Integrin activation and structural rearrangement

Immunological Reviews

Volumn 186, Issue , 2002, Pages 141-163

  Takagi, Junichi ^a   Springer, Timothy A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; EPIDERMAL GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; LIGAND;

ALPHA CHAIN; BINDING AFFINITY; BINDING SITE; BLOOD VESSEL INJURY; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DISULFIDE BOND; ELECTRON MICROSCOPY; INFLAMMATION; LEUKOCYTE; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE; ANIMAL; CHEMISTRY; HUMAN; IMMUNOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

ANIMALS; CELL ADHESION; HUMANS; INTEGRINS; LIGANDS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0036697001     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-065X.2002.18613.x     Document Type: Review

References (111)

1. Hynes RO, Integrins. Versatility, modulation, and signaling in cell adhesion. Cell 1992;69:11-25.
2. Humphries MJ. Integrin structure. Biochem Soc Trans 2000;28:311-339.
3. Bennett JS, Vilaire G. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 1979;64:1393-1401
4. Dustin ML, Springer TA. T cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 1989;341:619-624.
5. Diamond MS, Springer TA. The dynamic regulation of integrin adhesiveness. Curr Biol 1994;4:506-517.
6. Loftus JC, Smith JW, Ginsberg MH. Integrin mediated cell adhesion: The extracellular face. J Biol Chem 1994;269:25235-25238.
7. Faull RJ, Kovach NL, Harlan HM, Ginsberg MH. Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: Two mechanisms with divergent biological consequences. J Exp Med 1994;179:1307-1316.
8. Stewart M, Hogg N. Regulation of leukocyte integrin function: Affinity vs. avidity. J Cell Biochem 1996;61:554-561.
9. Bazzoni G, Hemler ME. Are changes in integrin affinity and conformation overemphasized? Trends Biochem Sci 1998;23:30-34.
10. van Kooyk Y, van Vliet SJ, Figdor CG. The actin cytoskeleton regulates LFA-1 ligand binding through avidity rather than affinity changes. J Biol Chem 1999;274:26869-26877.
11. Xiong J-P, et al. Crystal structure of the extracellular segment of integrin αVβ3. Science 2001;294:339-345.
12. Weisel JW, Nagaswami C, Vilaire G, Bennett JS. Examination of the platelet membrane glycoprotein IIb-IIIa complex and its interaction with fibrinogen and other ligands by electron microscopy. J Biol Chem 1992;267:16637-16643.
13. 3. J Biol Chem 1993;268:23087-23092.
14. Takagi J, Erickson HP, Springer TA. C-terminal opening mimics 'inside-out' activation of integrin α5β1. Nat Struct Biol 2001;8:412-416.
15. Takagi J, Debottis DP, Erickson HP, Springer TA. The role of specificity-determining loop of the integrin β-subunit I-like domain in folding, association with the α subunit, and ligand binding. Biochemistry 2002;41:4339-4347.
16. Xiong JP, et al. Crystal structure of the extracellular segment of integrin αVβ3 in complex with an Arg-Gly-Asp ligand. Science 2002;296:151-155.
17. Takagi J, Petre BM, Walz T, Springer TA. A global conformational rearrangement in β3 integrins regulates affinity for ligands. Cell 2002, in press.
18. de Pereda JM, Wiche G, Liddington RC. Crystal structure of a tandem pair of fibronectin type III domains from the cytoplasmic tail of integrin α6β4. EMBO J 1999;18:4087-4095.
19. Beglova N, Blacklow SC, Takagi J, Springer TA. Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat Struct Biol 2002;9:282-287.
20. Springer TA. Folding of the N-terminal, ligand-binding region of integrin α-subunits into a β-propeller domain. Proc Natl Acad Sci USA 1997;94:65-72.
21. Oxvig C, Springer TA. Experimental support for a β-propeller domain in integrin α-sub-units and a calcium binding site on its lower surface. Proc Natl Acad Sci USA 1998;95:4870-4875.
22. 2+-binding β-hairpin loop better resembles integrin sequence motifs than the EF-hand. Cell 2000;102:275-277.
