Lipid-modulated sequence-specific association of glycophorin a in membranes

Biophysical Journal

Volumn 99, Issue 1, 2010, Pages 284-292

  Janosi, Lorant ^a   Prakash, Anupam ^a   Doxastakis, Manolis ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPHORIN; LIPID BILAYER; MEMBRANE LIPID;

AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; LIPID BILAYER; METABOLISM; MOLECULAR GENETICS; MONTE CARLO METHOD; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; THERMODYNAMICS;

AMINO ACID SEQUENCE; CELL MEMBRANE; GLYCOPHORIN; LIPID BILAYERS; MEMBRANE LIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONTE CARLO METHOD; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

EID: 77954354757     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.04.005     Document Type: Article

References (63)

1. Cao, H., L. Bangalore, D. F. Stern. 1992. A subdomain in the transmembrane domain is necessary for p185neu* activation, EMBO J. 11:923-932.
2. Lemmon, M. A., and D. M. Engelman. 1992. Helix-helix interactions inside lipid bilayers. Curr. Opin. Struct. Biol. 2:511-518.
3. Lemmon, M. A., J. M. Flanagan, D. M. Engelman. 1992. Glycophorin A dimerization is driven by specific interactions between transmembrane α-helices. J. Biol. Chem. 267:7683-7689.
4. Lemmon, M. A., H. R. Treutlein, D. M. Engelman. 1994. A dimerization motif for transmembrane α-helices. Nat. Struct. Biol., 1:157-163.
5. Adams, P. D., D. M. Engelman, and A. T. Brunger. 1996. Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching. Proteins. 26:257-261.
6. Fleming, K. G., A. L. Ackerman, and D. M. Engelman. 1997. The effect of point mutations on the free energy of transmembrane α-helix dimerization. J. Mol. Biol. 272:266-275.
7. Brosig, B., and D. Langosch. 1998. The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci. 7:1052-1056.
8. Russ, W. P., and D. M. Engelman. 2000. The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296:911-919.
9. Mackenzie, K. R. 2006. Folding and stability of α-helieal integral membrane proteins. Chem. Rev. 106:1931-1977.
10. MacKenzie, K. R., and K. G. Fleming. 2008. Association energetics of membrane spanning α-helices. Curr. Opin. Struct. Biol. 18:412-419.
11. Moore, D. T., B. W. Berger, and W. F. DeGrado. 2008. Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure. 16:991-1001.
12. MacKenzie, K. R., J. H. Prestegard, and D. M. Engelman. 1997. A transmembrane helix dimer: structure and implications. Science. 276:131-133.
13. MacKenzie, K. R., and D. M. Engelman. 1998. Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A. dimerization. Proc. Natl. Acad. Sci. USA. 95:3583-3590.
14. Doura, A. K., and K. G. Fleming. 2004. Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer. J. Mol. Biol. 343:1487-1497.
15. Mendrola, J. M., M. B. Berger, M. A. Lemmon. 2002. The single transmembrane domains of ErbB receptors self-associate in cell membranes. J. Biol. Chem. 277:4704-4712.
16. Treutlein, H. R., M. A. Lemmon, A. T. Brünger. 1992. The glycophorin. A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices. Biochemistry. 31:12726-12732.
17. Braun, R., D. M. Engelman, and K. Schulten. 2004. Molecular dynamics simulations of micelle formation around dimeric glycophorin A transmembrane helices. Biophys. J. 87:754-763.
18. Petrache, H. I., A. Grossfield, T. B. Woolf. 2000. Modulation of glycophorin A transmembrane helix interactions by lipid bilayers: molecular dynamics calculations. J. Mol. Biol. 302:727-746.
19. Kokubo, H., and Y. Okamoto. 2004. Prediction of membrane protein structures by replica-exchange Monte Carlo simulations: case of two helices. J. Chem. Phys. 120:10837-10847.
20. Cuthbertson, J. M., P. J. Bond, and M. S. P. Sansom. 2006. Transmembrane helix-helix interactions: comparative simulations of the glycophorin a dimer. Biochemistry. 45:14298-14310.
21. Hénin, J., A. Pohorille, and C. Chipot. 2005. Insights into the recognition and association of transmembrane α-helices. The free energy of α-helix dimerization in glycophorin A. J. Am. Chem. Soc. 127: 8478-8484.
22. Mottamal, M., J. Zhang, and T. Lazaridis. 2006. Energetics of the native and non-native states of the glycophorin transmembrane helix dimer. Proteins. 62:996-1009.
23. Bu, L., W. Im, and C. L. Brooks, 3rd. 2007. Membrane assembly of simple helix homo-oligomers studied via molecular dynamics imulations. Biophys. J. 92:854-863.
24. Zhang, J., and T. Lazaridis. 2006. Calculating the free energy of association of transmembrane helices. Biophys. J. 91:1710-1723.
25. Gervais, C., T. Wüst, Y. Xu. 2009. Application of the Wang-Landau algorithm to the dimerization of glycophorin. A. J. Chem. Phys. 130:215106.
26. Gil, T., J. H. Ipsen, M. J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid membranes. Biochim. Biophys. Acta. 1376:245-266.
27. Mall, S., R. Broadbridge, A. G. Lee. 2001. Self-association of model transmembrane α-helices is modulated by lipid structure. Biochemistry. 40:12379-12386.
28. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87.
29. Vigh, L., P. V. Escriba, J. L. Harwood. 2005. The significance of lipid composition for membrane activity: new concepts and ways of assessing function. Prog. Lipid Res. 44:303-344.
