Differential attenuation of β2 integrin–dependent and –independent neutrophil migration by Ly6G ligation

Blood Advances - Tập 3 - Trang 256-267 - 2019
Pierre Cunin1, Pui Y. Lee1,2, Edy Kim3, Angela B. Schmider4, Nathalie Cloutier5, Alexandre Pare6,7, Matthias Gunzer8, Roy J. Soberman4, Steve Lacroix6,7, Eric Boilard5, Craig T. Lefort9, Peter A. Nigrovic1,2
1Division of Rheumatology, Immunology and Allergy, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA
2Division of Immunology, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA
3Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA
4Division of Nephrology, Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA
5Département de Microbiologie et Immunologie, Faculté de Médecine de l'Université Laval, Centre de Recherche du Centre Hospitalier Universitaire de Québec, Québec City, QC, Canada
6Axe Neurosciences, Centre de Recherche du Centre Hospitalier Universitaire de Québec, Québec City, QC, Canada
7Département de Médecine Moléculaire, Université Laval, Québec City, QC, Canada
8Institute for Experimental Immunology and Imaging, University of Duisburg-Essen, University Hospital Essen, Essen, Germany
9Division of Surgical Research, Department of Surgery, Rhode Island Hospital, Alpert Medical School, Brown University, Providence, RI

Tóm tắt

AbstractAntibody ligation of the murine neutrophil surface protein Ly6G disrupts neutrophil migration in some contexts but not others. We tested whether this variability reflected divergent dependence of neutrophil migration on β2 integrins, adhesion molecules that interact with Ly6G at the neutrophil surface. In integrin-dependent murine arthritis, Ly6G ligation attenuated joint inflammation, even though mice lacking Ly6G altogether developed arthritis normally. By contrast, Ly6G ligation had no impact on integrin-independent neutrophil migration into inflamed lung. In peritoneum, the role of β2 integrins varied with stimulus, proving dispensable for neutrophil entry in Escherichia coli peritonitis but contributory in interleukin 1 (IL-1)–mediated sterile peritonitis. Correspondingly, Ly6G ligation attenuated only IL-1 peritonitis, disrupting the molecular association between integrins and Ly6G and inducing cell-intrinsic blockade restricted to integrin-dependent migration. Consistent with this observation, Ly6G ligation impaired integrin-mediated postadhesion strengthening for neutrophils arresting on activated cremaster endothelium in vivo. Together, these findings identify selective inhibition of integrin-mediated neutrophil emigration through Ly6G ligation, highlighting the marked site and stimulus specificity of β2 integrin dependence in neutrophil migration.

