Neutrophil interactions with epithelial-expressed ICAM-1 enhances intestinal mucosal wound healing

Mucosal Immunology - Tập 9 Số 5 - Trang 1151-1162 - 2016
Ronen Sumagin1, Jennifer Brazil2, Porfirio Nava3, Hikaru Nishio4, Ashfaqul Alam4, Anny‐Claude Luissint2, Dominique A. Weber4, Andrew S. Neish4, Asma Nusrat2, Charles A. Parkos2
1Department of Pathology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
2Department of Pathology, University of Michigan Medical School, Ann Arbor, Michigan, USA
3Departamento de Fisiología, Biofísica y Neurociencias, Centro de Investigación y de Estudios Avanzados, Instituto Politécnico Nacional, Mexico, Mexico
4Department of Pathology, Emory University School of Medicine, Atlanta, Georgia, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Koch, 2011, The Wnt antagonist Dkk1 regulates intestinal epithelial homeostasis and wound repair, Gastroenterology, 141, 259, 10.1053/j.gastro.2011.03.043

Sumagin, 2013, Activation of PKCbetaII by PMA facilitates enhanced epithelial wound repair through increased cell spreading and migration, PLoS ONE, 8, e55775, 10.1371/journal.pone.0055775

Nava, 2010, Interferon-gamma regulates intestinal epithelial homeostasis through converging beta-catenin signaling pathways, Immunity, 32, 392, 10.1016/j.immuni.2010.03.001

Brand, 2006, IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration, Am. J. Physiol. Gastrointest. Liver Physiol., 290, G827, 10.1152/ajpgi.00513.2005

Nava, 2011, JAM-A regulates epithelial proliferation through Akt/beta-catenin signalling, EMBO Rep., 12, 314, 10.1038/embor.2011.16

Xavier, 2007, Unravelling the pathogenesis of inflammatory bowel disease, Nature, 448, 427, 10.1038/nature06005

Laroux, 2001, Dysregulation of intestinal mucosal immunity: implications in inflammatory bowel disease, News Physiol. Sci., 16, 272

Nusrat, 1997, Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair, Gastroenterology, 113, 1489, 10.1053/gast.1997.v113.pm9352851

Chin, 2006, Neutrophil transepithelial migration and epithelial barrier function in IBD: potential targets for inhibiting neutrophil trafficking, Ann. N. Y. Acad. Sci., 1072, 276, 10.1196/annals.1326.018

Ginzberg, 2001, Neutrophil-mediated epithelial injury during transmigration: role of elastase, Am. J. Physiol. Gastrointest. Liver Physiol., 281, G705, 10.1152/ajpgi.2001.281.3.G705

Weber, 2014, Neutrophil-derived JAML inhibits repair of intestinal epithelial injury during acute inflammation, Mucosal Immunol., 7, 1221, 10.1038/mi.2014.12

Sylvia, 2003, The role of neutrophil apoptosis in influencing tissue repair, J. Wound Care, 12, 13, 10.12968/jowc.2003.12.1.26458

Serhan, 2007, Resolution of inflammation: state of the art, definitions and terms, FASEB J., 21, 325, 10.1096/fj.06-7227rev

Zemans, 2011, Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling, Proc. Natl Acad. Sci. USA, 108, 15990, 10.1073/pnas.1110144108

Zemans, 2013, Role of beta-catenin-regulated CCN matricellular proteins in epithelial repair after inflammatory lung injury, Am. J. Physiol. Lung Cell Mol. Physiol., 304, L415, 10.1152/ajplung.00180.2012

Lawrence, 2003, Antiadhesive role of apical decay-accelerating factor (CD55) in human neutrophil transmigration across mucosal epithelia, J. Exp. Med., 198, 999, 10.1084/jem.20030380

Brazil, 2010, Neutrophil migration across intestinal epithelium: evidence for a role of CD44 in regulating detachment of migrating cells from the luminal surface, J. Immunol., 185, 7026, 10.4049/jimmunol.1001293

Sumagin, 2014, Transmigrated neutrophils in the intestinal lumen engage ICAM-1 to regulate the epithelial barrier and neutrophil recruitment, Mucosal Immunol., 7, 905, 10.1038/mi.2013.106

Sumagin, 2008, Leukocyte-endothelial cell interactions are linked to vascular permeability via ICAM-1-mediated signaling, Am. J. Physiol. Heart Circ. Physiol., 295, H969, 10.1152/ajpheart.00400.2008

Lawson, 2009, ICAM-1 signaling in endothelial cells, Pharmacol. Rep., 61, 22, 10.1016/S1734-1140(09)70004-0

Liu, 2012, ICAM-1-activated Src and eNOS signaling increase endothelial cell surface PECAM-1 adhesivity and neutrophil transmigration, Blood, 120, 1942, 10.1182/blood-2011-12-397430

Fang, 2007, Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity, J. Biol. Chem., 282, 11221, 10.1074/jbc.M611871200

Nava, 2014, IFNgamma-induced suppression of beta-catenin signaling: evidence for roles of Akt and 14.3.3zeta, Mol. Biol. Cell, 25, 2894, 10.1091/mbc.e13-09-0512

Rubel, 2001, Fibrinogen promotes neutrophil activation and delays apoptosis, J. Immunol., 166, 2002, 10.4049/jimmunol.166.3.2002

Coxon, 1999, Cytokine-activated endothelial cells delay neutrophil apoptosis in vitroin vivo. A role for granulocyte/macrophage colony-stimulating factor, J. Exp. Med., 190, 923, 10.1084/jem.190.7.923

Velnar, 2009, The wound healing process: an overview of the cellular and molecular mechanisms, J. Int. Med. Res., 37, 1528, 10.1177/147323000903700531

