Visualizing association of lipidated signaling proteins in heterogeneous membranes-Partitioning into subdomains, lipid sorting, interfacial adsorption, and protein association

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 7, 2010, Pages 1409-1417

  Weise, Katrin ^a   Triola, Gemma ^a   Janosch, Sascha ^a   Waldmann, Herbert ^a   Winter, Roland ^a  

^a TU DORTMUND UNIVERSITY   (Germany)

Author keywords

AFM; Fluorescence microscopy; Lipidated protein; Model biomembrane; Ras signaling

Indexed keywords

MEMBRANE PROTEIN; PROTEIN N RAS; RAS PROTEIN; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; FLUORESCENCE MICROSCOPY; LIPID BILAYER; LIPID RAFT; LIPID VESICLE; LOW TEMPERATURE; NONHUMAN; PHASE SEPARATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; TEMPERATURE DEPENDENCE;

ANIMALS; HUMANS; KINETICS; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MODELS, BIOLOGICAL; PHASE TRANSITION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS P21(RAS); UNILAMELLAR LIPOSOMES;

EID: 77954728132     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.12.006     Document Type: Article

References (43)

1. Jacobson K., Mouritsen O.G., Anderson R.G. Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 2007, 9:7-14.
2. Munro S. Lipid rafts: elusive or illusive?. Cell 2003, 115:377-388.
3. Semrau S., Schmidt T. Membrane heterogeneity- from lipid domains to curvature effects. Soft Matter 2009, 5:3174-3186.
4. Ipsen H.J., Karlstrom G., Mouritsen O.G., Wennerstrom H., Zuckermann M.J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim. Biophys. Acta 1987, 905:162-172.
5. Goni F.M., Alonso A., Bagatolli L.A., Brown R.E., Marsh D., Prieto M., Thewalt J.L. Phase diagrams of lipid mixtures relevant to the study of membrane rafts. Biochim. Biophys. Acta 2008, 1781:665-684.
6. Honerkamp-Smith A.R., Cicuta P.C., Collins M.D., Veatch S.L., den Nijs M., Schick M., Keller S.L. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophys. J. 2008, 95:236-246.
7. Kahya N., Brown D.A., Schwille P. Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles. Biochemistry 2005, 44:7479-7489.
8. Wang T.Y., Leventis R., Silvius J.R. Fluorescence-based evaluation of the partitioning of lipids and lipidated peptides into liquid-ordered microdomains: a model for molecular partitioning into 'lipid rafts'. Biophys. J. 2000, 79:919-933.
9. Chiantia S., Ries J., Kahya N., Schwille P. Combined AFM and two-focus SFCS study of raft-exhibiting model membranes. ChemPhysChem 2006, 7:2409-2418.
10. Gutlederer E., Gruhn T., Lipowsky R. Polymorphyism of vesicles with multidomain patterns. Soft Matter 2009, 5:3303-3311.
11. Hancock J.F. Lipid rafts: contentious only from simplistic viewpoints. Nat. Rev. Mol. Cell Biol. 2006, 7:456-462.
12. Omerovic J., Prior I.A. Compartmentalized signalling: Ras proteins and signalling nanoclusters. FEBS J. 2009, 276:1817-1825.
13. Bagatolli L., Kumar P.B.S. Phase behavior of multicomponent membranes: experimental and computational techniques. Soft Matter 2009, 5:3234-3248.
14. Jørgensen K., Mouritsen O.G. Phase separation dynamics and lateral organization of two-component lipid membranes. Biophys. J. 1995, 69:942-954.
15. Parasassi T., Gratton E., Yu W.M., Wilson P., Levi M. Two-photon fluorescence microscopy of Laurdan generalized polarization domains in model and natural membranes. Biophys. J. 1997, 72:2413-2429.
16. Winter R., Gabke A., Czeslik C., Pfeifer P. Power-law fluctuations in phase-separated lipid membranes. Phys. Rev. E 1999, 60:7354-7359.
17. Korlach J., Schwille P., Webb W.W., Feigensen G.W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8461-8466.
18. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1:31-41.
19. Edidin M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 2003, 32:257-283.
20. Curran A.R., Templer R.H., Booth P.J. Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer. Biochemistry 1999, 38:9328-9336.
