Dependence of M13 major coat protein oligomerization and lateral segregation on bilayer composition

Biophysical Journal

Volumn 85, Issue 4, 2003, Pages 2430-2441

  Fernandes, Fábio ^a   Loura, Luís M S ^a,b   Prieto, Manuel ^a   Koehorst, Rob ^c   Spruijt, Ruud B ^c   Hemminga, Marcus A ^c  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^b UNIVERSITY OF ÉVORA   (Portugal)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAMIDE DERIVATIVE; COAT PROTEIN; DIERUCOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLGLYCEROL; N (4,4 DIFLUORO 5,7 DIMETHYL 4 BORA 3A,4A, DIAZA S INDACEN 3 YL)METHYLIODOACETAMIDE; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE M13; FLUORESCENCE SPECTROSCOPY; LIPID BILAYER; MOLECULAR DYNAMICS; OLIGOMERIZATION; PROTEIN LIPID INTERACTION;

STAPHYLOCOCCUS PHAGE 3A;

EID: 0141785142     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74666-9     Document Type: Article

References (56)

1. Ahn, T., and H. Kim. 1998. Effects of non-lamellar-prone lipids on the ATPase activity of SecA bound to model membranes. J. Biol. Chem. 273:21692-21698.
2. Almgren, M. 1991. Kinetics of excited states processes in micellar media. In Kinetics and Catalysis in Microheterogeneous Systems. M. Gratzel, and K. Kalyanasundaram, editors. Marcel Dekker, New York. 63-113.
3. Berberan-Santos, M. N., and M. J. E. Prieto. 1987. Energy transfer in spherical geometry. Application to micelles. J. Chem. Soc. Faraday Trans. 283:1391-1409.
4. Bergström, F., I. Mikhalyov, P. Hägglöf, R. Wortmann, T. Ny, and L.B.-A. Johansson. 2001. Dimers of dipyrrometheneboron difluoride (BODIPY) with light spectroscopic applications in chemistry and biology. J. Am. Chem. Soc. 124:196-204.
5. Burnell, E., L. Van Alphen, A. Verkleij, and B. De Kruijff. 1980. 31P Nuclear magnetic resonance and freeze-fracture electron microscopy studies on Escherichia coli. I. Cytoplasmic membrane and total phospholipids. Biochim. Biophys. Acta. 597:492-501.
6. Chamberlain, B. K., Y. Nozaki, C. Tanford, and R. E. Webster. 1978. Association of the major coat protein of FD bacteriophage with phospholipid vesicles. Biochim. Biophys. Acta. 510:18-37.
7. Davenport, L., R. E. Dale, R. H. Bisby, and R. B. Cundall. 1985. Transverse location of the fluorescent probe 1,6-diphenyl-1,3,5-hexatriene in model lipid bilayer membrane systems by resonance energy transfer. Biochemistry. 24:4097-4108.
8. Deber, C. M., A. R. Khan, Z. Li, C. Joensson, and M. Glibowicka. 1993. Val → Ala mutations selectively alter helix-helix packing in the transmembrane segment of phage M13 coat protein. Proc. Natl. Acad. Sci. USA. 90:11648-11652.
9. Dumas, F., M. M. Sperotto, M.-C. Lebrun, J.-F. Tocanne, and O. G. Mouritsen. 1997. Molecular sorting of lipids by bacteriorhodopsin in dilauroylphosphatidylcholine/distearoylphosphatidylcholine lipid bilayers. Biophys. J. 73:1940-1953.
10. 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.
11. Eaton, D. F. 1988. Reference materials for fluorescence measurement. Pure Appl. Chem. 60:1107-1114.
12. Fahsel, S., E. M. Pospiech, M. Zein, T. L. Hazlet, E. Gratton, and R. Winter. 2002. Modulation of concentration fluctuations in phase-separated lipid membranes by polypeptide insertion. Biophys. J. 83:334-344.
13. Gil, T., J. H. Ipsen, O. G. Mouritsen, M. C. Sabra, M. M. Sperotto, and M. J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid bilayers. Biochim. Biophys. Acta. 1376:245-266.
14. Hemminga, M. A., J. C. Sanders, C. J. A. M. Wolfs, and R. B. Spruijt. 1993. Lipid-protein interactions involved in bacteriophage M13 infection. In Protein-Lipid Interactions, New Comprehensive Biochemistry, Vol. 25. A. Watts, editor. Elsevier, Amsterdam. 191-212.
