Membrane protein frustration: Protein incorporation into hydrophobic mismatched binary lipid mixtures

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1408-1414

  Stopar, David ^a   Spruijt, Ruud B ^b   Hemminga, Marcus A ^b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; CAPSID PROTEIN; COAT PROTEIN, BACTERIOPHAGE M13;

ALPHA HELIX; ARTICLE; BACTERIOPHAGE M13; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENERGY; ESCHERICHIA COLI; EVOLUTION; HYDROPHOBICITY; LIPID BILAYER; LIPID COMPOSITION; NONHUMAN; PHASE TRANSITION; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; SITE DIRECTED MUTAGENESIS; SPIN LABELING; TEMPERATURE; CHEMISTRY; GENETICS; MUTATION; PROTEIN TERTIARY STRUCTURE;

ESCHERICHIA COLI;

BACTERIOPHAGE M13; CAPSID PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROPHOBICITY; LIPID BILAYERS; MUTATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE;

EID: 62649148922     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.029     Document Type: Article

References (39)

1. 31P-NMR spectroscopy. Biophys. J. 83:994-1003.
2. Galbraith, T. P., and B. A. Wallace. 1999. Phospholipid chain length alters the equilibrium between pore and channel forms of gramicidin. Faraday Discuss. 111:159-164. (Pubitemid 128531898)
3. Cornea, R. L., and D. D. Thomas. 1994. Effects of membrane thickness on the molecular dynamics and enzymatic activity of reconstituted Ca-ATPase. Biochemistry. 33:2912-2920. (Pubitemid 24103351)
4. Dumas, F., J. F. Tocanne, G. Leblanc, and M. C. Lebrun. 2000. Consequences of hydrophobic mismatch between lipids and melibiose permease on melibiose transport. Biochemistry. 39:4846-4854. (Pubitemid 30225350)
5. Mouritsen, O. G. 1991. Theoretical models of phospholipid phase transitions. Chem. Phys. Lipids. 57:179-194.
6. Nielsen, L. K., A. Vishnyakov, K. Jørgensen, T. Bjørnholm, and O. G. Mouritsen. 2000. Nanometre-scale structure of fluid lipid membranes. J. Phys. Condens. Matter. 12:A309-A314.
7. Lee, A. G. 2003. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta. 1612:1-40.
8. Stopar, D., R. B. Spruijt, C. J. Wolfs, and M. A. Hemminga. 2003. Protein-lipid interactions of bacteriophage M13 major coat protein. Biochim. Biophys. Acta. 1611:5-15. (Pubitemid 36351428)
9. Stopar, D., R. B. Spruijt, and M. A. Hemminga. 2006. Anchoring mechanisms of membrane-associated M13 major coat protein. Chem. Phys. Lipids. 141:83-93. (Pubitemid 43728802)
10. Fernandes, F., L. M. Loura, M. Prieto, R. Koehorst, R. B. Spruijt, et al. 2003. Dependence of M13 major coat protein oligomerization and lateral segregation on bilayer composition. Biophys. J. 85:2430-2441.
11. Marsh, D. 2008. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta. 1778:1545-1575.
12. Morein, S., A. -S. Andersson, L. Rilfors, and G. Lindblom. 1996. Wildtype Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures. J. Biol. Chem. 271:6801-6809.
13. Dong, H., S. E. Paramonov, L. Aulisa, E. L. Bakota, and J. D. Hartgerink. 2007. Self-assembly of multidomain peptides: balancing molecular frustration controls conformation and nanostructure. J. Am. Chem. Soc. 129:12468-12472.
14. Meijer, A. B., R. B. Spruijt, C. J. A. M. Wolfs, and M. A. Hemminga. 2001. Membrane-anchoring interactions of M13 major coat protein. Biochemistry. 40:8815-8820. (Pubitemid 32709514)
15. Spruijt, R. B., A. B. Meijer, C. J. A. M. Wolfs, and M. A. Hemminga. 2000. Localization and rearrangement modulation of the N-terminal arm of the membrane-bound major coat protein of bacteriophage M13. Biochim. Biophys. Acta. 1509:311-323.
16. Spruijt, R. B., C. J. A. M. Wolfs, and M. A. Hemminga. 1989. Aggregation-related conformational change of membrane-associated coat protein of bacteriophage M13. Biochemistry. 28:9158-9165. (Pubitemid 19283485)
17. Spruijt, R. B., C. J. M. Wolfs, and M. A. Hemminga. 2004. Membrane assembly of M13 major coat protein: evidence for a structural adaptation in the hinge region and a tilted transmembrane domain. Biochemistry. 43:13972-13980.
