An internal ligand-bound, metastable state of a leukocyte integrin, αXβ2

Journal of Cell Biology

Volumn 203, Issue 4, 2013, Pages 629-642

  Sen, Mehmet ^a,b   Yuki, Koichi ^a,b   Springer, Timothy A ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; BETA3 INTEGRIN; CD18 ANTIGEN;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; LEUKOCYTE; LEUKOCYTE ADHERENCE; LIGAND BINDING; MOTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; UPREGULATION; VASCULARIZATION;

EID: 84890230123     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201308083     Document Type: Article

References (44)

1. Adams, P.D., P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221. http://dx.doi.org/10.1107/S0907444909052925
2. Alonso, J.L., M. Essafi, J.P. Xiong, T. Stehle, and M.A. Arnaout. 2002. Does the integrin alphaA domain act as a ligand for its betaA domain? Curr. Biol. 12:R340-R342. http://dx.doi.org/10.1016/S0960-9822(02)00852-7
3. Astrof, N.S., A. Salas, M. Shimaoka, J.F. Chen, and T.A. Springer. 2006. Importance of force linkage in mechanochemistry of adhesion receptors. Biochemistry. 45:15020-15028. http://dx.doi.org/10.1021/bi061566o
4. Bilsland, C.A.G., M.S. Diamond, and T.A. Springer. 1994. The leukocyte integrin p150,95 (CD11c/CD18) as a receptor for iC3b. Activation by a heterologous β subunit and localization of a ligand recognition site to the I domain. J. Immunol. 152:4582-4589.
5. Chen, X., C. Xie, N. Nishida, Z. Li, T. Walz, and T.A. Springer. 2010. Requirement of open headpiece conformation for activation of leukocyte integrin alphaXbeta2. Proc. Natl. Acad. Sci. USA. 107:14727-14732. http://dx.doi.org/10.1073/pnas.1008663107
6. Chen, X., Y. Yu, L.-Z. Mi, T. Walz, and T.A. Springer. 2012. Molecular basis for complement recognition by integrin αXβ2. Proc. Natl. Acad. Sci. USA. 109:4586-4591. http://dx.doi.org/10.1073/pnas.1202051109
7. Davis, I.W., A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, X. Wang, L.W. Murray, W.B. Arendall III, J. Snoeyink, J.S. Richardson, and D.C. Richardson. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35(Web Server issue):W375-W383. http://dx.doi.org/10.1093/nar/gkm216
8. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158
9. Emsley, J., C.G. Knight, R.W. Farndale, M.J. Barnes, and R.C. Liddington. 2000. Structural basis of collagen recognition by integrin α2β1. Cell. 101:47-56. http://dx.doi.org/10.1016/S0092-8674(00)80622-4
10. Gahmberg, C.G., S.C. Fagerholm, S.M. Nurmi, T. Chavakis, S. Marchesan, and M. Grönholm. 2009. Regulation of integrin activity and signalling. Biochim. Biophys. Acta. 1790:431-444. http://dx.doi.org/10.1016/j.bbagen.2009.03.007
11. Huth, J.R., E.T. Olejniczak, R. Mendoza, H. Liang, E.A. Harris, M.L. Lupher Jr., A.E. Wilson, S.W. Fesik, and D.E. Staunton. 2000. NMR and mutagenesis evidence for an I domain allosteric site that regulates lymphocyte function-associated antigen 1 ligand binding. Proc. Natl. Acad. Sci. USA. 97:5231-5236. http://dx.doi.org/10.1073/pnas.97.10.5231
12. Kabsch, W. 2001. Chapter 25.2.9 XDS. In International Tables for Crystallography, Volume F: Crystallography of Biological Macromolecules. M.G. Rossmann and E.V. Arnold, editors. Kluwer Academic Publishers, Dordrecht. 730-734.
13. Karplus, P.A., and K. Diederichs. 2012. Linking crystallographic model and data quality. Science. 336:1030-1033. http://dx.doi.org/10.1126/science.1218231
