The physiological roles of ICAM-1 and ICAM-2 in neutrophil migration into tissues

Purpose of reviewNeutrophil extravasation from the blood into tissues is initiated by tethering and rolling of neutrophils on endothelial cells, followed by neutrophil integrin activation and shear resistant arrest, crawling, diapedesis and breaching the endothelial basement membrane harbouring pericytes. Endothelial intercellular cell adhesion molecule (ICAM)-1 and ICAM-2, in conjunction with ICAM-1 on pericytes, critically contribute to each step. In addition, epithelial ICAM-1 is involved in neutrophil migration to peri-epithelial sites. The most recent findings on the role of ICAM-1 and ICAM-2 for neutrophil migration into tissues will be reviewed here. Recent findingsSignalling via endothelial ICAM-1 and ICAM-2 contributes to stiffness of the endothelial cells at sites of chronic inflammation and junctional maturation, respectively. Endothelial ICAM-2 contributes to neutrophil crawling and initiation of paracellular diapedesis, which then proceeds independent of ICAM-2. Substantial transcellular neutrophil diapedesis across the blood–brain barrier is strictly dependent on endothelial ICAM-1 and ICAM-2. Endothelial ICAM-1 or ICAM-2 is involved in neutrophil-mediated plasma leakage. ICAM-1 on pericytes assists the final step of neutrophil extravasation. Epithelial ICAM-1 rather indirectly promotes neutrophil migration to peri-epithelial sites. SummaryICAM-1 and ICAM-2 are involved in each step of neutrophil extravasation, and have redundant but also distinct functions. Analysis of the role of endothelial ICAM-1 requires simultaneous consideration of ICAM-2.

[1]  C. Figdor,et al.  Actin-binding proteins differentially regulate endothelial cell stiffness, ICAM-1 function and neutrophil transmigration , 2014, Journal of Cell Science.

[2]  S. Nourshargh,et al.  Neutrophils recruited by chemoattractants in vivo induce microvascular plasma protein leakage through secretion of TNF , 2014, The Journal of experimental medicine.

[3]  S. Barnum,et al.  ICAM-1: Isoforms and Phenotypes , 2014, The Journal of Immunology.

[4]  Jia-feng Wang,et al.  Blockade of ICAM-1 Improves the Outcome of Polymicrobial Sepsis via Modulating Neutrophil Migration and Reversing Immunosuppression , 2014, Mediators of inflammation.

[5]  J. V. van Buul,et al.  Rho-GTPase signaling in leukocyte extravasation , 2014, Cell adhesion & migration.

[6]  Lei Xiao,et al.  New paradigms in inflammatory signaling in vascular endothelial cells. , 2014, American journal of physiology. Heart and circulatory physiology.

[7]  S. Nourshargh,et al.  ICAM-2 facilitates luminal interactions between neutrophils and endothelial cells in vivo , 2014, Journal of Cell Science.

[8]  B. Engelhardt,et al.  β2 Integrin–Mediated Crawling on Endothelial ICAM-1 and ICAM-2 Is a Prerequisite for Transcellular Neutrophil Diapedesis across the Inflamed Blood–Brain Barrier , 2014, The Journal of Immunology.

[9]  A. Nusrat,et al.  Transmigrated neutrophils in the intestinal lumen engage ICAM 1 to regulate the epithelial barrier and neutrophil recruitment , 2013, Mucosal Immunology.

[10]  N. Dryden,et al.  ICAM-2 regulates vascular permeability and N-cadherin localization through ezrin-radixin-moesin (ERM) proteins and Rac-1 signalling , 2014, Cell Communication and Signaling.

[11]  Szabina Fodor,et al.  Neutrophil cell surface receptors and their intracellular signal transduction pathways , 2013, International immunopharmacology.

[12]  B. Engelhardt,et al.  Kindlin-3 regulates integrin activation and adhesion reinforcement of effector T cells , 2013, Proceedings of the National Academy of Sciences.

[13]  E. Dejana,et al.  VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. , 2013, Developmental cell.

[14]  M. Sperandio,et al.  The molecular basis of leukocyte recruitment and its deficiencies. , 2013, Molecular immunology.

[15]  K. Ley,et al.  Neutrophil rolling at high shear: flattening, catch bond behavior, tethers and slings. , 2013, Molecular immunology.

[16]  S. Biswal,et al.  Aquaporin 5 regulates cigarette smoke induced emphysema by modulating barrier and immune properties of the epithelium , 2013, Tissue barriers.

