Leukotriene B4-Neutrophil Elastase Axis Drives Neutrophil Reverse Transendothelial Cell Migration InVivo

Immunity

Volumn 42, Issue 6, 2015, Pages 1075-1086

  Colom, Bartomeu ^a   Bodkin, Jennifer V ^a   Beyrau, Martina ^a   Woodfin, Abigail ^a   Ody, Christiane ^b   Rourke, Claire ^a   Chavakis, Triantafyllos ^c   Brohi, Karim ^a   Imhof, Beat A ^b   Nourshargh, Sussan ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; JUNCTIONAL ADHESION MOLECULE C; LEUKOCYTE ELASTASE; LEUKOTRIENE B4; BENZOIC ACID DERIVATIVE; CELL ADHESION MOLECULE; ETALOCIB; IMMUNOGLOBULIN; JAM3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME MECHANISM; HUMAN; IN VIVO STUDY; INFLAMMATION; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL JUNCTION; DRUG EFFECTS; ENDOTHELIUM CELL; GENETICS; IMMUNOLOGY; INJURY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; REPERFUSION INJURY; VENULE;

ANIMALS; BENZOATES; CELL ADHESION MOLECULES; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; IMMUNOGLOBULINS; INTERCELLULAR JUNCTIONS; LEUKOCYTE ELASTASE; LEUKOTRIENE B4; MACROPHAGE-1 ANTIGEN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; REPERFUSION INJURY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; VENULES; WOUNDS AND INJURIES;

EID: 84937634493     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.05.010     Document Type: Article

References (48)

