Organization, dynamics, and segregation of Ras nanoclusters in membrane domains

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 21, 2012, Pages 8097-8102

  Janosi, Lorant ^a,b   Li, Zhenlong ^a   Hancock, John F ^a   Gorfe, Alemayehu A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Lipid bilayer; Lipidated Ras proteins; Molecular dynamics simulation; Nanoclusters nanodomains; Plasma membrane

Indexed keywords

CHOLESTEROL; MEMBRANE PROTEIN; RAS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL AGGREGATION; CYTOSOL; HYDROPHOBICITY; LIPID BILAYER; LIPID COMPOSITION; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; SIMULATION;

CELL MEMBRANE; CHOLESTEROL; COMPUTER SIMULATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID BILAYERS; LIPOYLATION; MICROSCOPY, ELECTRON; MODELS, CHEMICAL; PRENYLATION; PROTEIN STRUCTURE, TERTIARY; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84861438588     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1200773109     Document Type: Article

References (44)

1. Plowman SJ, Muncke C, Parton RG, Hancock JF (2005) H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci USA 102:15500-15505. (Pubitemid 41528086)
2. Abankwa D, Gorfe AA, Hancock JF (2007) Ras nanoclusters: molecular structure and assembly. Semin Cell Dev Biol 18:599-607. (Pubitemid 350026427)
3. Sharma P, et al. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116:577-589. (Pubitemid 38264434)
4. Tian TH, et al. (2007) Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol 9:905-914.
5. Harding AS, Hancock JF (2008) Using plasma membrane nanoclusters to build better signaling circuits. Trends Cell Biol 18:364-371.
6. Parton RG, Hancock JF (2004) Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol 14:141-147. (Pubitemid 38293457)
7. Bos JL (1989) Ras oncogenes in human cancer: a review. Cancer Res 49:4682-4689.
8. Karnoub AE, Weinberg RA (2008) Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 9:517-531. (Pubitemid 351881844)
9. Fernandez-Medarde A, Santos E (2011) Ras in cancer and developmental diseases. Genes & Cancer 2:344-358.
10. Kholodenko BN, Hancock JF, Kolch W (2010) Signalling ballet in space and time. Nat Rev Mol Cell Biol 11:414-426.
11. Abankwa D, Gorfe AA, Inder K, Hancock JF (2010) Ras membrane orientation and nanodomain localization generate isoform diversity. Proc Natl Acad Sci USA 107:1130-1135.
12. Hancock JF (2006) Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 7:456-462.
13. Nicolini C, et al. (2006) Visualizing association of N-Ras in lipid microdomains: influence of domain structure and interfacial adsorption. J Am Chem Soc 128:192-201. (Pubitemid 43100871)
14. Weise K, et al. (2011) Membrane-mediated induction and sorting of K-Ras microdomain signaling platforms. J Am Chem Soc 133:880-887.
15. Ayton GS, Blood PD, Voth GA (2007) Membrane remodeling from N-BAR domain interactions: Insights from multi-scale simulation. Biophys J 92:3595-3602. (Pubitemid 46698648)
16. Arkhipov A, Yin Y, Schulten K (2008) Four-scale description of membrane sculpting by BAR domains. Biophys J 95:2806-2821.
17. Risselada HJ, Marrink SJ (2008) The molecular face of lipid rafts in model membranes. Proc Natl Acad Sci USA 105:17367-17372.
18. Schafer LV, Marrink SJ (2010) Partitioning of lipids at domain boundaries in model membranes. Biophys J 99:L91-L93.
19. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111:7812-7824. (Pubitemid 47169693)
20. Monticelli L, et al. (2008) The MARTINI coarse-grained force field: Extension to proteins. J Chem Theory Comput 4:819-834.
21. Venturoli M, Sperotto MM, Kranenburg M, Smit B (2006) Mesoscopic models of biological membranes. Physics Reports 437:1-54. (Pubitemid 44739752)
22. Ayton GS, Voth GA (2009) Systematic multiscale simulation of membrane protein systems. Curr Opin Struct Biol 19:138-144.
23. Shinoda W, DeVane R, Klein ML (2010) Zwitterionic lipid assemblies: molecular dynamics studies of monolayers, bilayers, and vesicles using a new coarse grain force field. J Phys Chem B 114:6836-6849.
24. Baoukina S, Monticelli L, Risselada HJ, Marrink SJ, Tieleman DP (2008) The molecular mechanism of lipid monolayer collapse. Proc Natl Acad Sci USA 105:10803-10808.
25. Risselada HJ, Marrink SJ (2009) Curvature effects on lipid packing and dynamics in liposomes revealed by coarse grained molecular dynamics simulations. Phys Chem Chem Phys 11:2056-2067.
26. Smirnova YG, Marrink SJ, Lipowsky R, Knecht V (2010) Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. J Am Chem Soc 132:6710-6718.
27. Schafer LV, et al. (2011) Lipid packing drives the segregation of transmembrane helices into disordered lipid domains in model membranes. Proc Natl Acad Sci USA 108:1343-1348.
28. Janosi L, Prakash A, Doxastakis M (2010) Lipid-modulated sequence-specific association of Glycophorin A in membranes. Biophys J 99:284-292.
29. Prakash A, Janosi L, Doxastakis M (2010) Self-association of models of transmembrane domains of ErbB receptors in a lipid bilayer. Biophys J 99:3657-3665.
30. Parton DL, Klingelhoefer JW, Sansom MS (2011) Aggregation of model membrane proteins, modulated by hydrophobic mismatch, membrane curvature, and protein class. Biophys J 101:691-699.
31. Murakoshi H, et al. (2004) Single-molecule imaging analysis of Ras activation in living cells. Proc Natl Acad Sci USA 101:7317-7322. (Pubitemid 38638030)
32. Roy S, et al. (2005) Individual palmitoyl residues serve distinct roles in H-ras trafficking, microlocalization, and signaling. Mol Cell Biol 25:6722-6733. (Pubitemid 41023244)
33. Gorfe AA, McCammon JA (2008) Similar membrane affinity of mono- and di-S-acylated Ras membrane anchors: a new twist in the role of protein lipidation. J Am Chem Soc 130:12624-12625.
34. Kuzmin PI, Akimov SA, Chizmadzhev YA, Zimmerberg J, Cohen FS (2005) Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys J 88:1120-1133. (Pubitemid 40975943)
35. Garcia-Saez AJ, Chiantia S, Schwille P (2007) Effect of line tension on the lateral organization of lipid membranes. J Biol Chem 282:33537-33544. (Pubitemid 350159535)
36. Zimmerberg J, KozlovMM(2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7:9-19. (Pubitemid 43361568)
37. Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425:821-824. (Pubitemid 37351463)
38. Baumgart T, Das S, Webb WW, Jenkins JT (2005) Membrane elasticity in giant vesicles with fluid phase coexistence. Biophys J 89:1067-1080. (Pubitemid 41098989)
39. Ollila OH, et al. (2009) 3D pressure field in lipid membranes and membrane-protein complexes. Phys Rev Lett 102:078101-078104.
40. Mayor S, Rao M (2004) Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 5:231-240. (Pubitemid 38455746)
41. Reynwar BJ, et al. (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:461-464. (Pubitemid 46816743)
42. Rotblat B, et al. (2004) Three separable domains regulate GTP-dependent association of H-ras with the plasma membrane. Mol Cell Biol 24:6799-6810. (Pubitemid 38944358)
43. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447.
44. Humphrey W, Dalke A, Schulten K (1996) VMD-Visual Molecular Dynamics. J Mol Graphics 14:33-38.