Escherichia Coli Induces Transuroepithelial Neutrophil Migration by an Intercellular Adhesion Molecule-1-dependent Mechanism

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 1995 Oct 1

PMID 7558319

Citations 43

Authors

W W Agace

M Patarroyo

M Svensson

E Carlemalm

C Svanborg

Affiliations

Soon will be listed here.

Abstract

During bacterial infections at mucosal sites, neutrophils migrate to the mucosa and cross the epithelial barrier. We have examined neutrophil migration across Escherichia coli-stimulated uroepithelial cell layers in an attempt to more fully understand this process. Stimulation of uroepithelial cells with E. coli or interleukin-1 alpha (IL-1 alpha) induced transepithelial neutrophil migration in a time- and stimulant dose-dependent manner. Uroepithelial cell lines and nontransformed uroepithelial cells expressed intercellular adhesion molecule-1 (ICAM-1) but not ICAM-2, E-selectin, or P-selectin. Epithelial ICAM-1 expression was enhanced after stimulation with E. coli or IL-1 alpha. Anti-ICAM-1 antibody reduced transepithelial neutrophil migration by 61 to 85%, indicating that neutrophils bound ICAM-1 on the epithelial surface. Antibodies to CD18 and CD11b reduced migration by 70 to 79%, suggesting that CD11b/CD18 (Mac-1) was acting as the neutrophil receptor for ICAM-1 in this process. Anti-CD11a antibodies had no effect on neutrophil migration. In conclusion, E. coli induced ICAM-1- and Mac-1-dependent transepithelial neutrophil migration. Previous studies have shown that urinary tract epithelial cells secrete IL-8 when exposed to E. coli or IL-1 alpha. These observations suggest that epithelial cells play an active role in neutrophil migration during urinary tract infections.

Citing Articles

A Dynamic Interplay of Innate Immune Responses During Urinary Tract Infection.

Naskar M, Choi H Immune Netw. 2024; 24(4):e31.

PMID: 39246616 PMC: 11377947. DOI: 10.4110/in.2024.24.e31.

Phenotypic Assessment of Clinical Escherichia coli Isolates as an Indicator for Uropathogenic Potential.

Shea A, Frick-Cheng A, Smith S, Mobley H mSystems. 2022; 7(6):e0082722.

PMID: 36445110 PMC: 9765037. DOI: 10.1128/msystems.00827-22.

LEUKOCYTE-EPITHELIAL INTERACTIONS: A DOUBLE-EDGED SWORD THAT PROTECTS AND INJURES DURING HEALTH AND DISEASE.

Parkos C Trans Am Clin Climatol Assoc. 2022; 132:22-33.

PMID: 36196189 PMC: 9480551.

Transcriptional alterations in bladder epithelial cells in response to infection with different morphological states of uropathogenic Escherichia coli.

Persson K, Petersson U, Johansson C, Demirel I, Kruse R Sci Rep. 2022; 12(1):486.

PMID: 35017565 PMC: 8752619. DOI: 10.1038/s41598-021-04396-0.

Dynamic persistence of UPEC intracellular bacterial communities in a human bladder-chip model of urinary tract infection.

Sharma K, Dhar N, Thacker V, Simonet T, Signorino-Gelo F, Knott G Elife. 2021; 10.

PMID: 34219648 PMC: 8354636. DOI: 10.7554/eLife.66481.

References

Parkos C, Delp C, Arnaout M, Madara J . Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J Clin Invest. 1991; 88(5):1605-12. PMC: 295682. DOI: 10.1172/JCI115473. View

Nortamo P, Li R, Renkonen R, Timonen T, Prieto J, Patarroyo M . The expression of human intercellular adhesion molecule-2 is refractory to inflammatory cytokines. Eur J Immunol. 1991; 21(10):2629-32. DOI: 10.1002/eji.1830211049. View

Somersalo K, Tarkkanen J, Patarroyo M, Saksela E . Involvement of beta 2-integrins in the migration of human natural killer cells. J Immunol. 1992; 149(2):590-8. View