23. Kamata T, Tieu KK, Springer TA, Takada Y. Amino acid residues in the αIIb subunit that are critical for ligand binding to integrin αIIbβ3 are clustered in the β- propeller model. J Biol Chem 2001;276:44275-44283.
24. Michishita M, Videm V, Arnaout MA. A novel divalent cation-binding site in the A domain of the β2 integrin CR3 (CD11b/CD18) is essential for ligand binding. Cell 1993;72:857-867.
25. Diamond MS, Garcia-Aguilar J, Bickford JK, Corbi AL, Springer TA. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J Cell Biol 1993;120:1031-1043.
26. Lee J-O, Rieu P, Arnaout MA, Liddington R. Crystal structure of the A domain from the α subunit of integrin CR3 (CD11b/CD18). Cell 1995;80:631-638.
27. Lu C, Oxvig C, Springer TA. The structure of the β-propeller domain and C-terminal region of the integrin αM subunit. J Biol Chem 1998;273:15138-15147.
28. Bork P, Doerks T, Springer TA, Snel B. Domains in plexins: Links to integrins and transcription factors. Trends Biochem Sci 1999;24:261-263.
29. Calvete JJ, Henschen A, González-Rodríguez J. Assignment of disulphide bonds in human platelet GPIIIa. A disulphide pattern for the β-subunits of the integrin family. Biochem J 1991;274:63-71.
30. Zang Q, Springer TA. Amino acid residues in the PSI domain and cysteine-rich repeats of the integrin β2 subunit that restrain activation of the integrin αXβ2. J Biol Chem 2001;276:6922-6929.
31. Ponting CP, Schultz J, Copley RR, Andrade MA, Bork P. Evolution of domain families. Adv Protein Chem 2000;54:185-244.
32. 2 subunit requires association with the α subunit. Proc Natl Acad Sci USA 1997;94:3156-3161.
33. 2 subunit. Proc Natl Acad Sci USA 1997;94:3162-3167.
34. Puzon-McLaughlin W, Kamata T, Takada Y. Multiple discontinuous ligand-mimetic antibody binding sites define a ligand binding pocket in integrin αIIbβ3. J Biol Chem 2000;275:7795-7802.
35. Zang Q, Lu C, Huang C, Takagi J, Springer TA. The top of the I-like domain of the integrin LFA-1 β subunit contacts the α subunit β-propeller domain near β-sheet 3. J Biol Chem 2000;275:22202-22212.
36. 7 subunit. J Biol Chem 1992;267:7352-7358.
37. Takagi J, Beglova N, Yalamanchili P, Blacklow SC, Springer TA. Definition of EGF-like, closely interacting modules that bear activation epitopes in integrin β subunits. Proc Natl Acad Sci USA 2001;98:11175-11180.
38. Tan S-M, et al. Defining the repeating elements in the cysteine-rich region (CRR) of the CD18 integrin β2 subunit. FEBS Lett 2001;505:27-30.
39. Lu C, Ferzly M, Takagi J, Springer TA. Epitope mapping of antibodies to the C-terminal region of the integrin β2 subunit reveals regions that become exposed upon receptor activation. J Immunol 2001;166:5629-5637.
40. Lee J-O, Bankston LA, Arnaout MA, Liddington RC. Two conformations of the integrin A-domain (I-domain): A pathway for activation? Structure 1995;3:1333-1340.
41. Baldwin ET, et al. Cation binding to the integrin CD11b I domain and activation model assessment. Structure 1998;6:923-935.
42. Lβ2) integrin. Proc Natl Acad Sci USA 1995;92:10277-10281.
43. Qu A, Leahy DJ. The role of the divalent cation in the structure of the I domain from the CD11a/CD18 integrin. Structure 1996;4:931-942.
44. Legge GB, et al. NMR solution structure of the inserted domain of human leukocyte function associated antigen-1. J Mol Biol 2000;295:1251-1264.
45. Kallen J, et al. Structural basis for LFA-1 inhibition upon lovastatin binding to the CD11a I-domain. J Mol Biol 1999;292:1-9.
46. Emsley J, King SL, Bergelson JM, Liddington RC. Crystal structure of the I domain from integrin α2β1. J Biol Chem 1997;272:28512-28517.
47. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC. Structural basis of collagen recognition by integrin α2β1. Cell 2000;101:47-56.
48. Nolte M, Pepinsky KB, Venyaminov SY, Koteliansky V, Gotwals PJ, Karpusas M. Crystal structure of the α1β1 integrin I-domain: Insights into integrin I-domain function. FEBS Lett 1999;452:379-385.
49. Rich RL, et al. Trench-shaped binding sites promote multiple classes of interactions between collagen and the adherence receptors, α1β1 integrin and Staphylococcus aureus Cna MSCRAMM. J Biol Chem 1999;274:24906-24913.
50. Liddington R, Bankston L. The integrin I domain: Crystals, metals and related artefacts. Structure 1998;6:937-938.
51. Staunton DE, Dustin ML, Erickson HP, Springer TA. The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell 1990;61:243-254.
52. Lollo BA, Chan KWH, Hanson EM, Moy VT, Brian AA. Direct evidence for two affinity states for lymphocyte function-associated antigen 1 on activated T cells. J Biol Chem 1993;268:21693-21700.
53. Diamond MS, Springer TA. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J Cell Biol 1993;120:545-556.
54. Oxvig C, Lu C, Springer TA. Conformational changes in tertiary structure near the ligand binding site of an integrin I domain. Proc Natl Acad Sci USA 1999;96:2215-2220.
55. Shimaoka M, Shifman JM, Jing H, Takagi J, Mayo SL, Springer TA. Computational design of an integrin I domain stabilized in the open, high affinity conformation. Nat Struct Biol 2000;7:674-678.
56. Dahiyat BI, Mayo SL. De novo protein design: Fully automated sequence selection. Science 1997;278:82-87.
57. Xiong J-P, Li R, Essafi M, Stehle T, Arnaout MA. An isoleucine-based allosteric switch controls affinity and shape shifting in integrin CD11b A-domain. J Biol Chem 2000;275:38762-38767.
58. Shimaoka M, Lu C, Palframan R, von Andrian UH, Takagi J, Springer TA. Reversibly locking a protein fold in an active conformation with a disulfide bond: Integrin α L I domains with high affinity and antagonist activity in vivo. Proc Natl Acad Sci USA 2001;98:6009-6014.
59. Lu C, Shimaoka M, Ferzly M, Oxvig C, Takagi J, Springer TA. An isolated, surface-expressed I domain of the integrin αLβ2 is sufficient for strong adhesive function when locked in the open conformation with a disulfide. Proc Natl Acad Sci USA 2001;98:2387-2392.
60. Lu C, Shimaoka M, Zang Q, Takagi J, Springer TA. Locking in alternate conformations of the integrin αLβ2, I domain with disulfide bonds reveals functional relationships among integrin domains. Proc Natl Acad Sci USA 2001;98:2393-2398.
61. Labadia ME, Jeanfavre DD, Caviness GO, Morelock MM. Molecular regulation of the interaction between leukocyte function-associated antigen-1 and soluble ICAM-1 by divalent metal cations. J Immunol 1998;161:836-842.
62. Huth JR, et al. NMR and mutagenesis evidence for an I domain allosteric site that regulates lymphocyte function-associated antigen 1 ligand binding. Proc Natl Acad Sci USA 2000;97:5231-5236.
63. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multi-step paradigm. Cell 1994;76:301-314.
64. Bouvard D, et al. Functional consequences of integrin gene mutations in mice. Circ Res 2001;89:211-223.
65. Gottlieb A, et al. Effects of administration of a single dose of a humanized monoclonal antibody to CD11a on the immunobiology and clinical activity of psoriasis. J Am Acad Dermatol 2000;42:428-435.
66. Kelly TA, et al. Cutting edge: a small molecule antagonist of LFA-1-mediated cell adhesion. J Immunol 1999;163:5173-5177.
67. Weitz-Schmidt G, et al. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nat Med 2001;7:687-692.
68. Liu G, et al. Discovery of novel p-arylthio cinnamides as antagonists of leukocyte function-associated antigen-1/intracellular adhesion molecule-1 interaction. 1. Identification of an additional binding pocket based on an anilino diaryl sulfide lead. J Med Chem 2000;43:4025-4040.
