Epithelial permeability induced by neutrophil transmigration is potentiated by hypoxia: Role of intracellular cAMP

Journal of Cellular Physiology

Volumn 176, Issue 1, 1998, Pages 76-84

  Friedman, Gary B ^a   Taylor, Cormac T ^a   Parkos, Charles A ^b,c   Colgan, Sean P ^a,d  

^a Center for Experimental Therapeutics and Reperfusion Injury   (United States)

^b HARVARD UNIVERSITY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC AMP; CYCLIC AMP;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CROHN DISEASE; HUMAN; HUMAN CELL; HYPOXIC CELL; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; ISCHEMIA; NEUTROPHIL; PRIORITY JOURNAL; REPERFUSION INJURY;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ADENOSINE MONOPHOSPHATE; ANOXIA; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD47; CARRIER PROTEINS; CELL ADHESION MOLECULES; CELL MEMBRANE PERMEABILITY; CELL MOVEMENT; CELLS, CULTURED; CYCLIC AMP; ELECTROPHYSIOLOGY; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; MACROPHAGE-1 ANTIGEN; NEUTROPHILS; OXYGEN;

EID: 0031808059     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199807)176:1<76::AID-JCP9>3.0.CO;2-5     Document Type: Article

References (48)

1. Barnstable, C.J., Bodmer, W.F., Brown, G., Galfre, G., Milstein, C., Williams, A.F., and Ziegler, A. (1978) Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens - New tools for genetic analysis. Cell, 14:9-20.
2. Barrett, K.E., Huott, P.A., Shah, S.S., Dharmsathaphorn, K., and Wassermann, S.I. (1989) Differing effects of apical and basolateral adenosine on the colonic epithelial cell line T84. Am. J. Physiol., 256:C197-C203.
3. Colgan, S.P., Parkos, C.A., Delp, C., Arnaout, M.A., and Madara, J.L. (1993) Neutrophil migration across cultured intestinal epithelial monolayers is modulated by epithelial exposure to interferon-gamma in a highly polarized fashion. J. Cell. Biol., 120:785-795.
4. Colgan, S.P., Dzus, A.L., and Parkos, C.A. (1996) Epithelial exposure to hypoxia modulates neutrophil transepithelial migration. J. Exp. Med., 184:1003-1015.
5. Cramer, E.B., Milks, L.C., and Ojakian, G.K. (1980) Transepithelial migration of human neutrophils: An in vitro model system. Proc. Natl. Acad. Sci. USA, 77:4069-4073.
6. Dharmsathaphorn, K., and Madara, J.L. (1990) Established intestinal cell lines as model systems for electrolyte transport studies. Methods Enzymol., 192:354-89.
7. Duffey, M.E., Hainau, B., Ho, S., and Bentzel, C.J. (1981) Regulation of epithelial tight junction permeability by cyclic AMP. Nature, 294:451-453.
8. Granger, D.N. (1994) The microcirculation and inflammation: Modulation of leukocyte-endothelial cell adhesion. J. Leukoc. Biol., 55:662-675.
9. Haglund, U.H., Bulkley, G.B., and Granger, D.N. (1987) On the pathophysiology of intestinal ischemia injury. Acta Chir. Scand., 153:321-324.
10. Hawker, P.C., McKay, J.S., and Turnberg, L.A. (1980) Electrolyte transport across colonic mucosa from patients with inflammatory bowel disease. Gastroenterology, 79:508-11.
11. Henson, P., and Oades, Z.G. (1975) Stimulation of human neutrophils by soluble and insoluble immunoglobulin aggregates. J. Clin. Invest., 56:1053-1061.
12. Hofman, P., D'Andrea, L., Carnes, D., Colgan, S.P., and Madara, J.L. (1996) Intestinal epithelial cytoskeleton selectively constrains lumen-to-tissue migration of neutrophils. Am. J. Physiol., 271:C312-C320.
13. Hollander, D. (1992) The intestinal permeability barrier. A hypothesis as to its regulation and involvement in Crohn's disease. Scand. J. Gastroenterol., 27:721-726.
