Claudins of intestine and nephron - a correlation of molecular tight junction structure and barrier function

Acta Physiologica

Volumn 201, Issue 1, 2011, Pages 133-140

  Amasheh, S ^a   Fromm, M ^a   Gunzel D ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Barrier; Claudins; Intestine; Tight junctions

Indexed keywords

CLAUDIN; CLAUDIN 1; CLAUDIN 11; CLAUDIN 14; CLAUDIN 19; CLAUDIN 3; CLAUDIN 4; CLAUDIN 5; CLAUDIN 8; UNCLASSIFIED DRUG;

CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STRUCTURE; HUMAN; INTESTINE; INTESTINE EPITHELIUM; KIDNEY TUBULE EPITHELIUM; NEPHRON; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

CLAUDINS; EPITHELIUM; INFLAMMATORY BOWEL DISEASES; INTESTINES; MULTIGENE FAMILY; NEPHRONS; PERMEABILITY; PROTEIN ISOFORMS; TIGHT JUNCTIONS; TISSUE DISTRIBUTION;

EID: 78650062278     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2010.02148.x     Document Type: Review

References (72)

1. Acharya, P., Beckel, J., Ruiz, W.G., Wang, E., Rojas, R., Birder, L. & Apodaca, G. 2004. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol 287, F305-F318.
2. Agarwal, R., Mori, Y., Cheng, Y., Jin, Z., Olaru, A.V., Hamilton, J.P., David, S., Selaru, F.M., Yang, J., Abraham, J.M., Montgomery, E., Morin, P.J. & Meltzer, S.J. 2009. Silencing of claudin-11 is associated with increased invasiveness of gastric cancer cells. PLoS ONE 4, e8002.
3. + conductance in LLC-PK1 cells. J Cell Sci 118, 2683-2693.
4. - permeability. Biochem Biophys Res Commun 357, 87-91.
5. Amasheh, S., Meiri, N., Gitter, A.H., Schöneberg, T., Mankertz, J., Schulzke, J.D. & Fromm, M. 2002. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115, 4969-4976.
6. Amasheh, S., Schmidt, T., Mahn, M., Florian, P., Mankertz, J., Tavalali, S., Gitter, A.H., Schulzke, J.D. & Fromm, M. 2005. Expression of claudin-5 contributes to barrier properties in tight junctions of epithelial cells. Cell Tissue Res 321, 89-96.
7. Amasheh, S., Dullat, S., Fromm, M., Schulzke, J.D., Buhr, H.J. & Kroesen, A.J. 2009a. Inflamed pouch mucosa possesses altered tight junctions indicating recurrence of inflammatory bowel disease. Int J Colorectal Dis 24, 1149-1156.
8. + absorption defends from paracellular back-leakage by claudin-8 upregulation. Biochem Biophys Res Commun 378, 45-50.
9. Angelow, S., Kim, K.J. & Yu, A.S. 2006. Claudin-8 modulates paracellular permeability to acidic and basic ions in MDCK II cells. J Physiol 571, 15-26.
10. Angelow, S., El-Husseini, R., Kanzawa, S.A. & Yu, A.S. 2007. Renal localization and function of the tight junction protein, claudin-19. Am J Physiol Renal Physiol 293, F166-F177.
11. Ben-Yosef, T., Belyantseva, I.A., Saunders, T.L., Hughes, E.D., Kawamoto, K., Van Itallie, C.M., Beyer, L.A., Halsey, K., Gardner, D.J., Wilcox, E.R. et al. 2003. Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum Mol Genet 12, 2049-2061.
12. Bürgel, N., Bojarski, C., Mankertz, J., Zeitz, M., Fromm, M. & Schulzke, J.D. 2002. Mechanisms of diarrhea in collagenous colitis. Gastroenterology 123, 433-443.
13. Cole, D.E. & Quamme, G.A. 2000. Inherited disorders of renal magnesium handling. J Am Soc Nephrol 11, 1937-1947.
14. Elkouby-Naor, L., Abassi, Z., Lagziel, A., Gow, A. & Ben-Yosef, T. 2008. Double gene deletion reveals lack of cooperation between claudin 11 and claudin 14 tight junction proteins. Cell Tissue Res 333, 427-438.
15. Fujita, K., Katahira, J., Horiguchi, Y., Sonoda, N., Furuse, M. & Tsukita, S. 2000. Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett 476, 258-261.