18. Ahyayauch, H., B. Larijani, A. Alonso, and F. M. Goñi. 2006. Detergent solubilization of phosphatidylcholine bilayers in the fluid state: influence of the acyl chain structure. Biochim. Biophys. Acta. 1758:190-196.
19. Koynova, R., and M. Caffrey. 1998. Phases and phase transitions of the phosphatidylcholines. Biochim. Biophys. Acta. 1376:91-145. (Pubitemid 28321526)
20. Stopar, D., J. Štrancar, R. B. Spruijt, and M. A. Hemminga. 2005. Exploring the local conformational space of a membrane protein by site-directed spin labeling. J. Chem. Inf. Model. 45:1621-1627.
21. Stopar, D., R. B. Spruijt, C. J. A. M. Wolfs, and M. A. Hemminga. 1996. Local dynamics of the M13 major coat protein in different membrane-mimicking systems. Biochemistry. 35:15467-15473. (Pubitemid 26408884)
22. Stopar, D., R. B. Spruijt, C. J. A. M. Wolfs, and M. A. Hemminga. 1997. In situ aggregational state of M13 bacteriophage major coat protein in sodium cholate and lipid bilayers. Biochemistry. 36:12268-12275.
23. Stopar, D., R. B. Spruijt, C. J. A. M. Wolfs, and M. A. Hemminga. 1998. Mimicking initial interactions of bacteriophage M13 coat protein disassembly in model membrane systems. Biochemistry. 37:10181-10187. (Pubitemid 28366373)
24. Stopar, D., R. B. Spruijt, C. J. A. M. Wolfs, and M. A. Hemminga. 2002. Structural characterization of bacteriophage M13 solubilization by amphiphiles. Biochim. Biophys. Acta. 1594:54-63. (Pubitemid 34131725)
25. Wolkers, W. F., R. B. Spruijt, A. Kaan, R. N. H. Konings, and M. A. Hemminga. 1997. Conventional and saturation-transfer ESR of spin-labeled mutant bacteriophage M13 coat protein in phospholipid bilayers. Biochim. Biophys. Acta. 1327:5-16. (Pubitemid 27283394)
26. Stopar, D., J. Štrancar, R. B. Spruijt, and M. A. Hemminga. 2006. Motional restrictions of membrane proteins: a site-directed spin labeling study. Biophys. J. 91:3341-3348.
27. Koehorst, R. B. M., R. B. Spruijt, F. J. Vergeldt, and M. A. Hemminga. 2004. Lipid bilayer topology of the transmembrane α-helix of M13 major coat protein and bilayer polarity profile by site-directed fluorescence spectroscopy. Biophys. J. 87:1445-1455. (Pubitemid 39167005)
28. Vos, W. L., R. B. M. Koehorst, R. B. Spruijt, and M. A. Hemminga. 2005. Membrane-bound conformation of M13 major coat protein: a structure validation through FRET-derived constraints. J. Biol. Chem. 280:38522-38527.
29. Vos, W. L., M. Schor, P. V. Nazarov, R. B. M. Koehorst, R. B. Spruijt, et al. 2007. Structure of membrane-embedded M13 major coat protein is insensitive to hydrophobic stress. Biophys. J. 93:3541-3547.
30. Veatch, S. L., and S. L. Keller. 2005. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta. 1746:172-185.
31. Sankaram, M. B., D. Marsh, and T. E. Thompson. 1992. Determination of fluid and gel domain sizes in two-component, two-phase lipid bilayers. An electron spin resonance spin label study. Biophys. J. 63:340-349.
32. Chandrashekar, I. R., and S. M. Cowsik. 2003. Three-dimensional structure of the mammalian tachykinin peptide neurokinin A bound to lipid micelles. Biophys. J. 85:4002-4011. (Pubitemid 37490309)
33. 2H nuclear magnetic resonance order parameter profiles suggest a change of molecular shape for phosphatidylcholines containing a polyunsaturated acyl chain. Biophys. J. 68:2396-2403.
34. 2H NMR spectroscopy. Biophys. J. 79:3172-3192.
35. Fernandes, F., L. M. S. Loura, R. B. M. Koehorst, R. B. Spruijt, M. A. Hemminga, et al. 2004. Quantification of protein-lipid selectivity using FRET. Application to the M13 major coat protein. Biophys. J. 87:344-352.
36. Wickner, W. 1976. Asymmetric orientation of phage M13 coat protein in Escherichia coli cytoplasmic membranes and in synthetic lipid vesicles. Proc. Natl. Acad. Sci. USA. 73:1159-1163.
37. Shogomori, H., A. T. Hammond, A. G. Ostermeyer-Fay, D. J. Barr, G. W. Feigenson, et al. 2005. Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells. J. Biol. Chem. 280:18931-18942.
38. Brown, D. A. 2006. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda). 21:430-439.
39. Strandberg, E., and J. A. Killian. 2003. Snorkeling of lysine side chains in transmembrane helices: how easy can it get? FEBS Lett. 544:69-73.