14. Hollander, D., Vadheim, C.M., Brettholtz, E., Petersen, G.M., Delahunty, T.J., and Rotter, J.I. (1986) Increased intestinal permeability in patients with Crohn's disease and their relatives. Ann. Int. Med., 105:883-885.
15. Kurtel, H., Tso, P., and Granger, D.N. (1992) Granulocyte accumulation in postischemic intestine: Role of leukocyte adhesion glycoprotein CD11/CD18. Am. J. Physiol., 262:G878-G882.
16. Madara, J.L. (1988) Tight junction dynamics: Is paracellular transport regulated? Cell, 53:497-498.
17. Madara, J.L., and Dharmsathaphorn, K. (1985) Occluding junction structure-function relationships in a cultured monolayer. J. Cell. Biol., 101:2124-2133.
18. Madara, J.L., Stafford, J., Barenberg, D., and Carlson, S. (1988) Functional coupling of tight junctions and microfilaments in T84 monolayers. Am. J. Physiol., 254:G416-G423.
19. Madara, J.L., Patapoff, T.W., Gillece-Castro, B., Colgan, S.P., Parkos, C.A., Delp, C., and Mrsny, R.J. (1993) 5′-Adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J. Clin. Invest., 91:2320-2325.
20. Madara, J.L., Colgan, S.P., Nusrat, A., Delp, C., and Parkos, C.A. (1992a) A simple approach to measurement of electrical parameters of cultured epithelial monolayers: Use in assessing neutrophil epithelial interactions. J. Tissue Cult. Res., 14:209-216.
21. - secretion in a model intestinal epithelium induced by a neutrophil-derived secretagogue. J. Clin. Invest., 89:1938-1944.
22. Matthews, J.B., Smith, J.A., Tally, K.J., Awtrey, C.S., Nguyen, H., Rich, J., and Madara, J.L. (1994) Na-K-2Cl cotransport in intestinal epithelial cells. Influence of chloride efflux and F-actin on regulation of cotransporter activity and bumetanide binding. J. Biol. Chem., 269:15703-15709.
23. McCormick, B.A., Colgan, S.P., Delp-Archer, C., Miller, S.I., and Madara, J.L. (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: Transcellular signaling to subepithelial neutrophils. J. Cell Biol., 123:895-907.
24. Milks, L.C., Conyers, G.P., and Cramer, E.B. (1986) The effect of neutrophil migration on epithelial permeability. J. Cell Biol., 103:2729-2738.
25. Nash, S., Stafford, J., and Madara, J.L. (1987) Effects of polymorphonuclear leukocyte transmigration on barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest., 80:1104-1113.
26. Nusrat, A., Delp, C., and Madara, J.L. (1992) Intestinal epithelial restitution: Characterization of a cell culture model and mapping cytoskeletal elements in migrating cells. J. Clin. Invest., 89:1501-1511.
27. Nusrat, A., Parkos, C.A., Liang, T.W., Carnes, D.K., and Madara, J.L. (1997) Neutrophil migration across model intestinal epithelia: Monolayer disruption and subsequent events in epithelial repair. Gastroenterology, 113:1489-1500.
28. Ogawa, S., Gerlach, H., Esposito, C., Pasagian-Macaulay, A., Brett, J., and Stern, D. (1990) Hypoxia modulates the barrier and coagulant function of cultured bovine endothelium: Increased monolayer permeability and induction of procoagulant properties. J. Clin. Invest., 85:1090-1098.
29. Ogawa, S., Koga, S., Kuwabara, K., Brett, J., Morrow, B., Morris, S.A., Bilezikian, J.P., Silverstein, S.C., and Stern, D. (1992) Hypoxia-induced increased permeability of endothelial monolayers occurs through lowering of cellular cAMP levels. Am. J. Physiol., 262:C546-C554.
