Lateral diffusion of membrane proteins: Consequences of hydrophobic mismatch and lipid composition

Biophysical Journal

Volumn 99, Issue 5, 2010, Pages 1482-1489

  Ramadurai, Sivaramakrishnan ^a   Duurkens, Ria ^a   Krasnikov, Victor V ^a   Poolman, Bert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77956595226     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.06.036     Document Type: Article

References (71)

1. Oursel, D., C. Loutelier-Bourhis, C. M. Lange. 2007. Lipid composition of membranes of Escherichia coli by liquid chromatography/tandem mass spectrometry using negative electrospray ionization. Rapid Commun. Mass Spectrom. 21:1721-1728.
2. Oursel, D., C. Loutelier-Bourhis, C. M. Lange. 2007. Identification and relative quantification of fatty acids in Escherichia coli membranes by gas chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 21:3229-3233.
3. Dowhan, W. 1997. Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu. Rev. Biochem. 66:199-232.
4. McIntosh, T. J., and S. A. Simon. 2006. Roles of bilayer material properties in function and distribution of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 35:177-198.
5. Bretscher, M. S., and S. Munro. 1993. Cholesterol and the Golgi apparatus. Science. 261:1280-1281.
6. Sprong, H., P. van der Sluijs, and G. van Meer. 2001. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2:504-513.
7. Andersen, O. S., and R. E. Koeppe, 2nd. 2007. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36:107-130.
8. Perozo, E., A. Kloda, B. Martinac. 2002. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9:696-703.
9. Owen, D. M., D. Williamson, K. Gaus. 2009. Quantitative microscopy: protein dynamics and membrane organization. Traffic. 10:962-971.
10. Frick, M., K. Schmidt, and B. J. Nichols. 2007. Modulation of lateral diffusion in the plasma membrane by protein density. Curr. Biol. 17:462-467.
11. Caffrey, M., and G. W. Feigenson. 1981. Fluorescence quenching in model membranes. 3. Relationship between calcium adenosinetriphosphatase enzyme activity and the affinity of the protein for phosphatidylcholines with different acyl chain characteristics. Biochemistry. 20:1949-1961.
12. East, J. M., and A. G. Lee. 1982. Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid. Biochemistry. 21:4144-4151.
13. +)-ATPase. Biochim. Biophys. Acta. 641:416-421.
14. Cornelius, F., N. Turner, and H. R. Christensen. 2003. Modulation of Na, K-ATPase by phospholipids and cholesterol. II. Steady-state and presteady-state kinetics. Biochemistry. 42:8541-8549.
15. 't Veld, G., A. J. Driessen, W. N. Konings. 1991. Hydrophobic membrane thickness and lipid-protein interactions of the leucine transport system of Lactococcus lactis. Biochim. Biophys. Acta. 1065:203-212.
16. Uratani, Y., N. Wakayama, and T. Hoshino. 1987. Effect of lipid acyl chain length on activity of sodium-dependent leucine transport system in Pseudomonas aeruginosa. J. Biol. Chem. 262:16914-16919.
17. Pilot, J. D., J. M. East, and A. G. Lee. 2001. Effects of bilayer thickness on the activity of diacylglycerol kinase of Escherichia coli. Biochemistry. 40:8188-8195.
18. Criado, M., H. Eibl, and F. J. Barrantes. 1984. Functional properties of the acetylcholine receptor incorporated in model lipid membranes. Differential effects of chain length and head group of phospholipids on receptor affinity states and receptor-mediated ion translocation. J. Biol. Chem. 259:9188-9198.
19. Carruthers, A., and D. L. Melchior. 1984. Human erythrocyte hexose transporter activity is governed by bilayer lipid composition in reconstituted vesicles. Biochemistry. 23:6901-6911.
20. Dumas, F., J. F. Tocanne, M. C. Lebrun. 2000. Consequences of hydrophobic mismatch between lipids and melibiose permease on melibiose transport. Biochemistry. 39:4846-4854.
