Immobilized IL-8 Triggers Progressive Activation of Neutrophils Rolling In Vitro on P-Selectin and Intercellular Adhesion Molecule-11

The chemokine IL-8 is found on the luminal side of vascular endothelial cells, where it is postulated to be immobilized during inflammation. In this study, we observed that immobilized IL-8 can stimulate neutrophils to firmly adhere to a substrate containing ICAM-1 in a static adhesion assay. Soluble IL-8 was then perfused over neutrophils rolling on P-selectin (P-sel) and ICAM-1, confirming that IL-8 in solution can quickly cause rolling neutrophils to arrest. To mimic a blood vessel wall with IL-8 expressed on the luminal surface of endothelial cells, IL-8 was immobilized along with P-sel and ICAM-1 at defined site densities to a surface. Neutrophils rolled an average of 200 μm on surfaces of P-sel, ICAM-1, and IL-8 before firmly adhering through ICAM-1-β2 integrin interactions at 2 dynes/cm2 wall shear stress. Increasing the density of IL-8 from 60 to 350 sites/μm2 on the surface decreased by 50% the average distance and time the neutrophils rolled before becoming firmly adherent. Temporal dynamics of ICAM-1-β2 integrin interactions of rolling neutrophils following IL-8 exposure suggest the existence of two classes of β2 integrin-ICAM-1 interactions, a low avidity interaction with a 65% increase in pause times as compared with P-sel-P-sel glycoprotein ligand-1 interactions, and a high avidity interaction with pause times 400% greater than the selectin interactions. Based on the proportionality between IL-8 site density and time to arrest, it appears that neutrophils may need to sample a critical number of IL-8 molecules presented by the vessel wall before forming a sufficient number of high avidity β2 integrin bonds for firm adhesion.

[1]  G. Zimmerman,et al.  Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: a juxtacrine system for adhesion and activation of neutrophils , 1991, The Journal of cell biology.

[2]  M. Auer,et al.  Transcytosis and Surface Presentation of IL-8 by Venular Endothelial Cells , 1997, Cell.

[3]  Lee,et al.  Endothelial-Leukocyte Adhesion Molecule 1 Stimulates the Adhesive Activity of Leukocyte Integrin CR3 (CD11b/CD18, Mac-1, CiJ2) on Human Neutrophils , 2003 .

[4]  M. Cybulsky,et al.  Intravascular IL-8. Inhibitor of polymorphonuclear leukocyte accumulation at sites of acute inflammation. , 1991, Journal of immunology.

[5]  G. Nash,et al.  Endothelial-borne platelet-activating factor and interleukin-8 rapidly immobilize rolling neutrophils. , 1997, The American journal of physiology.

[6]  E. Kunkel,et al.  Leukocyte Arrest During Cytokine-Dependent Inflammation In Vivo1 , 2000, The Journal of Immunology.

[7]  Eric J. Kunkel,et al.  Threshold Levels of Fluid Shear Promote Leukocyte Adhesion through Selectins (CD62L,P,E) , 1997, The Journal of cell biology.

[8]  D. Adams,et al.  T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-lβ , 1993, Nature.

[9]  M. Gimbrone,et al.  Interleukin‐8 induces changes in human neutrophil actin conformation and distribution: relationship to inhibition of adhesion to cytokine‐activated endothelium , 1992, Journal of leukocyte biology.

[10]  A. Weyrich,et al.  Engagement of P-selectin Glycoprotein Ligand-1 Enhances Tyrosine Phosphorylation and Activates Mitogen-activated Protein Kinases in Human Neutrophils* , 1997, The Journal of Biological Chemistry.

[11]  S Kaplanski,et al.  Granulocyte-endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow. , 1993, Biophysical journal.

[12]  C. Dong,et al.  In vitro side-view imaging technique and analysis of human T-leukemic cell adhesion to ICAM-1 in shear flow. , 1998, Microvascular research.

[13]  R. Mayer,et al.  Activation of Human Leukocytes Reduces Surface P-Selectin Glycoprotein Ligand-1 (PSGL-1, CD162) and Adhesion to P-Selectin In Vitro1 , 2000, The Journal of Immunology.

[14]  F. Luscinskas,et al.  In vitro inhibitory effect of IL-8 and other chemoattractants on neutrophil-endothelial adhesive interactions. , 1992, Journal of immunology.

[15]  E. Berg,et al.  Rolling of lymphocytes and neutrophils on peripheral node addressin and subsequent arrest on ICAM‐1 in shear flow , 1995, European journal of immunology.

[16]  P. Murphy,et al.  Cloning of complementary DNA encoding a functional human interleukin-8 receptor. , 1991, Science.

[17]  S Neelamegham,et al.  Synergy between L-selectin signaling and chemotactic activation during neutrophil adhesion and transmigration. , 1997, Journal of immunology.

[18]  S Neelamegham,et al.  Molecular dynamics of the transition from L-selectin- to beta 2-integrin-dependent neutrophil adhesion under defined hydrodynamic shear. , 1996, Biophysical journal.

[19]  Rodger P. McEver,et al.  Rapid neutrophil adhesion to activated endothelium mediated by GMP-140 , 1990, Nature.

[20]  M. Baggiolini,et al.  Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Cybulsky,et al.  Intravenous interleukin-8 inhibits granulocyte emigration from rabbit mesenteric venules without altering L-selectin expression or leukocyte rolling. , 1993, Journal of immunology.