14. Kuhlman, B., G. Dantas, G.C. Ireton, G. Varani, B.L. Stoddard, and D. Baker. 2003. Design of a novel globular protein fold with atomic-level accuracy. Science. 302:1364-1368. http://dx.doi.org/10.1126/science.1089427
15. Lee, J.-O., L.A. Bankston, M.A. Arnaout, and R.C. Liddington. 1995. Two conformations of the integrin A-domain (I-domain): a pathway for activation? Structure. 3:1333-1340. http://dx.doi.org/10.1016/S0969-2126 (01)00271-4
16. Lu, C., M. Ferzly, J. Takagi, and T.A. Springer. 2001. Epitope mapping of antibodies to the C-terminal region of the integrin β2 subunit reveals regions that become exposed upon receptor activation. J. Immunol. 166:5629-5637.
17. Luo, B.-H., C.V. Carman, and T.A. Springer. 2007. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25:619-647. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141618
18. McCoy, A.J., R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read. 2007. Phaser crystallographic software. J. Appl. Cryst. 40:658-674. http://dx.doi.org/10.1107/S0021889807021206
19. Mi, L.Z., M.J. Grey, N. Nishida, T. Walz, C. Lu, and T.A. Springer. 2008. Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs. Biochemistry. 47:10314-10323. http://dx.doi.org/10.1021/bi801006s
20. Muller, N., P. Girard, D.L. Hacker, M. Jordan, and F.M. Wurm. 2005. Orbital shaker technology for the cultivation of mammalian cells in suspension. Biotechnol. Bioeng. 89:400-406. http://dx.doi.org/10.1002/bit.20358
21. Nagae, M., S. Re, E. Mihara, T. Nogi, Y. Sugita, and J. Takagi. 2012. Crystal structure of α5β1 integrin ectodomain: atomic details of the fibronectin receptor. J. Cell Biol. 197:131-140. http://dx.doi.org/10.1083/jcb.201111077
22. Nishida, N., C. Xie, M. Shimaoka, Y. Cheng, T. Walz, and T.A. Springer. 2006. Activation of leukocyte β2 integrins by conversion from bent to extended conformations. Immunity. 25:583-594. http://dx.doi.org/10.1016/j.immuni.2006.07.016
23. O'Shea, E.K., K.J. Lumb, and P.S. Kim. 1993. Peptide 'Velcro': design of a heterodimeric coiled coil. Curr. Biol. 3:658-667. http://dx.doi.org/10.1016/0960-9822(93)90063-T
24. Reeves, P.J., N. Callewaert, R. Contreras, and H.G. Khorana. 2002. Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. USA. 99:13419-13424. http://dx.doi.org/10.1073/pnas.212519299
25. Salas, A., M. Shimaoka, A.N. Kogan, C. Harwood, U.H. von Andrian, and T.A. Springer. 2004. Rolling adhesion through an extended conformation of integrin alphaLbeta2 and relation to α I and β I-like domain interaction. Immunity. 20:393-406. http://dx.doi.org/10.1016/S1074-7613(04)00082-2
26. Schürpf, T., and T.A. Springer. 2011. Regulation of integrin affinity on cell surfaces. EMBO J. 30:4712-4727. http://dx.doi.org/10.1038/emboj.2011.333
27. Shamri, R., V. Grabovsky, J.M. Gauguet, S. Feigelson, E. Manevich, W. Kolanus, M.K. Robinson, D.E. Staunton, U.H. von Andrian, and R. Alon. 2005. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat. Immunol. 6:497-506. http://dx.doi.org/10.1038/ni1194
28. Shimaoka, M., J. Takagi, and T.A. Springer. 2002. Conformational regulation of integrin structure and function. Annu. Rev. Biophys. Biomol. Struct. 31:485-516. http://dx.doi.org/10.1146/annurev.biophys.31.101101.140922
