The physiology of leukocyte recruitment: An in vivo perspective

Journal of Immunology

Volumn 180, Issue 10, 2008, Pages 6439-6446

  Petri, Björn ^a   Phillipson, Mia ^b   Kubes, Paul ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; SELECTIN;

CHEMOTAXIS; GLYCOCALYX; HUMAN; LEUKOCYTE ADHERENCE; LEUKOCYTE CRAWLING; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; LEUKOCYTE RECRUITMENT; LEUKOCYTE ROLLING; MICROCIRCULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SHEAR STRESS; VASCULITIS; ANIMAL; IMMUNOLOGY; INFLAMMATION; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; HUMANS; INFLAMMATION;

EID: 45549106551     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.10.6439     Document Type: Review

References (92)

1. Kansas, G. S. 1996. Selectins and their ligands: current concepts and controversies. Blood 88: 3259-3287.
2. Kelly, M., J. M. Hwang, and P. Kubes. 2007. Modulating leukocyte recruitment in inflammation. J. Allergy Clin. Immunol. 120: 3-10.
3. Petri, B., and M. G. Bixel. 2006. Molecular events during leukocyte diapedesis. FEBS J. 273: 4399-4407.
4. Yao, L, J. Pan, H. Setiadi, K. D. Patel, and R. P. McEver. 1996. Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J. Exp. Med. 184: 81-92.
5. Woltmann, G., C. A. McNulty, G. Dewson, F. A. Symon, and A. J. Wardtaw. 2000. Interleukin-13 induces PSGL-1/P-selectin-dependent adhesion of eosinophils, but not neutrophils, to human umbilical vein endothelial cells under flow. Blood 95: 3146-3152.
6. Pan, J., L. Xia, and R. P. McEver. 1998. Comparison of promoters for the murine and human P-selectin genes suggests species-specific and conserved mechanisms for tran-scriptional regulation in endothelial cells. J. Biol. Chem. 273: 10058-10067.
7. Yao, L., H. Setiadi, L. Xia, Z. Laszik, F. B. Taylor, and R. P. McEver. 1999. Divergent inducible expression of P-selectin and E-selectin in mice and primates. Blood 94: 3820-3828.
8. + lymphocyte homing and initiation of late phase inflammation in contact sensitivity. J. Exp. Med. 199: 1223-1234.
9. Kunkel, E. J., and K. Ley. 1996. Distinct phenotype of E-selectin-dcficicnt mice. E-selectin is required for slow leukocyte rolling in vivo. Circ. Res. 79: 1196-1204.
10. Kunkel, E. J., J. L. Dunne, and K. Ley. 2000. Leukocyte arrest during cytokine-dependent inflammation in vivo. J. Immunol. 164: 3301-3308.
11. x-dependent alterations in leukocyte kinetics in vivo. Circ. Res. 77: 879-887.
12. Setiadi, H., and R. P. McEver. 2003. Signal-dependent distribution of cell surface P-selectih in clathrin-coated pits affects leukocyte rolling under flow. J. Cell Biol. 163: 1385-1395.
13. Patel, K. D., M. U. Nollert, and R. P. McEver. 1995. P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils. J. Cell Biol. 131: 1893-1902.
14. Reitsma, S., D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink. 2007. The endothelial glycocalyx: composition, functions, and visualization. Pflugen Arch. 454: 345-359.
15. Weinbaum, S., J. M. Tarbell, and E. R. Damiano. 2007. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 9:121-167.
16. Woodman, R. C., B. Johnston, M. J. Hickey, D. Teoh, P. Reinhardt, B. Y. Poon, and P. Kubes. 1998. The functional paradox of CD43 in leukocyte recruitment: a study using CD43-deficient mice. J. Exp. Med. 188: 2181-2186.
17. Von Andrian, U. H., S. R. Hasslen, R. D. Nelson, S. L. Erlandsen, and E. C. Butcher. 1995. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell. 82: 989-999.
