso, A., Imaging the early stages of phospholipase C/sphingomyelinase activity on vesicles containing coexisting ordered-disordered and gel-fluid domains. J. Lipid Res. 52 (2011), 635–645.
31. Kim, Y., Ho, S.O., Gassman, N.R., Korlann, Y., Landorf, E.V., Collart, F.R., Weiss, S., Efficient site-specific labeling of proteins via cysteines. Bioconjug. Chem. 19 (2008), 786–791.
32. Martínez, J., Vögler, O., Casas, J., Barceló, F., Alemany, R., Prades, J., Nagy, T., Baamonde, C., Kasprzyk, P.G., Terés, S., Saus, C., Escribá, P.V., Membrane structure modulation, protein kinase C alpha activation, and anticancer activity of minerval. Mol. Pharmacol. 67 (2005), 531–540.
33. Cardenas, A.E., Shrestha, R., Webb, L.J., Elber, R., Membrane permeation of a peptide: it is better to be positive. J. Phys. Chem. B 119 (2015), 6412–6420.
34. 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.
35. McCallum, J.F., Wise, A., Grassie, M.A., Magee, A.I., Guzzi, F., Parenti, M., Milligan, G., The role of palmitoylation of the guanine nucleotide binding protein G11 alpha in defining interaction with the plasma membrane. Biochem. J. 310:Pt 3 (1995), 1021–1027.
36. Clarke, S., Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu. Rev. Biochem. 61 (1992), 355–386.
37. Agnati, L.F., Guidolin, D., Leo, G., Fuxe, K., A boolean network modelling of receptor mosaics relevance of topology and cooperativity. J. Neural Transm. 114 (2007), 77–92.
38. Huang, C., Hepler, J.R., Chen, L.T., Gilman, A.G., Anderson, R.G., Mumby, S.M., Organization of G proteins and adenylyl cyclase at the plasma membrane. Mol. Biol. Cell 8 (1997), 2365–2378.
39. Neubig, R.R., Membrane organization in G-protein mechanisms. FASEB J. 8 (1994), 939–946.
40. Escribá, P.V., Ozaita, A., Ribas, C., Miralles, A., Fodor, E., Farkas, T., García-Sevilla, J.A., Role of lipid polymorphism in G protein-membrane interactions: nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 11375–11380.
41. Novotny, J., Durchankova, D., Ward, R.J., Carrillo, J.J., Svoboda, P., Milligan, G., Functional interactions between the alpha1b-adrenoceptor and Galpha11 are compromised by de-palmitoylation of the G protein but not of the receptor. Cell. Signal. 18 (2006), 1244–1251.
42. Epand, R.M., Epand, R.F., Ahmed, N., Chen, R., Promotion of hexagonal phase formation and lipid mixing by fatty acids with varying degrees of unsaturation. Chem. Phys. Lipids 57 (1991), 75–80.
43. Oh, P., Schnitzer, J.E., Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol. Biol. Cell 12 (2001), 685–698.
44. González-Horta, A., Andreu, D., Morrow, M.R., Pérez-Gil, J., Effects of palmitoylation on dynamics and phospholipid-bilayer-perturbing properties of the N-terminal segment of pulmonary surfactant protein SP-C as shown by 2H-NMR. Biophys. J. 95 (2008), 2308–2317.
45. Melkonian, K.A., Ostermeyer, A.G., Chen, J.Z., Roth, M.G., Brown, D.A., Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274 (1999), 3910–3917.
46. Funari, S.S., Prades, J., Escribá, P.V., Barceló, F., Farnesol and geranylgeraniol modulate the structural properties of phosphatidylethanolamine model membranes. Mol. Membr. Biol. 22 (2005), 303–311.
47. Barceló, F., Prades, J., Encinar, J.A., Funari, S.S., Vögler, O., González-Ros, J.M., Escribá, P.V., Interaction of the C-terminal region of the Ggamma protein with model membranes. Biophys. J. 93 (2007), 2530–2541.
48. Simonds, W.F., Butrynski, J.E., Gautam, N., Unson, C.G., Spiegel, A.M., G-protein beta gamma dimers. Membrane targeting requires subunit coexpression and intact gamma C-A-A-X domain. J. Biol. Chem. 266 (1991), 5363–5366.
49. Fong, T.M., McNamee, M.G., Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25 (1986), 830–840.
50. Escribá, P.V., Membrane-lipid therapy: a new approach in molecular medicine. Trends Mol. Med. 12 (2006), 34–43.
51. Escribá, P.V., González-Ros, J.M., Goñi, F.M., Kinnunen, P.K., Vigh, L., Sánchez-Magraner, L., Fernández, A.M., Busquets, X., Horvath, I., Barceló-Coblijn, G., Membranes: a meeting point for lipids, proteins and therapies. J. Cell. Mol. Med. 12 (2008), 829–875.
52. Vigh, L., Literati, P.N., Horvath, I., Torok, Z., Balogh, G., Glatz, A., Kovacs, E., Boros, I., Ferdinandy, P., Farkas, B., Jaszlits, L., Jednakovits, A., Koranyi, L., Maresca, B., Bimoclomol: a nontoxic, hydroxylamine derivative with stress protein-inducing activity and cytoprotective effects. Nat. Med. 3 (1997), 1150–1154.
53. López, D.J., Egido-Gabas, M., López-Montero, I., Busto, J.V., Casas, J., Garnier, M., Monroy, F., Larijani, B., Goñi, F.M., Alonso, A., Accumulated bending energy elicits neutral sphingomyelinase activity in human red blood cells. Biophys. J. 102:9 (2012), 2077–2085.
54. Lenaz, G., Lipid fluidity and membrane protein dynamics. Biosci. Rep. 7 (1987), 823–837.
55. Ibarguren, M., López, D.J., Encinar, J.A., González-Ros, J.M., Busquets, X., Escribá, P.V., Partitioning of liquid-ordered/liquid-disordered membrane microdomains induced by the fluidifying effect of 2-hydroxylated fatty acid derivatives. Biochim. Biophys. Acta 1828 (2013), 2553–2563.
56. Escribá, P.V., Busquets, X., Inokuchi, J.I., Balogh, G., Torok, Z., Horvath, I., Harwood, J.L., Vigh, L., Membrane lipid therapy: modulation of the cell membrane composition and structure as a molecular base for drug discovery and new disease treatment. Prog. Lipid Res., 2015.
57. Lladó, V., Terés, S., Higuera, M., Álvarez, R., Noguera-Salva, M.A., Halver, J.E., Escribá, P.V., Busquets, X., Pivotal role of dihydrofolate reductase knockdown in the anticancer activity of 2-hydroxyoleic acid. Proc. Natl. Acad. Sci. 106 (2009), 13754–13758.