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

Volumn 117, Issue 26, 2011, Pages 7042-7052

  Feigelson, Sara W ^a   Grabovsky, Valentin ^a   Manevich Mendelson, Eugenia ^a   Pasvolsky, Ronit ^a   Shulman, Ziv ^a   Shinder, Vera ^a   Klein, Eugenia ^a   Etzioni, Amos ^b   Aker, Memet ^c   Alon, Ronen ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b MEYER CHILDREN S HOSPITAL   (Israel)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; INTERCELLULAR ADHESION MOLECULE 1; KINDLIN 3; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PROTEIN; SECONDARY LYMPHOID TISSUE CHEMOKINE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; CELL MOTILITY; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; LYMPHOCYTE MIGRATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 79959858924     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-12-322859     Document Type: Article

References (55)

1. Stinchcombe JC, Bossi G, Booth S, Griffiths GM. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity. 2001;15(5):751-761. (Pubitemid 34008503)
2. Henrickson SE, Mempel TR, Mazo IB, et al. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol. 2008;9(3):282-291. (Pubitemid 351267325)
3. Zheng H, Jin B, Henrickson SE, Perelson AS, von Andrian UH, Chakraborty AK. How antigen quantity and quality determine T-cell decisions in lymphoid tissue. Mol Cell Biol. 2008;28(12):4040-4051. (Pubitemid 351812989)
4. Scholer A, Hugues S, Boissonnas A, Fetler L, Amigorena S. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity. 2008;28(2):258-270. (Pubitemid 351222655)
5. Anikeeva N, Somersalo K, Sims TN, Thomas VK, Dustin ML, Sykulev Y. Distinct role of lymphocyte function-associated antigen-1 in mediating effective cytolytic activity by cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 2005;102(18):6437-6442. (Pubitemid 40617461)
6. Dustin ML, Springer TA. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 1989;341(6243):619-624. (Pubitemid 19257309)
7. Sims TN, Dustin ML. The immunological synapse: integrins take the stage. Immunol Rev. 2002;186:100-117.
8. Dustin ML. Hunter to gatherer and back: immunological synapses and kinapses as variations on the theme of amoeboid locomotion. Annu Rev Cell Dev Biol. 2008;24:577-596.
9. Simonson WT, Franco SJ, Huttenlocher A. Talin1 regulates TCR-mediated LFA-1 function. J Immunol. 2006;177(11):7707-7714. (Pubitemid 44846286)
10. 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.
11. 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.
12. 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.
13. 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.
14. Bajénoff M, Egen JG, Koo LY, et al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity. 2006;25(6):989-1001. (Pubitemid 44914055)
15. Beals CR, Edwards AC, Gottschalk RJ, Kuijpers TW, Staunton DE. CD18 activation epitopes induced by leukocyte activation. J Immunol. 2001;167(11):6113-6122. (Pubitemid 33081537)
16. Bolomini-Vittori M, Montresor A, Giagulli C, et al. Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat Immunol. 2009;10(2):185-194.
17. Sigal A, Bleijs DA, Grabovsky V, et al. The LFA-1 integrin supports rolling adhesions on ICAM-1 under physiological shear flow in a permissive cellular environment. J Immunol. 2000;165(1):442-452. (Pubitemid 30429538)
18. Grabovsky V, Feigelson S, Chen C, et al. Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med. 2000;192(4):495-506.
19. Woolf E, Grigorova I, Sagiv A, et al. Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat Immunol. 2007;8(10):1076-1085. (Pubitemid 47423755)
20. Brown MJ, Nijhara R, Hallam JA, et al. Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood. 2003;102(12):3890-3899. (Pubitemid 37486967)
21. Shulman Z, Pasvolsky R, Woolf E, et al. DOCK2 regulates chemokine-triggered lateral lymphocyte motility but not transendothelial migration. Blood. 2006;108(7):2150-2158. (Pubitemid 44497494)
22. Feigelson SW, Pasvolsky R, Cemerski S, et al. Occupancy of lymphocyte LFA-1 by surface-immobilized ICAM-1 is critical for TCR- but not for chemokine-triggered LFA-1 conversion to an open headpiece high-affinity state. J Immunol. 2010;185(12):7394-7404.
23. Barda-Saad M, Braiman A, Titerence R, Bunnell SC, Barr VA, Samelson LE. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol. 2005;6(1):80-89. (Pubitemid 40136699)
24. Robert P, Canault M, Farnarier C, et al. A novel leukocyte adhesion deficiency III variant: Kindlin-3 deficiency results in integrin and nonintegrin-related defects in different steps of leukocyte adhesion. J Immunol. 2011;186(9):5273-5283.
25. Brossard C, Feuillet V, Schmitt A, et al. Multifocal structure of the T cell- dendritic cell synapse. Eur J Immunol. 2005;35(6):1741-1753. (Pubitemid 40862322)
