Roughness of Transmembrane Helices Reduces Lipid Membrane Dynamics
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
PubMed
30508721
PubMed Central
PMC6277224
DOI
10.1016/j.isci.2018.11.026
PII: S2589-0042(18)30216-5
Knihovny.cz E-zdroje
- Klíčová slova
- Biophysics, Computational Molecular Modelling, Membrane Architecture, Protein Physics,
- Publikační typ
- časopisecké články MeSH
The dynamics of cellular membranes is primarily determined by lipid species forming a bilayer. Proteins are considered mainly as effector molecules of diverse cellular processes. In addition to large assemblies of proteins, which were found to influence properties of fluid membranes, biological membranes are densely populated by small, highly mobile proteins. However, little is known about the effect of such proteins on the dynamics of membranes. Using synthetic peptides, we demonstrate that transmembrane helices interfere with the mobility of membrane components by trapping lipid acyl chains on their rough surfaces. The effect is more pronounced in the presence of cholesterol, which segregates from the rough surface of helical peptides. This may contribute to the formation or stabilization of membrane heterogeneities. Since roughness is a general property of helical transmembrane segments, our results suggest that, independent of their size or cytoskeleton linkage, integral membrane proteins affect local membrane dynamics and organization.
Zobrazit více v PubMed
Anderson R.G., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 2002;296:1821–1825. PubMed
Andrews N.L., Lidke K.A., Pfeiffer J.R., Burns A.R., Wilson B.S., Oliver J.M., Lidke D.S. Actin restricts FcεRI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell Biol. 2008;10:955–963. PubMed PMC
Benda A., Benes M., Marecek V., Lhotsky A., Hermens W.T., Hof M. How to determine diffusion coefficients in planar phospholipid systems by confocal fluorescence correlation spectroscopy. Langmuir. 2003;19:4120–4126.
Bernardino de la Sern A.J., Schutz G.J., Eggeling C., Cebecauer M. There is no simple model of the plasma membrane organization. Front. Cell Dev. Biol. 2016;4:106. PubMed PMC
Bienvenue A., Bloom M., Davis J.H., Devaux P.F. Evidence for protein-associated lipids from deuterium nuclear magnetic-resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. J. Biol. Chem. 1982;257:3032–3038. PubMed
Brocchieri L., Karlin S. Protein length in eukaryotic and prokaryotic proteomes. Nucleic Acids Res. 2005;33:3390–3400. PubMed PMC
Brotherus J.R., Griffith O.H., Brotherus M.O., Jost P.C., Silvius J.R., Hokin L.E. Lipid-protein multiple binding equilibria in membranes. Biochemistry. 1981;20:5261–5267. PubMed
Camley B.A., Esposito C., Baumgart T., Brown F.L. Lipid bilayer domain fluctuations as a probe of membrane viscosity. Biophys. J. 2010;99:L44–L46. PubMed PMC
Cebecauer M., Spitaler M., Serge A., Magee A.I. Signalling complexes and clusters: functional advantages and methodological hurdles. J. Cell Sci. 2010;123:309–320. PubMed
de Planque M.R., Greathouse D.V., Koeppe R.E., 2nd, Schafer H., Marsh D., Killian J.A. Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A 2H NMR and ESR study using designed transmembrane alpha-helical peptides and gramicidin A. Biochemistry. 1998;37:9333–9345. PubMed
de Planque M.R., Killian J.A. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 2003;20:271–284. PubMed
de Planque M.R.R., Kruijtzer J.A.W., Liskamp R.M.J., Marsh D., Greathouse D.V., Koeppe R.E., de Kruijff B., Killian J.A. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides. J. Biol. Chem. 1999;274:20839–20846. PubMed
Dupuy A.D., Engelman D.M. Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. U S A. 2008;105:2848–2852. PubMed PMC
