Chemokine signaling to lymphocyte integrins under shear flow

Microcirculation

Volumn 16, Issue 1, 2009, Pages 3-16

  Alon, Ronen ^a   Feigelson, Sara W ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

G proteins; Inflammation; Integrins; Shear flow; Trafficking

Indexed keywords

ALPHA4 INTEGRIN; CHEMOKINE; CHEMOKINE RECEPTOR CCR2; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; PERTUSSIS TOXIN; RAP1 PROTEIN; RHO FACTOR; STROMAL CELL DERIVED FACTOR 1; THYMUS AND ACTIVATION REGULATED CHEMOKINE; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4;

CELL ADHESION; CELL LINE; CONFORMATIONAL TRANSITION; GENE ACTIVATION; HUMAN; IMMOBILIZED CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SHEAR FLOW; SHEAR STRENGTH; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; VASCULAR ENDOTHELIUM;

ANIMALS; CELL ADHESION; CHEMOKINES; CHEMOTAXIS; ENDOTHELIUM, VASCULAR; GTP PHOSPHOHYDROLASES; HUMANS; INTEGRINS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; SHEAR STRENGTH;

EID: 59649105507     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680802026076     Document Type: Review

References (74)

1. Alon, R., Aker, M., Feigelson, S., Sokolovsky-Eisenberg, M., Staunton, DE, Cinamon, G., Grabovsky, V., Shamri, R. and Etzioni, A. (2003) A novel genetic leukocyte adhesion deficiency in subsecond triggering of integrin avidity by endothelial chemokines results in impaired leukocyte arrest on vascular endothelium under shear flow. Blood, 101, pp. 4437-4445.
2. Alon, R. and Dustin, ML. (2007) Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity, 26, pp. 17-27.
3. Alon, R., Feigelson, SW, Rose, DM, Schmitz, J., Manevich, E., Overby, DR, Winter, E., Grabovsky, V., Shinder, V., Matthews, BD, Sokolovsky-Eisenberg, M., Ingber, DE, Benoit, M. and Ginsberg, MH. (2005) Integrin α4β1(VLA-4)-dependent T cell tethering and adhesion strengthening under shear stress requires paxillin binding to the α4 cytoplasmic domain. J Cell Biol, 171, pp. 1073-1084.
4. Alon, R., Grabovsky, V. and Feigelson, S. (2003) Chemokine induction of integrin adhesiveness on rolling and arrested leukocytes: Local signaling events or global stepwise activation?. Microcirculation, 10, pp. 297-311.
5. Astrof, NS, Salas, A., Shimaoka, M., Chen, J. and Springer, TA. (2006) Importance of force linkage in mechanochemistry of adhesion receptors. Biochemistry, 45, pp. 15020-15028.
6. Atarashi, K., Hirata, T., Matsumoto, M., Kanemitsu, N. and Miyasaka, M. (2005) Rolling of Th1 cells via P-selectin glycoprotein ligand-1 stimulates LFA-1-mediated cell binding to ICAM-1. J Immunol, 174, pp. 1424-1432.
7. Bargatze, RF and Butcher, EC. (1993) Rapid G-protein-regulated activation event involved in lymphocyte binding to high endothelial venules. J Exp Med, 178, pp. 367-372.
8. Berlin, C., Bargatze, RF, Campbell, JJ, von Andrian, UH, Szabo, MC, Hasslen, SR, Nelson, RD, Berg, EL, Erlandsen, SL and Butcher, EC. (1995) 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell, 80, pp. 413-422.
9. Berlin, C., Berg, EL, Briskin, MJ, Andrew, DP, Kilshaw, PJ, Holzmann, B., Weissman, IL, Hamann, A. and Butcher, EC. (1993) Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular address in MAdCAM-1. Cell, 74, p. 185.
10. Butcher, EC. (1991) Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity. Cell, 67, pp. 1033-1036.