21. Yuan, C., R. J. O'Connell, S. N. Treistman. 2007. Regulation of the gating of BKCa channel by lipid bilayer thickness. J. Biol. Chem. 282:7276-7286.
22. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
23. Mouritsen, O. G., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
24. Webb, R. J., J. M. East, A. G. Lee. 1998. Hydrophobic mismatch and the incorporation of peptides into lipid bilayers: a possible mechanism for retention in the Golgi. Biochemistry. 37:673-679.
25. Freites, J. A., D. J. Tobias, S. H. White. 2005. Interface connections of a transmembrane voltage sensor. Proc. Natl. Acad. Sci. USA. 102:15059-15064.
26. White, S. H., and G. von Heijne. 2005. Transmembrane helices before, during, and after insertion. Curr. Opin. Struct. Biol. 15:378-386.
27. Killian, J. A., and T. K. Nyholm. 2006. Peptides in lipid bilayers: the power of simple models. Curr. Opin. Struct. Biol. 16:473-479.
28. van Klompenburg, W., I. Nilsson, B. de Kruijff. 1997. Anionic phospholipids are determinants of membrane protein topology. EMBO J. 16:4261-4266.
29. Zhang, W., H. A. Campbell, W. Dowhan. 2005. Phospholipids as determinants of membrane protein topology. Phosphatidylethanolamine is required for the proper topological organization of the γ-aminobutyric acid permease (GabP) of Escherichia coli. J. Biol. Chem. 280:26032-26038.
30. Zhang, W., M. Bogdanov, W. Dowhan. 2003. Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. J. Biol. Chem. 278:50128-50135.
31. Dowhan, W., and M. Bogdanov. 2009. Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78:515-540.
32. Seu, K. J., L. R. Cambrea, J. S. Hovis. 2006. Influence of lipid chemistry on membrane fluidity: tail and headgroup interactions. Biophys. J. 91:3727-3735.
33. Groeneveld, M., and D. J. Slotboom. 2007. Rigidity of the subunit interfaces of the trimeric glutamate transporter GltT during translocation. J. Mol. Biol. 372:565-570.
34. Ermolova, N. V., I. N. Smirnova, H. R. Kaback. 2005. Interhelical packing modulates conformational flexibility in the lactose permease of Escherichia coli. Biochemistry. 44:7669-7677.
35. Slotboom, D. J., I. Sobczak, J. S. Lolkema. 1999. A conserved Serine-rich stretch in the glutamate transporter family forms a substrate-sensitive reentrant loop. Proc. Natl. Acad. Sci. USA. 96:14282-14287.
36. Majumdar, D. S., I. Smirnova, H. R. Kaback. 2007. Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc. Natl. Acad. Sci. USA. 104:12640-12645.
37. Ramadurai, S., A. Holt, B. Poolman. 2009. Lateral diffusion of membrane proteins. J. Am. Chem. Soc. 131:12650-12656.
38. Doeven, M. K., J. H. Folgering, B. Poolman. 2005. Distribution, lateral mobility and function of membrane proteins incorporated into giant unilamellar vesicles. Biophys. J. 88:1134-1142.
39. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
40. Knol, J., L. Veenhoff, B. Poolman. 1996. Unidirectional reconstitution into detergent-destabilized liposomes of the purified lactose transport system of Streptococcus thermophilus. J. Biol. Chem. 271:15358-15366.
41. Girard, P., J. Pécréaux, P. Bassereau. 2004. A new method for the reconstitution of membrane proteins into giant unilamellar vesicles. Biophys. J. 87:419-429.
42. Gaillard, I., D. J. Slotboom, W. N. Konings. 1996. Purification and reconstitution of the glutamate carrier GltT of the thermophilic bacterium Bacillus stearothermophilus. Biochemistry. 35:6150-6156.
43. Magde, D., E. L. Elson, and W. W. Webb. 1974. Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers. 13:29-61.
44. Petrásek, Z., and P. Schwille. 2008. Precise measurement of diffusion coefficients using scanning fluorescence correlation spectroscopy. Biophys. J. 94:1437-1448.
45. Abramson, J., I. Smirnova, S. Iwata. 2003. Structure and mechanism of the lactose permease of Escherichia coli. Science. 301:610-615.
