Claudin-4 forms a paracellular barrier, revealing the interdependence of claudin expression in the loose epithelial cell culture model opossum kidney cells

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 12, 2012, Pages

  Borovac, Jelena ^a   Barker, Reid S ^a   Rievaj, Juraj ^a   Rasmussen, Andrew ^a   Pan, Wanling ^a   Wevrick, Rachel ^a   Alexander, R Todd ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Claudin 2; Claudin 4; Opossum kidney cells; Paracellular transport

Indexed keywords

CHLORIDE; CLAUDIN 1; CLAUDIN 11; CLAUDIN 12; CLAUDIN 15; CLAUDIN 20; CLAUDIN 4; CLAUDIN 6; CLAUDIN 9; MEMBRANE PROTEIN; MESSENGER RNA; SODIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CELL TRANSPORT; EPITHELIUM CELL; KIDNEY CELL; NONHUMAN; OPOSSUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TIGHT JUNCTION;

ANIMALS; CATIONS, MONOVALENT; CELLS, CULTURED; CLAUDIN-4; CLAUDINS; DOGS; EPITHELIAL CELLS; GENE SILENCING; KIDNEY; OPOSSUMS; PERMEABILITY; TIGHT JUNCTIONS;

DIDELPHIDAE;

EID: 84871298212     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00434.2011     Document Type: Article

References (43)