18. Stein, J. V., G. Cheng, B. M. Stockton, B. P. Fors, E. C. Butcher, and U. H. Von Andrian. 1999. L-selectin-mediated leukocyte adhesion in vivo: microvillous distribution determines tethering efficiency, but not rolling velocity. J. Exp. Med. 189: 37-50.
19. Walcheck, B., K. L. Moore, R. P. McEver, and T. K. Kishimoto. 1996. Neutrophil-neutrophil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1. A mechanism that amplifies initial leukocyte accumulation on P-selectin in vitro. J. Clin. Invest. 98: 1081-1087.
20. Mitchell, D. J., P. Li, P. H. Reinhardt, and P. Kubes. 2000. Importance of L-selectin-dependent leukocyte-leukocyte interactions in human whole blood. Blood 95: 2954-2959.
21. Kunkel, E. J., J. E. Chomas, and K. Ley. 1998. Role of primary and secondary capture for leukocyte accumulation in vivo. Circ. Res. 82:30-38.
22. Eriksson, E. E., X. Xie, J. Werr, P. Thoren, and L. Lindbom. 2001. Importance of primary capture and L-selectin-dependent secondary capture in leukocyte accumulation in inflammation and atherosclerosis in vivo. J. Exp. Med. 194: 205-218.
23. Sperandio, M., M. L. Smith, S. B. Forlow, T. S. Olson, L Xia, R. P. McEver, and K. Ley. 2003. P-selectin glycoprotein ligand-1 mediates L-sclectin-dependent leukocyte rolling in venules. J. Exp. Med. 197: 1355-1363.
24. Kubes, P., M. Jutila, and D. Payne. 1995. Therapeutic potential of inhibiting leukocyte rolling in ischemia/reperfusion. J. Clin. Invest. 95: 2510-2519.
25. Gaboury, J. P., and P. Kubes. 1994. Reductions in physiologic shear rates lead to CD11/CD18-dependcnt, selectin-independent leukocyte rolling in vivo. Blood 83: 345-350.
26. 2 in an intermediate affinity state. J. Biol. Chem. 281: 10876-10882.
27. 2 integrin-mediated rolling on intercellular adhesion molecule-1. Immunity. 26: 773-783.
28. 4 integrin in the inflammatory response of neutrophils. J. Exp. Med. 194: 219-226.
29. Mizgerd, J. P., B. B. Meek, G. J. Kutkoski, D. C. Bullard, A. L. Beaudet, and C. M. Doerschuk. 1996. Selectins and neutrophil traffic: margination and Streptococcus pneumoniae-induced emigration in murine lungs. J. Exp. Med. 184: 639-645.
30. Wong, J., B. Johnston, S. S. Lee, D. C. Bullard, C. W. Smith, A. L. Beaudet, and P. Kubes. 1997. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J. Clin. Invest. 99: 2782-2790.
31. Alon, R., P. D. Kassner, M. W. Carr, E. B, Finger, M. E. Hemler, and T. A. Springer. 1995. The integrin VLA-4 supports tethering and rolling in flow on VCAM-1. J. Cell Biol. 128: 1243-1253.
32. 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 80: 413-422.
33. 4-integrin supports leukocyte rolling and adhesion in chronically inflamed posteapillary venules in vivo. J. Exp. Med. 181: 1995-2006.
34. DeGrendele, H. C., P. Estess, L. J. Picker, and M. H. Siegelman. 1996. CD44 and its ligand hyaluronate mediate rolling under physiologic flow: a novel lymphocyte-endo-thelial cell primary adhesion pathway. J. Exp. Med. 183: 1119-1130.
35. Salmi, M., and S. Jalkanen. 1996. Human vascular adhesion protein 1 (VAP-1) is a unique sialoglycoprotein that mediates carbohydrate-dependent binding of lymphocytes to endothelial cells. J. Exp. Med. 183: 569-579.
