Variation in One Residue Associated with the Metal Ion-Dependent Adhesion Site Regulates αIIbβ3 Integrin Ligand Binding Affinity

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Raborn, Joel ^a,e   Fu, Ting ^b,c,d   Wu, Xue ^b,c   Xiu, Zhilong ^c   Li, Guohui ^b   Luo, Bing Hao ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^c DALIAN UNIVERSITY OF TECHNOLOGY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^e UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2B BETA3 INTEGRIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENTROPY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LIGAND BINDING; METAL ION DEPENDENT ADHESION SITE; MOLECULAR DYNAMICS; MUTATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASPARTIC ACID; BINDING SITES; BINDING, COMPETITIVE; CELL ADHESION; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; LIGANDS; METALS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84885159441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076793     Document Type: Article

References (51)

1. Hynes RO, (2002) Integrins: bi-directional, allosteric, signalling machines. Cell 110: 673-687. doi:10.1016/S0092-8674(02)00971-6. PubMed: 12297042.
2. Luo BH, Carman CV, Springer TA, (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25: 619-647. doi:10.1146/annurev.immunol.25.022106.141618. PubMed: 17201681.
3. Mould AP, Akiyama SK, Humphries MJ, (1995) Regulation of integrin a5b1-fibronectin interactions by divalent cations. J Biol Chem 270: 26270-26277. doi:10.1074/jbc.270.44.26270. PubMed: 7592835.
4. Chen JF, Salas A, Springer TA, (2003) Bistable regulation of integrin adhesiveness by a bipolar metal ion cluster. Nat Struct Biol 10: 995-1001. doi:10.1038/nsb1011. PubMed: 14608374.
5. Mould AP, Symonds EJ, Buckley PA, Grossmann JG, McEwan PA, et al. (2003) Structure of an integrin-ligand complex deduced from solution X-ray scattering and site-directed mutagenesis. J Biol Chem 278: 39993-39999. doi:10.1074/jbc.M304627200. PubMed: 12871973.
6. Chen JF, Takagi J, Xie C, Xiao T, Luo B-H, et al. (2004) The relative influence of metal ion binding sites in the I-like domain and the interface with the hybrid domain on rolling and firm adhesion by integrin a4b7. J Biol Chem 279: 55556-55561. doi:10.1074/jbc.M407773200. PubMed: 15448154.
7. Lee J-O, Rieu P, Arnaout MA, Liddington R, (1995) Crystal structure of the A domain from the a subunit of integrin CR3 (CD11b/CD18). Cell 80: 631-638. doi:10.1016/0092-8674(95)90517-0. PubMed: 7867070.
8. Tozer EC, Liddington RC, Sutcliffe MJ, Smeeton AH, Loftus JC, (1996) Ligand binding to integrin aIIbb3 is dependent on a MIDAS-like domain in the 3 subunit. J Biol Chem 271: 21978-21984. doi:10.1074/jbc.271.36.21978. PubMed: 8703003.
9. Hynes RO, Zhao Q, (2000) The evolution of cell adhesion. J Cell Biol 150: F89-F96. doi:10.1083/jcb.150.1.89. PubMed: 10908592.
10. Harding MM, (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 57: 401-411. doi:10.1107/S0907444900019168. PubMed: 11223517.
11. Cierniewska-Cieslak A, Cierniewski CS, Blecka K, Papierak M, Michalec L, et al. (2002) Identification and characterization of two cation binding sites in the integrin {beta}{sub}3 subunit. J Biol Chem 277: 11126-11134. doi:10.1074/jbc.M112388200. PubMed: 11796735.
12. Whittaker CA, Hynes RO, (2002) Essay from the Genome Annotation Series: Distribution and Evolution of the von Willebrand/Integrin A domain: a widely dispersed domain with roles in cell adhesion and elsewhere. Mol Cell Biol 13: 3369-3387. doi:10.1091/mbc.E02-05-0259.
13. Xiong JP, Stehle T, Zhang R, Joachimiak A, Frech M, et al. (2002) Crystal structure of the extracellular segment of integrin aVb3 in complex with an Arg-Gly-Asp ligand. Science 296: 151-155. doi:10.1126/science.1069040. PubMed: 11884718.
14. Mould AP, Barton SJ, Askari JA, Craig SE, Humphries MJ, (2003) Role of ADMIDAS cation-binding site in ligand recognition by integrin a5b1. J Biol Chem 278: 51622-51629. doi:10.1074/jbc.M306655200. PubMed: 14532288.
15. Shimaoka M, Xiao T, Liu J-H, Yang Y, Dong Y, et al. (2003) Structures of the aL I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112: 99-111. doi:10.1016/S0092-8674(02)01257-6. PubMed: 12526797.
