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Expression and Polarization of Intercellular Adhesion Molecule-1 on Human Intestinal Epithelia: Consequences for CD11b/CD18-Mediated Interactions with Neutrophils

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Abstract

Background

Epithelial dysfunction and patient symptoms in inflammatory intestinal diseases such as ulcerative colitis and Crohn’s disease correlate with migration of neutrophils (PMN) across the intestinal epithelium. In vitro modeling of PMN transepithelial migration has revealed distinct differences from transendothelial migration. By using polarized monolayers of human intestinal epithelia (T84), PMN transepithelial migration has been shown to be dependent on the leukocyte integrin CD11b/CD18 (Mac-1), but not on CD11a/CD18 (LFA-1). Since intercellular adhesion molecule-1 (ICAM-1) is an important endothelial counterreceptor for these integrins, its expression in intestinal epithelia and role in PMN-intestinal epithelial interactions was investigated.

Materials and Methods

A panel of antibodies against different domains of ICAM-1, polarized monolayers of human intestinal epithelia (T84), and natural human colonic epithelia were used to examine the polarity of epithelial ICAM-1 surface expression and the functional role of ICAM-1 in neutrophil-intestinal epithelial adhesive interactions.

Results

While no surface expression of ICAM-1 was detected on unstimulated T84 cells, interferon-γ (IFNγ) elicited a marked expression of ICAM-1 that selectively polarized to the apical epithelial membrane. Similarly, apically restricted surface expression of ICAM-1 was detected in natural human colonic epithelium only in association with active inflammation. With or without IFNγ pre-exposure, physiologically directed (basolateral-to-apical) transepithelial migration of PMN was unaffected by blocking monoclonal antibodies (mAbs) to ICAM-1. In contrast, PMN migration across IFNγ-stimulated monolayers in the reverse (apical-to-basolateral) direction was inhibited by anti-ICAM-1 antibodies. Adhesion studies revealed that T84 cells adhered selectively to purified CD11b/CD18 and such adherence, with or without IFNγ pre-exposure, was unaffected by ICAM-1 mAb. Similarly, freshly isolated epithelial cells from inflamed human intestine bound to CD11b/CD18 in an ICAM-1-independent fashion.

Conclusions

These data indicate that ICAM-1 is strictly polarized in intestinal epithelia and does not represent a counterreceptor for neutrophil CD11b/CD18 during physiologically directed transmigration, but may facilitate apical membrane-PMN interactions after the arrival of PMN in the intestinal lumen.

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Acknowledgments

This work was supported in part by a research grant from the Crohn’s and Colitis Foundation of America and by National Institutes of Health Grants HL54229, CA31798, CA31799, DK47662, DK7662, DK35932, and DK33506. The authors thank Denice Carnes for excellent tissue culture support and Susan Carlson for assistance in preparing the figures.

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  1. Michael S. Diamond

    Present address: Department of Medicine, UCSF, Box 0120, San Francisco, CA, 94143, USA

Authors and Affiliations

  1. Department of Pathology, Division of Gastrointestinal Pathology, Brigham and Women’s Hospital, 75 Francis Street, Boston, Massachusetts, 02115, USA

    Charles A. Parkos, Asma Nusrat, Tony W. Liang & James L. Madara

  2. Department of Anesthesia, Division of Gastrointestinal Pathology, Brigham and Women’s Hospital, Boston, Massachusetts, USA

    Sean P. Colgan

  3. Center for Blood Research and Harvard Digestive Diseases Center, Harvard Medical School, Boston, Massachusetts, USA

    Michael S. Diamond & Timothy A. Springer

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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 2, 489–505 (1996). https://doi.org/10.1007/BF03401908

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