15. + channel-associated peptide in a lipid bilayer: conformation, lipid-protein interactions, and rotational diffusion. Biochemistry. 34:3893-3898.
16. + channel-associated peptide in the 8-conformation; spin-label electron spin resonance studies. Biophys. J. 73:2588-2594.
17. Hudson, E. N., and G. Weber. 1973. Synthesis and characterization of two fluorescent sulfhydryl reagents. Biochemistry, 12:4154-4161.
18. Hunter, G. W., S. Negash, and T. C. Squier, 1999. Phosphatidylethanolamine modulates Ca-ATPase function and dynamics. Biochemistry. 38:1356-1364.
19. Karlsson, O. P., M. Rytomaa, A. Dahqvist, P. K. Kinnunnen, and A. Wieslander. 1996. Correlation between bilayer dynamics and activity of the diglucosyldiacylglycerol synthase from Acholeplasma laidlawii membranes. Biochemistry. 35:10094-10102.
20. Karolin, J., J. B.-Å. Johansson, L. Strandberg, and T. Ny. 1994. Fluorescence and absorption spectroscopic properties of dipyrrometheneboron difluoride (BODIPY) derivatives in lipids, lipid membranes, and proteins. J. Am. Chem. Soc. 116:7801-7806.
21. Killian, J. A. 1998. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta. 1376:401-416.
22. Lakowicz, J. R. 1999. Principles of Fluorescence Spectroscopy, 2nd Ed. Kluwer Academic/Plenum Press, New York. Chap. 8.
23. Lewis, B. A., and D. M. Engelman. 1983. Bacteriorhodopsin remains dispersed in fluid phospholipid bilayers over a wide range of bilayer thickness. J. Mol. Biol. 166:203-210.
24. Lehtonen, J. Y. A., J. M. Holopainen, and P. K. J. Kinnunen. 1996. Evidence for the formation of microdomains in liquid crystalline large unilamellar vesicles caused by hydrophobic mismatch of the constituent phospholipids. Biophys. J. 70:1753-1760.
25. Lehtonen, J. Y. A., and P. K. J. Kinnunen. 1997. Evidence for phospholipid microdomain formation in liquid crystalline liposomes reconstituted with Escherichia coli lactose permease. Biophys. J. 72:1247-1257.
26. Liu, W., Y. Chen, H. Watrob, S. G. Bartlett, L. Jen-Jacobson, and M. D. Barkley. 1998. N-termini of EcoRI restriction endonuclease dimers are in close proximity on the protein surface. Biochemistry. 37:15457-15465.
27. Loura, L. M. S., A. Fedorov, and M. Prieto. 1996. Resonance energy transfer in a model system of membranes: application to gel and liquid crystalline phases. Biophys. J. 71:11323-1836.
28. Loura, L. M. S., A. Fedorov, and M. Prieto. 2000. Membrane probe distribution heterogeneity: a resonance energy transfer study. J. Phys. Chem. B. 104:6920-6931.
29. Loura, L. M. S., R. F. M. de Almeida, and M. Prieto. 2001. Detection and characterization of membrane microheterogeneity by resonance energy transfer. J. Fluoresc. 11:197-209.
30. Mall, S., R. Broadbridge, R. P. Sharma, J. M. East, and A. G. Lee. 2001. Self-association of model transmembrane helix is modulated by lipid structure. Biochemistry. 40:12379-12386.
31. Marquardt, D. W. 1963. An algorithm for least-squares estimation of non-linear parameters. J. Soc. Ind. Appl. Math. 11:431-441.
32. 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.
33. Melnyk, R., A. Partridge, and C. Deber. 2002, Transmembrane domain mediated self-assembly of major coat protein subunits from FF bacteriophage. J. Mol. Biol. 315:63-72.
34. Mobashery, N., C. Nielsen, and O. S. Andersen. 1997. The conformational preference of gramicidin channels is a function of lipid bilayer thickness. FEBS Lett. 412:15-20.
35. Mouritsen, O. G., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