16. Fujita, H., Chiba, H., Yokozaki, H., Sakai, N., Sugimoto, K., Wada, T., Kojima, T., Yamashita, T. & Sawada, N. 2006. Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J Histochem Cytochem 54, 933-944.
17. 2+ absorption between enterocytes. Mol Biol Cell 19, 1912-1921.
18. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., Tsukita, S. & Tsukita, S. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123, 1777-1788.
19. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K. & Tsukita, S. 1998. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141, 1539-1550.
20. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A. & Tsukita, S. 2002. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156, 1099-1111.
21. Gitter, A.H., Schulzke, J.D., Sorgenfrei, D. & Fromm, M. 1997. Ussing chamber for high-frequency transmural impedance analysis of epithelial tissues. J Biochem Biophys Methods 35, 81-88.
22. Gitter, A.H., Schulzke, J.D. & Fromm, M. 1998. Impedance analysis for determination of epithelial and subepithelial resistance in intestinal tissues. J Biochem Biophys Methods 37, 35-46.
23. Gonzalez-Mariscal, L., Namorado Mdel, C., Martin, D., Sierra, G. & Reyes, J.L. 2006. The tight junction proteins claudin-7 and -8 display a different subcellular localization at Henle's loops and collecting ducts of rabbit kidney. Nephrol Dial Transplant 21, 2391-2398.
24. Gow, A., Southwood, C.M., Li, J.S., Pariali, M., Riordan, G.P., Brodie, S.E., Danias, J., Bronstein, J.M., Kachar, B. & Lazzarini, R.A. 1999. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99, 649-659.
25. Gow, A., Davies, C., Southwood, C.M., Frolenkov, G., Chrustowski, M., Ng, L., Yamauchi, D., Marcus, D.C. & Kachar, B. 2004. Deafness in Claudin 11-null mice reveals the critical contribution of basal cell tight junctions to stria vascularis function. J Neurosci 24, 7051-7062.
26. Gröne, J., Weber, B., Staub, E., Heinze, M., Klaman, I., Pilarsky, C., Hermann, K., Castanos-Velez, E., Röpcke, S., Mann, B., Rosenthal, A. & Buhr, H.J. 2007. Differential expression of genes encoding tight junction proteins in colorectal cancer: frequent dysregulation of claudin-1, -8 and -12. Int J Colorectal Dis 22, 651-659.
27. Günzel, D. & Yu, A.S. 2009. Function and regulation of claudins in the thick ascending limb of Henle. Pflugers Arch 458, 77-88.
28. Günzel, D., Stuiver, M., Kausalya, P.J., Haisch, L., Krug, S.M., Rosenthal, R., Meij, I.C., Hunziker, W., Fromm, M. & Müller, D. 2009a. Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function. J Cell Sci 122, 1507-1517.
29. Günzel, D., Haisch, L., Pfaffenbach, S., Krug, S.M., Milatz, S., Amasheh, S., Hunziker, W. & Müller, D. 2009b. Claudin function in the thick ascending limb of Henle's loop. Ann N Y Acad Sci 1165, 152-162.
30. - secretion in MDCK cells. J Physiol 587, 3777-3793.
31. Heller, F., Florian, P., Bojarski, C., Richter, J., Christ, M., Hillenbrand, B., Mankertz, J., Gitter, A.H., Bürgel, N., Fromm, M., Zeitz, M., Fuss, I., Strober, W. & Schulzke, J.D. 2005. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550-564.
32. Holmes, J.L., Van Itallie, C.M., Rasmussen, J.E. & Anderson, J.M. 2006. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr Patterns 6, 581-588.
33. Hou, J., Paul, D.L. & Goodenough, D.A. 2005. Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 118, 5109-5118.
34. Hou, J., Renigunta, A., Konrad, M., Gomes, A.S., Schneeberger, E.E., Paul, D.L., Waldegger, S. & Goodenough, D.A. 2008. Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest 118, 619-628.
