Annular anionic lipids stabilize the integrin αiIbβ3 Transmembrane Complex

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8283-8293

  Schmidt, Thomas ^a   Suk, Jae Eun ^a   Ye, Feng ^b   Situ, Alan J ^a   Mazumder, Parichita ^a   Ginsberg, Mark H ^b   Ulmer, Tobias S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; LIPIDS;

ANIONIC LIPIDS; DESTABILIZING EFFECT; GENERAL NATURE; INTEGRINS; MEMBRANE PROTEINS; TRANSMEMBRANES;

PROTEINS;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; ALPHA INTEGRIN; ALPHA2 INTEGRIN; AMPHOLYTE; ANIONIC LIPID; ARGININE; FIBROBLAST GROWTH FACTOR RECEPTOR 3; INTEGRIN ALPHA2B BETA3; INTEGRIN RECEPTOR; LIPID; MEMBRANE PROTEIN; NANODISC; UNCLASSIFIED DRUG; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOSERINE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; FIBRINOGEN RECEPTOR; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE;

ALPHA HELIX; ARTICLE; COMPLEX FORMATION; ENTHALPY; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROGEN BOND; LIPID BILAYER; LIPID COMPOSITION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PERSISTENT ORGANIC POLLUTANT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STATIC ELECTRICITY; STOICHIOMETRY; AMINO ACID SEQUENCE; CHEMISTRY; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLSERINES; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY;

EID: 84925832837     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.623504     Document Type: Article

References (58)