11. Campbell, JJ, Haraldsen, G., Pan, J., Rottman, J., Qin, S., Ponath, P., Andrew, DP, Warnke, R., Ruffing, N., Kassam, N., Wu, L. and Butcher, EC. (1999) The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature, 400, pp. 776-780.
12. Campbell, JJ, Hedrick, J., Zlotnik, A., Siani, MA and Thompson, DA. (1998) Chemokines and the arrest of lymphocytes rolling under flow conditions. Science, 279, pp. 381-384.
13. Campbell, JJ, Qin, S., Bacon, KB, Mackay, CR and Butcher, EC. (1996) Biology of chemokine and classical chemoattractant receptors: differential requirements for adhesion-triggering versus chemotactic responses in lymphoid cells. J Cell Biol, 134, pp. 255-266.
14. Carr, MW, Roth, SJ, Luther, E., Rose, SS and Springer, TA. (1994) Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci USA, 91, pp. 3652-3656.
15. Chen, C., Mobley, JL, Dwir, O., Shimron, F., Grabovsky, V., Lobb, RL, Shimizu, Y. and Alon, R. (1999) High-affinity VLA-4 subsets expressed on T cells are mandatory for spontaneous adhesion strengthening but not for rolling on VCAM-1 in shear flow. J Immunol, 162, pp. 1084-1095.
16. Chong, LD, Traynor-Kaplan, A., Bokoch, GM and Schwartz, MA. (1994) The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell, 79, pp. 507-513.
17. Cinamon, G. and Alon, R. (2003) A real-time in vitro assay for studying leukocyte transendothelial migration under physiological flow conditions. J Immunol Meth, 273, pp. 53-62.
18. Cinamon, G., Shinder, V., Shamri, R. and Alon, R. (2004) Chemoattractant signals and β2 integrin occupancy at apical endothelial contacts combine with shear stress signals to promote transendothelial neutrophil migration. J Immunol, 173, pp. 7282-7291.
19. Constantin, G., Majeed, M., Giagulli, C., Piccio, L., Kim, JY, Butcher, EC and Laudanna, C. (2000) Chemokines trigger immediate β2 integrin affinity and mobility changes: Differential regulation and roles in lymphocyte arrest under flow. Immunity, 13, pp. 759-769.
20. Crittenden, JR, Bergmeier, W., Zhang, Y., Piffath, CL, Liang, Y., Wagner, DD, Housman, DE and Graybiel, AM. (2004) CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat Med, 10, pp. 982-986.
21. D'Ambrosio, D., Albanesi, C., Lang, R., Girolomoni, G., Sinigaglia, F. and Laudanna, C. (2002) Quantitative differences in chemokine receptor engagement generate diversity in integrin-dependent lymphocyte adhesion. J Immunol, 169, pp. 2303-2312.
22. del Pozo, MA, Nieto, M., Serrador, JM, Sancho, D., Vicente-Manzanares, M., Martinez, C. and Sanchez-Madrid, F. (1998) The two poles of the lymphocyte: Specialized cell compartments for migration and recruitment. Cell Adhes Commun, 6, pp. 125-133.
23. del Pozo, MA, Sanchez Mateos, P, Nieto, M. and Sanchez Madrid, F. (1995) Chemokines regulate cellular polarization and adhesion receptor redistribution during lymphocyte interaction with endothelium and extracellular matrix. Involvement of cAMP signaling pathway. J Cell Biol, 131, pp. 495-508.
24. DiVietro, JA, Brown, DC, Sklar, LA, Larson, RS and Lawrence, MB. (2007) Immobilized stromal cell-derived factor-1alpha triggers rapid VLA-4 affinity increases to stabilize lymphocyte tethers on VCAM-1 and subsequently initiate firm adhesion. J Immunol, 178, pp. 3903-3911.
25. Fitzhugh, DJ, Naik, S., Caughman, SW and Hwang, ST. (2000) Cutting edge: C-C chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J Immunol, 165, pp. 6677-6681.