[17]  J. Pober,et al.  Transendothelial Migration Enables Subsequent Transmigration of Neutrophils through Underlying Pericytes , 2013, PloS one.

[18]  G. Turino,et al.  Neutrophil Elastase-Mediated Lung Disease , 2013, COPD.

[19]  S. Nourshargh,et al.  Neutrophil Transmigration: Emergence of an Adhesive Cascade within Venular Walls , 2013, Journal of Innate Immunity.

[20]  P. Kubes,et al.  Neutrophil recruitment and function in health and inflammation , 2013, Nature Reviews Immunology.

[21]  N. Hogg,et al.  T lymphocytes orient against the direction of fluid flow during LFA-1-mediated migration. , 2013, Biophysical journal.

[22]  W. Muller.  Getting Leukocytes to the Site of Inflammation , 2013, Veterinary pathology.

[23]  W. Muller,et al.  Neutrophil and monocyte recruitment by PECAM, CD99, and other molecules via the LBRC , 2013, Seminars in Immunopathology.

[24]  M. Arcangeli,et al.  Function of Junctional Adhesion Molecules (JAMs) in Leukocyte Migration and Homeostasis , 2013, Archivum Immunologiae et Therapiae Experimentalis.

[25]  Robert Pless,et al.  Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs , 2012, Nature Immunology.

[26]  B. Engelhardt,et al.  The anatomical and cellular basis of immune surveillance in the central nervous system , 2012, Nature Reviews Immunology.

[27]  K. Ley,et al.  Slings enable neutrophil rolling at high shear , 2012, Nature.

[28]  F. D’Acquisto,et al.  Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo , 2012, The Journal of experimental medicine.

[29]  D. Frommhold,et al.  The Mammalian Actin-Binding Protein 1 Is Critical for Spreading and Intraluminal Crawling of Neutrophils under Flow Conditions , 2012, The Journal of Immunology.

[30]  K. Ley,et al.  Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. , 2011, Blood.

[31]  Cynthia A. Reinhart-King,et al.  Age-Related Intimal Stiffening Enhances Endothelial Permeability and Leukocyte Transmigration , 2011, Science Translational Medicine.

[32]  A. Zarbock,et al.  Stabilizing the VE‐cadherin–catenin complex blocks leukocyte extravasation and vascular permeability , 2011, The EMBO journal.

[33]  C. Betsholtz,et al.  Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. , 2011, Developmental cell.

[34]  P. Meda,et al.  Junctional adhesion molecule-C (JAM-C) regulates polarized neutrophil transendothelial cell migration in vivo , 2011, Nature immunology.

[35]  Tobias Tenenbaum,et al.  Transcellular migration of neutrophil granulocytes through the blood-cerebrospinal fluid barrier after infection with Streptococcus suis , 2011, Journal of Neuroinflammation.

[36]  B. Engelhardt,et al.  Comparison of Immortalized bEnd5 and Primary Mouse Brain Microvascular Endothelial Cells as in vitro Blood–Brain Barrier Models for the Study of T Cell Extravasation , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[37]  N. Borregaard,et al.  Neutrophils, from marrow to microbes. , 2010, Immunity.

[38]  D. Frommhold,et al.  RAGE and ICAM-1 cooperate in mediating leukocyte recruitment during acute inflammation in vivo. , 2010, Blood.

[39]  S. Rankin,et al.  Neutrophil kinetics in health and disease , 2010, Trends in immunology.

[40]  B. Engelhardt,et al.  Culture-Induced Changes in Blood—Brain Barrier Transcriptome: Implications for Amino-Acid Transporters in vivo , 2009, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  C. Carman,et al.  Settings and mechanisms for trans-cellular diapedesis. , 2009, Frontiers in bioscience.

[42]  R. Gower,et al.  Vav1 Is Essential for Mechanotactic Crawling and Migration of Neutrophils out of the Inflamed Microvasculature1 , 2009, The Journal of Immunology.

[43]  Klaus Ley,et al.  New insights into leukocyte recruitment by intravital microscopy. , 2009, Current topics in microbiology and immunology.

[44]  A. Sonnenberg,et al.  Filamin B Mediates ICAM-1-driven Leukocyte Transendothelial Migration* , 2008, Journal of Biological Chemistry.

[45]  R. Alon,et al.  Integrin modulation and signaling in leukocyte adhesion and migration , 2007, Immunological reviews.

[46]  C. Carman,et al.  Structural basis of integrin regulation and signaling. , 2007, Annual review of immunology.

