Membrane thickness varies around the circumference of the transmembrane protein BtuB

Biophysical Journal

Volumn 100, Issue 5, 2011, Pages 1280-1287

  Ellena, Jeffrey F ^a   Lackowicz, Pawel ^a   Mongomery, Hillary ^a,b   Cafiso, David S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RUMEX;

EID: 79953850814     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.01.055     Document Type: Article

References (57)

1. 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. (Pubitemid 46998112)
2. Jensen, M. O., and O. G. Mouritsen. 2004. Lipids do influence protein function-the hydrophobic matching hypothesis revisited. Biochim. Biophys. Acta. 1666:205-226. (Pubitemid 39429479)
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. Lee, A. G. 1998. How lipids interact with an intrinsic membrane protein: the case of the calcium pump. Biochim. Biophys. Acta. 1376:381-390. (Pubitemid 28517887)
5. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87. (Pubitemid 39425199)
6. 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. (Pubitemid 28123801)
7. Hong, H., and L. K. Tamm. 2004. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. USA. 101:4065-4070. (Pubitemid 38405884)
8. 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.
9. Weiss, T. M., P. C. van der Wel, . , H. W. Huang. 2003. Hydrophobic mismatch between helices and lipid bilayers. Biophys. J. 84:379-385. (Pubitemid 36026406)
10. Anbazhagan, V., J. Qu, D. Marsh. 2008. Incorporation of outer membrane protein OmpG in lipid membranes: protein-lipid interactions and β-barrel orientation. Biochemistry. 47:6189-6198. (Pubitemid 351812831)
11. Anbazhagan, V., N. Vijay, D. Marsh. 2008. Protein-lipid interactions with Fusobacterium nucleatum major outer membrane protein FomA: spin-label EPR and polarized infrared spectroscopy. Biochemistry. 47:8414-8423.
12. Ramakrishnan, M., J. Qu, D. Marsh. 2005. Orientation of β-barrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism. Biochemistry. 44:3515-3523. (Pubitemid 40322021)
13. Marsh, D., B. Shanmugavadivu, and J. H. Kleinschmidt. 2006. Membrane elastic fluctuations and the insertion and tilt of β-barrel proteins. Biophys. J. 91:227-232. (Pubitemid 44015322)
14. Xu, Q., M. Kim, D. S. Cafiso. 2008. Membrane hydrocarbon thickness modulates the dynamics of a membrane transport protein. Biophys. J. 95:2849-2858.
15. Dumas, F., M. C. Lebrun, and J. F. Tocanne. 1999. Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions? FEBS Lett. 458:271-277. (Pubitemid 29433818)
16. Piknova, B., E. Perochon, and J. F. Tocanne. 1993. Hydrophobie mismatch and long-range protein/lipid interactions in bacteriorhodopsin/ phosphatidylcholine vesicles. Eur. J. Biochem. 218:385-396. (Pubitemid 24003752)
17. Marsh, D. 2008. Energetics of hydrophobic matching in lipid-protein interactions. Biophys. J. 94:3996-4013.
18. Lee, D., K. F. Walter, C. Griesinger. 2008. Bilayer in smallbicelles revealed by lipid-protein interactions using NMR spectroscopy. J. Am. Chem. Soc. 130:13822-13823.
19. Postle, K., and R. J. Kadner. 2003. Touch and go: tying TonB to transport. Mol. Microbiol. 49:869-882. (Pubitemid 36981335)
20. Páli, T., and D. Marsh. 2001. Tilt, twist, and coiling in β-barrel membrane proteins: relation to infrared dichroism. Biophys. J. 80: 2789-2797. (Pubitemid 32521652)
21. Lomize, A. L., I. D. Pogozheva, H. I. Mosberg. 2006. Positioning of proteins in membranes: a computational approach. Protein Sci. 15:1318-1333. (Pubitemid 43800004)
22. Tusnády, G. E., Z. Dosztányi, and I. Simon. 2004. Transmembrane proteins in the Protein DataBank: identification and classification. Bioinformatics. 20:2964-2972. (Pubitemid 39619188)
23. Scott, K. A., P. J. Bond, . , M. S. Sansom. 2008. Coarse-grained MD simulations of membrane protein-bilayer self-assembly. Structure. 16:621-630. (Pubitemid 351458703)
24. 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.
25. Snyder, S., D. Kim, and T. J. McIntosh. 1999. Lipopolysaccharide bilayer structure: effect of chemotype, core mutations, divalent cations, and temperature. Biochemistry. 38:10758-10767.
26. Wilkinson, S. G., and C. Ratledge. 1988. Gram-negative bacteria. In Microbial Lipids.. Academic Press, San Diego, CA. 299-488.
27. Fanucci, G. E., and D. S. Cafiso. 2006. Recent advances and applications of site-directed spin labeling. Curr. Opin. Struct. Biol. 16: 644-653. (Pubitemid 44466409)
28. Hubbell, W. L., D. S. Cafiso, and C. A. Altenbach. 2000. Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7:735-739.
29. Hubbell, W. L., A. Gross, . , M. A. Lietzow. 1998. Recent advances in site-directed spin labeling of proteins. Curr. Opin. Struct. Biol. 8: 649-656. (Pubitemid 28486394)
