Relating conformation to function in integrin α5 β1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 27, 2016, Pages E3872-E3881

  Su, Yang ^a,b   Xia, Wei ^a,b   Li, Jing ^a,b   Walz, Thomas ^c   Humphries, Martin J ^d   Vestweber, Dietmar ^e   Cabañas, Carlos ^f   Lu, Chafen ^a,b   Springer, Timothy A ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^f CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN F(AB) FRAGMENT 12G10; IMMUNOGLOBULIN F(AB) FRAGMENT 8E3; IMMUNOGLOBULIN F(AB) FRAGMENT 9EG7; IMMUNOGLOBULIN F(AB) FRAGMENT HUTS 4; IMMUNOGLOBULIN F(AB) FRAGMENT N29; IMMUNOGLOBULIN F(AB) FRAGMENT SNAKA51; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 13; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ADSORPTION; ALGORITHM; ALLOSTERISM; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ARTICLE; BINDING SITE; CELL ADHESION; CELL SURFACE; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; EPITOPE MAPPING; GEL FILTRATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; K562 CELL LINE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; STRUCTURE ACTIVITY RELATION;

ESCHERICHIA COLI; FIBRONECTINS; HUMANS; INTEGRIN ALPHA5BETA1; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84977271155     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605074113     Document Type: Article

References (45)