Agace W, Hedges S, Andersson U, Andersson J, Ceska M, Svanborg C . Selective cytokine production by epithelial cells following exposure to Escherichia coli. Infect Immun. 1993; 61(2):602-9. PMC: 302770. DOI: 10.1128/iai.61.2.602-609.1993. View

Colgan S, Parkos C, Delp C, Arnaout M, Madara J . Neutrophil migration across cultured intestinal epithelial monolayers is modulated by epithelial exposure to IFN-gamma in a highly polarized fashion. J Cell Biol. 1993; 120(3):785-98. PMC: 2119532. DOI: 10.1083/jcb.120.3.785. View

Bevilacqua M, Nelson R . Selectins. J Clin Invest. 1993; 91(2):379-87. PMC: 287934. DOI: 10.1172/JCI116210. View

Hedges S, Agace W, Svensson M, Svanborg C . Cyclosporin A does not inhibit IL-1 alpha-induced epithelial cell IL-6 secretion. Scand J Immunol. 1993; 37(5):581-6. DOI: 10.1111/j.1365-3083.1993.tb02575.x. View

Elgavish A . Effects of Escherichia coli and E. coli lipopolysaccharides on the function of human ureteral epithelial cells cultured in serum-free medium. Infect Immun. 1993; 61(8):3304-12. PMC: 281004. DOI: 10.1128/iai.61.8.3304-3312.1993. View

Agace W, Hedges S, Ceska M, Svanborg C . Interleukin-8 and the neutrophil response to mucosal gram-negative infection. J Clin Invest. 1993; 92(2):780-5. PMC: 294914. DOI: 10.1172/JCI116650. View

10.

McCormick B, Colgan S, MILLER S, Madara J . Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol. 1993; 123(4):895-907. PMC: 2200157. DOI: 10.1083/jcb.123.4.895. View

11.

Lawrence M, Springer T . Neutrophils roll on E-selectin. J Immunol. 1993; 151(11):6338-46. View

12.

Hedges S, Agace W, Svensson M, Sjogren A, Ceska M, Svanborg C . Uroepithelial cells are part of a mucosal cytokine network. Infect Immun. 1994; 62(6):2315-21. PMC: 186514. DOI: 10.1128/iai.62.6.2315-2321.1994. View

13.

Svensson M, Lindstedt R, RADIN N, Svanborg C . Epithelial glucosphingolipid expression as a determinant of bacterial adherence and cytokine production. Infect Immun. 1994; 62(10):4404-10. PMC: 303123. DOI: 10.1128/iai.62.10.4404-4410.1994. View

14.

Salcedo R, Patarroyo M . Constitutive alpha V beta 3 integrin-mediated adhesion of human lymphoid B cells to vitronectin substrate. Cell Immunol. 1995; 160(2):165-72. DOI: 10.1016/0008-8749(95)80023-c. View

15.

Yardley J, Donowitz M . Colo-rectal biopsy in inflammatory bowel disease. Monogr Pathol. 1977; (18):50-94. View

16.

Eden C, Freter R, Hagberg L, Hull R, Hull S, Leffler H . Inhibition of experimental ascending urinary tract infection by an epithelial cell-surface receptor analogue. Nature. 1982; 298(5874):560-2. DOI: 10.1038/298560a0. View

17.

Weiland J, DAVIS W, Holter J, Mohammed J, Dorinsky P, Gadek J . Lung neutrophils in the adult respiratory distress syndrome. Clinical and pathophysiologic significance. Am Rev Respir Dis. 1986; 133(2):218-25. DOI: 10.1164/arrd.1986.133.2.218. View

18.

Pober J, Bevilacqua M, Mendrick D, Lapierre L, Fiers W, Gimbrone Jr M . Two distinct monokines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells. J Immunol. 1986; 136(5):1680-7. View

19.

Pober J, Gimbrone Jr M, Lapierre L, Mendrick D, Fiers W, Rothlein R . Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol. 1986; 137(6):1893-6. View

20.

Patarroyo M, Clark E, Prieto J, Kantor C, Gahmberg C . Identification of a novel adhesion molecule in human leukocytes by monoclonal antibody LB-2. FEBS Lett. 1987; 210(2):127-31. DOI: 10.1016/0014-5793(87)81321-2. View