1. Abuazza G, Becker A, Williams SS, Chakravarty S, Truong HT, Lin F, Baum M. Claudins 6, 9, and 13 are developmentally expressed renal tight junction proteins. Am J Physiol Renal Physiol 291: F1132-F1141, 2006.
2. + exchanger 3 is in large complexes in the center of the apical surface of proximal tubule-derived OK cells. Am J Physiol Cell Physiol 283: C927-C940, 2002.
3. Amasheh S, Fromm M, Gunzel D. Claudins of intestine and nephron-a correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf) 201: 133-140, 2011.
4. Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, Schulzke JD, Fromm M. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115: 4969-4976, 2002.
5. Amemiya M, Loffing J, Lotscher M, Kaissling B, Alpern RJ, Moe OW. Expression of NHE-3 in the apical membrane of rat renal proximal tubule and thick ascending limb. Kidney Int 48: 1206-1215, 1995.
6. Amemiya M, Yamaji Y, Cano A, Moe OW, Alpern RJ. Acid incubation increases NHE-3 mRNA abundance in OKP cells. Am J Physiol Cell Physiol 269: C126-C133, 1995.
7. Angelow S, Schneeberger EE, Yu AS. Claudin-8 expression in renal epithelial cells augments the paracellular barrier by replacing endogenous claudin-2. J Membr Biol 215: 147-159, 2007.
8. Bello-Reuss E. Cell membranes and paracellular resistances in isolated renal proximal tubules from rabbit and Ambystoma. J Physiol 370: 25-38, 1986.
9. Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM. Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol 283: C142-C147, 2002.
10. Eisenman G, Horn R. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J Membr Biol 76: 197-225, 1983.
11. Enck AH, Berger UV, Yu ASL. Claudin-2 is selectively expressed in proximal nephron in mouse kidney. Am J Physiol Renal Physiol 281: F966-F974, 2001.
12. 2+ absorption between enterocytes. Mol Biol Cell 19: 1912-1921, 2008.
13. Furuse M, Furuse K, Sasaki H, Tsukita S. Conversion of Zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 153: 263-272, 2001.
14. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156: 1099-1111, 2002.
15. Garcia NH, Ramsey CR, Knox FG. Understanding the role of paracellular transport in the proximal tubule. News Physiol Sci 13: 38-43, 1998.
16. Gunzel D, Stuiver M, Kausalya PJ, Haisch L, Krug SM, Rosenthal R, Meij IC, Hunziker W, Fromm M, Muller D. Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function. J Cell Sci 122: 1507-1517, 2009.
17. Hansson GC, Simons K, van Meer G. Two strains of the Madin-Darby canine kidney (MDCK) cell line have distinct glycosphingolipid compositions. EMBO J 5: 483-489, 1986.
18. Hou J, Gomes AS, Paul DL, Goodenough DA. Study of claudin function by RNA interference. J Biol Chem 281: 36117-36123, 2006.
19. Hou J, Paul DL, Goodenough DA. Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 118: 5109-5118, 2005.
20. Hou J, Renigunta A, Konrad M, Gomes AS, Schneeberger EE, Paul DL, Waldegger S, Goodenough DA. Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest 118: 619-628, 2008.
21. Hou J, Renigunta A, Yang J, Waldegger S. Claudin-4 forms paracellular chloride channel in the kidney and requires claudin-8 for tight junction localization. Proc Natl Acad Sci USA 107: 18010-18015, 2010.
22. Inai T, Kobayashi J, Shibata Y. Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur J Cell Biol 78: 849-855, 1999.
23. + exchanger via modulating membrane surface potential. Channels (Austin) 5: 308-313, 2011.
24. Kimizuka H, Koketsu K. Ion transport through cell membrane. J Theor Biol 6: 290-305, 1964.
25. Kirk A, Campbell S, Bass P, Mason J, Collins J. Differential expression of claudin tight junction proteins in the human cortical nephron. Nephrol Dial Transplant 25: 2107-2119, 2010.
26. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13: 875-886, 2002.
27. Koyama H, Goodpasture C, Miller MM, Teplitz RL, Riggs AD. Establishment and characterization of a cell line from the American opossum (Didelphys virginiana). In Vitro 14: 239-246, 1978.
28. Kozak M. An analysis of 5=-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15: 8125-8148, 1987.
29. Liang M, Ramsey CR, Knox FG. The paracellular permeability of opossum kidney cells, a proximal tubule cell line. Kidney Int 56: 2304-2308, 1999.
30. McCarthy KM, Francis SA, McCormack JM, Lai J, Rogers RA, Skare IB, Lynch RD, Schneeberger EE. Inducible expression of claudin-1-myc but not occludin-VSV-G results in aberrant tight junction strand formation in MDCK cells. J Cell Sci 113: 3387-3398, 2000.
31. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, Jurka J, Kamal M, Mauceli E, Searle SM, Sharpe T, Baker ML, Batzer MA, Benos PV, Belov K, Clamp M, Cook A, Cuff J, Das R, Davidow L, Deakin JE, Fazzari MJ, Glass JL, Grabherr M, Greally JM, Gu W, Hore TA, Huttley GA, Kleber M, Jirtle RL, Koina E, Lee JT, Mahony S, Marra MA, Miller RD, Nicholls RD, Oda M, Papenfuss AT, Parra ZE, Pollock DD, Ray DA, Schein JE, Speed TP, Thompson K, VandeBerg JL, Wade CM, Walker JA, Waters PD, Webber C, Weidman JR, Xie X, Zody MC, Graves JA, Ponting CP, Breen M, Samollow PB, Lander ES, Lindblad-Toh K. Genome of the marsupial Monodelphis domestica reveals innovation in noncoding sequences. Nature 447: 167-177, 2007.
32. Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, Saito K, Tamura A, Igarashi M, Endo T, Takeuchi K, Tsukita S. Predicted expansion of the claudin multigene family. FEBS Lett 585: 606-612, 2011.
33. Mitic LL, Van Itallie CM, Anderson JM. Molecular physiology and pathophysiology of tight junctions. I. Tight junction structure and function: lessons from mutant animals and proteins. Am J Physiol Gastrointest Liver Physiol 279: G250-G254, 2000.
34. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA 107: 8011-8016, 2010.
35. Prozialeck WC, Edwards JR, Lamar PC, Smith CS. Epithelial barrier characteristics and expression of cell adhesion molecules in proximal tubule-derived cell lines commonly used for in vitro toxicity studies. Toxicol In Vitro 20: 942-953, 2006.
36. Reyes JL, Lamas M, Martin D, del Carmen Namorado M, Islas S, Luna J, Tauc M, Gonzalez-Mariscal L. The renal segmental distribution of claudins changes with development. Kidney Int 62: 476-487, 2002.
37. Sas D, Hu M, Moe OW, Baum M. Effect of claudins 6 and 9 on paracellular permeability in MDCK II cells. Am J Physiol Regul Integr Comp Physiol 295: R1713-R1719, 2008.
38. Seely JF. Variation in electrical resistance along length of rat proximal convoluted tubule. Am J Physiol 225: 48-57, 1973.
39. + deficiency and glucose malabsorption in mouse small intestine. Gastroenterology 140: 913-923, 2011.
40. Van Itallie C, Rahner C, Anderson JM. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest 107: 1319-1327, 2001.
41. Van Itallie CM, Fanning AS, Anderson JM. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol 285: F1078-F1084, 2003.
42. Wills NK, Lewis SA, Eaton DC. Active and passive properties of rabbit descending colon: a microelectrode and nystatin study. J Membr Biol 45: 81-108, 1979.
43. Yu AS, Enck AH, Lencer WI, Schneeberger EE. Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278: 17350-17359, 2003.