1. Luo B-H, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25:619-647.
2. Xiong J-P, et al. (2001) Crystal structure of the extracellular segment of integrin αVbeta3. Science 294(5541):339-345.
3. Xiong JP, et al. (2002) Crystal structure of the extracellular segment of integrin αVbeta3 in complex with an Arg-Gly-Asp ligand. Science 296(5565):151-155.
4. Zhu J, et al. (2008) Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell 32(6): 849-861.
5. Xie C, et al. (2010) Structure of an integrin with an alphaI domain, complement receptor type 4. EMBO J 29(3):666-679.
6. Dong X, et al. (2012) α(V)β(3) integrin crystal structures and their functional implications. Biochemistry 51(44):8814-8828.
7. Takagi J, Petre BM, Walz T, Springer TA (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110(5): 599-611.
8. Nishida N, et al. (2006) Activation of leukocyte β2 integrins by conversion from bent to extended conformations. Immunity 25(4):583-594.
9. Chen X, et al. (2010) Requirement of open headpiece conformation for activation of leukocyte integrin alphaXbeta2. Proc Natl Acad Sci USA 107(33):14727-14732.
10. Eng ET, Smagghe BJ, Walz T, Springer TA (2011) Intact alphaIIbbeta3 integrin is extended after activation as measured by solution X-ray scattering and electron microscopy. J Biol Chem 286(40):35218-35226.
11. Takagi J, Strokovich K, Springer TA, Walz T (2003) Structure of integrin α5β1 in complex with fibronectin. EMBO J 22(18):4607-4615.
12. Zhu J, Zhu J, Springer TA (2013) Complete integrin headpiece opening in eight steps. J Cell Biol 201(7):1053-1068.
13. Schürpf T, et al. (2012) The RGD finger of Del-1 is a unique structural feature critical for integrin binding. FASEB J 26(8):3412-3420.
14. Luo B-H, Strokovich K, Walz T, Springer TA, Takagi J (2004) Allosteric β1 integrin antibodies that stabilize the low affinity state by preventing the swing-out of the hybrid domain. J Biol Chem 279(26):27466-27471.
15. Mould AP, et al. (2003) Structure of an integrin-ligand complex deduced from solution X-ray scattering and site-directed mutagenesis. J Biol Chem 278(41): 39993-39999.
16. Luque A, et al. (1996) Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355-425) of the common β1 chain. J Biol Chem 271(19):11067-11075.
17. Mould AP, Akiyama SK, Humphries MJ (1996) The inhibitory anti-beta1 integrin monoclonal antibody 13 recognizes an epitope that is attenuated by ligand occupancy. Evidence for allosteric inhibition of integrin function. J Biol Chem 271(34): 20365-20374.
18. Lenter M, et al. (1993) A monoclonal antibody against an activation epitope on mouse integrin chain β1 blocks adhesion of lymphocytes to the endothelial integrin α6β1. Proc Natl Acad Sci USA 90(19):9051-9055.
19. Bazzoni G, Ma L, Blue M-L, Hemler ME (1998) Divalent cations and ligands induce conformational changes that are highly divergent among β1 integrins. J Biol Chem 273(12):6670-6678.
20. Mould AP, et al. (2005) Evidence that monoclonal antibodies directed against the integrin β subunit plexin/semaphorin/integrin domain stimulate function by inducing receptor extension. J Biol Chem 280(6):4238-4246.
21. Mould AP, Garratt AN, Askari JA, Akiyama SK, Humphries MJ (1995) Identification of a novel anti-integrin monoclonal antibody that recognises a ligand-induced binding site epitope on the β1 subunit. FEBS Lett 363(1-2):118-122.
22. Byron A, et al. (2009) Anti-integrin monoclonal antibodies. J Cell Sci 122(Pt 22): 4009-4011.
23. Mould AP, et al. (2002) Integrin activation involves a conformational change in the alpha1 helix of the beta subunit A-domain. J Biol Chem 277(22):19800-19805.
24. Mould AP, et al. (2003) Conformational changes in the integrin βA domain provide a mechanism for signal transduction via hybrid domain movement. J Biol Chem 278(19): 17028-17035.
25. Nagae M, et al. (2012) Crystal structure of α5 β1 integrin ectodomain: Atomic details of the fibronectin receptor. J Cell Biol 197(1):131-140.
26. Takagi J, Erickson HP, Springer TA (2001) C-terminal opening mimics 'inside-out' activation of integrin α5β1. Nat Struct Biol 8(5):412-416.
27. Leahy DJ, Aukhil I, Erickson HP (1996) 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell 84(1):155-164.
28. Schwarzbauer JE, DeSimone DW (2011) Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb Perspect Biol 3(7):1-19.
29. Askari JA, et al. (2010) Focal adhesions are sites of integrin extension. J Cell Biol 188(6):891-903.
30. Clark K, et al. (2005) A specific alpha5beta1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. JCellSci118(Pt 2):291-300.
31. Takada Y, Puzon W (1993) Identification of a regulatory region of integrin β1 subunit using activating and inhibiting antibodies. J Biol Chem 268(23):17597-17601.
32. Mould AP, Garratt AN, Puzon-McLaughlin W, Takada Y, Humphries MJ (1998) Regulation of integrin function: Evidence that bivalent-cation-induced conformational changes lead to the unmasking of ligand-binding sites within integrin alpha5beta1. Biochem J 331(Pt 3):821-828.
33. Bazzoni G, Hemler ME (1998) Are changes in integrin affinity and conformation overemphasized? Trends Biochem Sci 23(1):30-34.
34. Lin FY, Zhu J, Eng ET, Hudson NE, Springer TA (2016) β-Subunit binding is sufficient for ligands to open the integrin αIIbβ3 headpiece. J Biol Chem 291(9):4537-4546.
35. Ohi M, Li Y, Cheng Y, Walz T (2004) Negative staining and image classification-Powerful tools in modern electron microscopy. Biol Proced Online 6:23-34.
36. Xia W, Springer TA (2014) Metal ion and ligand binding of integrin α5 β1 . Proc Natl Acad Sci USA 111(50):17863-17868.
37. Sen M, Yuki K, Springer TA (2013) An internal ligand-bound, metastable state of a leukocyte integrin, αX β2 . J Cell Biol 203(4):629-642.
38. Huang C, Zang Q, Takagi J, Springer TA (2000) Structural and functional studies with antibodies to the integrin β2 subunit. A model for the I-like domain. J Biol Chem 275(28):21514-21524.
39. Lu C, Shimaoka M, Zang Q, Takagi J, Springer TA (2001) Locking in alternate conformations of the integrin alphaLbeta2 I domain with disulfide bonds reveals functional relationships among integrin domains. Proc Natl Acad Sci USA 98(5):2393-2398.
40. Ni H, Li A, Simonsen N, Wilkins JA (1998) Integrin activation by dithiothreitol or Mn2+ induces a ligand-occupied conformation and exposure of a novel NH2-terminal regulatory site on the beta1 integrin chain. J Biol Chem 273(14):7981-7987.
41. Akiyama SK, Yamada SS, Chen WT, Yamada KM (1989) Analysis of fibronectin receptor function with monoclonal antibodies: Roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J Cell Biol 109(2):863-875.
42. Rees I, Langley E, Chiu W, Ludtke SJ (2013) EMEN2: An object oriented database and electronic lab notebook. Microsc Microanal 19(1):1-10.
43. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116(1):190-199.
44. Mi LZ, et al. (2011) Simultaneous visualization of the extracellular and cytoplasmic domains of the epidermal growth factor receptor. Nat Struct Mol Biol 18(9):984-989.
45. Yang Z, Fang J, Chittuluru J, Asturias FJ, Penczek PA (2012) Iterative stable alignment and clustering of 2D transmission electron microscope images. Structure 20(2):237-247.