[22]  M. Gunn,et al.  A high endothelial cell-derived chemokine induces rapid, efficient, and subset-selective arrest of rolling T lymphocytes on a reconstituted endothelial substrate. , 1998, Journal of immunology.

[23]  A. Weyrich,et al.  Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B translocation. , 1995, The Journal of clinical investigation.

[24]  R. Warnke,et al.  A novel P-selectin glycoprotein ligand-1 monoclonal antibody recognizes an epitope within the tyrosine sulfate motif of human PSGL-1 and blocks recognition of both P- and L-selectin. , 1998, Blood.

[25]  G S Kansas,et al.  Selectins and their ligands: current concepts and controversies. , 1996, Blood.

[26]  D. Adams,et al.  Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. , 1993, Immunology today.

[27]  G. Zimmerman,et al.  Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces. , 1995, The Journal of clinical investigation.

[28]  A. Weyrich,et al.  Monocyte Tethering by P-Selectin Regulates Monocyte Chemotactic Protein-1 and Tumor Necrosis Factor-a Secretion Signal Integration and NF-cB Translocation , 2022 .

[29]  M. Topham,et al.  Inflammatory roles of P-selectin. , 1993, The Journal of clinical investigation.

[30]  D. Vestweber,et al.  Stimulation of P‐selectin glycoprotein ligand‐1 on mouse neutrophils activates β2 ‐integrin mediated cell attachment to ICAM‐1 , 1998, European journal of immunology.

[31]  S. Wright,et al.  Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD11b/CD18, Mac-1, alpha m beta 2) on human neutrophils , 1991, The Journal of experimental medicine.

[32]  Obin,et al.  Endothelial interleukin-8: a novel inhibitor of leukocyte-endothelial interactions. , 1989, Science.

[33]  T. Springer Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm , 1994, Cell.

[34]  W. Wood,et al.  Characterization of two high affinity human interleukin-8 receptors. , 1992, The Journal of biological chemistry.

[35]  E L Berg,et al.  A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. , 1999, Biophysical journal.

[36]  D. Hammer,et al.  Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow , 1995, Nature.

[37]  G. Zimmerman,et al.  Adhesion and signaling in vascular cell-cell interactions. , 1996, The Journal of clinical investigation.

[38]  E. Butcher,et al.  Chemokines and the arrest of lymphocytes rolling under flow conditions. , 1998, Science.

[39]  A. Huber,et al.  Regulation of transendothelial neutrophil migration by endogenous interleukin-8. , 1991, Science.

[40]  A. Rot Neutrophil attractant/activation protein‐1 (interleukin‐8) induces in vitro neutrophil migration by haptotactic mechanism , 1993, European journal of immunology.

[41]  Michael Loran Dustin,et al.  Low affinity of cell surface lymphocyte function-associated antigen-1 (LFA-1) generates selectivity for cell-cell interactions. , 1997, Journal of immunology.

[42]  M. Baggiolini,et al.  Neutrophil-activating protein 1/interleukin 8 stimulates the binding activity of the leukocyte adhesion receptor CD11b/CD18 on human neutrophils , 1990, The Journal of experimental medicine.

[43]  D. Hammer,et al.  Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow , 1995, Nature.

[44]  S. Simon,et al.  GlyCAM-1, a physiologic ligand for L-selectin, activates beta 2 integrins on naive peripheral lymphocytes , 1996, The Journal of experimental medicine.

[45]  G. Pellegrini,et al.  P-selectin induces the expression of tissue factor on monocytes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S I Simon,et al.  Neutrophil CD18-dependent arrest on intercellular adhesion molecule 1 (ICAM-1) in shear flow can be activated through L-selectin. , 1997, Journal of immunology.

[47]  S. Simon,et al.  Neutrophil Tethering on E-Selectin Activates β2 Integrin Binding to ICAM-1 Through a Mitogen-Activated Protein Kinase Signal Transduction Pathway1 , 2000, The Journal of Immunology.

[48]  F. Luscinskas,et al.  MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions , 1999, Nature.

[49]  Michael Loran Dustin,et al.  The Lymphocyte Function–associated Antigen 1 I Domain Is a Transient Binding Module for Intercellular Adhesion Molecule (ICAM)-1 and ICAM-3 in Hydrodynamic Flow , 1997, The Journal of experimental medicine.

[50]  V. Moy,et al.  Direct evidence for two affinity states for lymphocyte function-associated antigen 1 on activated T cells. , 1993, The Journal of biological chemistry.

[51]  J. Strominger,et al.  Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[52]  U. V. von Andrian,et al.  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 , 2000, The Journal of experimental medicine.

[53]  C. Smith,et al.  Possible Steps Involved in the Transition to Stationary Adhesion of Rolling Neutrophils: A Brief Review , 2000, Microcirculation.

[54]  S. Simon,et al.  L-selectin (CD62L) cross-linking signals neutrophil adhesive functions via the Mac-1 (CD11b/CD18) beta 2-integrin. , 1995, Journal of immunology.

[55]  R. Cooke,et al.  Identification of a glycosaminoglycan binding surface on human interleukin-8. , 1998, Biochemistry.

[56]  W I Wood,et al.  Structure and functional expression of a human interleukin-8 receptor. , 1991, Science.

[57]  C W Smith,et al.  Recognition of an endothelial determinant for CD 18-dependent human neutrophil adherence and transendothelial migration. , 1988, The Journal of clinical investigation.