[47]  A. Beaudet,et al.  Intercellular Adhesion Molecule-1 Expression Is Required on Multiple Cell Types for the Development of Experimental Autoimmune Encephalomyelitis1 , 2007, The Journal of Immunology.

[48]  Bryan Heit,et al.  Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade , 2006, The Journal of experimental medicine.

[49]  Sheila M. Thomas,et al.  Endothelial Cell Cortactin Coordinates Intercellular Adhesion Molecule-1 Clustering and Actin Cytoskeleton Remodeling during Polymorphonuclear Leukocyte Adhesion and Transmigration1 , 2006, The Journal of Immunology.

[50]  F. Luscinskas,et al.  ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. , 2005, Blood.

[51]  K. Zen,et al.  Leukocyte-epithelial interactions. , 2003, Current opinion in cell biology.

[52]  Cheng Zhu,et al.  Direct observation of catch bonds involving cell-adhesion molecules , 2003, Nature.

[53]  J. Greenwood,et al.  ICAM-1-Coupled Cytoskeletal Rearrangements and Transendothelial Lymphocyte Migration Involve Intracellular Calcium Signaling in Brain Endothelial Cell Lines1 , 2000, The Journal of Immunology.

[54]  B. Vainer,et al.  Comparative studies of the colonic in situ expression of intercellular adhesion molecules (ICAM-1, -2, and -3), beta2 integrins (LFA-1, Mac-1, and p150,95), and PECAM-1 in ulcerative colitis and Crohn's disease. , 2000, The American journal of surgical pathology.

[55]  B. Engelhardt,et al.  Ultrastructural localization of adhesion molecules in the healthy , 1999, Cell and Tissue Research.

[56]  B. Engelhardt,et al.  Prolonged eosinophil accumulation in allergic lung interstitium of ICAM-2 deficient mice results in extended hyperresponsiveness. , 1999, Immunity.

[57]  A. Vaheri,et al.  Association of Ezrin with Intercellular Adhesion Molecule-1 and -2 (ICAM-1 and ICAM-2) , 1998, The Journal of Biological Chemistry.

[58]  N. Takahashi,et al.  Ezrin/Radixin/Moesin (ERM) Proteins Bind to a Positively Charged Amino Acid Cluster in the Juxta-Membrane Cytoplasmic Domain of CD44, CD43, and ICAM-2 , 1998, The Journal of cell biology.

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

[60]  C. Gahmberg,et al.  Binding of the Cytoplasmic Domain of Intercellular Adhesion Molecule-2 (ICAM-2) to α-Actinin* , 1996, The Journal of Biological Chemistry.

[61]  M. Diamond,et al.  Expression and Polarization of Intercellular Adhesion Molecule-1 on Human Intestinal Epithelia: Consequences for CD11b/CD18-Mediated Interactions with Neutrophils , 1996, Molecular medicine.

[62]  B. Engelhardt,et al.  ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro. , 1996, The American journal of pathology.

[63]  S. Colgan,et al.  CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia , 1996, The Journal of cell biology.

[64]  C. Gahmberg,et al.  Intercellular adhesion molecule-2 (CD102) binds to the leukocyte integrin CD11b/CD18 through the A domain. , 1995, Journal of immunology.

[65]  R. Cotran,et al.  Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice , 1994, The Journal of experimental medicine.

[66]  A. Beaudet,et al.  Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[67]  C. Gahmberg,et al.  A peptide from ICAM-2 binds to the leukocyte integrin CD11a/CD18 and inhibits endothelial cell adhesion. , 1993, The Journal of biological chemistry.

[68]  T. Springer,et al.  Isolation, characterization, and expression of mouse ICAM-2 complementary and genomic DNA. , 1992, Journal of immunology.

[69]  D. Staunton,et al.  Association of intercellular adhesion molecule-1 (ICAM-1) with actin- containing cytoskeleton and alpha-actinin , 1992, The Journal of cell biology.

[70]  T. Springer,et al.  Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1 , 1991, The Journal of experimental medicine.

[71]  Michael Loran Dustin,et al.  Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1 , 1989, Nature.

[72]  C. Smith,et al.  Quantitation of Intracellular Mac-i (CD1 i b/CDi 8) Pools in Human Neutrophils , 1988 .

[73]  L. Lindbom,et al.  A monoclonal antibody to the membrane glycoprotein complex CD18 inhibits polymorphonuclear leukocyte accumulation and plasma leakage in vivo , 1987 .

[74]  T. Williams,et al.  Control of vascular permeability by polymorphonuclear leukocytes in inflammation , 1981, Nature.