46. Yernool, D., O. Boudker, E. Gouaux. 2004. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature. 431:811-818.
47. Lewis, B. A., and D. M. Engelman. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211-217.
48. Kahya, N., and P. Schwille. 2006. How phospholipid-cholesterol interactions modulate lipid lateral diffusion, as revealed by fluorescence correlation spectroscopy. J. Fluoresc. 16:671-678.
49. Ramadurai, S., A. Holt, B. Poolman. 2010. Influence of hydrophobic mismatch and amino acid composition on the lateral diffusion of transmembrane peptides. Biophys. J., In press.
50. Shahidullah, K., and E. London. 2008. Effect of lipid composition on the topography of membrane-associated hydrophobic helices: stabilization of transmembrane topography by anionic lipids. J. Mol. Biol. 379:704-718.
51. Saffman, P. G., and M. Delbrück. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
52. Saffman, P. G. 1976. Brownian motion in thin sheets of viscous fluid. J. Fluid Mech. 73:593-602.
53. Kucerka, N., S. Tristram-Nagle, and J. F. Nagle. 2005. Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J. Membr. Biol. 208:193-202.
54. Kucerka, N., Y. Liu, J. F. Nagle. 2005. Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using x-ray scattering from oriented multilamellar arrays and from unilamellar vesicles. Biophys. J. 88:2626-2637.
55. Damodaran, K. V., and K. M. Merz. 1993. Head group water interactions in lipid bilayers-a comparison between DMPC-based and DLPE-based lipid bilayers. Langmuir. 9:1179-1183.
56. Jensen, M. O., and O. G. Mouritsen. 2004. Lipids do influence protein function-the hydrophobic matching hypothesis revisited. Biochim. Biophys. Acta. 1666:205-226.
57. Krepkiy, D., M. Mihailescu, K. J. Swartz. 2009. Structure and hydration of membranes embedded with voltage-sensing domains. Nature. 462:473-479.
58. Aranda-Espinoza, H., A. Berman, S. Safran. 1996. Interaction between inclusions embedded in membranes. Biophys. J. 71:648-656.
59. Brannigan, G., and F. L. Brown. 2006. A consistent model for thermal fluctuations and protein-induced deformations in lipid bilayers. Biophys. J. 90:1501-1520.
60. Bennett, M., R. D'Rozario, P. L. Yeagle. 2006. Asymmetric stability among the transmembrane helices of lactose permease. Biochemistry. 45:8088-8095.
61. Yeagle, P. L., M. Bennett, A. Watts. 2007. Transmembrane helices of membrane proteins may flex to satisfy hydrophobic mismatch. Biochim. Biophys. Acta. 1768:530-537.
62. Le Coutre, J., L. R. Narasimhan, H. R. Kaback. 1997. The lipid bilayer determines helical tilt angle and function in lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA. 94:10167-10171.
63. Reyes, N., C. Ginter, and O. Boudker. 2009. Transport mechanism of a bacterial homologue of glutamate transporters. Nature. 462:880-885.
64. Gekko, K., and H. Noguchi. 1979. Compressibility of globular-proteins in water at 25°C. J. Phys. Chem. 83:2706-2714.
65. Liu, N. I., and R. L. Kay. 1977. Redetermination of the pressure dependence of the lipid bilayer phase transition. Biochemistry. 16:3484-3486.
66. Hochmuth, R., P. Worthy, and E. Evans. 1978. Measurement of membrane viscosity. Biophys. J. 21: A27.
67. Naji, A., A. J. Levine, and P. A. Pincus. 2007. Corrections to the Saffman-Delbruck mobility for membrane bound proteins. Biophys. J. 93: L49-L51.
68. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87.
69. Damodaran, K. V., and K. M. Merz, Jr. 1994. A comparison of DMPC-and DLPE-based lipid bilayers. Biophys. J. 66:1076-1087.
70. de Vries, A. H., A. E. Mark, and S. J. Marrink. 2004. The binary mixing behavior of phospholipids in a bilayer: a molecular dynamics study. J. Phys. Chem. B. 108:2454-2463.
71. Leekumjorn, S., and A. K. Sum. 2006. Molecular simulation study of structural and dynamic properties of mixed DPPC/DPPE bilayers. Biophys. J. 90:3951-3965.