Topics

    Inside-out signaling versus Outside-in signaling[Edit]

    Different signaling pathways can initiate integrin activation via:

    a) Inside-out signaling

    Signals received by other receptors foster the binding of talin and kindlin to cytoplasmic end of the integrin β subunit [1], at sites of actin polymerization. Substantial information on signaling pathway leading activation is available for integrin αIIbβ3 [2]. 

    Talin binds to integrin β-tail via F3 phospho-tyrosine binding (PTB) domain [3], a unique interaction with the membrane proximal (MP) region of the integrin (NPxY motif). This permits competition between conserved lysine on talin and an aspartic acid on integrin α essential for α/β salt bridge disruption and sufficient for integrin activation [45]. Addition interactions through the basic patches in the FERM subdomain F2 helps to orient the β-subunit to promote spatial separation of the cytoplasmic domains [67]. 

    Kindlin is also an essential co-activator of integrin [89] and binds to a membrane distal NxxY motif on β-integrin via its FERM F3 subdomain [10]. A preceding threonine patch on integrins β1 and β3 that gets phosphorylated [1011] and a tryptophan on kindlin F3 are also required for binding. However, kindlins are not known to activate integrins on their own but may render integrin-specific effects (reviewed in [12]). 

    The mechanism of crosstalk between integrin, talin and kindlin are not well established (reviewed in [13]). However, substantial data on the order of their binding is available. Latest Findings Talin is recruited directly to FAs from the cytosol suggesting that it does not bind to free diffusing integrins outside FAs [14] and also requires vinculin and F-actin for its activation [15]. Hence it is believed that only F-actin anchored talin at FAs bind free diffusing integrin promoting its activation [14]. Talin can directly connect to actin while kindlin links through adaptors such as migfilin, filaminFAKVASP and α-actinin (reviewed in [12]).

    b) Outside-in signaling
     
    Ligand binding to external domain causes conformational changes that increase ligand affinity, modify protein-interaction sites in the cytoplasmic domains and thence the resulting signals. 

    Besides conformational changes that extend integrin dimers ([16], reviewed in [1718]), multivalent ligand binding leads to clustering of integrins, which in turn activates Src family of kinases (SFKs) by autophosphorylation [19]. SFKs phosphorylate tyrosines of the integrin cytoplasmic domain (NPxY motifs) [2021] and other proteins [2223] leading to 
    a) control of ligand binding strength 
    b) alteration of binding with signaling molecules (kinases, GTPases and adaptors) [24], that constitute dynamic adhesion structures such as focal adhesions and podosomes (reviewed in [2526]). 

    Nevertheless, whether clustering triggers outside-in signaling to facilitate integrin activation or occurs after integrin activation is uncertain (reviewed in [2725]). 