21. Wittinghofer A., Waldmann H. Ras - a molecular switch involved in tumor formation. Angew. Chem. Int. Ed. 2000, 39:4192-4214.
22. Brunsveld L., Kuhlmann J., Alexandrov K., Wittinghofer A., Goody R.S., Waldmann H. Lipidated Ras and Rab peptides and proteins - synthesis, structure, and function. Angew. Chem. Int. Ed. 2006, 45:6622-6646.
23. Brunsveld L., Waldmann H., Huster D. Membrane binding of lipidated Ras peptides and proteins - the structural point of view. Biochim. Biophys. Acta 2009, 1788:273-288.
24. Hancock J.F. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 2003, 4:373-384.
25. Rocks O., Peyker A., Kahms M., Verveer P.J., Koerner C., Lumbierres M., Kuhlmann J., Waldmann H., Wittinghofer A., Bastiaens P. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 2005, 307:1746-1752.
26. Charron G., Wilson J., Hang H.C. Chemical tools for understanding protein lipidation in eukaryotes. Curr. Opin. Chem. Biol. 2009, 13:382-391.
27. Fahsel S., Pospiech E.M., Zein M., Hazlett T.L., Gratton E., Winter R. Modulation of concentration fluctuations in phase-separated lipid membranes by polypeptide insertion. Biophys. J. 2002, 83:334-344.
28. Janosch S., Nicolini C., Ludolph B., Peters C., Völkert M., Hazlet T.L., Gratton E., Waldmann H., Winter R. Partitioning of dual-lipidated peptides into membrane microdomains: lipid sorting vs. peptide aggregation. J. Am. Chem. Soc. 2004, 126:7496-7503.
29. Nicolini C., Baranski J., Schlummer S., Palomo J., Lumbierres-Burgues M., Kahms M., Kuhlmann J., Sanchez S., Gratton E., Waldmann H., Winter R. Visualizing association of N-Ras in lipid microdomains: influence of domain structure and interfacial adsorption. J. Am. Chem. Soc. 2006, 128:192-201.
30. Meister A., Nicolini C., Waldmann H., Kuhlmann J., Kerth A., Winter R., Blume A. Insertion of lipidated Ras proteins into lipid monolayers studied by infrared reflection absorption spectroscopy (IRRAS). Biophys. J. 2006, 91:1388-1401.
31. Reuther G., Tan K.T., Vogel A., Nowak C., Arnold K., Kuhlmann J., Waldmann H., Huster D. The lipidated membrane anchor of full length N-Ras protein shows an extensive dynamics as revealed by solid-state NMR spectroscopy. J. Am. Chem. Soc. 2006, 128:13840-13846.
32. 2H solid-state NMR and molecular dynamics simulations. Biophys. J. 2007, 93:2697-2712.
33. Weise K., Triola G., Brunsveld L., Waldmann H., Winter R. Influence of the lipidation motif on the partitioning and association of N-Ras in model membrane subdomains. J. Am. Chem. Soc. 2009, 131:1557-1564.
34. Ludolph B., Waldmann H. The synthesis of acid- and base-labile lipopeptides on solid support. Chem. Eur. J. 2003, 9:3683-3691.
35. Bader B., Kuhn K., Owen D.J., Waldmann H., Wittinghofer A., Kuhlmann J. Bioorganic synthesis of lipid-modified proteins for the study of signal transduction. Nature 2000, 403:223-226.
36. Angelova M.I., Soléau S., Meléard Ph., Faucon J.F., Bothorel P. Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Prog. Colloid Polym. Sci. 1992, 98:127-131.
37. Bagatolli L.A., Gratton E. Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles. Biophys. J. 1999, 77:2090-2101.
38. Cicuta P., Keller S.L., Veatch S.L. Diffusion of lipid domains in lipid bilayer membranes. J. Phys. Chem. B 2007, 111:3328-3331.
39. S. Janosch, Ph.D. Thesis, TU Dortmund University, Dortmund, 2004.
40. de Almeida R.F., Federov A., Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 2003, 85:2406-2416.
41. Veatch S.L., Keller S.L. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta 2005, 1746:172-185.
42. Rinia H.A., Snel M.M., van der Eerden J.P., de Kruijff B. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 2001, 501:92-96.
43. Nielsen L.K., Vishnyakov A., Jørgensen K., Bjørnholm T., Mouritsen O.G. Nanometre-scale structure of fluid lipid membranes. J. Phys.: Condens. Matter 2000, 12:A309-A314.