A Transmembrane Polar Interaction Is Involved in the Functional Regulation of Integrin αLβ2

Journal of Molecular Biology

Volumn 398, Issue 4, 2010, Pages 569-583

  Vararattanavech, Ardcharaporn ^a   Chng, Choon Peng ^b   Parthasarathy, Krupakar ^a   Tang, Xiao Yan ^a   Torres, Jaume ^a   Tan, Suet Mien ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b INSTITUTE OF HIGH PERFORMANCE COMPUTING   (Singapore)

Author keywords

Affinity regulation; Cell adhesion; Integrins; Protein conformation; Transmembrane domain

Indexed keywords

ALPHALBETA2 INTEGRIN; ALPHAMBETA2 INTEGRIN; ALPHAXBETA2 INTEGRIN; BETA2 INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MEMBRANE LIPID;

ARTICLE; CELL ADHESION; CELL ELONGATION; CELL POLARITY; CELL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROGEN BOND; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE DAMAGE; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTAGENESIS; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SPECIES COMPARISON; WILD TYPE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL LINE; CHEMICAL MODEL; CHEMICAL STRUCTURE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN ANALYSIS; PROTEIN BINDING; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL LINE; HUMANS; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MEMBRANE LIPIDS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SEQUENCE ALIGNMENT;

EID: 77951926371     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.03.027     Document Type: Article

References (69)

1. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
2. Harburger D.S., Calderwood D.A. Integrin signalling at a glance. J. Cell Sci. 2009, 122:159-163.
3. Streuli C.H. Integrins and cell-fate determination. J. Cell Sci. 2009, 122:171-177.
4. Luo B.H., Carman C.V., Springer T.A. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 2007, 25:619-647.
5. Arnaout M.A., Goodman S.L., Xiong J.P. Structure and mechanics of integrin-based cell adhesion. Curr. Opin. Cell Biol. 2007, 19:495-507.
6. Wegener K.L., Campbell I.D. Transmembrane and cytoplasmic domains in integrin activation and protein-protein interactions. Mol. Membr. Biol. 2008, 25:376-387.
7. Gottschalk K.E., Adams P.D., Brunger A.T., Kessler H. Transmembrane signal transduction of the alpha;IIbβ3 integrin. Protein Sci. 2002, 11:1800-1812.
8. Adair B.D., Xiong J.P., Maddock C., Goodman S.L., Arnaout M.A., Yeager M. Three-dimensional EM structure of the ectodomain of integrin αVβ3 in a complex with fibronectin. J. Cell Biol. 2005, 168:1109-1118.
9. Luo B.H., Springer T.A., Takagi J. A specific interface between integrin transmembrane helices and affinity for ligand. PLoS Biol. 2004, 2:776-786.
10. Lau T.L., Kim C., Ginsberg M.H., Ulmer T.S. The structure of the integrin alpha;IIbβ3 transmembrane complex explains integrin transmembrane signalling. EMBO J. 2009, 28:1351-1361.
11. Yang J., Ma Y.Q., Page R.C., Misra S., Plow E.F., Qin J. Structure of an integrin alpha;IIbβ3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc. Natl Acad. Sci. USA 2009, 106:17729-17734.
12. Zhu J., Luo B.H., Barth P., Schonbrun J., Baker D., Springer T.A. The structure of a receptor with two associating transmembrane domains on the cell surface: integrin alpha;IIbβ3. Mol. Cell 2009, 34:234-249.
13. Vararattanavech A., Lin X., Torres J., Tan S.M. Disruption of the integrin αLβ2 transmembrane domain interface by β2 Thr-686 mutation activates αLβ2 and promotes micro-clustering of the αL subunits. J. Biol. Chem. 2009, 284:3239-3249.
14. Kinashi T. Integrin regulation of lymphocyte trafficking: lessons from structural and signaling studies. Adv. Immunol. 2007, 93:185-227.
15. Curran A.R., Engelman D.M. Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Curr. Opin. Struct. Biol. 2003, 13:412-417.
16. Gratkowski H., Lear J.D., DeGrado W.F. Polar side chains drive the association of model transmembrane peptides. Proc. Natl Acad. Sci. USA 2001, 98:880-885.
17. Vararattanavech A., Tang M.L., Li H.Y., Wong C.H., Law S.K., Torres J., Tan S.M. Permissive transmembrane helix heterodimerization is required for the expression of a functional integrin. Biochem. J. 2008, 410:495-502.
18. Robinson M.K., Andrew D., Rosen H., Brown D., Ortlepp S., Stephens P., Butcher E.C. Antibody against the Leu-CAM β chain (CD18) promotes both LFA-1- and CR3-dependent adhesion events. J. Immunol. 1992, 148:1080-1085.
19. Tang M.L., Kong L.S., Law S.K., Tan S.M. Down-regulation of integrin αMβ2 ligand-binding function by the urokinase-type plasminogen activator receptor. Biochem. Biophys. Res. Commun. 2006, 348:1184-1193.
20. Luo B.H., Carman C.V., Takagi J., Springer T.A. Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering. Proc. Natl Acad. Sci. USA 2005, 102:3679-3684.
21. Stephens P., Romer J.T., Spitali M., Shock A., Ortlepp S., Figdor C.G., Robinson M.K. KIM127, an antibody that promotes adhesion, maps to a region of CD18 that includes cysteine-rich repeats. Cell. Adhes. Commun. 1995, 3:375-384.
22. Beglova N., Blacklow S.C., Takagi J., Springer T.A. Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat. Struct. Biol. 2002, 9:282-287.
23. Chigaev A., Buranda T., Dwyer D.C., Prossnitz E.R., Sklar L.A. FRET detection of cellular α4 integrin conformational activation. Biophys. J. 2003, 85:3951-3962.
24. Chigaev A., Waller A., Zwartz G.J., Buranda T., Sklar L.A. Regulation of cell adhesion by affinity and conformational unbending of α4β1 integrin. J. Immunol. 2007, 178:6828-6839.
25. Torres J., Adams P.D., Arkin I.T. Use of a new label, (13)C (18)O, in the determination of a structural model of phospholamban in a lipid bilayer. Spatial restraints resolve the ambiguity arising from interpretations of mutagenesis data. J. Mol. Biol. 2000, 300:677-685.
26. Torres J., Kukol A., Goodman J.M., Arkin I.T. Site-specific examination of secondary structure and orientation determination in membrane proteins: the peptidic (13)C (18)O group as a novel infrared probe. Biopolymers 2001, 59:396-401.
27. Parthasarathy K., Lin X., Tan S.M., Law S.K., Torres J. Transmembrane helices that form two opposite homodimeric interactions: an asparagine scan study of βM and β2 integrins. Protein Sci. 2008, 17:930-938.
28. Torres J., Briggs J.A., Arkin I.T. Multiple site-specific infrared dichroism of CD3-ζ, a transmembrane helix bundle. J. Mol. Biol. 2002, 316:365-374.
29. Parthasarathy K., Ng L., Lin X., Liu D.X., Pervushin K., Gong X., Torres J. Structural flexibility of the pentameric SARS coronavirus envelope protein ion channel. Biophys. J. 2008, 95:39-41.
30. Torres J., Parthasarathy K., Lin X., Saravanan R., Kukol A., Liu D.X. Model of a putative pore: the pentameric α-helical bundle of SARS coronavirus E protein in lipid bilayers. Biophys. J. 2006, 91:938-947.
31. Gan S.W., Ng L., Lin X., Gong X., Torres J. Structure and ion channel activity of the human respiratory syncytial virus (hRSV) small hydrophobic protein transmembrane domain. Protein Sci. 2008, 17:813-820.
32. Baker E.N., Hubbard R.E. Hydrogen bonding in globular proteins. Prog. Biophys. Mol. Biol. 1984, 44:97-179.