69. Last-Barney K, et al. Binding site elucidation of hydantoin-based antagonists of LFA-1 using multidisciplinary technologies: Evidence for the allosteric inhibition of a protein-protein interaction. J Am Chem Soc 2001;123:5643-5650.
70. Woska JR Jr, Shih D, Taqueti VR, Hogg N, Kelly TA, Kishimoto TK. A small-molecule antagonist of LFA-1 blocks a conformational change important for LFA-1 function. J Leukoc Biol 2001;70:329-334.
71. Liu G, et al. Novel p-arylthio cinnamides as antagonists of leukocyte function- associated antigen-1/intracellular adhesion molecule-1 interaction. 2. Mechanism of inhibition and structure-based improvement of pharmaceutical properties. J Med Chem 2001;44:1202-1210.
72. Burdick DJ. Antagonists for treatment of CD11/CD18 adhesion receptor mediated disorders. PCT International Application WO9949856. San Francisco: Genentech; 1999.
73. Fotouhi N, Gillespie P, Guthrie R, Pietranico-Cole S, Yun W. Diaminopropionic acid derivatives. PCT International Application WO0021920. Basel: Hoffmann-La Roche; 1999.
74. Welzenbach K, Hommel U, Weitz-Schmidt G. Small molecule inhibitors induce conformational changes in the I domain and the I-like domain of lymphocyte function-associated antigen-1: Molecular insights into integrin inhibition. J Biol Chem 2002;277:10590-10598.
75. Gadek TR, et al. Generation of an LFA-1 antagonist by the transfer of the ICAM-1 immunoregulatory epitope to a small molecule. Science 2002;295:1086-1089.
76. Zhang L, Plow EF. A discrete site modulates activation of I domains. J Biol Chem 1996;271:29953-29957.
77. Emsley J, Cruz M, Handin R, Liddington R. Crystal structure of the von Willebrand factor A1 domain and implications for the binding of platelet glycoprotein Ib. J Biol Chem 1998;273:10396-10401.
78. Ma Q, Shimaoka M, Lu C, Jing H, Carman CV, Springer TA. Activation induced conformational changes in the I domain region of LFA-1. J Biol Chem 2002;277:10638-10641.
79. Huang C, Springer TA. A binding interface on the I domain of lymphocyte function associated antigen-1 (LFA-1) required for specific interaction with intercellular adhesion molecule 1 (ICAM-1). J Biol Chem 1995;270:19008-19016.
80. Parise LV, Helgerson SL, Steiner B, Nannizzi L, Phillips DR. Synthetic peptides derived from fibrinogen and fibronectin change the conformation of purified platelet glycoprotein IIb-IIIa. J Biol Chem 1987;262:12597-12602.
81. Sims PJ, Ginsberg MH, Plow EF, Shattil SJ. Effect of platelet activation on the conformation of the plasma membrane glycoprotein IIb-IIIa complex. J Biol Chem 1991;266:7345-7352.
82. Honda S, et al. Topography of ligand-induced binding sites, including a novel cation-sensitive epitope (AP5) at the amino terminus, of the human integrin β3 subunit. J Biol Chem 1995;270:11947-11954.
83. Frelinger AL, Lam SCT, Plow EF, Smith MA, Loftus JC, Ginsberg MH. Occupancy of an adhesive glycoprotein receptor modulates expression of an antigenic site involved in cell adhesion. J Biol Chem 1988;263:12397-12402.
84. 3 (glycoprotein IIb-IIIa) alter receptor affinity, specificity, and function. J Biol Chem 1991;266:17106-17111.
85. 1 integrin epitope induced by soluble ligand and manganese, but inhibited by calcium. J Biol Chem 1995;270:25570-25577.
86. 1 integrin-dependent cell adhesion is regulated by a low affinity receptor pool that is conformationally responsive to ligand. J Biol Chem 1995;270:28740-28750.
87. O'Toole TE, et al. Integrin cytoplasmic domains mediate inside-out signal transduction. J Cell Biol 1994;124:1047-1059.
88. Hughes PE, et al. Breaking the integrin hinge. J Biol Chem 1996;271:6571-6574.
89. Hibbs ML, Xu H, Stacker SA, Springer TA. Regulation of adhesion to ICAM-1 by the cytoplasmic domain of LFA-1 integrin beta subunit. Science 1991;251:1611-1613.
