The study of barrier characteristics of Peyer’s patches epithelium in rats

Evgeny Falchuk; Alexander Markov

doi:10.21638/spbu03.2015.307

Authors

Evgeny Falchuk Saint Petersburg State University, 7–9, Universitetskaya nab., Saint Petersburg, 199034, Russian Federation
Alexander Markov Saint Petersburg State University, 7–9, Universitetskaya nab., Saint Petersburg, 199034, Russian Federation

DOI:

https://doi.org/10.21638/spbu03.2015.307

Abstract

The aim of the study was to investigate the barrier function of Peyer’s patches epithelium, which covers the clusters of organized lymphoid tissues in the small intestinal. We used the Ussing chamber method to determine electrophysiological characteristics of epithelium and Western blot method and immunohistochemistry to investigate expression of tight junction proteins. We revealed that Peyer’s patches epithelium, which is specialized in sampling and transporting of antigen structures, has lower conductance compare to adjacent intestinal villous epithelium, the main function of which is to uptake ions, water and nutrients. On molecular level Peyer’s patch epithelium has lower expression of claudin-2 and claudin-7, which increases the permeability of the intercellular space, and higher expression of claudin-5 and -8, which decreases the paracellular pathway. Immunohistochemistry confirmed localization of claudins in the tight junction complex. We suggest that the restriction of paracellular transport is a prerequisite for the antigen presentation through specialized M-cells in Peyer’s patches epithelium. Refs 29. Figs 4.

Keywords:

Peyer’s patches, epithelium, small intestinal, paracellular pathway, tight junction, claudins, electrophysiology, conductance

Downloads

Download data is not yet available.

References

Jung C., Hugot J. P., Barreau F. Peyer’s Patches: The Immune Sensors of the Intestine. Int. J. Inflam, 2010. https://doi.org/10.4061/2010/823710" target="_blank">https://doi.org/10.4061/2010/823710

Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology, 1974, vol. 66, no. 2, pp. 189–203.

Boehm M., Hoy B., Rohde M. et al. Rapid paracellular transmigration of Campylobacter jejuni across polarized epithelial cells without affecting TER: role of proteolytic-active HtrA cleaving E-cadherin but not fibronectin. Gut Pathog, 2012, vol. 4. https://doi.org/10.1186/1757-4749-4-3" target="_blank">https://doi.org/10.1186/1757-4749-4-3

Kops S. K., Lowe D. K., Bement W. M. et al. Migration of Salmonella typhi through intestinal epithelial monolayers: an in vitro study. Microbiol. Immunol, 1996, vol. 40, no. 11, pp. 799–811.

Hopkins S. A., Niedergang F., Corthesy-Theulaz I. E. et al. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer’s patch dendritic cells. Cell Microbiol, 2000, vol. 2, no. 1, pp. 59–68.

Rescigno M., Urbano M., Valzasina B. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol, 2001, vol. 2, no. 4, pp. 361–367.

Günzel D., Fromm M. Claudins and other tight junction proteins. Compr. Physiol, 2012, vol. 2, no. 3, pp. 1819–1852.

Furuse M., Hata M., Furuse K. et al. Claudin-based tight junctions are crucial for themammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol., 2002, vol. 156, pp. 1099–1111.

Milatz S., Krug S. M., Rosenthal R. et al. Claudin-3 acts as a sealing component of the tight junction for ions of either charge and uncharged solutes. Biochim. Biophys. Acta, 2010, vol. 1798, no. 11, pp. 2048–2057.

Amasheh S., Meiri N., Gitter A. H. et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J. Cell Sci., 2002, vol. 15, no, 115, pp. 4969–4976.

Krug S. M., Günzel D., Conrad M. P. et al. Charge-selective claudin channels. Ann. NY Acad. Sci., 2012, vol. 1257, pp. 20–28.

Markov A. G., Veshnyakova A., Fromm M. et al. Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine. J. Comp. Physiol., B. 2010, vol. 180, no. 4, pp. 591–598.