36. Jalkanen, S., M. Karikoski, N. Mercier, K. Kosldncn, T, Henttinen, K. Elima, K. Salmivirra, and M. Salmi. 2007. The oxidase activity of vascular adhesion procein-l (VAP-I) induces cndothelial E- and P-selectins and leukocyte binding. Blood. 110: 1864-1870.
37. Salmi, M., S. Tohka, and S. Jalkanen. 2000. Human vascular adhesion protein-1 (VAP-1) plays a critical role in lymphocyte-endothelial cell adhesion cascade under shear. Ore. Res. 86: 1245-1251.
38. Gallin, J. I., and R. Snyderman, eds. 1999. Inflammation: Basic Principles and Clinical Correlates, 3rd Ed. Lippincott, Williams, and Wilkins, Philadelphia.
39. Luo, B. H., C. V. Carman, and T. A. Springer. 2007. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25:619-647.
40. 2- integrin on neutrophils. J. Immunol 172:7780-7790.
41. 2 integrin occupancy at apical cndothelial contacts combine with shear stress signals to promote transendothelial neutrophil migration. J. Immunol. 173: 7282-7291.
42. Staunton, D. E., M. L. D us tin, H. P. Erickson, and T. A. Springer. 1990. The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovims. Cell 61: 243-254.
43. Diamond, M. S., D. E. Staunton, S. D. Marlin, and T. A. Springer. 1991. Binding of the integrin Mac-1 (CD11b/CDl8) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylarion. Cell 65: 961-971.
44. Altieri, D. C., R. Bader, P. M. Mannucci, and T. S. Edgington. 1988. Oligospecificity of the cellular adhesion receptor Mac-1 encompasses an inducible recognition specificity for fibrinogen. J. Cell Biol. 107: 1893-1900.
45. Wojciechowski, J., and I. H. Sarelius. 2005. Preferential binding of leukocytes to the endothelial junction region in venules in situ. Microcircuiation 12: 349-359.
46. Schenkel, A. R., Z. Mamdouh, and W. A. Muller. 2004. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat. Immunol. 5: 393-400.
47. Burns, A. R., R. A. Bowden, Y. Abe, D. C. Walker, S. I. Simon, M. L. Entman, and C. W. Smith. 1999. P-selectin mediates neutrophil adhesion to endothelial cell borders. J. Leukocyte Biol. 65: 299-306.
48. Phillipson, M., B. Heit, P. Colarusso, L. Liu, C. M. Ballanryne, and P. Kubes. 2006. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203: 2569-2575.
49. 1 integrin receptors in human neutrophils. J. Leukocyte Biol. 68: 553-560.
50. 2 integrins are critically involved in neurrophil locomotion in extravascular tissue in vivo. J. Exp. Med. 187: 2091-2096.
51. Cinamon, G., V. Shinder, and R. Alon. 2001. Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat. Immunol 2: 515-522.
52. Cuvelier, S. L., and K. D. Patel. 2001. Shear-dependent eosinophil transmigration on interleukin 4-stimulated endothelial cells: a role for endotheliurn-associated eotaxin-3. J. Exp. Med. 194: 1699-1709.
53. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population ofmonocytes with patrolling behavior. Science 317: 666-670.
54. + NKT cells patrolling liver sinusoids. PLoS Biol 3: el 13.
55. Lee, W. Y., and P. Kubes. 2007. Leukocyte adhesion in liver: distinct adhesion paradigm from other organs. J. Hepatol. 48: 504-512.
56. Burns, A. R., R. A. Bowden, S. D. MacDonell, D. C. Walker, T. O. Odebunmi, E. M. Donnachie, S. I. Simon, M. L. Entman, and C. W. Smith. 2000. Analysis of tight junctions during neutrophil transendothelial migration. J. Cell Sci. 113: 45-57.
57. Carman, C. V., and T. A. Springer. 2004. A transmigratory cup in leukocyte diape-desis both through individual vascular endothelial cells and between them. J. Cell Biol. 167: 377-388.