26. Fukui, Y., Hashimoto, O., Sanui, T., Oono, T., Koga, H., Abe, M., Inayoshi, A., Noda, M., Oike, M., Shirai, T. and Sasazuki, T. (2001) Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration. Nature, 412, pp. 826-831.
27. Garcia-Bernal, D., Sotillo-Mallo, E., Nombela-Arrieta, C., Samaniego, R., Fukui, Y., Stein, JV and Teixido, J. (2006) DOCK2 is required for chemokine-promoted human T lymphocyte adhesion under shear stress mediated by the integrin alpha4beta1. J Immunol, 177, pp. 5215-5225.
28. Garcia-Bernal, D., Wright, N., Sotillo-Mallo, E., Nombela-Arrieta, C., Stein, JV, Bustelo, XR and Teixido, J. (2005) Vav1 and Rac control chemokine-promoted T lymphocyte adhesion mediated by the integrin α4β1. Mol Biol Cell, 16, pp. 3223-3235.
29. Ghandour, H., Cullere, X., Alvarez, A., Luscinskas, FW and Mayadas, TN. (2007) 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, 110, pp. 3682-3690.
30. Giagulli, C., Scarpini, E., Ottoboni, L., Narumiya, S., Butcher, EC, Constantin, G. and Laudanna, C. (2004) RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines. Critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity, 20, pp. 25-35.
31. Grabovsky, V., Feigelson, S., Chen, C., Bleijs, R., Peled, A., Cinamon, G., Baleux, F., Arenzana-Seisdedos, F., Lapidot, T., van Kooyk, Y., Lobb, R. and Alon, R. (2000) Subsecond induction of α4 integrin clustering by immobilized chemokines enhances leukocyte capture and rolling under flow prior to firm adhesion to endothelium. J Exp Med, 192, pp. 495-505.
32. Katagiri, K., Maeda, A., Shimonaka, M. and Kinashi, T. (2003) RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat Immunol, 4, pp. 741-748.
33. Kim, M., Carman, CV and Springer, TA. (2003) Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science, 301, pp. 1720-1725.
34. Kim, M., Carman, CV, Yang, W., Salas, A. and Springer, TA. (2004) The primacy of affinity over clustering in regulation of adhesiveness of the integrin α1;Lβ2. J Cell Biol, 167, pp. 1241-1253.
35. Kinashi, T. (2005) Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol, 5, pp. 546-559.
36. Kinashi, T., Aker, M., Sokolovsky-Eisenberg, M., Grabovsky, V., Tanaka, C., Shamri, R., Feigelson, S., Etzioni, A. and Alon, R. (2004) LAD-III, a leukocyte adhesion deficiency syndrome associated with defective Rap1 activation and impaired stabilization of integrin bonds. Blood, 103, pp. 1033-1036.
37. Kubes, P. (2002) Introduction: The complexities of leukocyte recruitment. Semin Immunol, 14, pp. 65-72.
38. Laudanna, C. (2004) Analysis of integrin-dependent rapid adhesion under laminar-flow conditions. Meth Mol Biol, 239, pp. 17-26.
39. Laudanna, C. and Alon, R. (2006) Right on the spot. Chemokine triggering of integrin-mediated arrest of rolling leukocytes. Thromb Haemost, 95, pp. 5-11.
40. Lawrence, MB, Berg, EL, Butcher, EC and Springer, TA. (1995) Rolling of lymphocytes and neutrophils on peripheral node addressin and subsequent arrest on ICAM-1 in shear flow. Eur J Immunol, 25, pp. 1025-1031.
41. Lawrence, MB and Springer, TA. (1991) Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins. Cell, 65, pp. 859-873.
42. Ley, K. (2003) Arrest chemokines. Microcirculation, 10, pp. 289-295.
43. Ley, K., Laudanna, C., Cybulsky, MI and Nourshargh, S. (2007) Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol, 7, pp. 678-689.