26. Tseng SY, Waite JC, Liu M, Vardhana S, Dustin ML. T cell-dendritic cell immunological synapses contain TCR-dependent CD28-CD80 clusters that recruit protein kinase C theta. J Immunol. 2008;181(7):4852-4863.
27. Dwir O, Kansas GS, Alon R. Cytoplasmic anchorage of L-selectin controls leukocyte capture and rolling by increasing the mechanical stability of the selectin tether. J Cell Biol. 2001;155(1):145-156. (Pubitemid 34286215)
28. Alon R, Feigelson SW, Manevich E, et al. Alpha4beta1-dependent adhesion strengthening under mechanical strain is regulated by paxillin association with the alpha4-cytoplasmic domain. J Cell Biol. 2005;171(6):1073-1084. (Pubitemid 41815838)
29. Manevich E, Grabovsky V, Feigelson SW, Alon R. Talin 1 and paxillin facilitate distinct steps in rapid VLA-4-mediated adhesion strengthening to vascular cell adhesion molecule 1. J Biol Chem. 2007;282(35):25338-25348. (Pubitemid 47372824)
30. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619-647. (Pubitemid 46697919)
31. Askari JA, Tynan CJ, Webb SE, Martin-Fernandez ML, Ballestrem C, Humphries MJ. Focal adhesions are sites of integrin extension. J Cell Biol. 2010;188(6):891-903.
32. Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol. 2010;11(4):288-300.
33. Moser M, Legate KR, Zent R, Fassler R. The tail of integrins, talin, and kindlins. Science. 2009;324(5929):895-899.
34. Larjava H, Plow EF, Wu C. Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep. 2008;9(12):1203-1208.
35. Hogg N, Laschinger M, Giles K, McDowall A. T-cell integrins: more than just sticking points. J Cell Sci. 2003;116(pt 23):4695-4705. (Pubitemid 37541213)
36. 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. (Pubitemid 350159637)
37. Constantin G, Majeed M, Giagulli C, et al. Chemokines trigger immediate beta2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity. 2000;13(6):759-769. (Pubitemid 32041799)
38. Thelen M, Stein JV. How chemokines invite leukocytes to dance. Nat Immunol. 2008;9(9):953-959.
39. Shamri R, Grabovsky V, Gauguet JM, et al. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol. 2005;6(5):497-506. (Pubitemid 41716763)
40. Bromley SK, Peterson DA, Gunn MD, Dustin ML. Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation. J Immunol. 2000;165(1):15-19. (Pubitemid 30429484)
41. Bromley SK, Dustin ML. Stimulation of naive T-cell adhesion and immunological synapse formation by chemokine-dependent and -independent mechanisms. Immunology. 2002;106(3):289-298. (Pubitemid 34748122)
42. Friedman RS, Jacobelli J, Krummel MF. Surface-bound chemokines capture and prime T cells for synapse formation. Nat Immunol. 2006;7(10):1101-1108. (Pubitemid 44420655)
43. Schumann K, Lammermann T, Bruckner M, et al. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity. 2010;32(5):703-713.
44. Negulescu PA, Krasieva TB, Khan A, Kerschbaum HH, Cahalan MD. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity. 1996;4(5):421-430. (Pubitemid 26354652)
45. Wei X, Tromberg BJ, Cahalan MD. Mapping the sensitivity of T cells with an optical trap: polarity and minimal number of receptors for Ca(2+) signaling. Proc Natl Acad Sci U S A. 1999;96(15):8471-8476. (Pubitemid 29354815)
46. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427(6970):154-159. (Pubitemid 38094955)
47. Grakoui A, Bromley SK, Sumen C, et al. The immunological synapse: a molecular machine controlling T cell activation. Science. 1999;285(5425):221- 227. (Pubitemid 29329988)
48. Kaizuka Y, Douglass AD, Varma R, Dustin ML, Vale RD. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc Natl Acad Sci U S A. 2007;104(51):20296-20301.
49. Chen W, Lou J, Zhu C. Forcing Switch from Short- to Intermediate- and Long-lived States of the {alpha}A Domain Generates LFA-1/ICAM-1 Catch Bonds. J Biol Chem. 2010;285(46):35967-35978.
50. Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, Springer TA. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell. 2008;32(6):849-861.
51. Astrof NS, Salas A, Shimaoka M, Chen J, Springer TA. Importance of force linkage in mechanochemistry of adhesion receptors. Biochemistry. 2006;45(50):15020-15028. (Pubitemid 44937014)
52. Cairo CW, Mirchev R, Golan DE. Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. Immunity. 2006;25(2):297-308. (Pubitemid 44224146)
53. Alon R, Dustin ML. Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity. 2007;26(1):17-27. (Pubitemid 46109349)
54. Moser M, Nieswandt B, Ussar S, Pozgajova M, Fassler R. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med. 2008;14(3):325-330. (Pubitemid 351347914)
55. Malinin NL, Plow EF, Byzova TV. Kindlins in FERM adhesion. Blood. 2010;115(20):4011-4017.