Role of the Intestinal Epithelium in Orchestrating Innate and   Adaptive Mucosal Immunity

C. Maaser; M. F. Kagnoff

doi:10.1055/s-2002-32808

Zeitschrift für Gastroenterologie, Inhaltsverzeichnis

Z Gastroenterol 2002; 40(7): 525-529
DOI: 10.1055/s-2002-32808

Übersicht

Role of the Intestinal Epithelium in Orchestrating Innate and Adaptive Mucosal Immunity

Rolle des intestinalen Epithels im Rahmen der angeborenen und erworbenen ImmunitätC. Maaser¹ , M. F. Kagnoff²

²Medizinische Klinik und Poliklinik B, Universitätsklinikum Münster, Germany
¹Laboratory of Mucosal Immunology, University of California, San Diego, La Jolla, USA

Abstract

Zusammenfassung

Die Mukosa, welche das humane Kolon und den Dünndarm begrenzt, ist ein Gebiet von chronischer, regulierter, „physiologischer” Entzündung. Dies stellt einen deutlichen Gegensatz zu anderen mukosalen Gebieten des Körpers dar, denn fänden sich die gleiche Anzahl von T- und B-Lymphozyten, Eosinophilen, Mastzellen, Makrophagen und dendritischen Zellen, wie sie im humanen Intestinaltrakt vorhanden sind, in anderen Bereichen, so würde man diese Orte als Orte von chronisch pathologischer Entzündung bezeichnen. Diese Übersicht beschreibt die Rolle des intestinalen Epithels bei der Entstehung dieser „physiologischen”, intestinalen, mukosalen Entzündung und konzentriert sich dabei auf dessen Rolle im Rahmen der Initiierung und Vermittlung von angeborenen und erworbenen mukosalen Immunantworten.

Abstract

The mucosa that lines the human colon and small intestine is a site of chronic regulated “physiologic” inflammation. This contrasts markedly with other mucosal sites in that if the numbers of T and B cells, eosinophils, mast cells, macrophages, and dendritic cells that are present in the human intestinal tract were to be present in other sites, those sites would be considered to be sites of chronic pathological inflammation. This review examines the role of the intestinal epithelium in the development of “physiologic” intestinal mucosal inflammation and focuses on its role in signalling and mediating host innate and adaptive mucosal immune responses.

