Loss of the Rap1 effector RIAM results in leukocyte adhesion deficiency due to impaired β2 integrin function in mice

Blood

Volumn 126, Issue 25, 2015, Pages 2704-2712

  Klapproth, Sarah ^a,b   Sperandio, Markus ^b   Pinheiro, Elaine M ^c   Prünster, Monika ^b   Soehnlein, Oliver ^b,d,e   Gertler, Frank B ^c   Fässler, Reinhard ^a   Moser, Markus ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^e ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; CD18 ANTIGEN; CXCL1 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN; RAP1 GUANOSINE TRIPHOSPHATE INTERACTING ADAPTER MOLECULE; RAP1 PROTEIN; TALIN; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; MEMBRANE PROTEIN; RIAM PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VERY LATE ACTIVATION ANTIGEN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL POPULATION; CONTROLLED STUDY; FAMILY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ADHERENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CELL ADHESION; CELL SEPARATION; FLOW CYTOMETRY; KNOCKOUT MOUSE; LEUKOCYTE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD18; BLOTTING, WESTERN; CELL ADHESION; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; INTEGRIN ALPHA4BETA1; LEUKOCYTES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; RAP1 GTP-BINDING PROTEINS; TALIN;

EID: 84951325487     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-05-647453     Document Type: Article

References (53)

