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. 1983 May 1;96(5):1241–1247. doi: 10.1083/jcb.96.5.1241

Epithelial permeability and the transepithelial migration of human neutrophils

PMCID: PMC2112640  PMID: 6841447

Abstract

Although polymorphonuclear leukocytes (PMN's) can migrate through every epithelium in the body regardless of its permeability, very little is known about the effect of epithelial permeability on PMN migration and the effect of emigrating PMN's on the permeability of the epithelium. In an in vitro model system of transepithelial migration, human PMN's were stimulated by 0.1 micrometer fMet-Leu-Phe to traverse confluent, polarized canine kidney epithelial monolayers of varying permeabilities. Epithelial permeability was determined by both conductance measurement and horseradish peroxidase (HRP) tracer studies. As epithelial permeability increased, the number of PMN invasion sites as well as the number of PMN's that traversed the monolayer increased. The effect of PMN migration on epithelial permeability was examined using the ultrastructural tracers HRP and lanthanum nitrate. PMN's traversing the monolayer made close cell-to- cell contacts with other invading PMNs and with adjacent epithelial cells. These close contacts appeared to prevent leakage of tracer across invasion sites. Following PMN emigration, epithelial junctional membranes reapproximated and were impermeable to the tracers. These results indicated that, in the absence of serum and connective tissue factors, (a) the number of PMN invasion sites and the number of PMN's that traversed an epithelium were a function of the conductance of the epithelium and (b) PMN's in the process of transepithelial migration maintained close cell-cell contacts and prevented the leakage of particles (greater than 5 nm in diameter) across the invasion site.

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Selected References

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  1. Bisbee C. A., Machen T. E., Bern H. A. Mouse mammary epithelial cells on floating collagen gels: transepithelial ion transport and effects of prolactin. Proc Natl Acad Sci U S A. 1979 Jan;76(1):536–540. doi: 10.1073/pnas.76.1.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  3. Cereijido M., Meza I., Martínez-Palomo A. Occluding junctions in cultured epithelial monolayers. Am J Physiol. 1981 Mar;240(3):C96–102. doi: 10.1152/ajpcell.1981.240.3.C96. [DOI] [PubMed] [Google Scholar]
  4. Cereijido M., Robbins E. S., Dolan W. J., Rotunno C. A., Sabatini D. D. Polarized monolayers formed by epithelial cells on a permeable and translucent support. J Cell Biol. 1978 Jun;77(3):853–880. doi: 10.1083/jcb.77.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cereijido M., Stefani E., Palomo A. M. Occluding junctions in a cultured transporting epithelium: structural and functional heterogeneity. J Membr Biol. 1980 Mar 31;53(1):19–32. doi: 10.1007/BF01871169. [DOI] [PubMed] [Google Scholar]
  6. Claude P. Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludens. J Membr Biol. 1978 Mar 10;39(2-3):219–232. doi: 10.1007/BF01870332. [DOI] [PubMed] [Google Scholar]
  7. Cramer E. B., Milks L. C., Ojakian G. K. Transepithelial migration of human neutrophils: an in vitro model system. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4069–4073. doi: 10.1073/pnas.77.7.4069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crone C., Christensen O. Electrical resistance of a capillary endothelium. J Gen Physiol. 1981 Apr;77(4):349–371. doi: 10.1085/jgp.77.4.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dahlén S. E., Björk J., Hedqvist P., Arfors K. E., Hammarström S., Lindgren J. A., Samuelsson B. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3887–3891. doi: 10.1073/pnas.78.6.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fahimi H. D. An assessment of the DAB methods for cytochemical detection of catalase and peroxidase. J Histochem Cytochem. 1979 Oct;27(10):1365–1366. doi: 10.1177/27.10.92493. [DOI] [PubMed] [Google Scholar]
  11. HURLEY J. V. ACUTE INFLAMMATION: THE EFFECT OF CONCURRENT LEUCOCYTIC EMIGRATION AND INCREASED PERMEABILITY ON PARTICLE RETENTION BY THE VASCULAR WALL. Br J Exp Pathol. 1964 Dec;45:627–633. [PMC free article] [PubMed] [Google Scholar]
  12. HURLEY J. V. An electron microscopic study of leucocytic emigration and vascular permeability in rat skin. Aust J Exp Biol Med Sci. 1963 Apr;41:171–186. doi: 10.1038/icb.1963.17. [DOI] [PubMed] [Google Scholar]
  13. Issekutz A. C., Movat H. Z. The effect of vasodilator prostaglandins on polymorphonuclear leukocyte infiltration and vascular injury. Am J Pathol. 1982 Jun;107(3):300–309. [PMC free article] [PubMed] [Google Scholar]
  14. Johnson J. P., Steele R. E., Perkins F. M., Wade J. B., Preston A. S., Green S. W., Handler J. S. Epithelial organization and hormone sensitivity of toad urinary bladder cells in culture. Am J Physiol. 1981 Aug;241(2):F129–F138. doi: 10.1152/ajprenal.1981.241.2.F129. [DOI] [PubMed] [Google Scholar]
  15. Martinez-Palomo A., Meza I., Beaty G., Cereijido M. Experimental modulation of occluding junctions in a cultured transporting epithelium. J Cell Biol. 1980 Dec;87(3 Pt 1):736–745. doi: 10.1083/jcb.87.3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mason R. J., Williams M. C., Widdicombe J. H., Sanders M. J., Misfeldt D. S., Berry L. C., Jr Transepithelial transport by pulmonary alveolar type II cells in primary culture. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6033–6037. doi: 10.1073/pnas.79.19.6033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Misfeldt D. S., Hamamoto S. T., Pitelka D. R. Transepithelial transport in cell culture. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1212–1216. doi: 10.1073/pnas.73.4.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Perkins F. M., Handler J. S. Transport properties of toad kidney epithelia in culture. Am J Physiol. 1981 Sep;241(3):C154–C159. doi: 10.1152/ajpcell.1981.241.3.C154. [DOI] [PubMed] [Google Scholar]
  19. Schatzki P. F., Newsome A. Neutralized lanthanum solution: a largely noncolloidal ultrastructural tracer. Stain Technol. 1975 May;50(3):171–178. doi: 10.3109/10520297509117054. [DOI] [PubMed] [Google Scholar]
  20. Shaklai M., Tavassoli M. A modified technique to obtain uniform precipitation of lanthanum tracer in the extracellular space. J Histochem Cytochem. 1977 Aug;25(8):1013–1015. doi: 10.1177/25.8.330739. [DOI] [PubMed] [Google Scholar]
  21. Simionescu N. Enzymatic tracers in the study of vascular permeability. J Histochem Cytochem. 1979 Aug;27(8):1120–1130. doi: 10.1177/27.8.90073. [DOI] [PubMed] [Google Scholar]
  22. Simionescu N., Simionescu M., Palade G. E. Structural basis of permeability in sequential segments of the microvasculature of the diaphragm. II. Pathways followed by microperoxidase across the endothelium. Microvasc Res. 1978 Jan;15(1):17–36. doi: 10.1016/0026-2862(78)90002-x. [DOI] [PubMed] [Google Scholar]
  23. Wedmore C. V., Williams T. J. Control of vascular permeability by polymorphonuclear leukocytes in inflammation. Nature. 1981 Feb 19;289(5799):646–650. doi: 10.1038/289646a0. [DOI] [PubMed] [Google Scholar]

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