Skip to main content
SpringerLink
Log in

Catch Bonds of Integrin/Ligand Interactions

  • Chapter
  • First Online:
Single-molecule Studies of Proteins

Part of the book series: Biophysics for the Life Sciences ((BIOPHYS,volume 2))

Abstract

Interactions of integrins with ligands mediate cell adhesion in mechanical environments. Their association kinetics can be regulated biochemically by inducing integrin extension and/or opening its headpiece, which enhances on-rate. Their dissociation kinetics can be regulated mechanically by externally applied force. Increasing force prolongs integrin/ligand bond lifetimes, giving rise to counterintuitive catch bonds. Beyond an optimal level, further increase in force shortens bond lifetimes, yielding ordinary slip bonds. Structurally, catch bonds between αLβ2 integrin and its physiological ligand intercellular adhesion molecule 1 can be explained by a force-induced allosteric mechanism that involves the downward movement of the α7-helix of the αA domain but does not require the integrin ectodomain to assume a bent or extended conformation with the hybrid domain in closed or swing-out position.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. Garland Science, New York, NY

    Google Scholar 

  • Alon R, Dustin ML (2007) Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity 26:17–27

    Article  PubMed  CAS  Google Scholar 

  • Arnaout MA, Mahalingam B, Xiong JP (2005) Integrin structure, allostery, and bidirectional signaling. Annu Rev Cell Dev Biol 21:381–410

    Article  PubMed  CAS  Google Scholar 

  • Beglova N, Blacklow SC, Takagi J, Springer TA (2002) Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat Struct Biol 9:282–287

    Article  PubMed  CAS  Google Scholar 

  • Bell GI (1978) Models for the specific adhesion of cells to cells. Science 200:618–627

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Evans EA, McEver RP, Zhu C (2008a) Monitoring receptor-ligand interactions between surfaces by thermal fluctuations. Biophys J 94:694–701

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Zarnitsyna V, Sarangapani K, Huang J, Zhu C (2008b) Measuring receptor ligand binding kinetics on cell surfaces: from adhesion frequency to thermal fluctuation methods. Cellu Mol Bioeng 1:276–288

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Lou J, Zhu C (2010) Forcing switch from short- to intermediate- and long-lived states of the αA domain generates LFA-1/ICAM-1 catch bonds. J Biol Chem 285:35967–35978

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Lou J, Hsin J, Schulten K, Harvey SC, Zhu C (2011) Molecular dynamics simulations of forced unbending of integrin αVβ3. PLoS Comput Biol 7:e1001086

    Article  PubMed  CAS  Google Scholar 

  • Chesla SE, Selvaraj P, Zhu C (1998) Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys J 75:1553–1572

    Article  PubMed  CAS  Google Scholar 

  • Dembo M, Torney DC, Saxman K, Hammer D (1988) The reaction-limited kinetics of membrane-to- surface adhesion and detachment. Proc R Soc Lond B Biol Sci 234:55–83

    Article  PubMed  CAS  Google Scholar 

  • Evans E, Leung A, Heinrich V, Zhu C (2004) Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc Natl Acad Sci USA 101:11281–11286

    Article  PubMed  CAS  Google Scholar 

  • Friedland JC, Lee MH, Boettiger D (2009) Mechanically activated integrin switch controls α5β1 function. Science 323:642–644

    Article  PubMed  CAS  Google Scholar 

  • Guo B, Guilford WH (2006) Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc Natl Acad Sci. USA 103:9844–9849

    Article  PubMed  CAS  Google Scholar 

  • Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687

    Article  PubMed  CAS  Google Scholar 

  • Isacke CM, Horton MA (2000) The adhesion molecule factsbook. Elsevier, Amsterdam

    Google Scholar 

  • Jin M, Andricioaei I, Springer TA (2004) Conversion between three conformational states of integrin I domains with a C-terminal pull spring studied with molecular dynamics. Structure 12:2137–2147

    Article  PubMed  CAS  Google Scholar 

  • Kong F, Garcia A, Mould A, Humphries M, Zhu C (2009) Demonstration of catch bonds between an integrin and its ligand. J Cell Biol 185:1275–1284

    Article  PubMed  CAS  Google Scholar 

  • Le Trong I, Aprikian P, Kidd BA, Forero-Shelton M, Tchesnokova V, Rajagopal P, Rodriguez V, Interlandi G, Klevit R, Vogel V, Stenkamp RE, Sokurenko EV, Thomas WE (2010) Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell 141:645–655

    Article  PubMed  Google Scholar 

  • Lou J, Zhu C (2007) A structure-based sliding-rebinding mechanism for catch bonds. Biophys J 92:1471–1485

    Article  PubMed  CAS  Google Scholar 

  • Lou J, Yago T, Klopochi AG, Metha P, Chen W, Zarnitsyna VI, Bovin NV, Zhu C, McEver RP (2006) Flow-enhanced adhesion regulated by a selectin interdomain hinge. J Cell Biol 174:1107–1117

    Article  PubMed  CAS  Google Scholar 

  • Luo BH, Springer TA (2006) Integrin structures and conformational signaling. Curr Opin Cell Biol 18:579–586

    Article  PubMed  CAS  Google Scholar 

  • Luo BH, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25:619–647

    Article  PubMed  CAS  Google Scholar 

  • Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–193

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto A, Kamata T, Takagi J, Iwasaki K, Yura K (2008) Key interactions in integrin ectodomain responsible for global conformational change detected by elastic network normal-mode analysis. Biophys J 95:2895–2908

    Article  PubMed  CAS  Google Scholar 

  • McEver RP, Zhu C (2010) Rolling cell adhesion. Annu Rev Cell Dev Biol 26:363–396