16. Xiao T, Takagi J, Wang J-h, Coller BS, Springer TA, (2004) Structural basis for allostery in integrins and binding of fibrinogen-mimetic therapeutics. Nature 432: 59-67. doi:10.1038/nature02976. PubMed: 15378069.
17. Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, et al. (2008) Structure of a Complete Integrin Ectodomain in a Physiologic Resting State and Activation and Deactivation by Applied Forces. Mol Cell 32: 849-861. doi:10.1016/j.molcel.2008.11.018. PubMed: 19111664.
18. Goodman TG, Bajt ML, (1996) Identifying the putative metal ion-dependent adhesion site in the b2 (CD18) subunit required for aLb2 and aMb2 ligand interactions. J Biol Chem 271: 23729-23736. doi:10.1074/jbc.271.39.23729. PubMed: 8798597.
19. Lin ECK, Ratnikov BI, Tsai PM, Gonzalez ER, McDonald S, et al. (1997) Evidence that the integrin b3 and b5 subunits contain a metal ion-dependent adhesion site-like motif but lack an I domain. J Biol Chem 272: 14236-14243. doi:10.1074/jbc.272.22.14236. PubMed: 9162056.
20. Valdramidou D, Humphries MJ, Mould AP, (2008) Distinct Roles of β1 Metal Ion-dependent Adhesion Site (MIDAS), Adjacent to MIDAS (ADMIDAS), and Ligand-associated Metal-binding Site (LIMBS) Cation-binding Sites in Ligand Recognition by Integrin α2β1. J Biol Chem 283: 32704-32714. doi:10.1074/jbc.M802066200. PubMed: 18820259.
21. Chen JF, Yang W, Kim M, Carman CV, Springer TA, (2006) Regulation of outside-in signaling by the b2 I domain of integrin aLb2. Proc Natl Acad Sci U S A 103: 13062-13067. doi:10.1073/pnas.0605666103. PubMed: 16920795.
22. Murcia M, Jirouskova M, Jihong L, Coller BS, Filizola M, (2008) Functional and computational studies of the ligand-associated metal binding site of β3 integrins. Proteins 71: 1779-1791. doi:10.1002/prot.21859. PubMed: 18175315.
23. Salas A, Shimaoka M, Kogan AN, Harwood C, von Andrian UH, et al. (2004) Rolling adhesion through an extended conformation of integrin aLb2 and relation to a I and b I-like domain interaction. Immunity 20: 393-406. doi:10.1016/S1074-7613(04)00082-2. PubMed: 15084269.
24. Kamata T, Tieu KK, Tarui T, Puzon-McLaughlin W, Hogg N, et al. (2002) The role of the CPNKEKEC sequence in the beta(2) subunit I domain in regulation of integrin alpha (L)beta(2) (LFA-1). J Immunol 168: 2296-2301.
25. Raborn J, Wang W, Luo BH, (2011) Regulation of Integrin αIIbβ3 Ligand Binding and Signaling by the Metal Ion Binding Sites in the β I Domain. Biochemistry 50: 2084-2091. doi:10.1021/bi2000092. PubMed: 21309594.
26. 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: 599-611. doi:10.1016/S0092-8674(02)00935-2. PubMed: 12230977.
27. Luo B-H, Takagi J, Springer TA, (2004) Locking the b3 integrin I-like domain into high and low affinity conformations with disulfides. J Biol Chem 279: 10215-10221. PubMed: 14681220.
28. Luo BH, Karanicolas J, Harmacek LD, Baker D, Springer TA, (2009) Rationally Designed Integrin b3 Mutants Stabilized in the High Affinity Conformation. J Biol Chem 284: 3917-3924. PubMed: 19019827.
29. Yang W, Shimaoka M, Chen JF, Springer TA, (2004) Activation of integrin b subunit I-like domains by one-turn C-terminal a-helix deletions. Proc Natl Acad Sci U S A 101: 2333-2338. doi:10.1073/pnas.0307291101. PubMed: 14983010.
30. Bajt ML, Loftus JC, (1994) Mutation of a ligand binding domain of b3 integrin: integral role of oxygenated residues in aIIbb3 (GPIIb-IIIa) receptor function. J Biol Chem 269: 20913-20919. PubMed: 7520434.
31. Raborn J, Luo BH, (2012) Mutagenesis studies of the β I domain metal ion binding sites on integrin αVβ3 ligand binding affinity. J Cell Biochem 113: 1190-1197. doi:10.1002/jcb.23448. PubMed: 22095620.