Fastenberg M.E., Shogomori H., Xu X., Brown D.A., London E. Exclusion of a transmembrane-type peptide from ordered-lipid domains (rafts) detected by fluorescence quenching: extension of quenching analysis to account for the effects of domain size and domain boundaries. Biochemistry. 2003;42:12376–12390. PubMed
Frick M., Schmidt K., Nichols B.J. Modulation of lateral diffusion in the plasma membrane by protein density. Curr. Biol. 2007;17:462–467. PubMed
Gallova J., Uhrikova D., Hanulova M., Teixeira J., Balgavy P. Bilayer thickness in unilamellar extruded 1,2-dimyristoleoyl and 1,2-dierucoyl phosphatidylcholine vesicles: SANS contrast variation study of cholesterol effect. Colloids Surf. B Biointerfaces. 2004;38:11–14. PubMed
Harayama T., Riezman H. Understanding the diversity of membrane lipid composition. Nat. Rev. Mol. Cell Biol. 2018;19:281–296. PubMed
Heberle F.A., Feigenson G.W. Phase separation in lipid membranes. Cold Spring Harb. Perspect. Biol. 2011;3:1–13. PubMed PMC
Hite R.K., Li Z., Walz T. Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals. EMBO J. 2010;29:1652–1658. PubMed PMC
Jacobson K., Ishihara A., Inman R. Lateral diffusion of proteins in membranes. Annu. Rev. Physiol. 1987;49:163–175. PubMed
Jost P.C., Griffith O.H., Capaldi R.A., Vanderkooi G. Evidence for boundary lipid in membranes. Proc. Natl. Acad. Sci. U S A. 1973;70:480–484. PubMed PMC
Jost P.C., Nadakavukaren K.K., Griffith O.H. Phosphatidylcholine exchange between the boundary lipid and bilayer domains in cytochrome oxidase containing membranes. Biochemistry. 1977;16:3110–3114. PubMed
Kaiser H.J., Orlowski A., Rog T., Nyholm T.K., Chai W., Feizi T., Lingwood D., Vattulainen I., Simons K. Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching. Proc. Natl. Acad. Sci. U S A. 2011;108:16628–16633. PubMed PMC
Kanai R., Ogawa H., Vilsen B., Cornelius F., Toyoshima C. Crystal structure of a Na+-bound Na+,K+-ATPase preceding the E1P state. Nature. 2013;502:201–206. PubMed
Kozma D., Simon I., Tusnady G.E. PDBTM: protein Data Bank of transmembrane proteins after 8 years. Nucleic Acids Res. 2013;41:D524–D529. PubMed PMC
London E., Feigenson G. Fluorescence quenching in model membranes. An analysis of the local phospholipid environment of diphenylhexatrien and Gramicidin A. Biochim. Biophys. Acta. 1981;649:89–97.
Machan R., Jurkiewicz P., Olzynska A., Olsinova M., Cebecauer M., Marquette A., Bechinger B., Hof M. Peripheral and integral membrane binding of peptides characterized by time-dependent fluorescence shifts: focus on antimicrobial peptide LAH(4) Langmuir. 2014;30:6171–6179. PubMed
Marsh D. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta. 2008;1778:1545–1575. PubMed
Mouritsen O.G., Bloom M. Mattress model of lipid-protein interactions in membranes. Biophys. J. 1984;46:141–153. PubMed PMC
Mouritsen O.G., Zuckermann M.J. What's so special about cholesterol? Lipids. 2004;39:1101–1113. PubMed
Niemela P.S., Miettinen M.S., Monticelli L., Hammaren H., Bjelkmar P., Murtola T., Lindahl E., Vattulainen I. Membrane proteins diffuse as dynamic complexes with lipids. J. Am. Chem. Soc. 2010;132:7574–7575. PubMed
Nyholm T.K. Lipid-protein interplay and lateral organization in biomembranes. Chem. Phys. Lipids. 2015;189:48–55. PubMed
Nystrom J.H., Lonnfors M., Nyholm T.K. Transmembrane peptides influence the affinity of sterols for phospholipid bilayers. Biophys. J. 2010;99:526–533. PubMed PMC
Oppenheimer N., Diamant H. In-plane dynamics of membranes with immobile inclusions. Phys. Rev. Lett. 2011;107:258102. PubMed
Peters R., Cherry R.J. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbruck equations. Proc. Natl. Acad. Sci. U S A. 1982;79:4317–4321. PubMed PMC
Pieper U., Schlessinger A., Kloppmann E., Chang G.A., Chou J.J., Dumont M.E., Fox B.G., Fromme P., Hendrickson W.A., Malkowski M.G. Coordinating the impact of structural genomics on the human alpha-helical transmembrane proteome. Nat. Struct. Mol. Biol. 2013;20:135–138. PubMed PMC
Pitman M.C., Grossfield A., Suits F., Feller S.E. Role of cholesterol and polyunsaturated chains in lipid-protein interactions: molecular dynamics simulation of rhodopsin in a realistic membrane environment. J. Am. Chem. Soc. 2005;127:4576–4577. PubMed
Polozova A., Litman B.J. Cholesterol dependent recruitment of di22:6-PC by a G protein-coupled receptor into lateral domains. Biophys. J. 2000;79:2632–2643. PubMed PMC
Raffy S., Teissie J. Control of lipid membrane stability by cholesterol content. Biophys. J. 1999;76:2072–2080. PubMed PMC
Ramadurai S., Duurkens R., Krasnikov V.V., Poolman B. Lateral diffusion of membrane proteins: consequences of hydrophobic mismatch and lipid composition. Biophys. J. 2010;99:1482–1489. PubMed PMC
Ramadurai S., Holt A., Krasnikov V., van den Bogaart G., Killian J.A., Poolman B. Lateral diffusion of membrane proteins. J. Am. Chem. Soc. 2009;131:12650–12656. PubMed
Ramadurai S., Holt A., Schafer L.V., Krasnikov V.V., Rijkers D.T., Marrink S.J., Killian J.A., Poolman B. Influence of hydrophobic mismatch and amino acid composition on the lateral diffusion of transmembrane peptides. Biophys. J. 2010;99:1447–1454. PubMed PMC
Rog T., Murzyn K., Karttunen M., Pasenkiewicz-Gierula M. Nonpolar interactions between trans-membrane helical EGF peptide and phosphatidylcholines, sphingomyelins and cholesterol. Molecular dynamics simulation studies. J. Pept. Sci. 2008;14:374–382. PubMed
Rog T., Pasenkiewicz-Gierula M., Vattulainen I., Karttunen M. What happens if cholesterol is made smoother: importance of methyl substituents in cholesterol ring structure on phosphatidylcholine-sterol interaction. Biophys. J. 2007;92:3346–3357. PubMed PMC
Saffman P.G., Delbruck M. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. U S A. 1975;72:3111–3113. PubMed PMC
Saxton M.J. Lateral diffusion in an archipelago. The effect of mobile obstacles. Biophys. J. 1987;52:989–997. PubMed PMC
Schafer L.V., de Jong D.H., Holt A., Rzepiela A.J., de Vries A.H., Poolman B., Killian J.A., Marrink S.J. Lipid packing drives the segregation of transmembrane helices into disordered lipid domains in model membranes. Proc. Natl. Acad. Sci. U S A. 2011;108:1343–1348. PubMed PMC
Shezad K., Zhang K., Hussain M., Dong H., He C., Gong X., Xie X., Zhu J., Shen L. Surface roughness modulates diffusion and fibrillation of amyloid-beta peptide. Langmuir. 2016;32:8238–8244. PubMed
Sparr E., Ash W.L., Nazarov P.V., Rijkers D.T., Hemminga M.A., Tieleman D.P., Killian J.A. Self-association of transmembrane alpha-helices in model membranes: importance of helix orientation and role of hydrophobic mismatch. J. Biol. Chem. 2005;280:39324–39331. PubMed
Stefl M., Sachl R., Humpolickova J., Cebecauer M., Machan R., Kolarova M., Johansson L.B.A., Hof M. Dynamics and size of cross-linking-induced lipid nanodomains in model membranes. Biophys. J. 2012;102:2104–2113. PubMed PMC
van Meer G., Voelker D.R., Feigenson G.W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008;9:112–124. PubMed PMC
Wang D., He C., Stoykovich M.P., Schwartz D.K. Nanoscale topography influences polymer surface diffusion. ACS Nano. 2015;9:1656–1664. PubMed
Weiss K., Neef A., Van Q., Kramer S., Gregor I., Enderlein J. Quantifying the diffusion of membrane proteins and peptides in black lipid membranes with 2-focus fluorescence correlation spectroscopy. Biophys. J. 2013;105:455–462. PubMed PMC
Wilson B.S., Pfeiffer J.R., Oliver J.M. Observing FcεRI signaling from the inside of the mast cell membrane. J. Cell Biol. 2000;149:1131–1142. PubMed PMC