1. Afonso P.V., Janka-Junttila M., Lee Y.J., McCann C.P., Oliver C.M., Aamer K.A., Losert W., Cicerone M.T., Parent C.A. LTB4 is a signal-relay molecule during neutrophil chemotaxis. Dev. Cell 2012, 22:1079-1091.
2. Aikawa N., Ishizaka A., Hirasawa H., Shimazaki S., Yamamoto Y., Sugimoto H., Shinozaki M., Taenaka N., Endo S., Ikeda T., Kawasaki Y. Reevaluation of the efficacy and safety of the neutrophil elastase inhibitor, Sivelestat, for the treatment of acute lung injury associated with systemic inflammatory response syndrome; a phase IV study. Pulm. Pharmacol. Ther. 2011, 24:549-554.
3. Auner B., Geiger E.V., Henrich D., Lehnert M., Marzi I., Relja B. Circulating leukotriene B4 identifies respiratory complications after trauma. Mediators Inflamm. 2012, 2012:536156.
4. Belaaouaj A., McCarthy R., Baumann M., Gao Z., Ley T.J., Abraham S.N., Shapiro S.D. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat. Med. 1998, 4:615-618.
5. Beyrau M., Bodkin J.V., Nourshargh S. Neutrophil heterogeneity in health and disease: a revitalized avenue in inflammation and immunity. Open Biol. 2012, 2:120134.
6. Bradfield P.F., Scheiermann C., Nourshargh S., Ody C., Luscinskas F.W., Rainger G.E., Nash G.B., Miljkovic-Licina M., Aurrand-Lions M., Imhof B.A. JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood 2007, 110:2545-2555.
7. Buckley C.D., Ross E.A., McGettrick H.M., Osborne C.E., Haworth O., Schmutz C., Stone P.C., Salmon M., Matharu N.M., Vohra R.K., et al. Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J.Leukoc. Biol. 2006, 79:303-311.
8. Cai T.Q., Wright S.D. Human leukocyte elastase is an endogenous ligand for the integrin CR3 (CD11b/CD18, Mac-1, alpha M beta 2) and modulates polymorphonuclear leukocyte adhesion. J.Exp. Med. 1996, 184:1213-1223.
9. Campbell E.J., Owen C.A. The sulfate groups of chondroitin sulfate- and heparan sulfate-containing proteoglycans in neutrophil plasma membranes are novel binding sites for human leukocyte elastase and cathepsin G. J.Biol. Chem. 2007, 282:14645-14654.
10. Chen M., Lam B.K., Kanaoka Y., Nigrovic P.A., Audoly L.P., Austen K.F., Lee D.M. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J.Exp. Med. 2006, 203:837-842.
11. Chou R.C., Kim N.D., Sadik C.D., Seung E., Lan Y., Byrne M.H., Haribabu B., Iwakura Y., Luster A.D. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 2010, 33:266-278.
12. Donnelly S.C., MacGregor I., Zamani A., Gordon M.W., Robertson C.E., Steedman D.J., Little K., Haslett C. Plasma elastase levels and the development of the adult respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 1995, 151:1428-1433.
13. Finsterbusch M., Voisin M.B., Beyrau M., Williams T.J., Nourshargh S. Neutrophils recruited by chemoattractants invivo induce microvascular plasma protein leakage through secretion of TNF. J.Exp. Med. 2014, 211:1307-1314.
14. Fujii M., Miyagi Y., Bessho R., Nitta T., Ochi M., Shimizu K. Effect of a neutrophil elastase inhibitor on acute lung injury after cardiopulmonary bypass. Interact. Cardiovasc. Thorac. Surg. 2010, 10:859-862.
15. Iadecola C., Anrather J. The immunology of stroke: from mechanisms to translation. Nat. Med. 2011, 17:796-808.
16. Kim N.D., Chou R.C., Seung E., Tager A.M., Luster A.D. A unique requirement for the leukotriene B4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J.Exp. Med. 2006, 203:829-835.
17. Kolaczkowska E., Kubes P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 2013, 13:159-175.
18. Lämmermann T., Afonso P.V., Angermann B.R., Wang J.M., Kastenmüller W., Parent C.A., Germain R.N. Neutrophil swarms require LTB4 and integrins at sites of cell death invivo. Nature 2013, 498:371-375.
19. Ley K., Laudanna C., Cybulsky M.I., Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007, 7:678-689.
20. Manetti M., Guiducci S., Romano E., Rosa I., Ceccarelli C., Mello T., Milia A.F., Conforti M.L., Ibba-Manneschi L., Matucci-Cerinic M. Differential expression of junctional adhesion molecules in different stages of systemic sclerosis. Arthritis Rheum. 2013, 65:247-257.
21. Mantovani A., Cassatella M.A., Costantini C., Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 2011, 11:519-531.
22. Mathias J.R., Perrin B.J., Liu T.X., Kanki J., Look A.T., Huttenlocher A. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J.Leukoc. Biol. 2006, 80:1281-1288.
23. Matthay M.A., Zemans R.L. The acute respiratory distress syndrome: pathogenesis and treatment. Annu. Rev. Pathol. 2011, 6:147-163.
24. Mayadas T.N., Cullere X., Lowell C.A. The multifaceted functions of neutrophils. Annu. Rev. Pathol. 2014, 9:181-218.
25. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J.Exp. Med. 2013, 210:1283-1299.
26. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 2006, 6:173-182.
27. Nourshargh S., Alon R. Leukocyte migration into inflamed tissues. Immunity 2014, 41:694-707.
28. Nourshargh S., Hordijk P.L., Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 2010, 11:366-378.
29. Owen C.A., Campbell E.J. The cell biology of leukocyte-mediated proteolysis. J.Leukoc. Biol. 1999, 65:137-150.
30. Pham C.T. Neutrophil serine proteases: specific regulators of inflammation. Nat. Rev. Immunol. 2006, 6:541-550.
31. Phillipson M., Kubes P. The neutrophil in vascular inflammation. Nat. Med. 2011, 17:1381-1390.
32. Proebstl D., Voisin M.B., Woodfin A., Whiteford J., D'Acquisto F., Jones G.E., Rowe D., Nourshargh S. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls invivo. J.Exp. Med. 2012, 209:1219-1234.
33. Rabquer B.J., Amin M.A., Teegala N., Shaheen M.K., Tsou P.S., Ruth J.H., Lesch C.A., Imhof B.A., Koch A.E. Junctional adhesion molecule-C is a soluble mediator of angiogenesis. J.Immunol. 2010, 185:1777-1785.
34. Rainger G.E., Rowley A.F., Nash G.B. Adhesion-dependent release of elastase from human neutrophils in a novel, flow-based model: specificity of different chemotactic agents. Blood 1998, 92:4819-4827.
35. Rubenfeld G.D., Caldwell E., Peabody E., Weaver J., Martin D.P., Neff M., Stern E.J., Hudson L.D. Incidence and outcomes of acute lung injury. N.Engl. J. Med. 2005, 353:1685-1693.
36. Santoso S., Sachs U.J., Kroll H., Linder M., Ruf A., Preissner K.T., Chavakis T. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J.Exp. Med. 2002, 196:679-691.
37. Scheiermann C., Colom B., Meda P., Patel N.S., Voisin M.B., Marrelli A., Woodfin A., Pitzalis C., Thiemermann C., Aurrand-Lions M., et al. Junctional adhesion molecule-C mediates leukocyte infiltration in response to ischemia reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1509-1515.
38. Schulte D., Küppers V., Dartsch N., Broermann A., Li H., Zarbock A., Kamenyeva O., Kiefer F., Khandoga A., Massberg S., Vestweber D. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J. 2011, 30:4157-4170.
39. Smith P.D., Puskas F., Meng X., Lee J.H., Cleveland J.C., Weyant M.J., Fullerton D.A., Reece T.B. The evolution of chemokine release supports a bimodal mechanism of spinal cord ischemia and reperfusion injury. Circulation 2012, 126(1):S110-S117.
40. Souza D.G., Coutinho S.F., Silveira M.R., Cara D.C., Teixeira M.M. Effects of a BLT receptor antagonist on local and remote reperfusion injuries after transient ischemia of the superior mesenteric artery in rats. Eur. J. Pharmacol. 2000, 403:121-128.
41. Tak T., Tesselaar K., Pillay J., Borghans J.A., Koenderman L. What's your age again? Determination of human neutrophil half-lives revisited. J.Leukoc. Biol. 2013, 94:595-601.
42. Vestweber D., Wessel F., Nottebaum A.F. Similarities and differences in the regulation of leukocyte extravasation and vascular permeability. Semin. Immunopathol. 2014, 36:177-192.
43. Voisin M.B., Nourshargh S. Neutrophil transmigration: emergence of an adhesive cascade within venular walls. J.Innate Immun. 2013, 5:336-347.
44. Weninger W., Biro M., Jain R. Leukocyte migration in the interstitial space of non-lymphoid organs. Nat. Rev. Immunol. 2014, 14:232-246.
45. Wheeler A.P., Bernard G.R. Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 2007, 369:1553-1564.
46. Woodfin A., Voisin M.B., Beyrau M., Colom B., Caille D., Diapouli F.M., Nash G.B., Chavakis T., Albelda S.M., Rainger G.E., et al. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils invivo. Nat. Immunol. 2011, 12:761-769.
47. Yoo S.K., Huttenlocher A. Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J.Leukoc. Biol. 2011, 89:661-667.
48. Young R.E., Voisin M.B., Wang S., Dangerfield J., Nourshargh S. Role of neutrophil elastase in LTB4-induced neutrophil transmigration invivo assessed with a specific inhibitor and neutrophil elastase deficient mice. Br. J. Pharmacol. 2007, 151:628-637.