32. Xu B, Shen H, Zhu X, Li G, (2011) Fast and Accurate Computation Scheme for Vibrational Entropy of Proteins. J Comput Chem 32: 3188-3193. doi:10.1002/jcc.21900. PubMed: 21953554.
33. Wu J, Xia Z, Shen H, Li G, Ren P, (2011) Gay-Berne and Electrostatic Multipole based Coarse Grained Model and Application with Polyalanine in Implicit Solvent. J Chem Phys 135: 155104. doi:10.1063/1.3651626. PubMed: 22029338.
34. Xu B, Schones DE, Wang Y, Liang H, Li G, (2013) A Structural-Based Strategy for Recognition of Transcription Factor Binding Sites. PLOS ONE 8: e52460. doi:10.1371/journal.pone.0052460. PubMed: 23320072.
35. Wang J, Zhu W, Li G, Hansmann UH, (2011) Velocity-scaling optimized replica exchange molecular dynamics of proteins in a hybrid explicit/implicit solvent. J Chem Phys 135: 084115. doi:10.1063/1.3624401. PubMed: 21895167.
36. Zhang Y, Shen H, Zhang M, Li G, (2013) Exploring the Proton Conductance and Drug Resistance of BM2 Channel through Molecular Dynamics Simulations and Free Energy Calculations at Different pH Conditions. J Phys Chem B 117: 982-988. doi:10.1021/jp309682t. PubMed: 23286443.
37. Shen H, Sun H, Li G, (2012) What Is the Role of Motif D in the Nucleotide Incorporation Catalyzed by the RNA-dependent RNA Polymerase from Poliovirus? PLOS Comput Biol 8: e1002851. PubMed: 23300428.
38. Luo B-H, Springer TA, Takagi J, (2003) Stabilizing the open conformation of the integrin headpiece with a glycan wedge increases affinity for ligand. Proc Natl Acad Sci U S A 100: 2403-2408. doi:10.1073/pnas.0438060100. PubMed: 12604783.
39. Zhu J, Carman CV, Kim M, Shimaoka M, Springer TA, et al. (2007) Requirement of α and β subunit transmembrane helix separation for integrin outside-in signaling. Blood 110: 2475-2483. doi:10.1182/blood-2007-03-080077. PubMed: 17615290.
40. Springer TA, Zhu J, Xiao T, (2008) Structural basis for distinctive recognition of fibrinogen by the platelet integrin aIIbb3. J Cell Biol 182: 791-800. doi:10.1083/jcb.200801146. PubMed: 18710925.
41. Case D, Darden T, Cheatham T III, Simmerling C, Wang J, et al. (2008) AMBER10. San Francisco, CA: University of California.
42. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24: 1999-2012. doi:10.1002/jcc.10349. PubMed: 14531054.
43. Bradbrook G, Gleichmann T, Harrop S, Habash J, Raftery J, et al. (1998) X-ray and molecular dynamics studies of concanavalin-A glucoside and mannoside complexes- Relating structure to thermodynamics of binding. J Chem Soc Faraday Trans 94: 1603-1611. doi:10.1039/a800429c.
44. Jorgensen W, Chandrasekhar J, Madura J, Impey R, Klein M, (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935. doi:10.1063/1.445869.
45. Ryckaert J, Ciccotti G, Berendsen H, (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23: 327-341. doi:10.1016/0021-9991(77)90098-5.
46. Essman U, Perela L, Berkowitz M, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8592. doi:10.1063/1.470117.
47. Xie C, Zhu J, Chen X, Mi L, Nishida N, et al. (2010) Structure of an integrin with an alphaI domain, complement receptor type 4. EMBO J 29: 666-679. doi:10.1038/emboj.2009.367. PubMed: 20033057.
48. Wang W, Fu G, Luo B-H, (2010) Dissociation of the α-Subunit Calf-2 Domain and the β-Subunit I-EGF4 Domain in Integrin Activation and Signaling. Biochemistry 49: 10158-10165. doi:10.1021/bi101462h. PubMed: 21038860.
49. Amadei A, Linssen AB, Berendsen HJ, (1993) Essential dynamics of proteins. Proteins 17: 412-425. doi:10.1002/prot.340170408. PubMed: 8108382.
50. McEver RP, Zhu C, (2010) Rolling Cell Adhesion. Annu Rev Cell Dev Biol 26: 363-396. doi:10.1146/annurev.cellbio.042308.113238. PubMed: 19575676.
51. Salas A, Shimaoka M, Phan U, Kim M, Springer TA, (2006) Transition from rolling to firm adhesion can be mimicked by extension of integrin aLb2 in an intermediate-affinity state. J Biol Chem 281: 10876-10882. doi:10.1074/jbc.M512472200. PubMed: 16505487.