58. Nieminen, M., T. Henttinen, M. Merinen, F. Marttila-Ichihara, J. E. Eriksson, and S. Jalkanen. 2006. Vimentin function in lymphocyte adhesion and transcellular migration. Nat. Cell Biol. 8: 156-162.
59. Carman, C. V., P. T. Sage, T. E. Sciuto, M. A. de la Fuenre, R. S. Geha, H. D. Ochs, H. F. Dvorak, A. M. Dvorak, and T. A. Springer. 2007. Transcellular diapedesis is initiated by invasive podosomes. Immunity 26: 784-797.
60. Feng, D., J. A. Nagy, K. Pyne, H. F. Dvorak, and A. M. Dvorak. 1998. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med 187: 903-915.
61. Heit, B., S. Tavener, E. Raharjo, and P. Kubes. 2002. An intracellular signaling hierarchy determines direction of migration in opposing chemotacric gradients. J. Cell Biol. 159: 91-102.
62. Wegmann, F., B. Petri, A. G. Khandoga, C. Moser, A. Khandoga, S. Volkery, H. Li, I. Nasdala, O. Brandau, R. Fassler, et al. 2006. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med. 203: 1671-1677.
63. Yang, L., R. M. Froio, T. E. Sciuto, A. M. Dvorak, R. Alon, and F. W. Luscinskas. 2005. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular endothelium under flow. Blood 106: 584-592.
64. Huang, M. T., K. Y. Larbi, C. Scheiermann, A. Woodfin, N. Gerwin, D. O. Haskard, and S. Nourshargh. 2006. ICAM-2 mediates neutrophil transmigration in vivo: evidence for stimulus specificity and a role in PECAM-1-independenr transmigration. Blood 107: 4721-4727.
65. 6 integrin inhibits IL-1β-but not TNF-α-induced neutrophil transmigration in vivo. J. Leukocyte Biol 77: 159-165.
66. Young, R. E., R. D. Thompson, and S. Nourshargh. 2002. Divergent mechanisms of action of the inflammatory cytokines interleukm 1-β and tumour necrosis factor-α in mouse cremasteric venules. Br. J. Pharmacol. 137: 1237-1246.
67. Shaw, S. K., S. Ma, M. B. Kim, R. M. Rao, C. U. Hartman, R. M. Froio, L. Yang, T. Jones, Y. Liu, A. Nusrat, et al. 2004. Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J. Exp. Med. 200: 1571-1580.
68. Barreiro, O., M. Yanez-Mo, J. M. Serrador, M. C. Montoya, M. Vicente-Manzanares, R. Tejedor, H. Furthmayr, and F. Sanchez-Madrid. 2002. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol. 157: 1233-1245.
69. Barreiro, O., M. Vicente-Manzanares, A. Urzainqui, M. Yanez-Mo, and F. Sanchez-Madrid. 2004. Interactive protrusive structures during leukocyte adhesion and transendothelial migration. Front Biosci. 9: 1849-1863.
70. Phillipson, M., J. Kaur, P. Colarusso, C. M. Ballantyne, and P. Kubes. 2008. Endo-thelial domes encapsulate adherent neutrophils and minimize increases in vascular permeability in paracellular and transcellular emigration. PLoS ONE 3: e1649.
71. 4). Microvasc. Res. 35: 27-47.
72. 4. Microvasc. Res. 37: 53-69.
73. Mamdouh, Z., X. Chen, L. M. Pierini, F. R. Maxfield, and W. A. Muller. 2003. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 421: 748-753.
74. Wang, S., M. B. Voisin, K. Y. Larbi, J. Dangerfield, C. Scheiermann, M. Tran, P. H. Maxwell, L. Sorokin, and S. Nourshargh. 2006. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J. Exp. Med 203: 1519-1532.
75. Liu, L., and P. Kubes. 2003. Molecular mechanisms of leukocyte recruitment: organ-specific mechanisms of action. Thromb. Haemost. 89: 213-220.
76. Engelhardt, B. 2006. Molecular mechanisms involved in T cell migration across the blood-brain barrier. J. Neural Transm. 113: 477-485.