44. Lloyd, AR, Oppenheim, JJ, Kelvin, DJ and Taub, DD. (1996) Chemokines regulate T cell adherence to recombinant adhesion molecules and extracellular matrix proteins. J Immunol, 156, pp. 932-938.
45. Luster, AD, Alon, R. and von Andrian, UH. (2005) Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol, 6, pp. 1182-1190.
46. Mancuso, F., Flower, RJ and Perretti, M. (1995) Leukocyte transmigration, but not rolling or adhesion, is selectively inhibited by dexamethasone in the hamster post-capillary venule. Involvement of endogenous lipocortin 1. J Immunol, 155, pp. 377-386.
47. Manevich, E., Grabovsky, V., Feigelson, SW and Alon, R. (2007) Talin 1 and paxillin facilitate distinct steps in rapid VLA-4-mediated adhesion strengthening to vascular cell adhesion molecule 1. J Biol Chem, 282, pp. 25338-25348.
48. Nombela-Arrieta, C., Lacalle, RA, Montoya, MC, Kunisaki, Y., Megias, D., Marques, M., Carrera, AC, Manes, S., Fukui, Y., Martinez, AC and Stein, JV. (2004) Differential requirements for DOCK2 and phosphoinositide-3-kinase gamma during T and B lymphocyte homing. Immunity, 21, pp. 429-441.
49. Pachynski, RK, Wu, SW, Gunn, MD and Erle, DJ. (1998) Secondary lymphoid-tissue chemokine (SLC) stimulates integrin α4β7-mediated adhesion of lymphocytes to mucosal addressin cell adhesion molecule-1 (MAdCAM-1) under flow. J Immunol, 161, pp. 952-956.
50. Pasvolsky, R., Feigelson, SW, Kilic, SS, Simon, AJ, Tal-Lapidot, G., Grabovsky, V., Crittenden, JR, Amariglio, N., Safran, M., Graybiel, AM, Rechavi, G., Ben-Dor, S., Etzioni, A. and Alon, R. (2007) A LAD-III syndrome is associated with defective expression of the Rap-1 activator CalDAG-GEFI in lymphocytes, neutrophils, and platelets. J Exp Med, 204, pp. 1571-1582.
51. Pasvolsky, R., Grabovsky, V., Giagulli, C., Shulman, Z., Shamri, R., Feigelson, SW, Laudanna, C. and Alon, R. (2008) RhoA is involved in LFA-1 extension triggered by CXCL12 but not in a novel outside-in LFA-1 activation facilitated by CXCL9. J Immunol, 180, pp. 2815-2823.
52. Peled, A., Grabovsky, V., Habler, L., Sandbank, J., Arenzana-Seisdedos, F., Petit, I., Ben-Hur, H., Lapidot, T. and Alon, R. (1999) The chemokine SDF-1 stimulates integrin-mediated arrest of CD34+ cells on vascular endothelium under shear flow. J Clin Invest, 104, pp. 1199-1211.
53. Phillipson, M., Heit, B., Colarusso, P., Liu, L., Ballantyne, CM and Kubes, P. (2006) Intraluminal crawling of neutrophils to emigration sites: A molecularly distinct process from adhesion in the recruitment cascade. J Exp Med, 203, pp. 2569-2575.
54. Puklin-Faucher, E., Gao, M., Schulten, K. and Vogel, V. (2006) How the headpiece hinge angle is opened: New insights into the dynamics of integrin activation. J Cell Biol, 175, pp. 349-360.
55. Rot, A. and von Andrian, UH. (2004) Chemokines in innate and adaptive host defense: Basic chemokinese grammar for immune cells. Annu Rev Immunol, 22, pp. 891-928.
56. Schenkel, AR, Mamdouh, Z. and Muller, WA. (2004) Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol, 5, pp. 393-400.
57. Shamri, R., Grabovsky, V., Feigelson, S., Dwir, O., Van Kooyk, Y. and Alon, R. (2002) Chemokine-stimulation of lymphocyte α4 integrin avidity but not of LFA-1 avidity to endothelial ligands under shear flow requires cholesterol membrane rafts. J Biol Chem, 277, pp. 40027-40035.