Schlüsselwörter

Epithelzelle - Chemokin - Zytokin - Wirtsabwehr - Pathogene Bakterien

Key words

Epithelial Cell - Chemokine - Cytokine - Host Defence - Pathogenic Bacteria

Volltext

Referenzen

References

1 Anderson J M, Van Itallie C M. Tight junctions: closing in on the seal. Curr Biol. 1999; 9 R922-924
2 Youakim A, Ahdieh M. Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am J Physiol. 1999; 276 G1279-1288
3 Kucharzik T, Walsh S V, Chen J, Parkos C A, Nusrat A. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol. 2001; 159 2001-2009
4 Dignass A U, Podolsky D K. Cytokine modulation of intestinal epithelial cell restitution: central role of transforming growth factor beta. Gastroenterology. 1993; 105 1323-1332
5 Dignass A, Lynch-Devaney K, Kindon H, Thim L, Podolsky D K. Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. J Clin Invest. 1994; 94 376-383
6 Eckmann L, Kagnoff M F, Fierer J. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun. 1993; 61 4569-4574
7 Jung H C, Eckmann L, Yang S K. et al . A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995; 95 55-65
8 Yang S K, Eckmann L, Panja A, Kagnoff M F. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology. 1997; 113 1214-1223
9 Reinecker H C, Loh E Y, Ringler D J, Mehta A, Rombeau J L, MacDermott R P. Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology. 1995; 108 40-50
10 Izadpanah A, Dwinell M B, Eckmann L, Varki N M, Kagnoff M F. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am J Physiol Gastrointest Liver Physiol. 2001; 280 G710-719
11 Dwinell M B, Lugering N, Eckmann L, Kagnoff M F. Regulated Production of Interferon-Inducible T-Cell Chemoattractants by Human Intestinal Epithelial Cells. Gastroenterology. 2001; 120 49-59
12 Shibahara T, Wilcox J N, Couse T, Madara J L. Characterization of Epithelial Chemoattractants for Human Intestinal Intraepithelial Lymphocytes. Gastroenterology. 2001; 120 60-70
13 Kunkel E J, Campbell J J, Haraldsen G. et al . Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med. 2000; 192 761-768
14 Wurbel M A, Philippe J M, Nguyen C. et al . The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol. 2000; 30 262-271
15 Pan J, Kunkel E J, Gosslar U. et al . A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol. 2000; 165 2943-2949
16 Wang W, Soto H, Oldham E R. et al . A. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 2000. 275 22313-22323
17 Reinecker H C, MacDermott R P, Mirau S, Dignass A, Podolsky D K. Intestinal epithelial cells both express and respond to interleukin 15. Gastroenterology. 1996; 111 1706-1713
18 Eckmann L, Reed S L, Smith J R, Kagnoff M F. Entamoeba histolytica trophozoites induce an inflammatory cytokine response by cultured human cells through the paracrine action of cytolytically released interleukin-1 alpha. J Clin Invest. 1995; 96 1269-1279
19 Maaser C, Eckmann L, Paesold G, Kim H S, Kagnoff M F. Ubiquitous production of macrophage migration inhibitory factor by human gastric and intestinal epithelium. Gastroenterology. 2002; 122 667-680
20 Maaser C, Eckmann L, Birkenbach M P, Kagnoff M F. Human intestinal epithelium expresses EBI3, a potential modulator of the IL-12 response. Gastroenterology. 2001; 120 A-994
21 Maaser C, Schoeppner S, Kucharzik T, Kraft M, Schoenherr E, Domschke W, Luegering N. Colonic epithelial cells induce endothelial cell expression of ICAM-1 and VCAM-1 by a NF-kappaB-dependent mechanism. Clin Exp Immunol. 2001; 124 208-213
22 Eckmann L, Jung H C, Schurer-Maly C, Panja A, Morzycka-Wroblewska E, Kagnoff M F. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology. 1993; 105 1689-1697
23 Hase K, Eckmann L, Leopard J D, Varki N, Kagnoff M F. Cell Differentiation Is a Key Determinant of Cathelicidin LL-37/Human Cationic Antimicrobial Protein 18 Expression by Human Colon Epithelium. Infect Immun. 2002; 70 953-963
24 O’Neil D A, Porter E M, Elewaut D, Anderson G M, Eckmann L, Ganz T, Kagnoff M F. Expression and regulation of the human beta-defensins hBD-1 and hBD-2 in intestinal epithelium. J Immunol. 1999; 163 6718-6724
25 O’Neil D A, Cole S P, Martin-Porter E, Housley M P, Liu L, Ganz T, Kagnoff M F. Regulation of human beta-defensins by gastric epithelial cells in response to infection with Helicobacter pylori or stimulation with interleukin-1. Infect Immun. 2000; 68 5412-5415
26 Witthoft T, Eckmann L, Kim J M, Kagnoff M F. Enteroinvasive bacteria directly activate expression of iNOS and NO production in human colon epithelial cells. Am J Physiol. 1998; 275 G564-571
27 Eckmann L, Stenson W F, Savidge T C, Lowe D C, Barrett K E, Fierer J, Smith J R, Kagnoff M F. Role of intestinal epithelial cells in the host secretory response to infection by invasive bacteria. Bacterial entry induces epithelial prostaglandin h synthase-2 expression and prostaglandin E2 and F2alpha production. J Clin Invest 1997. 100 296-309
28 Casanova J E. Structure and function of the polimeric immunoglobulin receptor in epithelial cells. Kagnoff MF, H Kiyono H Essentials of mucosal immunology San Diego; Academic 1996: 151-166
29 Mestecky J, Lue C, Russell M W. Selective transport of IgA. Cellular and molecular aspects. Gastroenterol Clin North. Am 1991; 20 441-471
30 Mazanec M B, Kaetzel C S, Lamm M E, Fletcher D, Nedrud J G. Intracellular neutralization of virus by immunoglobulin A antibodies. Proc Natl Acad Sci U S A. 1992; 89 6901-6905