77. Doerschuk, C. M. 2001. Mechanisms of leukocyte sequestration in inflamed lungs. Microcircuiation. 8: 71-88.
78. Jaeschke, H. 1997. Cellular adhesion molecules: regulation and functional significance in the pathogenesis of liver diseases. Am. J. Physiol. 273: G602-G611.
79. + T cells in the liver. J. Immunol. 172: 5222-5229.
80. Sato, T., A. Habtezion, A. Beilhack, S. Schulz, E. Butcher, and H. Thorlacius. 2006. Short-term homing assay reveals a critical role for lymphocyte function-associated antigen-1 in the hepatic recruitment of lymphocytes in graft-versus-host disease. J. Hepatol. 44: 1132-1140.
81. + T cells is predominantly ICAM-l/LFA-1 dependent in mice. Hepatology 42: 1063-1071.
82. Bonder, C. S., M. U. Norman, M. G. Swain, L. D. Zbytnuik, J. Yamanouchi, P. Santamaria, M. Ajuebor, M. Salmi, S. Jalkanen, and P. Kubes. 2005. Rules of recruitment for Th1 and Th2 lymphocytes in inflamed liver: A role for α-4 integrin and vascular adhesion protein-1. Immunity 23: 153-163.
83. Lalor, P. F., S. Edwards, G. McNab, M. Salmi, S. Jalkanen, and D. H. Adams. 2002. Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells. J. Immunol. 169: 983-992.
84. Carvalho-Tavares, J., M. J. Hickey, J. Hutchison, J. Michaud, I. T. Sutcliffe, and P. Kubes. 2000. A role for platelets and endothelial selecrins in tumor necrosis factor-α-induced leukocyte recruitment in the brain microvasculature. Circ. Res. 87: 1141-1148.
85. Ishikawa, M., D. Cooper, J. Russell, J. W. Salter, J. H. Zhang, A. Nanda, and D. N. Granger. 2003. Molecular determinants of the prothrombogenic and inflammatory phenotype assumed by the postischemic cerebral microcircuiation. Stroke 34: 1777-1782.
86. Kuijper, P. H. M., H. I. G. Torres, J. A. M. van der Linden, J. W. J. Lammers, J. J. Sixma, L. Koenderman, and J. J. Zwaginga. 1996. Platelet-dependent primary hemostasis promotes selectin- and integrin-mediated neutrophil adhesion to damaged endothelium under flow conditions. Blood 87: 3271-3281.
87. llbβ3 and stimulated by platelet-activating factor. J. Clin. Invest. 100: 2085-2093.
88. Kuijper, P. H., H. I. Gallardo Tores, J. W. Lammers, J. J. Sixma, L. Koenderman, and J. J. Zwaginga. 1998. Platelet associated fibrinogen and ICAM-2 induce firm adhesion of neutrophils under flow conditions. Thromb. Haemost. 80: 443-448.
89. von Hundelshausen, P., F. Petersen, and E. Brandt. 2007. Platelet-derived chemokines in vascular biology. Thromb. Haemost. 97: 704-713.
90. Grady, M. S., R. F. Cody, Jr., D. O. Maris, T. D. McCall, H. Seckin, S. R. Sharar, and H. R. Winn. 1999. P-selectin blockade following fluid-percussion injury: behavioral and immunochemical sequelae. J. Neurotrauma 16: 13-25.
91. Suzuki, H., T. Hayashi, S. J. Tojo, H. Kitagawa, K. Kimura, M. Mizugaki, Y. Itoyama, and K. Abe. 1999. Anti-P-selectin antibody attenuates rat brain ischemic injury. Neurosci. Lett. 265: 163-166.
92. Doting, A., M. Wild, D. Vestweber, U. Deutsch, and B. Engelhardt. 2007. E- and P-selectin are not required for the development of experimental autoimmune enceph-alomyelitis in C57BL/6 and SJL mice. J. Immunol. 179: 8470-8479.