35. Hou, J., Renigunta, A., Gomes, A.S., Hou, M., Paul, D.L., Waldegger, S. & Goodenough, D.A. 2009. Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci USA 106, 15350-15355.
36. Ikari, A., Hirai, N., Shiroma, M., Harada, H., Sakai, H., Hayashi, H., Suzuki, Y., Degawa, M. & Takagi, K. 2004. Association of paracellin-1 with ZO-1 augments the reabsorption of divalent cations in renal epithelial cells. J Biol Chem 279, 54826-54832.
37. Ikari, A., Matsumoto, S., Harada, H., Takagi, K., Hayashi, H., Suzuki, Y., Degawa, M. & Miwa, M. 2006. Phosphorylation of paracellin-1 at Ser217 by protein kinase A is essential for localization in tight junctions. J Cell Sci 119, 1781-1789.
38. Ikari, A., Matsumoto, S., Harada, H., Takagi, K., Degawa, M., Takahashi, T., Sugatani, J. & Miwa, M. 2008. Dysfunction of paracellin-1 by dephosphorylation in Dahl salt-sensitive hypertensive rats. J Physiol Sci 56, 379-383.
39. Ikenouchi, J., Furuse, M., Furuse, K., Sasaki, H., Tsukita, S. & Tsukita, S. 2005. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171, 939-945.
40. 2+ transport function of Claudin-16. J Clin Invest 116, 878-891.
41. Kiuchi-Saishin, Y., Gotoh, S., Furuse, M., Takasuga, A., Tano, Y. & Tsukita, S. 2002. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13, 875-886.
42. Konrad, M., Schaller, A., Seelow, D., Pandey, A.V., Waldegger, S., Lesslauer, A., Vitzthum, H., Suzuki, Y., Luk, J.M., Becker, C. et al. 2006. Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet 79, 949-957.
43. Krug, S.M., Amasheh, S., Richter, J.F., Milatz, S., Günzel, D., Westphal, J.K., Huber, O., Schulzke, J.D. & Fromm, M. 2009. Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol Biol Cell 20, 3713-3724.
44. Li, W.Y., Huey, C.L. & Yu, A.S. 2004. Expression of claudin-7 and -8 along the mouse nephron. Am J Physiol Renal Physiol 286, F1063-F1071.
45. Mandel, L.J., Bacallao, R. & Zampighi, G. 1993. Uncoupling of the molecular 'fence' and paracellular 'gate' functions in epithelial tight junctions. Nature 361, 552-555.
46. Markov, A.G., Veshnyakova, A., Fromm, M., Amasheh, M. & Amasheh, S. 2010. Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine. Comp J Physiol Biochem B 80, 591-598.
47. Milatz, S., Krug, S., Rosenthal, R., Günzel, D., Fromm, M. & Amasheh, S. 2010. Functional characterization of the tight junction protein claudin-3. Acta Physiol 198(Suppl. 677), 40.
48. Miwa, N., Furuse, M., Tsukita, S., Niikawa, N., Nakamura, Y. & Furukawa, Y. 2001. Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 12, 469-476.
49. Miyamoto, T., Morita, K., Takemoto, D., Takeuchi, K., Kitano, Y., Miyakawa, T., Nakayama, K., Okamura, Y., Sasaki, H., Miyachi, Y., Furuse, M. & Tsukita, S. 2005. Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol 169, 527-538.
50. Morita, K., Furuse, M., Fujimoto, K. & Tsukita, S. 1999a. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96, 511-516.
51. Morita, K., Sasaki, H., Furuse, M. & Tsukita, S. 1999b. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 147, 185-194.
52. Morita, K., Sasaki, H., Fujimoto, K., Furuse, M. & Tsukita, S. 1999c. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145, 579-588.
53. Nitta, T., Hata, M., Gotoh, S., Seo, Y., Sasaki, H., Hashimoto, N., Furuse, M. & Tsukita, S. 2003. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161, 653-660.
54. Ohta, H., Adachi, H., Takiguchi, M. & Inaba, M. 2006. Restricted localization of claudin-16 at the tight junction in the thick ascending limb of Henle's loop together with claudins 3, 4, and 10 in bovine nephrons. J Vet Med Sci 68, 453-463.