90. Lu C, Springer TA. The α subunit cytoplasmic domain regulates the assembly and adhesiveness of integrin lymphocyte function-associated antigen-1 (LFA-1). J Immunol 1997;159:268-278.
91. IIb. Science 1991;254:845-847.
92. Hughes PE, O'Toole TE, Ylanne J, Shattil SJ, Ginsberg MH. The conserved membrane-proximal region of an integrin cytoplasmic domain specifies ligand binding affinity. J Biol Chem 1995;270:12411-12417.
93. 1 integrin. J Exp Med 1993;178:649-660.
94. Kawaguchi S, Hemler ME. Role of the α subunit cytoplamic domain in regulation of adhesive activity mediated by the integrin VLA-2. J Biol Chem 1993;268:16279-16285.
95. Lu C, Takagi J, Springer TA. Association of the membrane-proximal regions of the α and β subunit cytoplasmic domains constrains an integrin in the inactive state. J Biol Chem 2001;276:14642-14648.
96. Nermut MV, Green NM, Eason P, Yamada SS, Yamada KM. Electron microscopy and structural model of human fibronectin receptor. EMBO J 1988;7:4093-4099.
97. 3 subunit. J Biol Chem 1994;269:8754-8761.
98. Mehta RJ, et al. Transmembrane-truncated αVβ3 integrin retains high affinity for ligand binding: Evidence for an 'inside-out' suppressor? Biochem J 1998;330:861-869.
99. Smith JW, Piotrowicz RS, Mathis D. A mechanism for divalent cation regulation of β3-integrins. J Biol Chem 1994;269:960-967.
100. Kohli RM, Takagi J, Walsh CT. The thioesterase domain from a nonribosomal peptide synthetase as a cyclization catalyst for integrin binding peptides. Proc Natl Acad Sci USA 2002;99:1247-1252.
101. Du X, Plow EF, Frelinger AL III, O'Toole TE, Loftus JC, Ginsberg MH. Ligands 'activate' integrin αIIbβ3 (platelet GPIIb-IIIa). Cell 1991;65:409-416.
102. Kashiwagi H, et al. A mutation in the extracellular cysteine-rich repeat region of the β3 subunit activates integrins αIIbβ3 and αVβ3. Blood 1999;93:2559-2568.
103. Huang C, Zang Q, Takagi J, Springer TA. Structural and functional studies with antibodies to the integrin β2 subunit, a model for the I-like domain. J Biol Chem 2000;275:21514-21524.
104. 2+-dependent binding of collagen by the integrin α2 β1 in human platelets. J Biol Chem 2000;275:24560-24564.
105. Knorr R, Dustin ML. The lymphocyte function-associated antigen 1, I domain is a transient binding module for intercellular adhesion molecule (ICAM)-1 and ICAM-1 in hydrodynamic flow. J Exp Med 1997;186:719-730.
106. Plancon S, Morel-Kopp MC, Schaffner-Reckinger E, Chen P, Kieffer N. Green fluorescent protein (GFP) tagged to the cytoplasmic tail of αIIb or β3 allows the expression of a fully functional integrin αIIbβ3. Effect of β3GFP on αlIbβ3 ligand binding. Biochem J 2001;357:529-536.
107. Laukaitis CM, Webb DJ, Donais K, Horwitz AF. Differential dynamics of α 5 integrin, paxillin, and α-actinin during formation and disassembly of adhesions in migrating cells. J Cell Biol 2001;153:1427-1440.
108. Constantin G, et al. Chemokines trigger immediate β2 integrin affinity and mobility changes: Differential regulation and roles in lymphocyte arrest under flow. Immunity 2000;13:759-769.
109. Dustin ML, et al. Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J Biol Chem 1997;272:30889-30898.
110. Carson M. Ribbons. Meth Enzymol 1997;277:493-505.
111. Edwards CP, Fisher KL, Presta LG, Bodary SC. Mapping the intercellular adhesion molecule-1 and -2 binding site on the inserted domain of leukocyte function-associated antigen-1. J Biol Chem 1998;273:28937-28944.