    Article  PubMed  CAS  Google Scholar 

  • Nishida N, Xie C, Shimaoka M, Cheng Y, Walz T, Springer TA (2006) Activation of leukocyte β2 integrins by conversion from bent to extended conformations. Immunity 25:583–594

    Article  PubMed  CAS  Google Scholar 

  • Provasi D, Murcia M, Coller BS, Filizola M (2009) Targeted molecular dynamics reveals overall common conformational changes upon hybrid domain swing-out in beta3 integrins. Proteins 77:477–489

    Article  PubMed  CAS  Google Scholar 

  • Puklin-Faucher E, Vogel V (2009) Integrin activation dynamics between the RGD-binding site and the headpiece hinge. J Biol Chem 284:36557–36568

    Article  PubMed  CAS  Google Scholar 

  • Puklin-Faucher E, Gao M, Schulten K, Vogel V (2006) How the headpiece hinge angle is opened: new insights into the dynamics of integrin activation. J Cell Biol 175:349–360

    Article  PubMed  CAS  Google Scholar 

  • Salas A, Shimaoka M, Kogan AN, Harwood C, von Andrian UH, Springer TA (2004) Rolling adhesion through an extended conformation of integrin αLβ2 and relation to α I and β I-like domain interaction. Immunity 20:393–406

    Article  PubMed  CAS  Google Scholar 

  • Sarangapani KK, Yago T, Klopochi AG, Lawrence MB, Fieger CB, Rosen SD, McEver RP, Zhu C (2004) Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J Biol Chem 279:2291–2298

    Article  PubMed  CAS  Google Scholar 

  • Schurpf T, Springer TA (2011) Regulation of integrin affinity on cell surfaces. EMBO J 30:4712–4727

    Article  PubMed  CAS  Google Scholar 

  • Schwartz MA, DeSimone DW (2008) Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 20:551–556

    Article  PubMed  CAS  Google Scholar 

  • Shamri R, Grabovsky V, Gauguet JM, Feigelson S, Manevich E, Kolanus W, Robinson MK, Staunton DE, von Andrian UH, Alon R (2005) Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol 6:497–506

    Article  PubMed  CAS  Google Scholar 

  • Shimaoka M, Xiao T, Liu JH, Yang Y, Dong Y, Jun CD, McCormack A, Zhang R, Joachimiak A, Takagi J, Wang JH, Springer TA (2003) Structures of the αL I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112:99–111

    Article  PubMed  CAS  Google Scholar 

  • Takagi J, Springer TA (2002) Integrin activation and structural rearrangement. Immunol Rev 186:141–163

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–923

    Article  PubMed  CAS  Google Scholar 

  • Wayman AM, Chen W, McEver RP, Zhu C (2010) Triphasic force dependence of E-selectin/ligand dissociation governs cell rolling under flow. Biophys J 99:1166–1174

    Article  PubMed  CAS  Google Scholar 

  • Wu T, Lin J, Cruz MA, Dong JF, Zhu C (2010) Force-induced cleavage of single VWF-A1A2A3 tridomains by ADAMTS-13. Blood 115:370–378

    Article  PubMed  CAS  Google Scholar 

  • Xiang X, Lee C-, Li T, Chen W, Lou J, Zhu C (2011) Structural basis and kinetics of force-induced conformational changes of an αA domain-containing integrin. PLoS One 6(11):e27946

    Article  PubMed  CAS  Google Scholar 

  • Xiao T, Takagi J, Coller BS, Wang JH, Springer TA (2004) Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 432:59–67

    Article  PubMed  CAS  Google Scholar 

  • Xie C, Zhu J, Chen X, Mi L, Nishida N, Springer TA (2009) Structure of an integrin with an αI domain, complement receptor type 4. EMBO J. 29:666–679

    Article  PubMed  Google Scholar 

  • Yago T, Wu J, Wey CD, Klopocki AG, Zhu C, McEver RP (2004) Catch bonds govern adhesion through L-selectin at threshold shear. J Cell Biol 166:913–923

    Article  PubMed  CAS  Google Scholar 

  • Yago T, Lou J, Wu T, Yang J, Miner JJ, Coburn L, Lopez JA, Cruz MA, Dong JF, McIntire LV, McEver RP, Zhu C (2008) Platelet glycoprotein Ibα forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J Clin Invest 118:3195–3207

    PubMed  CAS  Google Scholar 

  • Yakovenko O, Sharma S, Forero M, Tchesnokova V, Aprikian P, Kidd B, Mach A, Vogel V, Sokurenko E, Thomas WE (2008) FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem 283:11596–11605

    Article  PubMed  CAS  Google Scholar 

  • Zarnitsyna VI, Zhu C (2011) Adhesion frequency assay for in situ kinetics analysis of cross- junctional molecular interactions at the cell-cell interface. J Vis Exp e3519

    Google Scholar 

  • Zhu C, Lou J, McEver RP (2005) Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42:443–462

    PubMed  CAS  Google Scholar 

  • Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, Springer TA (2008) Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell 32:849–861

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the coauthors of our original papers, the results of which are summarized here, especially Fang Kong and Jizhong Lou. This work was supported by NIH grant R01AI044902.

Author information

Authors and Affiliations

  1. The Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, GA, USA

    Cheng Zhu & Wei Chen

Authors
  1. Cheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cheng Zhu .

Editor information

Editors and Affiliations

  1. , Neuroscience and Cell Biology, University of Texas Medical Branch, 5.212A Research Building 17, Galveston, 77555-0620, Texas, USA

    Andres F. Oberhauser

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media New York

About this chapter

Cite this chapter

Zhu, C., Chen, W. (2012). Catch Bonds of Integrin/Ligand Interactions. In: Oberhauser, A. (eds) Single-molecule Studies of Proteins. Biophysics for the Life Sciences, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4921-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation