A role for LFA-1 in delaying T-lymphocyte egress from lymph nodes

EMBO Journal

Volumn 32, Issue 6, 2013, Pages 829-843

  Reichardt, Peter ^a   Patzak, Irene ^b   Jones, Kristian ^b   Etemire, Eloho ^c   Gunzer, Matthias ^a,c   Hogg, Nancy ^b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

LFA 1; lymph node; lymphatics; migration; T cells

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ARTICLE; CD4+ T LYMPHOCYTE; LYMPH NODE; MICROSCOPY; MULTIPHOTON MICROSCOPY; PARENCHYMA; PHOTON; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; CELLS, CULTURED; CHEMOKINE CCL21; CHEMOTAXIS, LEUKOCYTE; FEMALE; GLYCOPROTEINS; INTERCELLULAR ADHESION MOLECULE-1; LYMPH NODES; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPHINGOSINE; T-LYMPHOCYTES; TIME FACTORS;

EID: 84875470995     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.33     Document Type: Article

References (54)

1. Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25: 989-1001
2. Bajenoff M, Egen JG, Qi H, Huang AY, Castellino F, Germain RN (2007) Highways, byways and breadcrumbs: directing lymphocyte traffic in the lymph node. Trends Immunol 28: 346-352
3. Barnden MJ, Allison J, Heath WR, Carbone FR (1998) Defective TCR expression in transgenic mice constructed using cDNA-based alpha-and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol 76: 34-40
4. Berlin-Rufenach C, Otto F, Mathies M, Westermann J, Owen MJ, Hamann A, Hogg N (1999) Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J Exp Med 189: 1467-1478
5. Boscacci RT, Pfeiffer F, Gollmer K, Sevilla AI, Martin AM, Soriano SF, Natale D, Henrickson S, von Andrian UH, Fukui Y, Mellado M, Deutsch U, Engelhardt B, Stein JV (2010) Comprehensive analysis of lymph node stroma-expressed Ig superfamily members reveals redundant and nonredundant roles for ICAM-1, ICAM-2, and VCAM-1 in lymphocyte homing. Blood 116: 915-925
6. Bullard DC, Hu X, Schoeb TR, Collins RG, Beaudet AL, Barnum SR (2007) Intercellular adhesion molecule-1 expression is required on multiple cell types for the development of experimental autoimmune encephalomyelitis. J Immunol 178: 851-857
7. Carrasco YR, Fleire SJ, Cameron T, Dustin ML, Batista FD (2004) LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20: 589-599
8. Evans R, Lellouch AC, Svensson L, McDowall A, Hogg N (2011) The integrin LFA-1 signals through ZAP-70 to regulate expression of high affinity LFA-1 on T lymphocytes. Blood 117: 3331-3342
9. Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, Hogg N (2009) Integrins in immunity. J Cell Sci 122: 215-225
10. Girard JP, Moussion C, Forster R (2012) HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol 12: 762-773
11. Gordon EJ, Rao S, Pollard JW, Nutt SL, Lang RA, Harvey NL (2010) Macrophages define dermal lymphatic vessel calibre during development by regulating lymphatic endothelial cell proliferation. Development 137: 3899-3910
12. Gowans JL (1957) The effect of the continuous re-infusion of lymph and lymphocytes on the output of lymphocytes from the thoracic duct of unanaesthetized rats. Br J Exp Pathol 38: 67-78
13. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML (1999) The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227
14. Gretz JE, Norbury CC, Anderson AO, Proudfoot AE, Shaw S (2000) Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J Exp Med 192: 1425-1440
15. Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci USA 107: 20447-20452
16. Grigorova IL, Schwab SR, Phan TG, Pham TH, Okada T, Cyster JG (2009) Cortical sinus probing, S1P1-dependent entry and flowbased capture of egressing T cells. Nat Immunol 10: 58-65
17. Gunzer M, Schafer A, Borgmann S, Grabbe S, Zanker KS, Brocker EB, Kampgen E, Friedl P (2000) Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13: 323-332
18. Gunzer M, Weishaupt C, Hillmer A, Basoglu Y, Friedl P, Dittmar KE, Kolanus W, Varga G, Grabbe S (2004) A spectrum of biophysical interaction modes between T cells and different antigen-presenting cells during priming in 3-D collagen and in vivo. Blood 104: 2801-2809
19. Halin C, Scimone ML, Bonasio R, Gauguet JM, Mempel TR, Quackenbush E, Proia RL, Mandala S, von Andrian UH (2005) The S1P-analog FTY720 differentially modulates T-cell homing via HEV: T-cell-expressed S1P1 amplifies integrin activation in peripheral lymph nodes but not in Peyer patches. Blood 106: 1314-1322
20. Hamann A, Jablonski-Westrich D, Duijvestijn A, Butcher EC, Baisch H, Harder R, Thiele HG (1988) Evidence for an accessory role of LFA-1 in lymphocyte-high endothelium interaction during homing. J Immunol 140: 693-699
21. Heasman SJ, Carlin LM, Cox S, Ng T, Ridley AJ (2010) Coordinated RhoA signaling at the leading edge and uropod is required for T cell transendothelial migration. J Cell Biol 190: 553-563
22. Ho WY, Cooke MP, Goodnow CC, Davis MM (1994) Resting and anergic B cells are defective in CD28-dependent costimulation of naive CD4\+ T cells. J Exp Med 179: 1539-1549
23. Johnson LA, Clasper S, Holt AP, Lalor PF, Baban D, Jackson DG (2006) An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium. J Exp Med 203: 2763-2777
24. Katakai T, Hara T, Sugai M, Gonda H, Shimizu A (2004) Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med 200: 783-795
25. Klinger A, Gebert A, Bieber K, Kalies K, Ager A, Bell EB, Westermann J (2009) Cyclical expression of L-selectin (CD62L) by recirculating T cells. Int immunol 21: 443-455
26. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, Keller M, Forster R, Critchley DR, Fassler R, Sixt M (2008) Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453: 51-55
27. Ledgerwood LG, Lal G, Zhang N, Garin A, Esses SJ, Ginhoux F, Merad M, Peche H, Lira SA, Ding Y, Yang Y, He X, Schuchman EH, Allende ML, Ochando JC, Bromberg JS (2008) The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol 9: 42-53
28. Lehmann JC, Jablonski-Westrich D, Haubold U, Gutierrez-Ramos JC, Springer T, Hamann A (2003) Overlapping and selective roles of endothelial intercellular adhesion molecule-1 (ICAM-1) and ICAM-2 in lymphocyte trafficking. J Immunol 171: 2588-2593
29. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8: 1255-1265
30. Lo CG, Xu Y, Proia RL, Cyster JG (2005) Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J Exp Med 201: 291-301
31. Matheu MP, Cahalan MD, Parker I (2011) Immunoimaging: studying immune system dynamics using two-photon microscopy. Cold Spring Harb Protoc 2011: 147-155
32. Mempel TR, Henrickson SE, Von Andrian UH (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159
33. Miller MJ, Wei SH, Parker I, Cahalan MD (2002) Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296: 1869-1873
34. Nombela-Arrieta C, Mempel TR, Soriano SF, Mazo I, Wymann MP, Hirsch E, Martinez AC, Fukui Y, von Andrian UH, Stein JV (2007) A central role for DOCK2 during interstitial lymphocyte motility and sphingosine-1-phosphate-mediated egress. J Exp Med 204: 497-510
35. Paik JH, Chae S, Lee MJ, Thangada S, Hla T (2001) Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3-and beta1-containing integrins. J Biol Chem 276: 11830-11837
36. Park EJ, Peixoto A, Imai Y, Goodarzi A, Cheng G, Carman CV, von Andrian UH, Shimaoka M (2010) Distinct roles for LFA-1 affinity regulation during T-cell adhesion, diapedesis, and interstitial migration in lymph nodes. Blood 115: 1572-1581
37. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG (2008) S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28: 122-133
38. Podgrabinska S, Kamalu O, Mayer L, Shimaoka M, Snoeck H, Randolph GJ, Skobe M (2009) Inflamed lymphatic endothelium suppresses dendritic cell maturation and function via Mac-1/ICAM-1-dependent mechanism. J Immunol 183: 1767-1779
39. Randolph GJ, Angeli V, Swartz MA (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 5: 617-628
40. Reichardt P, Dornbach B, Rong S, Beissert S, Gueler F, Loser K, Gunzer M (2007a) Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood 110: 1519-1529
41. Reichardt P, Gunzer F, Gunzer M (2007b) Analyzing the physicodynamics of immune cells in a three-dimensional collagen matrix. Methods Mol Biol 380: 253-269
42. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, Don A, Marsolais D, Matheu MP, Wei SH, Parker I, Jo E, Cheng WC, Cahalan MD, Wong CH, Rosen H (2006) Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat Chem Biol 2: 434-441
43. Schumann K, Lammermann T, Bruckner M, Legler DF, Polleux J, Spatz JP, Schuler G, Forster R, Lutz MB, Sorokin L, Sixt M (2010) Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 32: 703-713
44. Shulman Z, Shinder V, Klein E, Grabovsky V, Yeger O, Geron E, Montresor A, Bolomini-Vittori M, Feigelson SW, Kirchhausen T, Laudanna C, Shakhar G, Alon R (2009) Lymphocyte crawling and transendothelial migration require chemokine triggering of highaffinity LFA-1 integrin. Immunity 30: 384-396
45. Sinha RK, Park C, Hwang IY, Davis MD, Kehrl JH (2009) B lymphocytes exit lymph nodes through cortical lymphatic sinusoids by a mechanism independent of sphingosine-1-phosphate-mediated chemotaxis. Immunity 30: 434-446
46. Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP, Pabst R, Lutz MB, Sorokin L (2005) The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 22: 19-29
47. Smith ME, Ford WL (1983) The recirculating lymphocyte pool of the rat: a systematic description of the migratory behaviour of recirculating lymphocytes. Immunology 49: 83-94
48. Svensson L, Howarth K, McDowall A, Patzak I, Evans R, Ussar S, Moser M, Metin A, Fried M, Tomlinson I, Hogg N (2009) Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat Med 15: 306-312
49. Tal O, Lim HY, Gurevich I, Milo I, Shipony Z, Ng LG, Angeli V, Shakhar G (2011) DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J Exp Med 208: 2141-2153
50. Tomura M, Yoshida N, Tanaka J, Karasawa S, Miwa Y, Miyawaki A, Kanagawa O (2008) Monitoring cellular movement in vivo with photoconvertible fluorescence protein "Kaede" transgenic mice. Proc Natl Acad Sci USA 105: 10871-10876
51. von Andrian UH, Mempel TR (2003) Homing and cellular traffic in lymph nodes. Nat Rev Immunol 3: 867-878
52. Wei SH, Rosen H, Matheu MP, Sanna MG,Wang SK, Jo E,Wong CH, Parker I, Cahalan MD (2005) Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat Immunol 6: 1228-1235
53. Westermann J, Bode U, Sahle A, Speck U, Karin N, Bell EB, Kalies K, Gebert A (2005) Naive, effector, and memory T lymphocytes efficiently scan dendritic cells in vivo: contact frequency in T cell zones of secondary lymphoid organs does not depend on LFA-1 expression and facilitates survival of effector Tcells. J Immunol 174: 2517-2524
54. Woolf E, Grigorova I, Sagiv A, Grabovsky V, Feigelson SW, Shulman Z, Hartmann T, Sixt M, Cyster JG, Alon R (2007) Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat Immunol 8: 1076-1085