ClC-2 regulates mucosal barrier function associated with structural changes to the villus and epithelial tight junction

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 299, Issue 2, 2010, Pages

  Nighot, Prashant K ^a   Blikslager, Anthony T ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Chloride channel; Mannitol flux; Myosin light chain kinase

Indexed keywords

CHLORIDE CHANNEL; CHLORIDE CHANNEL CIC 2; MANNITOL; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; CHLORIDE TRANSPORT; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENZYME INHIBITION; EX VIVO STUDY; ILEUM MUCOSA; IN VIVO STUDY; INTERCELLULAR SPACE; INTESTINE; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTESTINE VILLUS; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PRESSURE CHAMBER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SCANNING ELECTRON MICROSCOPY; SEROSA; TESTIS; TIGHT JUNCTION; TRANSEPITHELIAL ELECTRICAL RESISTANCE; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE;

ANIMALS; CHLORIDE CHANNELS; CHLORIDES; ELECTROPHYSIOLOGICAL PHENOMENA; ILEUM; INTESTINAL MUCOSA; MANNITOL; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, SCANNING; MICROVILLI; MYOSIN-LIGHT-CHAIN KINASE; PERMEABILITY; PHENOTYPE; TIGHT JUNCTIONS; ZINC COMPOUNDS;

EID: 77955593094     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00520.2009     Document Type: Article

References (36)