58. Shamri, R., Grabovsky, V., Gauguet, JM, Feigelson, S., Manevich, E., Kolanus, W., Robinson, MK, Staunton, DE, von Andrian, UH and Alon, R. (2005) Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol, 6, pp. 497-506.
59. Shimaoka, M., Kim, M., Cohen, EH, Yang, W., Astrof, N., Peer, D., Salas, A., Ferrand, A. and Springer, TA. (2006) AL-57, a ligand-mimetic antibody to integrin LFA-1, reveals chemokine-induced affinity up-regulation in lymphocytes. Proc Natl Acad Sci USA, 103, pp. 13991-13996.
60. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O. and Kinashi, T. (2003) Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J Cell Biol, 161, pp. 417-427.
61. Shulman, Z., Pasvolsky, R., Woolf, E., Grabovsky, V., Feigelson, SW, Erez, N., Fukui, Y. and Alon, R. (2006) DOCK2 regulates chemokine-triggered lateral lymphocyte motility but not transendothelial migration. Blood, 108, pp. 2150-2158.
62. Smith, A., Bracke, M., Leitinger, B., Porter, JC and Hogg, N. (2003) LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J Cell Sci, 116, pp. 3123-3133.
63. Springer, TA. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell, 76, pp. 301-314.
64. Stein, JV, Rot, A., Luo, Y., Narasimhaswamy, M., Nakano, H., Gunn, MD, Matsuzawa, A., Quackenbush, EJ, Dorf, ME and von Andrian, UH. (2000) The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, Exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J Exp Med, 191, pp. 61-76.
65. Tanaka, Y., Adams, DH, Hubscher, S., Hirano, H., Siebenlist, U. and Shaw, S. (1993) T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1 beta. Nature, 361, pp. 79-82.
66. Viola, A., Contento, RL and Molon, B. (2006) T cells and their partners: the chemokine dating agency. Trends Immunol, 27, pp. 421-427.
67. Warnock, RA, Askari, S., Butcher, EC and von Andrian, UH. (1998) Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J Exp Med, 187, pp. 205-216.
68. Warnock, RA, Campbell, JJ, Dorf, ME, Matsuzawa, A., McEvoy, LM and Butcher, EC. (2000) The role of chemokines in the microenvironmental control of T versus B cell arrest in Peyer's patch high endothelial venules. J Exp Med, 191, pp. 77-88.
69. Weber, C., Alon, R., Moser, B. and Springer, TA. (1996) Sequential regulation of alpha 4 beta 1 and alpha 5 beta 1 integrin avidity by CC chemokines in monocytes: Implications for transendothelial chemotaxis. J Cell Biol, 134, pp. 1063-1073.
70. Weber, C. and Springer, TA. (1998) Interaction of very late antigen-4 with VCAM-1 supports transendothelial chemotaxis of monocytes by facilitating lateral migration. J Immunol, 161, pp. 6825-6834.
71. Weber, C., Weber, KS, Klier, C., Gu, S., Wank, R., Horuk, R. and Nelson, PJ. (2001) Specialized roles of the chemokine receptors CCR1 and CCR5 in the recruitment of monocytes and Th1-like/CD45RO+ T cells. Blood, 97, pp. 1144-1146.
72. Woolf, E., Grigorova, I., Sagiv, A., Grabovsky, V., Feigelson, SW, Shulman, Z., Hartmann, T., Sixt, M., Cyster, JG and 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, pp. 1076-1085.
73. Zarbock, A., Lowell, CA and Ley, K. (2007) Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity, 26, pp. 773-783.
74. Zhang, H., Schaff, UY, Green, CE, Chen, H., Sarantos, MR, Hu, Y., Wara, D., Simon, SI and Lowell, CA. (2006) Impaired integrin-dependent function in Wiskott-Aldrich syndrome protein-deficient murine and human neutrophils. Immunity, 25, pp. 285-295.