1. Calderwood DA, Campbell ID, Critchley DR. Talins and kindlins: Partners in integrin-mediated adhesion. Nat Rev Mol Cell Biol. 2013;14(8): 503-517.
2. Ye F, Petrich BG, Anekal P, et al. The mechanism of kindlin-mediated activation of integrin aIIbb3. Curr Biol. 2013;23(22):2288-2295.
3. Nieswandt B, Moser M, Pleines I, et al. Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. J Exp Med. 2007;204(13): 3113-3118.
4. 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):325-330.
5. Lefort CT, Rossaint J, Moser M, et al. Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation. Blood. 2012;119(18): 4275-4282.
6. Moser M, Bauer M, Schmid S, et al. Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat Med. 2009; 15(3):300-305.
7. Goult BT, Xu XP, Gingras AR, et al. Structural studies on full-length talin1 reveal a compact auto-inhibited dimer: Implications for talin activation. J Struct Biol. 2013;184(1):21-32.
8. Martel V, Racaud-Sultan C, Dupe S, et al. Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J Biol Chem. 2001;276(24): 21217-21227.
9. Goksoy E, Ma YQ, Wang X, et al. Structural basis for the autoinhibition of talin in regulating integrin activation. Mol Cell. 2008;31(1):124-133.
10. Anthis NJ, Wegener KL, Ye F, et al. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 2009; 28(22):3623-3632.
11. Goult BT, Bate N, Anthis NJ, et al. The structure of an interdomain complex that regulates talin activity. J Biol Chem. 2009;284(22):15097-15106.
12. Goult BT, Gingras AR, Bate N, Barsukov IL, Critchley DR, Roberts GC. The domain structure of talin: Residues 1815-1973 form a five-helix bundle containing a cryptic vinculin-binding site. FEBS Lett. 2010;584(11):2237-2241.
13. Saltel F, Mortier E, Hytönen VP, et al. 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):715-731.
14. Bos JL, de Rooij J, Reedquist KA. Rap1 signalling: Adhering to new models. Nat Rev Mol Cell Biol. 2001;2(5):369-377.
15. Coló GP, Lafuente EM, Teixidó J. The MRL proteins: Adapting cell adhesion, migration and growth. Eur J Cell Biol. 2012;91(11-12):861-868.
16. Lafuente EM, van Puijenbroek AA, Krause M, et al. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell. 2004;7(4):585-595.
17. Ménasché G, Kliche S, Chen EJ, Stradal TE, Schraven B, Koretzky G. RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation. Mol Cell Biol. 2007;27(11):4070-4081.
18. Kliche S, Worbs T, Wang X, et al. CCR7-mediated LFA-1 functions in T cells are regulated by 2 independent ADAP/SKAP55 modules. Blood. 2012;119(3):777-785.
19. Han J, Lim CJ, Watanabe N, et al. Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr Biol. 2006;16(18): 1796-1806.
20. Watanabe N, Bodin L, Pandey M, et al. Mechanisms and consequences of agonistinduced talin recruitment to platelet integrin alphaIIbbeta3. J Cell Biol. 2008;181(7): 1211-1222.
21. Lee HS, Lim CJ, Puzon-McLaughlin W, Shattil SJ, Ginsberg MH. RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J Biol Chem. 2009;284(8):5119-5127.
22. Yang J, Zhu L, Zhang H, et al. Conformational activation of talin by RIAM triggers integrinmediated cell adhesion. Nat Commun. 2014;5: 5880.
23. Goult BT, Zacharchenko T, Bate N, et al. RIAM and vinculin binding to talin are mutually exclusive and regulate adhesion assembly and turnover. J Biol Chem. 2013;288(12):8238-8249.
24. Lee HS, Anekal P, Lim CJ, Liu CC, Ginsberg MH. Two modes of integrin activation form a binary molecular switch in adhesion maturation. Mol Biol Cell. 2013;24(9):1354-1362.
25. Stritt S, Wolf K, Lorenz V, et al. Rap1-GTPinteracting adaptor molecule (RIAM) is dispensable for platelet integrin activation and function in mice. Blood. 2015;125(2):219-222.
26. Scharffetter-Kochanek K, Lu H, Norman K, et al. Spontaneous skin ulceration and defective T cell function in CD18 null mice. J Exp Med. 1998; 188(1):119-131.
27. Lee PP, Fitzpatrick DR, Beard C, et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 2001;15(5):763-774.
28. Kühn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995; 269(5229):1427-1429.
29. Jones SL, Knaus UG, Bokoch GM, Brown EJ. Two signaling mechanisms for activation of alphaM beta2 avidity in polymorphonuclear neutrophils. J Biol Chem. 1998;273(17): 10556-10566.
30. Nathan C, Srimal S, Farber C, et al. Cytokineinduced respiratory burst of human neutrophils: Dependence on extracellular matrix proteins and CD11/CD18 integrins. J Cell Biol. 1989;109(3): 1341-1349.
31. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7(9):678-689.
32. Schmidt S, Moser M, Sperandio M. The molecular basis of leukocyte recruitment and its deficiencies. Mol Immunol. 2013;55(1):49-58.
33. Linder S, Kopp P. Podosomes at a glance. J Cell Sci. 2005;118(Pt 10):2079-2082.
34. Schmidt S, Nakchbandi I, Ruppert R, et al. Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J Cell Biol. 2011;192(5):883-897.
35. Horn J, Wang X, Reichardt P, et al. Src homology 2-domain containing leukocyte-specific phosphoprotein of 76 kDa is mandatory for TCRmediated inside-out signaling, but dispensable for CXCR4-mediated LFA-1 activation, adhesion, and migration of T cells. J Immunol. 2009;183(9): 5756-5767.
36. Wernimont SA, Wiemer AJ, Bennin DA, et al. Contact-dependent T cell activation and T cell stopping require talin1. J Immunol. 2011;187(12): 6256-6267.
37. Berlin-Rufenach C, Otto F, Mathies M, et al. Lymphocyte migration in lymphocyte functionassociated antigen (LFA)-1-deficient mice. J Exp Med. 1999;189(9):1467-1478.
38. Chrzanowska-Wodnicka M, Smyth SS, Schoenwaelder SM, Fischer TH, White GC II. Rap1b is required for normal platelet function and hemostasis in mice. J Clin Invest. 2005;115(3): 680-687.
39. Crittenden JR, Bergmeier W, Zhang Y, et al. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat Med. 2004;10(9):982-986.
40. Petrich BG, Marchese P, Ruggeri ZM, et al. Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J Exp Med. 2007; 204(13):3103-3111.
41. Bergmeier W, Goerge T, Wang HW, et al. Mice lacking the signaling molecule CalDAG-GEFI represent a model for leukocyte adhesion deficiency type III. J Clin Invest. 2007;117(6): 1699-1707.
42. Han DC, Shen TL, Guan JL. The Grb7 family proteins: Structure, interactions with other signaling molecules and potential cellular functions. Oncogene. 2001;20(44):6315-6321.
43. Han DC, Guan JL. Association of focal adhesion kinase with Grb7 and its role in cell migration. J Biol Chem. 1999;274(34):24425-24430.
44. Han DC, Shen TL, Guan JL. Role of Grb7 targeting to focal contacts and its phosphorylation by focal adhesion kinase in regulation of cell migration. J Biol Chem. 2000;275(37): 28911-28917.
45. Song X, Yang J, Hirbawi J, et al. A novel membrane-dependent on/off switch mechanism of talin FERM domain at sites of cell adhesion. Cell Res. 2012;22(11):1533-1545.
46. Bakolitsa C, Cohen DM, Bankston LA, et al. Structural basis for vinculin activation at sites of cell adhesion. Nature. 2004;430(6999):583-586.
47. Kamen LA, Schlessinger J, Lowell CA. Pyk2 is required for neutrophil degranulation and host defense responses to bacterial infection. J Immunol. 2011;186(3):1656-1665.
48. Wang D, Olman MA, Stewart J Jr, et al. Downregulation of FIP200 induces apoptosis of glioblastoma cells and microvascular endothelial cells by enhancing Pyk2 activity. PLoS One. 2011;6(5):e19629.
49. Duong LT, Rodan GA. PYK2 is an adhesion kinase in macrophages, localized in podosomes and activated by beta(2)-integrin ligation. Cell Motil Cytoskeleton. 2000;47(3):174-188.
50. Ghandour H, Cullere X, Alvarez A, Luscinskas FW, Mayadas TN. Essential role for Rap1 GTPase and its guanine exchange factor CalDAG-GEFI in LFA-1 but not VLA-4 integrin mediated human T-cell adhesion. Blood. 2007; 110(10):3682-3690.
51. Berlin C, Bargatze RF, Campbell JJ, et al. alpha 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell. 1995;80(3): 413-422.
52. Abitorabi MA, Pachynski RK, Ferrando RE, Tidswell M, Erle DJ. Presentation of integrins on leukocyte microvilli: A role for the extracellular domain in determining membrane localization. J Cell Biol. 1997;139(2):563-571.
53. Hyduk SJ, Rullo J, Cano AP, et al. Talin-1 and kindlin-3 regulate alpha4beta1 integrin-mediated adhesion stabilization, but not G protein-coupled receptor-induced affinity upregulation. J Immunol. 2011;187(8):4360-4368.