The b2 integrin-kindlin-3 interaction is essential for T-cell homing but dispensable for T-cell activation in vivo

Blood

Volumn 122, Issue 8, 2013, Pages 1428-1436

  Morrison, Vicky Louise ^a   MacPherson, Matthew ^a   Savinko, Terhi ^b   Lek, Hwee San ^a   Prescott, Alan ^c   Fagerholm, Susanna Carola ^a,b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD18 ANTIGEN; KINDLIN 3; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; GLUTATHIONE TRANSFERASE; KINDLIN 3 PROTEIN, MOUSE; KINDLIN-3 PROTEIN, MOUSE; MEMBRANE PROTEIN; MIG2B PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CONTROLLED STUDY; GENE MUTATION; IMMUNE RESPONSE; IN VIVO STUDY; LEUKOCYTE; LIGAND BINDING; LYMPH NODE; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SHEAR FLOW; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL MOTION; CELL STRAIN HEK293; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD18; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL MOVEMENT; CYTOSKELETAL PROTEINS; GLUTATHIONE TRANSFERASE; HEK293 CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM PROTEINS; T-LYMPHOCYTES;

EID: 84886813216     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-02-484998     Document Type: Article

References (34)

1. Andrew DP, Spellberg JP, Takimoto H, Schmits R., Mak TW, Zukowski MM. Transendothelial migration and trafficking of leukocytes in LFA-1-deficient mice. Eur J Immunol. 1998; 28(6): 1959-1969. (Pubitemid 28271713)
2. Sims TN, Dustin ML. The immunological synapse: integrins take the stage. Immunol Rev. 2002; 186: 100-117.
3. Perez OD, Mitchell D, Jager G.C., et al. Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat Immunol. 2003; 4(11): 1083-1092. (Pubitemid 37428036)
4. Graf B, Bushnell T, Miller J. LFA-1-mediated T cell costimulation through increased localization of TCR/class II complexes to the central supramolecular activation cluster and exclusion of CD45 from the immunological synapse. J Immunol. 2007; 179(3): 1616-1624.
5. Abraham C, Griffith J, Miller J. The dependence for leukocyte function-associated antigen-1/ICAM-1 interactions in T cell activation cannot be overcome by expression of high density TCR ligand. J Immunol. 1999; 162(8): 4399-4405. (Pubitemid 29314835)
6. Etzioni A. Genetic etiologies of leukocyte adhesion defects. Curr Opin Immunol. 2009; 21(5): 481-486.
7. Hogg N, Patzak I, Willenbrock F. The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol. 2011; 11(6): 416-426.
8. Fagerholm SC, Hilden TJ, Nurmi S.M., Gahmberg CG. Specific integrin alpha and beta chain phosphorylations regulate LFA-1 activation through affinity-dependent and -independent mechanisms. J Cell Biol. 2005; 171(4): 705-715. (Pubitemid 41668729)
9. Takala H, Nurminen E, Nurmi S.M., et al. Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding. Blood. 2008; 112(5): 1853-1862.
10. 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.
11. Kiema T, Lad Y, Jiang P., et al. The molecular basis of filamin binding to integrins and competition with talin. Mol Cell. 2006; 21(3): 337-347. (Pubitemid 43163529)
12. Lim J, Wiedemann A, Tzircotis G., Monkley SJ, Critchley DR, Caron E. An essential role for talin during alpha(M)beta(2)-mediated phagocytosis. Mol Biol Cell. 2007; 18(3): 976-985. (Pubitemid 46399501)
13. Wernimont SA, Wiemer AJ, Bennin D.A., et al. Contact-dependent T cell activation and T cell stopping require talin1. J Immunol. 2011; 187(12): 6256-6267.
14. 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. (Pubitemid 351347914)
15. Svensson L, Howarth K, McDowall A., et al. Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat Med. 2009; 15(3): 306-312.
16. Malinin NL, Zhang L, Choi J., et al. A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nat Med. 2009; 15(3): 313-318.
17. Fagerholm S, Morrice N, Gahmberg C.G., Cohen P. Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J Biol Chem. 2002; 277(3): 1728-1738. (Pubitemid 34968743)
18. Nurmi SM, Autero M, Raunio A.K., Gahmberg CG, Fagerholm SC. Phosphorylation of the LFA-1 integrin beta2-chain on Thr-758 leads to adhesion, Rac-1/Cdc42 activation, and stimulation of CD69 expression in human T cells. J Biol Chem. 2007; 282(2): 968-975. (Pubitemid 47076564)
19. Matthews SA, San Lek H, Morrison VL, et al. Protein kinase D isoforms are dispensable for integrin-mediated lymphocyte adhesion and homing to lymphoid tissues. Eur J Immunol. 2012; 42(5): 1316-1326.
20. Lek HS, Morrison VL, Conneely M, et al. The spontaneously adhesive leukocyte function-associated antigen-1 (LFA-1) integrin in effector T cells mediates rapid actin- and calmodulin-dependent adhesion strengthening to ligand under shear flow. J Biol Chem. 2013; 288(21): 14698-14708.
21. 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): 11485-11497.
22. Wegener KL, Partridge AW, Han J, et al. Structural basis of integrin activation by talin. Cell. 2007; 128(1): 171-182. (Pubitemid 46048890)
23. García-Alvarez B., de Pereda JM, Calderwood DA, et al. Structural determinants of integrin recognition by talin. Mol Cell. 2003; 11(1): 49-58. (Pubitemid 36131107)
24. Böttcher R.T., Stremmel C, Meves A., et al. Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail. Nat Cell Biol. 2012; 14(6): 584-592.
25. Marski M, Kandula S, Turner J.R., Abraham C. CD18 is required for optimal development and function of CD4+CD25+ T regulatory cells. J Immunol. 2005; 175(12): 7889-7897. (Pubitemid 41798349)
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. (Pubitemid 28328611)
27. Berlin-Rufenach C., Otto F, Mathies M., et al. Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J Exp Med. 1999; 189(9): 1467-1478. (Pubitemid 29227533)
28. Shulman Z, Cohen SJ, Roediger B, et al. Transendothelial migration of lymphocytes mediated by intraendothelial vesicle stores rather than by extracellular chemokine depots. Nat Immunol. 2012; 13(1): 67-76.
29. Waugh C, Sinclair L, Finlay D., Bayascas JR, Cantrell D. Phosphoinositide (3,4,5)-triphosphate binding to phosphoinositide-dependent kinase 1 regulates a protein kinase B/Akt signaling threshold that dictates T-cell migration, not proliferation. Mol Cell Biol. 2009; 29(21): 5952-5962.
30. Varga G, Balkow S, Wild M.K., et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood. 2007; 109(2): 661-669. (Pubitemid 46105967)
31. Balkow S, Heinz S, Schmidbauer P., et al. LFA-1 activity state on dendritic cells regulates contact duration with T cells and promotes T-cell priming. Blood. 2010; 116(11): 1885-1894.
32. Manevich-Mendelson E., Feigelson SW, Pasvolsky R, et al. Loss of Kindlin-3 in LAD-III eliminates LFA-1 but not VLA-4 adhesiveness developed under shear flow conditions. Blood. 2009; 114(11): 2344-2353.
33. Feigelson SW, Grabovsky V, Manevich-Mendelson E, et al. Kindlin-3 is required for the stabilization of TCR-stimulated LFA-1:ICAM-1 bonds critical for lymphocyte arrest and spreading on dendritic cells. Blood. 2011; 117(26): 7042-7052.
34. Kandula S, Abraham C. LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J Immunol. 2004; 173(7): 4443-4451. (Pubitemid 39280674)