30. Orzáez, M., D. Lukovic, I. Mingarro. 2005. Influence of hydrophobic matching on association of model transmembrane fragments containing a minimized glycophorin A dimerization motif. FEBS Lett. 579:1633-1638.
31. Fleming, K. G., and D. M. Engelman. 2001. Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants. Proc. Natl. Acad. Sci. USA. 98:14340-14344.
32. Lagüe, P., M. J. Zuckermann, and B. Roux. 1998. Protein inclusion in lipid membranes: a theory based on the hypernetted chain integral equation. Faraday Discuss. 111:165-172, discussion 225-246.
33. Lagüe, P., M. J. Zuckermann, and B. Roux. 2000. Lipid-mediated interactions between intrinsic membrane proteins: a theoretical study based on integral equations. Biophys. J. 79:2867-2879.
34. Lagüe, P., M. J. Zuckermann, and B. Roux. 2001. Lipid-mediated interactions between intrinsic membrane proteins: dependence on protein aze and lipid composition. Biophys. J. 81:276-284.
35. de Meyer, F. J.-M., M. Venturoli, and B. Smit. 2008. Molecular simulations of lipid-mediated protein-protein interactions. Biophys. J. 95:1851-1865.
36. Bond, P. J., and M. S. P. Sansom. 2006. Insertion and assembly of membrane proteins via simulation. J. Am. Chem. Soc. 128:2697-2704.
37. Periole, X., T. Huber, T. P. Sakmar. 2007. G protein-coupled receptors self-assemble in dynamics simulations of model bilayers. J. Am. Chem. Soc. 129:10126-10132.
38. Psachoulia, E., P. W. Fowler, M. S. Sansom. 2008. Helix-helix interactions in membrane proteins: coarse-grained simulations of glycophorin A helix dimerization. Biochemistry. 47:10503-10512.
39. Im, W., J. Lee, H. Rui. 2009. Novel free energy calculations to explore mechanisms and energetics of membrane protein structure and function. J. Comput. Chem. 30:1622-1633.
40. Marrink, S. J., H. J. Risselada, A. H. de Vries. 2007. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B. 111:7812-7824.
41. Monticelli, L., S. K. Kandasamy, S.-J. Marrink. 2008. The MARTINI coarse-grained force field: extension to proteins. J. Chem. Theory Comput. 4:819-834.
42. Popot, J. L., and D. M. Engelman. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry. 29:4031-4037.
43. Fisher, L. E., D. M. Engelman, and J. N. Sturgis. 1999. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293:639-651.
44. Ladbrooke, B. D., and D. Chapman. 1969. Thermal analysis of lipids, proteins and biological membranes. A review and summary of some recent studies. Chem. Phys. Lipids. 3:304-356.
45. Janosi, L., and M. Doxastakis. 2009. Accelerating flat-histogram methods for potential of mean force calculations. J. Chem. Phys. 131:054105.
46. Kim, E. B., R. Faller, J. J. de Pablo. 2002. Potential of mean force between a spherical particle suspended in a nematic liquid crystal and a substrate. J. Chem. Phys. 117:7781-7787.
47. Doxastakis, M., Y.-L. Chen, and J. J. de Pablo. 2005. Potential of mean force between two nanometer-scale particles in a polymer solution. J. Chem, Phys. 123:034901.
48. Wang, F. G., and D. P. Landau. 2001. Efficient, multiple-range random walk algorithm to calculate the density of states. Phys. Rev. Lett. 86:2050-2053.
49. Tuckerman, M. E., B. J. Berne, M. L. Klein. 1993. Efficient molecular-dynamics and hybrid Monte-Carlo algorithms for path-integrals. J. Chem. Phys. 99:2796-2808.
50. van Gunsteren, W., S. Billeter, I. Tironi. 1996. Biomolecular Simulation: The GROMOS 96 Manual and User Guide. Vdf, Zürich, Switzerland.
51. Oostenbrink, C., A. Villa, W. F. van Gunsteren. 2004. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 25:1656-1676.
52. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
53. Lee, J., and W. Im. 2008. Transmembrane helix tilting: insights from calculating the potential of mean force. Phys. Rev. Lett. 100:018103.
54. Chothia, C. M. Levitt, and D. Richardson. 1981. Helix to helix packing in proteins. J. Mol. Biol. 145:215-250.
55. Lee, J., and W. Im. 2008. Role of hydrogen bonding and helix-lipid interactions in transmembrane helix association. J. Am. Chem. Soc. 130:6456-6462.
56. Smith, S. O., D. Song, S. Aimoto. 2001. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry. 40:6553-6558.
57. Fleming, K. G. 2002. Standardizing the free energy change of transmembrane helix-helix interactions. J. Mol. Biol. 323:563-571.
58. Gilson, M. K., J. A. Given., J. A. McCammon. 1997. The statisticalthermodynamic basis for computation of binding affinities: a critical review. Biophys. J. 72:1047-1069.
59. Mihailescu, M., and M. K. Gilson. 2004. On the theory of noncovalent binding. Biophys. J. 87:23-36.
60. Chandler, D. 1987. Introduction to Modern Statistical Mechanics. Oxford University Press, Oxford, UK.
61. Fisher, L. E., D. M. Engelman, and J. N. Sturgis. 2003. Effect of detergents on the association of the glycophorin A transmembrane helix. Biophys. J. 85:3097-3105.
62. Fleishman, S. J., J. Schlessinger, and N. Ben-Tal. 2002. A putative molecular-activation switch in the transmembrane domain of erbB2. Proc. Natl, Acad. Sci. USA. 99:15937-15940.
63. Yiannourakou, M., L. Marsella, B. Smit. 2010. Towards anunderstanding of membrane-mediated protein-protein interactions. Faraday Discuss. 144:359-367, discussion 445-481.