30. Osborne, M.J., Hudson, M., Piasecki, C., Dhillon, A.P., Pounder, R.E., and Wakefield, A.J. (1993) Crohn's disease and anastomotic recurrence: Microvascular ischaemia and anastomotic healing in an animal model. Br. J. Surg., 80:226-229.
31. Parkos, C.A., Delp, C., Arnaout, M.A., and Madara, J.L. (1991) Neutrophil migration across a cultured intestinal epithelium: Dependence on a CD11b/CD18-mediated event and enhanced efficiency in the physiologic direction. J. Clin. Invest., 88:1605-1612.
32. Parkos, C.A., Colgan, S.P., Delp, C., Arnaout, M.A., and Madara, J.L. (1992) Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J. Cell. Biol., 117:757-764.
33. Parkos, C.A., Colgan, S.P., and Madara, J.L. (1994) Interactions of neutrophils with epithelial cells: Lessons from the intestine. J. Am. Soc. Nephrol., 5:1-15.
34. Parkos, C.A., Colgan, S.P., Liang, A., Nusrat, A., Bacarra, A.E., Carnes, D.K., and Madara, J.L. ( 1996) CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J. Cell Biol., 132:437-450.
35. Parks, D.A., and Granger, D.N. (1986) Contributions of ischemia and reperfusion to mucosal lesion formation. Am. J. Physiol., 250:G749-G753.
36. Rubin, L.L. (1992) Endothelial cells: Adhesion and tight junctions. Curr. Opin. Cell Biol., 4:830-833.
37. Sanders, S.E., Madara, J.L., McGuirk, D.K., Gelman, D.S., and Colgan, S.P. (1995) Assessment of inflammatory events on epithelial permeability: A rapid screening method using fluorescein dextrans. Epith. Cell Biol., 4:25-34.
38. - secretion in T84 cells. J. Clin. Invest., 87:1903-1909.
39. Strohmeier, G.R., Reppert, S.M., Lencer, W.I., and Madara, J.L. (1995) The A2b adenosine receptor mediates cAMP responses to adenosine receptor agonists in human intestinal epithelia. J. Biol. Chem., 270:2387-2394.
40. Taylor, C.T., Lisco, S.J., Awtrey, C.S., and Colgan, S.P. (1997) Hypoxia inhibits cyclic nucleotide-stimulated epithelial ion transport: Role for nucleotide cyclases as oxygen sensors. J. Pharmacol. Exp. Ther., (in press).
41. Teahon, K., Smethurst, P., Pearson, M., Levi, A.J., and Bjarnson, L. (1991) The effect of elemental diet on intestinal permeability and inflammation in Crohn's disease. Gastroenterology, 101:84-89.
42. Thompson, N.P., Wakefield, A.J., and Pounder, R.E. (1995) Inherited disorders of coagulation appear to protect against inflammatory bowel disease. Gastroenterology, 108:1011-1015.
43. Todd, R.F., Nadler, L.M., and Schlossman, S.F. (1981) Antigens on human monocyte identified by monoclonal antibodies. J. Immunol., 126:1435-1442.
44. Wakefield, A.J., Dhillon, A.P., Rowles, P.M., Sawyer, A.M., Pitilo, R.M., Lewis, A.A.M., and Pounder, R.E. (1989) Pathogenesis of Crohn's disease: Multifocal gastrointestinal infarction. Lancet, 2:1057-1062.
45. Wang, J.Y., and Johnson, L.R. (1989) Induction of gastric and duodenal mucosal ornithine decarboxylase during stress. Am. J. Physiol., 257:G259-G265.
46. Welbourne, C.R.B., Goldman, G., Valeri, C.R., Shepro, D., and Hechtman, H.B. (1991) Pathophysiology of ischaemia reperfusion injury: Central role of the neutrophil. Br. J. Surg., 78:651-655.
47. Yardley, J.H. (1986) Pathology of idiopathic inflammatory bowel disease and relevance of specific cell findings: An overview. In: Recent Developments in the Therapy of Inflammatory Bowel Disease. J.H. Yardley, ed., Williams and Wilkins, Baltimore, pp. 3-9.
48. Yardley, J.H., and Donowitz, M. (1977) Colo-rectal biopsies in inflammatory bowel disease. In: The Gastrointestinal Tract. J.H. Yardley and B.C. Morson, eds., Williams and Wilkins, Baltimore, pp. 57-94.