Tài liệu tham khảo

Kolaczkowska, 2013, Neutrophil recruitment and function in health and inflammation, Nat Rev Immunol, 13, 159, 10.1038/nri3399 Nourshargh, 2014, Leukocyte migration into inflamed tissues, Immunity, 41, 694, 10.1016/j.immuni.2014.10.008 Kourtzelis, 2017, From leukocyte recruitment to resolution of inflammation: the cardinal role of integrins, J Leukoc Biol, 102, 677, 10.1189/jlb.3MR0117-024R Kishimoto, 1987, Heterogeneous mutations in the beta subunit common to the LFA-1, Mac-1, and p150,95 glycoproteins cause leukocyte adhesion deficiency, Cell, 50, 193, 10.1016/0092-8674(87)90215-7 Hawkins, 1992, Leukocyte adhesion deficiency: clinical and postmortem observations, Pediatr Pathol, 12, 119, 10.3109/15513819209023288 Doerschuk, 1990, CD18-dependent and -independent mechanisms of neutrophil emigration in the pulmonary and systemic microcirculation of rabbits, J Immunol, 144, 2327, 10.4049/jimmunol.144.6.2327 Ramamoorthy, 1997, CD18 adhesion blockade decreases bacterial clearance and neutrophil recruitment after intrapulmonary E coli, but not after S. aureus, J Leukoc Biol, 61, 167, 10.1002/jlb.61.2.167 Hellewell, 1994, Disparate role of the beta 2-integrin CD18 in the local accumulation of neutrophils in pulmonary and cutaneous inflammation in the rabbit, Am J Respir Cell Mol Biol, 10, 391, 10.1165/ajrcmb.10.4.7510985 Qin, 1996, The roles of CD11/CD18 and ICAM-1 in acute Pseudomonas aeruginosa-induced pneumonia in mice, J Immunol, 157, 5016, 10.4049/jimmunol.157.11.5016 Mizgerd, 1999, Effects of CD18 deficiency on the emigration of murine neutrophils during pneumonia, J Immunol, 163, 995, 10.4049/jimmunol.163.2.995 Ong, 2003, E coli pneumonia induces CD18-independent airway neutrophil migration in the absence of increased lung vascular permeability, Am J Physiol Lung Cell Mol Physiol, 285, L879, 10.1152/ajplung.00134.2003 Mizgerd, 1997, Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice, J Exp Med, 186, 1357, 10.1084/jem.186.8.1357 Wilson, 2017, Activated β2 integrins restrict neutrophil recruitment during murine acute pseudomonal pneumonia, Am J Respir Cell Mol Biol, 56, 620, 10.1165/rcmb.2016-0215OC McDonald, 2010, Intravascular danger signals guide neutrophils to sites of sterile inflammation, Science, 330, 362, 10.1126/science.1195491 Wang, 2012, Ly6G ligation blocks recruitment of neutrophils via a β2-integrin-dependent mechanism, Blood, 120, 1489, 10.1182/blood-2012-01-404046 Phillipson, 2006, Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade, J Exp Med, 203, 2569, 10.1084/jem.20060925 Petri, 2011, Endothelial LSP1 is involved in endothelial dome formation, minimizing vascular permeability changes during neutrophil transmigration in vivo, Blood, 117, 942, 10.1182/blood-2010-02-270561 Yipp, 2012, Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo, Nat Med, 18, 1386, 10.1038/nm.2847 Yipp, 2013, Antibodies against neutrophil LY6G do not inhibit leukocyte recruitment in mice in vivo, Blood, 121, 241, 10.1182/blood-2012-09-454348 Hasenberg, 2015, Catchup: a mouse model for imaging-based tracking and modulation of neutrophil granulocytes, Nat Methods, 12, 445, 10.1038/nmeth.3322 Wipke, 2001, Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis, J Immunol, 167, 1601, 10.4049/jimmunol.167.3.1601 Watts, 2005, Manifestations of inflammatory arthritis are critically dependent on LFA-1, J Immunol, 174, 3668, 10.4049/jimmunol.174.6.3668 Coxon, 1996, A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation, Immunity, 5, 653, 10.1016/S1074-7613(00)80278-2 Mizgerd, 1998, Combinatorial requirements for adhesion molecules in mediating neutrophil emigration during bacterial peritonitis in mice, J Leukoc Biol, 64, 291, 10.1002/jlb.64.3.291 Mócsai, 2002, Syk is required for integrin signaling in neutrophils, Immunity, 16, 547, 10.1016/S1074-7613(02)00303-5 Mayadas, 2005, Neutrophil beta2 integrins: moderators of life or death decisions, Trends Immunol, 26, 388, 10.1016/j.it.2005.05.002 Scharffetter-Kochanek, 1998, Spontaneous skin ulceration and defective T cell function in CD18 null mice, J Exp Med, 188, 119, 10.1084/jem.188.1.119 Lefort, 2012, Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation, Blood, 119, 4275, 10.1182/blood-2011-08-373118 Horwitz, 2001, Mechanisms of granulocytosis in the absence of CD18, Blood, 97, 1578, 10.1182/blood.V97.6.1578 Lämmermann, 2013, Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo, Nature, 498, 371, 10.1038/nature12175 Lee, 2013, Ly6 family proteins in neutrophil biology, J Leukoc Biol, 94, 585, 10.1189/jlb.0113014 Daley, 2008, Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice, J Leukoc Biol, 83, 64, 10.1189/jlb.0407247 Fleming, 1993, Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family, J Immunol, 151, 2399, 10.4049/jimmunol.151.5.2399 Percopo, 2017, SiglecF+Gr1hi eosinophils are a distinct subpopulation within the lungs of allergen-challenged mice, J Leukoc Biol, 101, 321, 10.1189/jlb.3A0416-166R Tepper, 1992, An eosinophil-dependent mechanism for the antitumor effect of interleukin-4, Science, 257, 548, 10.1126/science.1636093 Norman, 2003, Combined anticoagulant and antiselectin treatments prevent lethal intravascular coagulation, Blood, 101, 921, 10.1182/blood-2001-12-0190 Abbitt, 2009, Antibody ligation of murine Ly-6G induces neutropenia, blood flow cessation, and death via complement-dependent and independent mechanisms, J Leukoc Biol, 85, 55, 10.1189/jlb.0507305 Ribechini, 2009, Gr-1 antibody induces STAT signaling, macrophage marker expression and abrogation of myeloid-derived suppressor cell activity in BM cells, Eur J Immunol, 39, 3538, 10.1002/eji.200939530 Ding, 1999, Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration, J Immunol, 163, 5029, 10.4049/jimmunol.163.9.5029 Lalezari, 1971, NB1, a new neutrophil-specific antigen involved in the pathogenesis of neonatal neutropenia, J Clin Invest, 50, 1108, 10.1172/JCI106582 Stroncek, 1996, Analysis of the expression of NB1 antigen using two monoclonal antibodies, Transfusion, 36, 168, 10.1046/j.1537-2995.1996.36296181931.x Stroncek, 2007, Neutrophil-specific antigen HNA-2a, NB1 glycoprotein, and CD177, Curr Opin Hematol, 14, 688, 10.1097/MOH.0b013e3282efed9e Wu, 2016, Heterogeneity of human neutrophil CD177 expression results from CD177P1 pseudogene conversion, PLoS Genet, 12, e1006067, 10.1371/journal.pgen.1006067 Sachs, 2007, The neutrophil-specific antigen CD177 is a counter-receptor for platelet endothelial cell adhesion molecule-1 (CD31), J Biol Chem, 282, 23603, 10.1074/jbc.M701120200 Bai, 2017, CD177 modulates human neutrophil migration through activation-mediated integrin and chemoreceptor regulation, Blood, 130, 2092, 10.1182/blood-2017-03-768507 Jerke, 2011, Complement receptor Mac-1 is an adaptor for NB1 (CD177)-mediated PR3-ANCA neutrophil activation, J Biol Chem, 286, 7070, 10.1074/jbc.M110.171256 Stroncek, 1998, The expression of the NB1 antigen on myeloid precursors and neutrophils from children and umbilical cords, Transfus Med, 8, 119, 10.1046/j.1365-3148.1998.00136.x Eulenberg-Gustavus, 2017, Gene silencing and a novel monoallelic expression pattern in distinct CD177 neutrophil subsets, J Exp Med, 214, 2089, 10.1084/jem.20161093 Xie, 2015, Characterization of a novel mouse model with genetic deletion of CD177, Protein Cell, 6, 117, 10.1007/s13238-014-0109-1 Harding, 2014, Neutrophil crawling in capillaries; a novel immune response to Staphylococcus aureus, PLoS Pathog, 10, e1004379, 10.1371/journal.ppat.1004379