1. Ahmed N, Ramjeesingh M, Wong S, Varga A, Garami E, Bear CE. Chloride channel activity of ClC-2 is modified by the actin cytoskeleton. Biochem J 352: 789-794, 2000.
2. Bao HF, Liu L, Self J, Duke BJ, Ueno R, Eaton DC. A synthetic prostone activates apical chloride channels in A6 epithelial cells. Am J Physiol Gastrointest Liver Physiol 295: G234-G251, 2008.
3. Barrett KE. New ways of thinking about (and teaching about) intestinal epithelial function. Adv Physiol Educ 32: 25-34, 2008.
4. Bijlsma PB, Kiliaan AJ, Scholten G, Heyman M, Groot JA, Taminiau JA. Carbachol, but not forskolin, increases mucosal-to-serosal transport of intact protein in rat ileum in vitro. Am J Physiol Gastrointest Liver Physiol 271: G147-G155, 1996. (Pubitemid 26299737)
5. Blanz J, Schweizer M, Auberson M, Maier H, Muenscher A, Hubner CA, Jentsch TJ. Leukoencephalopathy upon disruption of the chloride channel ClC-2. J Neurosci 27: 6581-6589, 2007.
6. - channel disruption. EMBO J 20: 1289-1299, 2001.
7. Cameron HL, Perdue MH. Muscarinic acetylcholine receptor activation increases transcellular transport of macromolecules across mouse and human intestinal epithelium in vitro. Neurogastroenterol Motil 19: 47-56, 2007.
8. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 115: 2702-2715, 2005.
9. Cuppoletti J, Malinowska DH, Tewari KP, Li QJ, Sherry AM, Patchen ML, Ueno R. SPI-0211 activates T84 cell chloride transport and recombinant human ClC-2 chloride currents. Am J Physiol Cell Physiol 287: C1173-C1183, 2004.
10. Dykstra MJ. A Manual of Applied Techniques for Biological Electron Microscopy. New York: Plenum, 1993.
11. Grunder S, Thiemann A, Pusch M, Jentsch TJ. Regions involved in the opening of CIC-2 chloride channel by voltage and cell volume. Nature 360: 759-762, 1992.
12. Gyomorey K, Yeger H, Ackerley C, Garami E, Bear CE. Expression of the chloride channel ClC-2 in the murine small intestine epithelium. Am J Physiol Cell Physiol 279: C1787-C1794, 2000.
13. - secretion in intestinal epithelia. Am J Physiol Cell Physiol 277: C441-C447, 1999.
14. Jordt SE, Jentsch TJ. Molecular dissection of gating in the ClC-2 chloride channel. EMBO J 16: 1582-1592, 1997.
15. Kirk KL. Chloride channels and tight junctions. Focus on "Expression of the chloride channel ClC-2 in the murine small intestine epithelium". Am J Physiol Cell Physiol 279: C1675-C1676, 2000.
16. Little D, Dean RA, Young KM, McKane SA, Martin LD, Jones SL, Blikslager AT. PI3K signaling is required for prostaglandin-induced mucosal recovery in ischemia-injured porcine ileum. Am J Physiol Gastrointest Liver Physiol 284: G46-G56, 2003.
17. Madara JL, Stafford J, Barenberg D, Carlson S. Functional coupling of tight junctions and microfilaments in T84 monolayers. Am J Physiol Gastrointest Liver Physiol 254: G416-G423, 1988.
18. - secretion and Na-K-2Cl cotransport. Am J Physiol Cell Physiol 272: C254-C262, 1997.
19. Moeser AJ, Haskell MM, Shifflett DE, Little D, Schultz BD, Blikslager AT. ClC-2 chloride secretion mediates prostaglandin-induced recovery of barrier function in ischemia-injured porcine ileum. Gastroenterology 127: 802-815, 2004.
20. Moeser AJ, Nighot PK, Engelke KJ, Ueno R, Blikslager AT. Recovery of mucosal barrier function in ischemic porcine ileum and colon is stimulated by a novel agonist of the ClC-2 chloride channel, lubiprostone. Am J Physiol Gastrointest Liver Physiol 292: G647-G656, 2007.
21. +/H+ exchanger isoform 2 stimulates recovery of barrier function in ischemia-injured intestine. Am J Physiol Gastrointest Liver Physiol 291: G885-G894, 2006.
22. Mohammad-Panah R, Gyomorey K, Rommens J, Choudhury M, Li C, Wang Y, Bear CE. ClC-2 contributes to native chloride secretion by a human intestinal cell line, Caco-2. J Biol Chem 276: 8306-8313, 2001.
23. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25: 747-806, 2004.
24. - current in salivary acinar cells from Clcn2 knockout mice. J Biol Chem 277: 23604-23611, 2002.
25. Niemeyer MI, Yusef YR, Cornejo I, Flores CA, Sepulveda FV, Cid LP. Functional evaluation of human ClC-2 chloride channel mutations associated with idiopathic generalized epilepsies. Physiol Genomics 19: 74-83, 2004.
26. Nighot PK, Moeser AJ, Ryan KA, Ghashghaei T, Blikslager AT. ClC-2 is required for rapid restoration of epithelial tight junctions in ischemic-injured murine jejunum. Exp Cell Res 315: 110-118, 2009.
27. Rajasekaran SA, Beyenbach KW, Rajasekaran AK. Interactions of tight junctions with membrane channels and transporters. Biochim Biophys Acta 1778: 757-769, 2008.
28. Rajasekaran SA, Hu J, Gopal J, Gallemore R, Ryazantsev S, Bok D, Rajasekaran AK. Na,K-ATPase inhibition alters tight junction structure and permeability in human retinal pigment epithelial cells. Am J Physiol Cell Physiol 284: C1497-C1507, 2003.
29. - channels in rabbit gastric mucosa. Am J Physiol Cell Physiol 280: C1599-C1606, 2001.
30. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22: 207-235, 2006.
31. Thiemann A, Grunder S, Pusch M, Jentsch TJ. A chloride channel widely expressed in epithelial and non-epithelial cells. Nature 356: 57-60, 1992.
32. Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169: 1901-1909, 2006.
33. Turner JR, Angle JM, Black ED, Joyal JL, Sacks DB, Madara JL. PKC-dependent regulation of transepithelial resistance: roles of MLC and MLC kinase. Am J Physiol Cell Physiol 277: C554-C562, 1999.
34. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol Cell Physiol 273: C1378-C1385, 1997.
35. Yoo J, Nichols A, Mammen J, Calvo I, Song JC, Worrell RT, Matlin K, Matthews JB. Bryostatin-1 enhances barrier function in T84 epithelia through PKC-dependent regulation of tight junction proteins. Am J Physiol Cell Physiol 285: C300-C309, 2003.
36. Zolotarevsky Y, Hecht G, Koutsouris A, Gonzalez DE, Quan C, Tom J, Mrsny RJ, Turner JR. A membrane-permeant peptide that inhibits MLC kinase restores barrier function in in vitro models of intestinal disease. Gastroenterology 123: 163-172, 2002.