29. Shimaoka, M., A. Salas, W. Yang, G. Weitz-Schmidt, and T.A. Springer. 2003a. Small molecule integrin antagonists that bind to the β2 subunit I-like domain and activate signals in one direction and block them in the other. Immunity. 19:391-402. http://dx.doi.org/10.1016/S1074-7613(03)00238-3
30. Shimaoka, M., T. Xiao, J.-H. Liu, Y. Yang, Y. Dong, C.-D. Jun, A. McCormack, R. Zhang, A. Joachimiak, J. Takagi, et al. 2003b. Structures of the α L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell. 112:99-111. http://dx.doi.org/10.1016/S0092-8674(02)01257-6
31. Springer, T.A., and M.L. Dustin. 2012. Integrin inside-out signaling and the immunological synapse. Curr. Opin. Cell Biol. 24:107-115. http://dx.doi.org/10.1016/j.ceb.2011.10.004
32. 3. J. Cell Biol. 182:791-800. http://dx.doi.org/10.1083/jcb.200801146
33. Takagi, J., H.P. Erickson, and T.A. Springer. 2001. C-terminal opening mimics 'inside-out' activation of integrin α5β1. Nat. Struct. Biol. 8:412-416. http://dx.doi.org/10.1038/87569
34. Takagi, J., B.M. Petre, T. Walz, and T.A. Springer. 2002. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell. 110:599-11. http://dx.doi.org/10.1016/S0092-8674(02)00935-2
35. Weitz-Schmidt, G., T. Schürpf, and T.A. Springer. 2011. The C-terminal αI domain linker as a critical structural element in the conformational activation of αI integrins. J. Biol. Chem. 286:42115-42122. http://dx.doi.org/10.1074/jbc.M111.282830
36. Whittaker, C.A., and R.O. Hynes. 2002. Distribution and evolution of the von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 13:3369-3387. http://dx.doi.org/10.1091/mbc.E02-05-0259
37. Xiao, T., J. Takagi, B.S. Coller, J.H. Wang, and T.A. Springer. 2004. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature. 432:59-67. http://dx.doi.org/10.1038/nature02976
38. Xie, C., J. Zhu, X. Chen, L. Mi, N. Nishida, and T.A. Springer. 2010. Structure of an integrin with an alphaI domain, complement receptor type 4. EMBO J. 29:666-679. http://dx.doi.org/10.1038/emboj.2009.367
39. Xiong, J.P., T. Stehle, R. Zhang, A. Joachimiak, M. Frech, S.L. Goodman, and M.A. Arnaout. 2002. Crystal structure of the extracellular segment of integrin αVβ3 in complex with an Arg-Gly-Asp ligand. Science. 296:151-155. http://dx.doi.org/10.1126/science.1069040
40. Yang, W., M. Shimaoka, A. Salas, J. Takagi, and T.A. Springer. 2004. Intersubunit signal transmission in integrins by a receptor-like interaction with a pull spring. Proc. Natl. Acad. Sci. USA. 101:2906-2911. http://dx.doi.org/10.1073/pnas.0307340101
41. Yu, Y., J. Zhu, L.Z. Mi, T. Walz, H. Sun, J.-F. Chen, and T.A. Springer. 2012. Structural specializations of α4β7, an integrin that mediates rolling adhesion. J. Cell Biol. 196:131-146. http://dx.doi.org/10.1083/jcb.201110023
42. Zang, Q., and T.A. Springer. 2001. Amino acid residues in the PSI domain and cysteine-rich repeats of the integrin β2 subunit that restrain activation of the integrin α(X)β(2). J. Biol. Chem. 276:6922-6929. http://dx.doi.org/10.1074/jbc.M005868200
43. Zhu, J., B.H. Luo, T. Xiao, C. Zhang, N. Nishida, and T.A. Springer. 2008. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol. Cell. 32:849-861. http://dx.doi.org/10.1016/j.molcel.2008.11.018
44. Zhu, J., J. Zhu, and T.A. Springer. 2013. Complete integrin headpiece opening in eight steps. J. Cell Biol. 201:1053-1068. http://dx.doi.org/10.1083/jcb.201212037