36. Mouritsen, O. G., and K. Jorgensen. 1994. Dynamical order and disorder in lipid bilayers. Chem. Phys. Lipids. 73:3-25.
37. Nezil, F. A., and M. Bloom. 1992. Combined influence of cholesterol and synthetic amphiphilic peptides upon bilayer thickness in model membranes. Biophys. J. 61:1176-1183.
38. Otoda, K., S. Kimura, and Y. Imanishi. 1993. Orientation and aggregation of hydrophobic helical peptides in phospholipid bilayer membrane. Biochim. Biophys. Acta. 1150:1-8.
39. Owen, C. S. 1975. Two-dimensional diffusion theory: cylindrical diffusion model applied to fluorescence quenching. J. Chem. Phys. 62:3204-3207.
40. Razi-Naqvi, K. 1974. Diffusion-controlled reactions in two-dimensional fluids: discussion of measurements of lateral diffusion of lipids in biological membranes. Chem. Phys. Lett. 28:280-284.
41. Ren, J., S. Lew, J. Wang, and E. London. 1999. Control of the transmembrane orientation and interhelical interactions within membranes by hydrophobic helix length. Biochemistry. 38:5905-5912.
42. Russel, M. 1991. Filamentous phage assembly. Mol. Microbiol. 5:1607-1613.
43. Sanders, J. C., N. A. J. van Nuland, O. Edholm, and M. Hemminga. 1991. Conformational and aggregation of M13 coat protein studied by molecular dynamics, Biophys. Chem. 41:193-202.
44. Shigematsu, D., M. Matsutani, T. Furuya, T. Kiyota, S. Lee, G. Sugihara, and S. Yamashita. 2002. Roles of peptide-peptide charge interaction and lipid phase separation in helix-helix association in lipid bilayer. Biochim. Biophys. Acta. 1564:271-280.
45. Smith, L. M., B. A. Smith, and H. M. McConnell. 1979. Lateral diffusion of M-13 coat protein in model membranes. Biochemistry. 18:2256-2259.
46. Smith, L. M., J. L. R. Rubenstein, J. W. Parce, and H. M. McConnel. 1980. Lateral diffusion of M-13 coat protein in mixtures of phosphatidylcholine and cholesterol. Biochemistry. 19:5907-5911.
47. Sperotto, M. M., and O. G. Mouritsen. 1993. Lipid enrichment and selectivity of integral membrane proteins in two-component lipid bilayers. Eur. Biophys. J. 22:323-328.
48. Spruijt, R. B., C. J. A. M. Wolfs, and M. A. Hemminga. 1989. Aggregation related conformational change of the membrane-associated coat protein of bacteriophage M13. Biochemistry. 28:9158-9165.
49. Spruijt, R. B., C. J. A. M. Wolfs, J. W. G. Verver, and M. A. Hemminga. 1996. Accessibility and environment probing using cysteine residues introduced along the putative transmembrane domain of the major coat protein of bacteriophage Biochemistry M13. 35:10383-10391.
50. 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 the bacteriophage MI 3. Biochim. Biophys. Acta. 1509:311-323.
51. 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.
52. Tristam-Nagle, S., H. I. Petrache, and J. F. Nagle. 1998. Structure and interactions of fully hydrated dioleoylphosphatidylcholine bilayers. Biophys. J. 75:917-925.
53. Umberger, J. Q., and V. K. Lamer. 1945. The kinetics of diffusion-controlled molecular and ionic reactions in solution as determined by measurements of the quenching of fluorescence. J. Ann. Chem. Soc. 67:1099-1109.
54. Webster, R. E., and N. G. Haigh. 1998. The major coat protein of filamentous bacteriophage F1 specifically pairs in the bacterial cytoplasmic membrane. J. Mol. Biol. 279:19-29.
55. Wolber, P. K., and B. S. Hudson. 1979. An analytical solution to the Förster energy transfer problem in two dimensions. Biophys. J. 28:197-210.
56. Woolford, J. L., Jr., J. S. Cashman, and R. E. Webster. 1974. F1 Coat protein synthesis and altered phospholipid metabolism in F1-infected Escherichia coli. Virology, 58:544-560.