    References

    1. Watanabe N., Bodin L., Pandey M., Krause M., Coughlin S., Boussiotis VA., Ginsberg MH., Shattil SJ. Mechanisms and consequences of agonist-induced talin recruitment to platelet integrin alphaIIbbeta3. J. Cell Biol. 2008; 181(7). [PMID: 18573917]
    2. Han J., Lim CJ., Watanabe N., Soriani A., Ratnikov B., Calderwood DA., Puzon-McLaughlin W., Lafuente EM., Boussiotis VA., Shattil SJ., Ginsberg MH. Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 2006; 16(18). [PMID: 16979556]
    3. Calderwood DA., Yan B., de Pereda JM., Alvarez BG., Fujioka Y., Liddington RC., Ginsberg MH. The phosphotyrosine binding-like domain of talin activates integrins. J. Biol. Chem. 2002; 277(24). [PMID: 11932255]
    4. Wegener KL., Partridge AW., Han J., Pickford AR., Liddington RC., Ginsberg MH., Campbell ID. Structural basis of integrin activation by talin. Cell 2007; 128(1). [PMID: 17218263]
    5. Anthis NJ., Wegener KL., Ye F., Kim C., Goult BT., Lowe ED., Vakonakis I., Bate N., Critchley DR., Ginsberg MH., Campbell ID. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 2009; 28(22). [PMID: 19798053]
    6. Saltel F., Mortier E., Hytönen VP., Jacquier MC., Zimmermann P., Vogel V., Liu W., Wehrle-Haller B. New PI(4,5)P2- and membrane proximal integrin-binding motifs in the talin head control beta3-integrin clustering. J. Cell Biol. 2009; 187(5). [PMID: 19948488]
    7. Kim M., Carman CV., Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 2003; 301(5640). [PMID: 14500982]
    8. Moser M., Nieswandt B., Ussar S., Pozgajova M., Fässler R. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat. Med. 2008; 14(3). [PMID: 18278053]
    9. Pluskota E., Dowling JJ., Gordon N., Golden JA., Szpak D., West XZ., Nestor C., Ma YQ., Bialkowska K., Byzova T., Plow EF. The integrin coactivator kindlin-2 plays a critical role in angiogenesis in mice and zebrafish. Blood 2011; 117(18). [PMID: 21378273]
    10. Harburger DS., Bouaouina M., Calderwood DA. Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 2009; 284(17). [PMID: 19240021]
    11. Nilsson S., Kaniowska D., Brakebusch C., Fässler R., Johansson S. Threonine 788 in integrin subunit beta1 regulates integrin activation. Exp. Cell Res. 2006; 312(6). [PMID: 16405888]
    12. Karaköse E., Schiller HB., Fässler R. The kindlins at a glance. J. Cell. Sci. 2010; 123(Pt 14). [PMID: 20592181]
    13. Moser M., Legate KR., Zent R., Fässler R. The tail of integrins, talin, and kindlins. Science 2009; 324(5929). [PMID: 19443776]
    14. Rossier O., Octeau V., Sibarita JB., Leduc C., Tessier B., Nair D., Gatterdam V., Destaing O., Albigès-Rizo C., Tampé R., Cognet L., Choquet D., Lounis B., Giannone G. Integrins β1 and β3 exhibit distinct dynamic nanoscale organizations inside focal adhesions. Nat. Cell Biol. 2012; 14(10). [PMID: 23023225]
    15. Banno A., Goult BT., Lee H., Bate N., Critchley DR., Ginsberg MH. Subcellular localization of talin is regulated by inter-domain interactions. J. Biol. Chem. 2012; 287(17). [PMID: 22351767]
    16. Zhu J., Carman CV., Kim M., Shimaoka M., Springer TA., Luo BH. Requirement of alpha and beta subunit transmembrane helix separation for integrin outside-in signaling. Blood 2007; 110(7). [PMID: 17615290]
    17. Takada Y., Ye X., Simon S. The integrins. Genome Biol. 2007; 8(5). [PMID: 17543136]
    18. Arnaout MA., Mahalingam B., Xiong JP. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol. 2005; 21. [PMID: 16212500]
    19. Arias-Salgado EG., Lizano S., Sarkar S., Brugge JS., Ginsberg MH., Shattil SJ. Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. U.S.A. 2003; 100(23). [PMID: 14593208]
    20. Law DA., DeGuzman FR., Heiser P., Ministri-Madrid K., Killeen N., Phillips DR. Integrin cytoplasmic tyrosine motif is required for outside-in alphaIIbbeta3 signalling and platelet function. Nature 1999; 401(6755). [PMID: 10548108]
    21. Datta A., Huber F., Boettiger D. Phosphorylation of beta3 integrin controls ligand binding strength. J. Biol. Chem. 2002; 277(6). [PMID: 11723131]
    22. Miyamoto S., Akiyama SK., Yamada KM. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 1995; 267(5199). [PMID: 7846531]
    23. Arias-Salgado EG., Lizano S., Shattil SJ., Ginsberg MH. Specification of the direction of adhesive signaling by the integrin beta cytoplasmic domain. J. Biol. Chem. 2005; 280(33). [PMID: 15937333]
    24. Anthis NJ., Haling JR., Oxley CL., Memo M., Wegener KL., Lim CJ., Ginsberg MH., Campbell ID. Beta integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation. J. Biol. Chem. 2009; 284(52). [PMID: 19843520]
    25. Ginsberg MH., Partridge A., Shattil SJ. Integrin regulation. Curr. Opin. Cell Biol. 2005; 17(5). [PMID: 16099636]
    26. Gahmberg CG., Fagerholm SC., Nurmi SM., Chavakis T., Marchesan S., Grönholm M. Regulation of integrin activity and signalling. Biochim. Biophys. Acta 2009; 1790(6). [PMID: 19289150]
    27. Shattil SJ., Kim C., Ginsberg MH. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 2010; 11(4). [PMID: 20308986]
    Updated on: Mon, 20 Oct 2014 09:41:15 GMT