Chloride channel CLC-2 modulates tight junction barrier function via intracellular trafficking of occludin

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 1, 2012, Pages

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

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Caco 2; Epithelium; Intestine; Permeability

Indexed keywords

CAVEOLIN 1; CHLORIDE CHANNEL; CHLORIDE CHANNEL CIC 2; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; HEAT SHOCK PROTEIN 90; METHYL BETA CYCLODEXTRIN; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CAVEOLA; CELL MIGRATION; CELL STRAIN CACO 2; CYTOPLASM; ENDOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEMBRANE DAMAGE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEOMICS; TIGHT JUNCTION;

CACO-2 CELLS; CAVEOLAE; CELL COMMUNICATION; CHLORIDE CHANNELS; HUMANS; INTRACELLULAR FLUID; MEMBRANE PROTEINS; PROTEIN TRANSPORT; TIGHT JUNCTIONS;

EID: 83655181098     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00072.2011     Document Type: Article

References (45)

1. Balda MS, Whitney JA, Flores C, Gonzalez S, Cereijido M, Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 134: 1031-1049, 1996.
2. Bosl MR, Stein V, Hubner C, Zdebik AA, Jordt SE, Mukhopadhyay AK, Davidoff MS, Holstein AF, Jentsch TJ. Male germ cells and photoreceptors, both dependent on close cell-cell interactions, degenerate upon ClC-2 Cl(-) channel disruption. EMBO J 20: 1289-1299, 2001.
3. Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 19: 923-933, 2005.
4. Chen X, Wang Z. Regulation of epidermal growth factor receptor endocytosis by wortmannin through activation of Rab5 rather than inhibition of phosphatidylinositol 3-kinase. EMBO Rep 2: 842-849, 2001.
5. Coyne CB, Shen L, Turner JR, Bergelson JM. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2: 181-192, 2007.
6. Dhani SU, Kim Chiaw P, Huan LJ, Bear CE. ATP depletion inhibits the endocytosis of ClC-2. J Cell Physiol 214: 273-280, 2008.
7. 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.
8. Hagiwara M, Shirai Y, Nomura R, Sasaki M, Kobayashi K, Tadokoro T, Yamamoto Y. Caveolin-1 activates Rab5 and enhances endocytosis through direct interaction. Biochem Biophys Res Commun 378: 73-78, 2009.
9. Hopkins AM, Walsh SV, Verkade P, Boquet P, Nusrat A. Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J Cell Sci 116: 725-742, 2003.
10. Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 15: 176-188, 2004.
11. 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.
12. Li Q, Zhang Q, Zhang M, Wang C, Zhu Z, Li N, Li J. Effect of n-3 polyunsaturated fatty acids on membrane microdomain localization of tight junction proteins in experimental colitis. FEBS J 275: 411-420, 2008.
13. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR, 2nd Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126, 2010.
14. McCarter SD, Johnson DL, Kitt KN, Donohue C, Adams A, Wilson JM. Regulation of tight junction assembly and epithelial polarity by a resident protein of apical endosomes. Traffic 11: 856-866, 2010.
15. McCarthy KM, Skare IB, Stankewich MC, Furuse M, Tsukita S, Rogers RA, Lynch RD, Schneeberger EE. Occludin is a functional component of the tight junction. J Cell Sci 109: 2287-2298, 1996.
16. Mitic LL, Anderson JM. Molecular architecture of tight junctions. Annu Rev Physiol 60: 121-142, 1998.
17. 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.
18. 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.
19. + exchanger 2 have impaired recovery of intestinal barrier function. Am J Physiol Gastrointest Liver Physiol 295: G791-G797, 2008.
20. 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.
21. Morimoto S, Nishimura N, Terai T, Manabe S, Yamamoto Y, Shinahara W, Miyake H, Tashiro S, Shimada M, Sasaki T. Rab13 mediates the continuous endocytic recycling of occludin to the cell surface. J Biol Chem 280: 2220-2228, 2005.
22. Mruk DD, Lau AS, Conway AM. Crosstalk between Rab GTPases and cell junctions. Contraception 72: 280-290, 2005.
23. 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.
24. Nighot PK, Blikslager AT. ClC-2 regulates mucosal barrier function associated with structural changes to the villus and epithelial tight junction. Am J Physiol Gastrointest Liver Physiol 299: G449-G556, 2010.
25. 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.
26. Pelkmans L, Burli T, Zerial M, Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118: 767-780, 2004.
27. Powell DW, Adegboyega PA, Di Mari JF, Mifflin RC. Epithelial cells and their neighbors I. Role of intestinal myofibroblasts in development, repair, and cancer. Am J Physiol Gastrointest Liver Physiol 289: G2-G7, 2005.
28. Rajasekaran SA, Beyenbach KW, Rajasekaran AK. Interactions of tight junctions with membrane channels and transporters. Biochim Biophys Acta 1778: 757-769, 2008.
29. Seltana A, Basora N, Beaulieu JF. Intestinal epithelial wound healing assay in an epithelial-mesenchymal co-culture system. Wound Repair Regen 18: 114-122, 2010.
30. Shen L, Turner JR. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16: 3919-3936, 2005.
31. Shen L, Weber CR, Turner JR. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J Cell Biol 181: 683-695, 2008.
32. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860, 2006.
33. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22: 207-235, 2006.
34. Takeuchi K, Tanigami M, Amagase K, Ochi A, Okuda S, Hatazawa R. Endogenous prostaglandin E2 accelerates healing of indomethacin-induced small intestinal lesions through upregulation of vascular endothelial growth factor expression by activation of EP4 receptors. J Gastroenterol Hepatol 25, Suppl 1: S67-74, 2010.
35. Terry SJ, Zihni C, Elbediwy A, Vitiello E, Leefa Chong San I.V., Balda MS, Matter K. Spatially restricted activation of RhoA signalling at epithelial junctions by p114RhoGEF drives junction formation and morphogenesis. Nat Cell Biol 13: 159-166, 2011.
36. Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 169: 1901-1909, 2006.
37. + exchanger NHE3. Am J Physiol Cell Physiol 279: C1918-C1924, 2000.
38. Utech M, Mennigen R, Bruewer M. Endocytosis and recycling of tight junction proteins in inflammation. J Biomed Biotechnol 2010: 484987, 2010.
39. Van Itallie CM, Fanning AS, Holmes J, Anderson JM. Occludin is required for cytokine-induced regulation of tight junction barriers. J Cell Sci 123: 2844-2852, 2010.
40. Van Landeghem L, Chevalier J, Mahe MM, Wedel T, Urvil P, Derkinderen P, Savidge T, Neunlist M. Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am J Physiol Gastrointest Liver Physiol 300: G976-G987, 2011.
41. Wang L, Srinivasan S, Theiss AL, Merlin D, Sitaraman SV. Interleukin-6 induces keratin expression in intestinal epithelial cells: potential role of keratin-8 in interleukin-6-induced barrier function alterations. J Biol Chem 282: 8219-8227, 2007.
42. Wong V, Gumbiner BM. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136: 399-409, 1997.
43. Xia W, Wong EW, Mruk DD, Cheng CY. TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrinmediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol 327: 48-61, 2009.
44. Yu AS, McCarthy KM, Francis SA, McCormack JM, Lai J, Rogers RA, Lynch RD, Schneeberger EE. Knockdown of occludin expression leads to diverse phenotypic alterations in epithelial cells. Am J Physiol Cell Physiol 288: C1231-C1241, 2005.
45. Yu D, Turner JR. Stimulus-induced reorganization of tight junction structure: the role of membrane traffic. Biochim Biophys Acta 1778: 709-716, 2008.