55. Rahner, C., Mitic, L.L. & Anderson, J.M. 2001. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut. Gastroenterology 120, 411-422.
56. Raleigh, D.R., Marchiando, A.M., Zhang, Y., Shen, L., Sasaki, H., Wang, Y., Long, M. & Turner, J.R. 2010. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21, 1200-1213.
57. Reyes, J.L., Lamas, M., Martin, D., Del Carmen Namorado, M., Islas, S., Luna, J., Tauc, M. & González-Mariscal, L. 2002. The renal segmental distribution of claudins changes with development. Kidney Int 62, 476-487.
58. Rosenthal, R., Milatz, S., Krug, S.M., Oelrich, B., Schulzke, J.D., Amasheh, S., Günzel, D. & Fromm, M. 2010. Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci 123, 1913-1921.
59. 2+ resorption. Science 285, 103-106.
60. Sonoda, N., Furuse, M., Sasaki, H., Yonemura, S., Katahira, J., Horiguchi, Y. & Tsukita, S. 1999. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J Cell Biol 147, 195-204.
61. Steed, E., Rodrigues, N.T., Balda, M.S. & Matter, K. 2009. Identification of MarvelD3 as a tight junction-associated transmembrane protein of the occludin family. BMC Cell Biol 10, 95. doi: .
62. Tamura, A., Kitano, Y., Hata, M., Katsuno, T., Moriwaki, K., Sasaki, H., Hayashi, H., Suzuki, Y., Noda, T., Furuse, M., Tsukita, S. & Tsukita, S. 2008. Megaintestine in claudin-15-deficient mice. Gastroenterology 134, 523-534.
63. Tatum, R., Zhang, Y., Salleng, K., Lu, Z., Lin, J.J., Lu, Q., Jeansonne, B.G., Ding, L. & Chen, Y.H. 2010. Renal salt wasting and chronic dehydration in claudin-7-deficient mice. Am J Physiol Renal Physiol 298, F24-F34.
64. Thorleifsson, G., Holm, H., Edvardsson, V., Walters, G.B., Styrkarsdottir, U., Gudbjartsson, D.F., Sulem, P., Halldorsson, B.V., De Vegt, F., D'Ancona, F.C. et al. 2009. Sequence variants in the CLDN14 gene associate with kidney stones and bone mineral density. Nat Genet 41, 926-930.
65. Van Itallie, C.M., Rahner, C. & Anderson, J.M. 2001. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest 107, 1319-1327.
66. Van Itallie, C.M., Fanning, A.S. & Anderson, J.M. 2003. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol 285, F1078-F1084.
67. Van Itallie, C.M., Rogan, S., Yu, A., Vidal, L.S., Holmes, J. & Anderson, J.M. 2006. Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am J Physiol Renal Physiol 291, F1288-F1299.
68. Wen, H., Watry, D.D., Marcondes, M.C. & Fox, H.S. 2004. Selective decrease in paracellular conductance of tight junctions: role of the first extracellular domain of claudin-5. Mol Cell Biol 24, 8408-8417.
69. Weng, X.H., Beyenbach, K.W. & Quaroni, A. 2005. Cultured monolayers of the dog jejunum with the structural and functional properties resembling the normal epithelium. Am J Physiol Gastrointest Liver Physiol 288, G705-G717.
70. Wilcox, E.R., Burton, Q.L., Naz, S., Riazuddin, S., Smith, T.N., Ploplis, B., Belyantseva, I., Ben-Yosef, T., Liburd, N.A., Morell, R.J., Kachar, B., Wu, D.K., Griffith, A.J., Riazuddin, S. & Friedman, T.B. 2001. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell 104, 165-172.
71. Yu, A.S., Enck, A.H., Lencer, W.I. & Schneeberger, E.E. 2003. Claudin-8 expression in MDCK cells augments the paracellular barrier to cation permeation. J Biol Chem 278, 17350-17359.
72. Zeissig, S., Bürgel, N., Günzel, D., Richter, J., Mankertz, J., Wahnschaffe, U., Kroesen, A.J., Zeitz, M., Fromm, M. & Schulzke, J.D. 2007. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 56, 61-72.