33. Lin X., Tan S.M., Law S.K., Torres J. Unambiguous prediction of human integrin transmembrane heterodimer interactions using only homologous sequences. Proteins 2006, 65:274-279.
34. Wegener K.L., Partridge A.W., Han J., Pickford A.R., Liddington R.C., Ginsberg M.H., Campbell I.D. Structural basis of integrin activation by talin. Cell 2007, 128:171-182.
35. Anthis N.J., Wegener K.L., Ye F., Kim C., Goult B.T., Lowe E.D., et al. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 2009, 284:36700-36710.
36. Shaw J.M., Al-Shamkhani A., Boxer L.A., Buckley C.D., Dodds A.W., Klein N., et al. Characterization of four CD18 mutants in leucocyte adhesion deficient (LAD) patients with differential capacities to support expression and function of the CD11/CD18 integrins LFA-1, Mac-1 and p150,95. Clin. Exp. Immunol. 2001, 126:311-318.
37. Weber K.S., York M.R., Springer T.A., Klickstein L.B. Characterization of lymphocyte function-associated antigen 1 (LFA-1)-deficient T cell lines: the αL and β2 subunits are interdependent for cell surface expression. J. Immunol. 1997, 158:273-279.
38. Semmrich M., Smith A., Feterowski C., Beer S., Engelhardt B., Busch D.H., et al. Importance of integrin LFA-1 deactivation for the generation of immune responses. J. Exp. Med. 2005, 201:1987-1998.
39. Lear J.D., Gratkowski H., Adamian L., Liang J., DeGrado W.F. Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry 2003, 42:6400-6407.
40. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 2000, 7:154-160.
41. Zhou F.X., Merianos H.J., Brunger A.T., Engelman D.M. Polar residues drive association of polyleucine transmembrane helices. Proc. Natl Acad. Sci. USA 2001, 98:2250-2255.
42. Choma C., Gratkowski H., Lear J.D., DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 2000, 7:161-166.
43. Bhunia A., Tang X.Y., Mohanram H., Tan S.M., Bhattacharjya S. NMR solution conformations and interactions of integrin αLβ2 cytoplasmic tails. J. Biol. Chem. 2009, 284:3873-3884.
44. Wright S.D., Rao P.E., Van Voorhis W.C., Craigmyle L.S., Iida K., Talle M.A., et al. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc. Natl Acad. Sci. USA 1983, 80:5699-5703.
45. Walters S.E., Tang R.H., Cheng M., Tan S.M., Law S.K. Differential activation of LFA-1 and Mac-1 ligand binding domains. Biochem. Biophys. Res. Commun. 2005, 337:142-148.
46. Tan S.M., Hyland R.H., Al-Shamkhani A., Douglass W.A., Shaw J.M., Law S.K. Effect of integrin β2 subunit truncations on LFA-1 (CD11a/CD18) and Mac-1 (CD11b/CD18) assembly, surface expression, and function. J. Immunol. 2000, 165:2574-2581.
47. Barclay A.N., Brown M.H., Law S.K., McKnight A.J., Tomlinson M.G., van der Merwe P.A. The Leucocyte Antigen Facts Book 1997, 2-613. Academic Press, London, UK. 2nd edit.
48. Tang X.Y., Li Y.F., Tan S.M. Intercellular adhesion molecule-3 binding of integrin αLβ2 requires both extension and opening of the integrin headpiece. J. Immunol. 2008, 180:4793-4804.
49. van der Spoel D. GROMACS: fast, flexible, and free. J. Comput. Chem. 2005, 26:1701-1718.
50. Hess B., Kutzner C., van der Spoel D., Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 2008, 4:435-447.
51. Tieleman D.P., Berendsen H.J.C. Molecular dynamic simulations of a fully hydrated dipalmitoylphosphatidylcholine bilayer with different macroscopic boundary conditions and parameters. J. Chem. Phys. 1996, 105:4871-4880.
52. Kandt C., Ash W.L., Tieleman D.P. Setting up and running molecular dynamics simulations of membrane proteins. Methods 2007, 41:475-488.
53. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., Hermans J. Intermolecular Forces 1981, Riedel Publishing Company, Dordrecht, The Netherlands. 1st edit. B. Pullman (Ed.).
54. Berger O., Edholm O., Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 1997, 72:2002-2013.
55. Essmann U.E.A. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103:8577-8593.
56. Bussi G., Donadio D., Parrinello M. Canonical sampling through velocity rescaling. J. Chem. Phys. 2007, 126:141011-141017.
57. Berendsen H.J.C., Postma J.P.M., van G.W.F., Dinola A., Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81:3684-3690.
58. Nose S.A. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 1984, 52:255-268.
59. Hoover W.G. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A 1985, 1695-1697.
60. Parrinello M., Rahman A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 1981, 103:8577-8593.
61. Hess B., Bekker H., Berendsen H.J.C., Fraaijie J.G.E.M. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 1997, 18:1463-1472.
62. Hess B. A parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput. 2008, 4:116-122.
63. Miyamoto S., Kollman P.A. SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 1992, 13:952-956.
64. Humphrey W., Dalke A., Schulten K. VMD: Visual Molecular Dynamics. J. Mol. Graphics 1996, 14:33-38.
65. Feig M., Karanicolas J., Brooks C.L. MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology. J. Mol. Graphics Modell. 2004, 22:377-395.
66. Marsh D. Quantitation of secondary structure in ATR infrared spectroscopy. Biophys. J. 1999, 77:2630-2637.
67. McGhie E.J., Hume P.J., Hayward R.D., Torres J., Koronakis V. Topology of the Salmonella invasion protein SipB in a model bilayer. Mol. Microbiol. 2002, 44:1309-1321.
68. Adams L.F., Visick J.E., Whiteley H.R. A 20-kilodalton protein is required for efficient production of the Bacillus thuringiensis subsp. israelensis 27-kilodalton crystal protein in Escherichia coli. J. Bacteriol. 1989, 171:521-530.
69. Arbely E., Khattari Z., Brotons G., Akkawi M., Salditt T., Arkin I.T. A highly unusual palindromic transmembrane helical hairpin formed by SARS coronavirus E protein. J. Mol. Biol. 2004, 341:769-779.