31 Burns J W, Siadat-Pajouh M, Krishnaney A A, Greenberg H B. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science. 1996; 272 104-107
32 Colgan S P, Hershberg R M, Furuta G T, Blumberg R S. Ligation of intestinal epithelial CD1d induces bioactive IL-10: critical role of the cytoplasmic tail in autocrine signaling. U S A; Proc Natl Acad Sci 1999 96: 13938-13943
33 Steinle A, Groh V, Spies T. Diversification, expression, and gamma delta T cell recognition of evolutionarily distant members of the MIC family of major histocompatibility complex class I-related molecules. Proc Natl Acad Sci U S A; 1998 95: 12510-12515
34 Varilek G W, Neil G A, Bishop W P. Caco-2 cells express type I interleukin-1 receptors: ligand binding enhances proliferation. Am J Physiol 1994 267: G1101-1107
35 Colgan S P, Resnick M B, Parkos C A. et al . IL-4 directly modulates function of a model human intestinal epithelium. J Immunol. 1994; 153 2122-2129
36 Reinecker H C, Podolsky D K. Human intestinal epithelial cells express functional cytokine receptors sharing the common gamma c chain of the interleukin 2 receptor. Proc Natl Acad Sci U S A. 1995; 92 8353-8357
37 Yamada K, Shimaoka M, Nagayama K, Hiroi T, Kiyono H, Honda T. Bacterial invasion induces interleukin-7 receptor expression in colonic epithelial cell line, T84. Eur J Immunol. 1997; 27 3456-3460
38 Panja A, Goldberg S, Eckmann L, Krishen P, Mayer L. The regulation and functional consequence of proinflammatory cytokine binding on human intestinal epithelial cells. J Immunol. 1998; 161 3675-3684
39 Fish S M, Proujansky R, Reenstra W W. Synergistic effects of interferon gamma and tumour necrosis factor alpha on T84 cell function. Gut. 1999; 45 191-198
40 Awane M, Andres P G, Li D J, Reinecker H C. NF-kappa B-inducing kinase is a common mediator of IL-17-, TNF-alpha-, and IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells. J Immunol. 1999; 162 5337-5344
41 Denning T L, Campbell N A, Song F. et al . Expression of IL-10 receptors on epithelial cells from the murine small and large intestine. Int Immunol. 2000; 12 133-139
42 Dwinell M B, Eckmann L, Leopard J D, Varki N M, Kagnoff M F. Chemokine receptor expression by human intestinal epithelial cells. Gastroenterology. 1999; 117 359-367
43 Delezay O, Koch N, Yahi N. et al . Co-expression of CXCR4/fusin and galactosylceramide in the human intestinal epithelial cell line HT-29. Aids. 1997; 11 1311-1318
44 Jordan N J, Kolios G, Abbot S E. et al . Expression of functional CXCR4 chemokine receptors on human colonic epithelial cells. J Clin Invest. 1999; 104 1061-1069
45 Brumell J H, Steele-Mortimer O, Finlay B B. Bacterial invasion: Force feeding by Salmonella. Curr Biol. 1999; 9 R277-280
46 Galan J E. Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol. 2001; 17 53-86
47 Kaisho T, Akira S. Critical roles of Toll-like receptors in host defense. Crit Rev Immunol. 2000; 20 393-405
48 Cario E, Rosenberg I M, Brandwein S L, Beck P L, Reinecker H C, Podolsky D K. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol. 2000; 164 966-972
49 Gewirtz A T, Simon P O Jr, Schmitt C K. et al . Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest. 2001; 107 99-109
50 Gewirtz A T, Navas T A, Lyons S, Godowski P J, Madara J L. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001; 167 1882-1885
51 Dogan A, Wang Z D, Spencer J. E-cadherin expression in intestinal epithelium. J Clin Pathol. 1995; 48 143-146
52 Huang G T, Eckmann L, Savidge T C, Kagnoff M F. Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM)-1) expression and neutrophil adhesion. J Clin Invest. 1996; 98 572-583
53 Kvale D, Krajci P, Brandtzaeg P. Expression and regulation of adhesion molecules ICAM-1 (CD54) and LFA-3 (CD58) in human intestinal epithelial cell lines. Scand J Immunol. 1992; 35 669-676
54 Morales V M, Christ A, Watt S M et al. Regulation of human intestinal intraepithelial lymphocyte cytolytic function by biliary glycoprotein (CD66a). J Immunol. 1999; 163 1363-1370
55 Parkos C A, Colgan S P, Diamond M S. et al . Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils. Mol Med. 1996; 2 489-505
56 Yio X Y, Mayer L. Characterization of a 180-kDa intestinal epithelial cell membrane glycoprotein, gp180. A candidate molecule mediating t cell-epithelial cell interactions. J Biol Chem. 1997; 272 12786-12792
57 Kelly C P, O’Keane J C, Orellana J. et al . Human colon cancer cells express ICAM-1 in vivo and support LFA-1-dependent lymphocyte adhesion in vitro. Am J Physiol. 1992; 263 G864-870
58 Elewaut D, DiDonato J A, Kim J M, Truong F, Eckmann L, Kagnoff M F. NF-kappa B is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol. 1999; 163 1457-1466
59 Meijer L K, Schesser K, Wolf-Watz H, Sassone-Corsi P, Pettersson S. The bacterial protein YopJ abrogates multiple signal transduction pathways that converge on the transcription factor CREB. Cell Microbiol. 2000; 2 231-238
60 Schesser K, Spiik A K, Dukuzumuremyi J M, Neurath M F, Pettersson S, Wolf-Watz H. The yopJ locus is required for Yersinia-mediated inhibition of NF- kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol. 1998; 28 1067-1079

Dr. med Christian Maaser

Medizinische Klinik und Poliklinik B, Westfälische Wilhelms-Universität Münster

Albert-Schweitzer-Straße 33

48129 Münster

eMail: maaser@uni-muenster.de