Sturm, 2008, Epithelial restitution and wound healing in inflammatory bowel disease, World J. Gastroenterol., 14, 348, 10.3748/wjg.14.348

Tong, 2005, Interferon-gamma inhibits T84 epithelial cell migration by redirecting transcytosis of beta1 integrin from the migrating leading edge, J. Immunol., 175, 4030, 10.4049/jimmunol.175.6.4030

Kaiserlian, 1991, Expression, function and regulation of the intercellular adhesion molecule-1 (ICAM-1) on human intestinal epithelial cell lines, Eur. J. Immunol., 21, 2415, 10.1002/eji.1830211018

Hentzen, 2000, Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1, Blood, 95, 911, 10.1182/blood.V95.3.911.003k36_911_920

Sumagin, 2010, LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ, J. Immunol., 185, 7057, 10.4049/jimmunol.1001638

Parkos, 1991, Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction, J. Clin. Invest., 88, 1605, 10.1172/JCI115473

Wang, 2000, Mimosine arrests cells in G1 by enhancing the levels of p27(Kip1), Exp. Cell Res., 254, 64, 10.1006/excr.1999.4743

Leoni, 2015, Annexin A1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair, J. Clin. Invest., 125, 1215, 10.1172/JCI76693

Leoni, 2015, Human neutrophil formyl peptide receptor phosphorylation and the mucosal inflammatory response, J. Leukoc. Biol., 97, 87, 10.1189/jlb.4A0314-153R

Smith, 1994, Neutrophils, host defense, and inflammation: a double-edged sword, J. Leukoc. Biol., 56, 672, 10.1002/jlb.56.6.672

Rigby, 2012, Neutrophils in innate host defense against Staphylococcus aureus infections, Semin. Immunopathol., 34, 237, 10.1007/s00281-011-0295-3

Chin, 2008, Neutrophil-mediated activation of epithelial protease-activated receptors-1 and -2 regulates barrier function and transepithelial migration, J. Immunol., 181, 5702, 10.4049/jimmunol.181.8.5702

Shimoda, 2007, Cathepsin g is required for sustained inflammation and tissue injury after reperfusion of ischemic kidneys, Am. J. Pathol., 170, 930, 10.2353/ajpath.2007.060486

Davey, 2011, Matrix metalloproteinases in acute lung injury: mediators of injury and drivers of repair, Eur. Respir. J., 38, 959, 10.1183/09031936.00032111

Medina, 2006, Matrix metalloproteinase-9 modulates intestinal injury in rats with transmural colitis, J. Leukoc. Biol., 79, 954, 10.1189/jlb.1005544

Lacy, 2006, Mechanisms of degranulation in neutrophils, Allergy Asthma Clin. Immunol., 2, 98, 10.1186/1710-1492-2-3-98

Zemans, 2009, Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury, Am. J. Respir. Cell Mol. Biol., 40, 519, 10.1165/rcmb.2008-0348TR

Biffl, 1996, Interleukin-6 delays neutrophil apoptosis via a mechanism involving platelet-activating factor, J. Trauma, 40, 575, 10.1097/00005373-199604000-00009

Klein, 2000, Granulocyte-macrophage colony-stimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways, J. Immunol., 164, 4286, 10.4049/jimmunol.164.8.4286

Kolaczkowska, 2013, Neutrophil recruitment and function in health and inflammation, Nat. Rev. Immunol., 13, 159, 10.1038/nri3399

Yoo, 2011, Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish, J. Leukoc. Biol., 89, 661, 10.1189/jlb.1010567

Parkos, 1996, Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils, Mol. Med., 2, 489, 10.1007/BF03401908

Lee, 2010, Phosphoinositide 3-kinase signaling mediates beta-catenin activation in intestinal epithelial stem and progenitor cells in colitis, Gastroenterology, 139, 869, 10.1053/j.gastro.2010.05.037

Hiscox, 1999, Ezrin regulates cell-cell and cell-matrix adhesion, a possible role with E-cadherin/beta-catenin, J. Cell Sci., 112, 3081, 10.1242/jcs.112.18.3081

Zhang, 2013, AKT activation by N-cadherin regulates beta-catenin signaling and neuronal differentiation during cortical development, Neural Dev., 8, 7, 10.1186/1749-8104-8-7

Watson, 2005, Interferon-gamma selectively increases epithelial permeability to large molecules by activating different populations of paracellular pores, J. Cell Sci., 118, 5221, 10.1242/jcs.02630

Boivin, 2009, Mechanism of interferon-gamma-induced increase in T84 intestinal epithelial tight junction, J. Interferon Cytokine Res., 29, 45, 10.1089/jir.2008.0128

Yang, 2006, Endothelial cell cortactin coordinates intercellular adhesion molecule-1 clustering and actin cytoskeleton remodeling during polymorphonuclear leukocyte adhesion and transmigration, J. Immunol., 177, 6440, 10.4049/jimmunol.177.9.6440

Yang, 2005, ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow, Blood, 106, 584, 10.1182/blood-2004-12-4942

Sumagin, 2007, A role for ICAM-1 in maintenance of leukocyte-endothelial cell rolling interactions in inflamed arterioles, Am. J. Physiol. Heart Circ. Physiol., 293, H2786, 10.1152/ajpheart.00720.2007

Parkos, 1992, Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways, J. Cell Biol., 117, 757, 10.1083/jcb.117.4.757

Chin, 2009, CD47 and TLR-2 cross-talk regulates neutrophil transmigration, J. Immunol., 183, 5957, 10.4049/jimmunol.0900789

Balsam, 1998, Functional mapping of CD11b/CD18 epitopes important in neutrophil-epithelial interactions: a central role of the I domain, J. Immunol., 160, 5058, 10.4049/jimmunol.160.10.5058