30. Schwieters, C. D., J. J. Kuszewski, and G. M. Clore. 2006. Using Xplor-NIH for NMR molecular structure determination. Prog. Nucl. Magn. Reson. Spectrosc. 48:47-62.
31. Fanucci, G. E., K. A. Coggshall, D. S. Cafiso. 2003. Substrateinduced conformational changes of the periplasmic N-terminus of an outer-membrane transporter by site-directed spin labeling. Biochemistry. 42:1391-1400. (Pubitemid 36205945)
32. Oh, K. J., C. Altenbach, W. L. Hubbell. 2000. Site-directed spin labeling of proteins. Applications to diphtheria toxin. Methods Mol. Biol. 145:147-169.
33. Altenbach, C., D. A. Greenhalgh, W. L. Hubbell. 1994. A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 91:1667-1671. (Pubitemid 24080266)
34. Frazier, A. A., C. R. Roller, .., D. S. Cafiso. 2003. Membrane-bound orientation and position of the synaptotagmin I C2A domain by sitedirected spin labeling. Biochemistry. 42:96-105. (Pubitemid 36083855)
35. Herrick, D. Z., S. Sterbling, .., D. S. Cafiso. 2006. Position of synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry. 45:9668-9674. (Pubitemid 44257414)
36. Herrick, D. Z., W. Kuo, D. S. Cafiso. 2009. Solution and membrane-bound conformations of the tandem C2A and C2B domains of synaptotagmin 1: evidence for bilayer bridging. J. Mol. Biol. 390:913-923.
37. Guo, Z., D. Cascio, ..., W. L. Hubbell. 2008. Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme. Protein Sci. 17:228-239. (Pubitemid 351171835)
38. Kucerka, N., J. F. Nagle, ..., J. Katsaras. 2008. Lipid bilayer structure determined by the simultaneous analysis of neutron and x-ray scattering data. Biophys. J. 95:2356-2367.
39. Wiener, M. C., and S. H. White. 1992. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61: 434-447.
40. Mchaourab, H. S., M. A. Lietzow, ..., W. L. Hubbell. 1996. Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry. 35:7692-7704. (Pubitemid 26202511)
41. Lietzow, M. A., and W. L. Hubbell. 2004. Motion of spin label side chains in cellular retinol-binding protein: correlation with structure and nearest-neighbor interactions in an antiparallel β-sheet. Biochemistry. 43:3137-3151. (Pubitemid 38352264)
42. Hubbell, W. L., and C. Altenbach. 1994. Investigation of structure and dynamics in membrane proteins using site-directed spin labeling. Curr. Opin. Struct. Biol. 4:566-573. (Pubitemid 24268990)
43. Killian, J. A. 1998. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta. 1376:401-415. (Pubitemid 28517889)
44. Mitra, K., I. Ubarretxena-Belandia, D. M. Engelman. 2004. Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl. Acad. Sci. USA. 101:4083-4088. (Pubitemid 38405887)
45. Elofsson, A., and G. von Heijne. 2007. Membrane protein structure: prediction versus reality. Annu. Rev. Biochem. 76:125-140.
46. Lomize, M. A., A. L. Lomize, ..., H. I. Mosberg. 2006. OPM: orientations of proteins in membranes database. Bioinformatics. 22:623-625. (Pubitemid 43372827)
47. Tusnády, G. E., Z. Dosztányi, and I. Simon. 2005. PDB-TM: selection and membrane localization of transmembrane proteins in the Protein DataBank. Nucleic Acids Res. 33(Database issue):D275-D278. (Pubitemid 40207877)
48. Chetwynd, A. P., K. A. Scott, . , M. S. Sansom. 2008. CGDB: a database of membrane protein/lipid interactions by coarse-grained molecular dynamics simulations. Mol. Membr. Biol. 25:662-669.
49. Cherezov, V., E. Yamashita, ..., M. Caffrey. 2006. In meso structure of the cobalamin transporter, BtuB, at 1.95 A resolution. J. Mol. Biol. 364:716-734. (Pubitemid 44737826)
50. Chimento, D. P., A. K. Mohanty, . , M. C. Wiener. 2003. Substrateinduced transmembrane signaling in the cobalamin transporter BtuB. Nat. Struct. Biol. 10:394-401. (Pubitemid 36523275)
51. O'Keeffe, A. H., J. M. East, and A. G. Lee. 2000. Selectivity in lipid binding to the bacterial outer membrane protein OmpF. Biophys. J. 79:2066-2074.
52. Law, C. J., C. N. Penfold, ..., C. Kleanthous. 2003. OmpF enhances the ability of BtuB to protect susceptible Escherichia coli cells from colicin E9 cytotoxicity. FEBS Lett. 545:127-132. (Pubitemid 36694688)
53. In '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.
54. Phillips, R., T. Ursell, P. Sens. 2009. Emerging roles for lipids in shaping membrane-protein function. Nature. 459:379-385.
55. McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces. Curr. Top. Membr. Transp. 9:71-144.
56. Osterberg, F., L. Rilfors, . , S. M. Gruner. 1995. Lipid extracts from membranes of Acholeplasma laidlawii A grown with different fatty acids have a nearly constant spontaneous curvature. Biochim. Biophys. Acta. 1257:18-24.
57. López, D., and R. Kolter. 2010. Functional microdomains in bacterial membranes. Genes Dev. 24:1893-1902.