Brayden D. J., Baird A. W. A distinctive electrophysiological signature from the Peyer’s patches of rabbit intestine. Br. J. Pharmacol., 1994, vol. 113, no. 2, pp. 593–599.

Clark M. A., Hirst B. H. Expression of junction-associated proteins differentiates mouse intestinal M cells from enterocytes. Histochem. Cell Biol., 2002, vol. 118, pp. 137–147.

Tamagawa H., Takahashi I., Furuse M. et al. Characteristics of claudin expression in follicleassociated epithelium of Peyer’s patches: preferential localization of claudin-4 at the apex of the dome region. Lab. Invest., 2003, vol. 83, no. 7, pp. 1045–1053.

Florian P., Amasheh S., Lessidrensky M. et al. Claudins in the tight junctions of stria vascularis marginal cells. Biochem. Biophys. Res. Commun., 2003, vol. 304, no. 1, pp. 5–10.

Markov A. G., Falchuk E. L., Kruglova N. M. et al. Comparative analysis of theophylline and cholera toxin in rat colon reveals an induction of sealing tight junction proteins. Pflugers Arch., 2014, vol. 466, no. 11, pp. 2059–2065.

Mason C. M., Jepson M. A., Simmons N. L. et al. Heterogenous Na⁺, K(⁺)-ATPase expression in the epithelia of rabbit gut-associated lymphoid tissues. Pflugers Arch., 1994, vol. 427, no. 3–4, pp. 343–347.

Yoshikawa T., Inoue R., Matsumoto M. et al. Comparative expression of hexose transporters, N SGLT1, GLUT1, GLUT2 and GLUT5) throughout the mouse gastrointestinal tract. Histochem. Cell Biol., 2011, vol. 135, no. 2, pp. 183–194.

Renes I. B., Verburg M., Bulsing N. P. et al. Protection of the Peyer’s patch-associated crypt and villus epithelium against methotrexate-induced damage is based on its distinct regulation of proliferation. J. Pathol., 2002, vol. 198, no. 1, pp. 60–68.

Freeman T. C., Bentsen B. S., Thwaites D. T. et al. H⁺/di-tripeptide transporter (PepT1) expression in the rabbit intestine. Pflugers Arch., 1995, vol. 430, no. 3, pp. 394–400.

Amasheh S., Schmidt T., MahN M. et al. Contribution of claudin-5 to barrier properties in tight junctions of epithelial cells. Cell Tissue Res., 2005, vol. 321, no. 1, pp. 89–96.

Hou J., Gomes A. S., Paul D. L. et al. Study of claudin function by RNA interference. J. Biol. Chem., 2006, vol. 281, no 47, pp. 36117–36123.

Yu A. S., Enck A. H., Lencer W. I. et al. Claudin-8 expression in Madin—Darby canine kidney cells augments the paracellular barrier to cation permeatio. J. Biol. Chem., 2003, vol. 278, no 19, pp. 17350–17359.

Angelow S., Kim K. J., Yu A. S. Claudin-8 modulates paracellular permeability to acidic and basic ions in MDCK II cells. J. Physiol., 2006, vol. 571, pp. 15–26.

Ulluwishewa D., AndersoN R. C., McNabb W. C. et al. Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr., 2011, vol. 141, no. 5, pp. 769–776.

Hering N. A., Andres S., Fromm A. et al. Transforming growth factor-β, a whey protein component, strengthens the intestinal barrier by upregulating claudin-4 in HT-29/B6 cells. J. Nutr., 2011, vol. 141, no. 5, pp. 783–789.

Raimondi F., Santoro P., Barone M. V. et al. Bile acids modulate tight junction structure and barrier function of Caco-2 monolayers via EGFR activation. Am. J. Physiol. Gastrointest. Liver Physiol., 2008, vol. 294, no. 4, pp. 906–913.

McKay D. M., Baird A. W. Cytokine regulation of epithelial permeability and ion transport. Gut., 1999, vol. 44, no. 2, pp. 283–289.