1. Marsh, D. (2008) Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta 1778, 1545-1575
2. Palsdottir, H., and Hunte, C. (2004) Lipids in membrane protein structures. Biochim. Biophys. Acta 1666, 2-18
3. Lee, A. G. (2011) Biological membranes: the importance of molecular detail. Trends Biochem. Sci. 36, 493-500
4. von Heijne, G. (1989) Control of topology and mode of assembly of a polytopic membrane-protein by positively charged residues. Nature 341, 456-458
5. van Klompenburg, W., Nilsson, I., von Heijne, G., and de Kruijff, B. (1997) Anionic phospholipids are determinants of membrane protein topology. EMBO J. 16, 4261-4266
6. Bogdanov, M., Xie, J., and Dowhan, W. (2009) Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. J. Biol. Chem. 284, 9637-9641
7. Hughes, P. E., Diaz-Gonzalez, F., Leong, L., Wu, C., McDonald, J. A., Shattil, S. J., and Ginsberg, M. H. (1996) Breaking the integrin hinge: a defined structural constraint regulates integrin signaling. J. Biol. Chem. 271, 6571-6574
8. 3 transmembrane complex explains integrin transmembrane signalling. EMBO J. 28, 1351-1361
9. Hynes, R. O. (2002) Integrins: Bidirectional, allosteric signaling machines. Cell 110, 673-687
10. Bennett, J. S., Berger, B. W., and Billings, P. C. (2009) The structure and function of platelet integrins. J. Thromb. Haemost. 7, 200-205
11. Lau, T.-L., Dua, V., and Ulmer, T. S. (2008) Structure of the integrin αIIb transmembrane segment. J. Biol. Chem. 283, 16162-16168
12. 3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry 47, 4008-4016
13. Pervushin, K., Riek, R., Wider, G., and Wüthrich, K. (1997) Attenuated T-2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371
14. Situ, A. J., Schmidt, T., Mazumder, P., and Ulmer, T. S. (2014) Characterization of membrane protein interactions by isothermal titration calorimetry. J. Mol. Biol. 426, 3670-3680
15. Zhang, Y. L., and Zhang, Z. Y. (1998) Low-affinity binding determined by titration calorimetry using a high-affinity coupling ligand: a thermodynamic study of ligand binding to protein tyrosine phosphatase 1B. Anal. Biochem. 261, 139-148
16. Sigurskjold, B. W. (2000) Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 277, 260-266
17. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179, 131-137
18. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866
19. Tellinghuisen, J. (2008) Isothermal titration calorimetry at very low c. Anal. Biochem. 373, 395-397
20. Fleming, K. G. (2002) Standardizing the free energy change of transmem-brane helix-helix interactions. J. Mol. Biol. 323, 563-571
21. Chou, J. J., Baber, J. L., and Bax, A. (2004) Characterization of phospholipid mixed micelles by translational diffusion. J. Biomol. NMR 29, 299-308
22. Mori, S., Abeygunawardana, C., Johnson, M. O., and van Zijl, P. C. (1995) Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. B 108, 94-98
23. Ulmer, T. S., Campbell, I. D., and Boyd, J. (2004) Amide proton relaxation measurements employing a highly deuterated protein. J. Magn. Reson. 166, 190-201
24. Ye, F., Hu, G., Taylor, D., Ratnikov, B., Bobkov, A. A., McLean, M. A., Sligar, S. G., Taylor, K. A., and Ginsberg, M. H. (2010) Recreation of the terminal events in physiological integrin activation. J. Cell Biol. 188, 157-173
25. 2+ activation when observed by cryoelectron tomography. J. Mol. Biol. 378, 976-986
26. Kouns, W. C., Hadvary, P., Haering, P., and Steiner, B. (1992) Conformational modulation of purified glycoprotein (Gp)-IIb-IIIa allows proteolytic generation of active fragments from either active or inactive GpIIb-IIIa. J. Biol. Chem. 267, 18844-18851
27. Nath, A., Atkins, W. M., and Sligar, S. G. (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46, 2059-2069
28. Denisov, I. G., Grinkova, Y. V., Lazarides, A. A., and Sligar, S. G. (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J. Am. Chem. Soc. 126, 3477-3487
29. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28
30. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
31. Ulmer, T. S. (2010) Structural basis of transmembrane domain interactions in integrin signaling. Cell Adh. Migr. 4, 243-248
32. Gumbart, J., Wang, Y., Aksimentiev, A., Tajkhorshid, E., and Schulten, K. (2005) Molecular dynamics simulations of proteins in lipid bilayers. Curr. Opin. Struct. Biol. 15, 423-431
33. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616
34. Feller, S. E., and MacKerell, A. D. (2000) An improved empirical potential energy function for molecular simulations of phospholipids. J. Phys. Chem. B 104, 7510-7515
35. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593
36. Miyamoto, S., and Kollman, P. A. (1992) Settle: an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem. 13, 952-962
37. Brunger, A., Brooks, C. L., and Karplus, M. (1984) Stochastic boundaryconditions for molecular-dynamics simulations of St2 water. Chem. Phys. Lett. 105, 495-500
38. Suk, J. E., Situ, A. J., and Ulmer, T. S. (2012) Construction of covalent membrane protein complexes and high-throughput selection of membrane mimics. J. Am. Chem. Soc. 134, 9030-9033
39. Kim, C., Lau, T.-L., Ulmer, T. S., and Ginsberg, M. H. (2009) Interactions of platelet integrin α IIb and β3 transmembrane domains in mammalian cell membranes and their role in integrin activation. Blood 113, 4747-4753
40. 3) content. Platelets 7, 195-205
41. Triba, M. N., Warschawski, D. E., and Devaux, P. F. (2005) Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys. J. 88, 1887-1901
42. Zwaal, R. F., Comfurius, P., and van Deenen, L. L. (1977) Membrane asymmetry and blood-coagulation. Nature 268, 358-360
43. Zwaal, R. F., Comfurius, P., and Bevers, E. M. (2004) Scott syndrome, a bleeding disorder caused by defective scrambling of membrane phospholipids. Biochim. Biophys. Acta 1636, 119-128
44. Suzuki, J., Umeda, M., Sims, P. J., and Nagata, S. (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468, 834-838
45. Smyth, S. S., Hillery, C. A., and Parise, L. V. (1992) Fibrinogen binding to purified platelet glycoprotein-IIb-IIIa (Integrin-αIIb-β3) is modulated by lipids. J. Biol. Chem. 267, 15568-15577
46. Conforti, G., Zanetti, A., Pasquali-Ronchetti, I., Quaglino, D., Jr., Neyroz, P., and Dejana, E. (1990) Modulation of vitronectin receptor-binding by membrane lipid-composition. J. Biol. Chem. 265, 4011-4019
47. Zhao, W., Róg, T., Gurtovenko, A. A., Vattulainen, I., and Karttunen, M. (2007) Atomic-scale structure and electrostatics of anionic palmitoyloleoylphosphatidylglycerol lipid bilayers with Na+counterions. Biophys. J. 92, 1114-1124
48. Petrache, H. I., Tristram-Nagle, S., Gawrisch, K., Harries, D., Parsegian, V. A., and Nagle, J. F. (2004) Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt. Biophys. J. 86, 1574-1586
49. Henry, G. D., and Sykes, B. D. (1995) Determination of the rotationaldynamics and pH-dependence of the hydrogen-exchange rates of the arginine guanidino group using NMR-spectroscopy. J. Biomol. NMR 6, 59-66
50. Koldso, H., and Sansom, M. S. (2013) Local lipid reorganization by a transmembrane protein domain. J. Phys. Chem. Lett. 3, 3498-3502
51. Li, E., You, M., and Hristova, K. (2006) FGFR3 dimer stabilization due to a single amino acid pathogenic mutation. J. Mol. Biol. 356, 600-612
52. Kalli, A. C., Hall, B. A., Campbell, I. D., and Sansom, M. S. (2011) A helix heterodimer in a lipid bilayer: prediction of the structure of an integrin transmembrane domain via multiscale simulations. Structure 19, 1477-1484
53. 3. Mol. Cell 34, 234-249
54. Lee, A. G. (2004) How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666, 62-87
55. Powl, A. M., East, J. M., and Lee, A. G. (2005) Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation. Biochemistry 44, 5873-5883
56. + channel Kir2.2 at 3.1 Angstrom resolution. Science 326, 1668-1674
57. 2+ pump: a study on different splicing variants of isoform. J. Biol. Chem. 285, 30779-30791
58. Arkhipov, A., Shan, Y. B., Das, R., Endres, N. F., Eastwood, M. P., Wemmer, D. E., Kuriyan, J., and Shaw, D. E. (2013) Architecture and membrane interactions of the EGF receptor. Cell 152, 557-569