Visualizing the dynamic coupling of claudin strands to the actin cytoskeleton through ZO-1

Molecular Biology of the Cell

Volumn 28, Issue 4, 2017, Pages 524-534

  Van Itallie, Christina M ^a   Tietgens, Amber Jean ^a   Anderson, James M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLAUDIN; CLAUDIN 2; GREEN FLUORESCENT PROTEIN; OCCLUDIN; PROTEIN ZO1; CLAUDIN 1; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN; PHOSPHOPROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL CONTACT; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; LIVE CELL IMAGING; NONHUMAN; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; RAT; TIGHT JUNCTION; ANIMAL; CELL LINE; CYTOSKELETON; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR IMAGING; PHYSIOLOGY; PROCEDURES;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELL LINE; CLAUDIN-1; CLAUDINS; CYTOSKELETAL PROTEINS; CYTOSKELETON; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MOLECULAR IMAGING; OCCLUDIN; PHOSPHOPROTEINS; RATS; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 85013321853     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-10-0698     Document Type: Article

References (42)

1. Anderson JM, Van Itallie CM (2009). Physiology and Function of the Tight Junction, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Berglund JJ, Riegler M, Zolotarevsky Y, Wenzl E, Turner JR (2001). Regulation of human jejunal transmucosal resistance and MLC phosphorylation by Na(+)-glucose cotransport. Am J Physiol Gastrointest Liver Physiol 281, G1487-G1493.
3. Boudaoud A, Burian A, Borowska-Wykret D, Uyttewaal M, Wrzalik R, Kwiatkowska D, Hamant O (2014). FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat Protoc 9, 457-463.
4. Chen X, Zaro JL, Shen WC (2013). Fusion protein linkers: property, design and functionality. Adv Drug Deliv Rev 65, 1357-1369.
5. Colegio OR, Van Itallie C, Rahner C, Anderson JM (2003). Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am J Physiol Cell Physiol 284, C1346-C1354.
6. Cording J, Berg J, Kading N, Bellmann C, Tscheik C, Westphal JK, Milatz S, Gunzel D, Wolburg H, Piontek J, et al (2013). In tight junctions, claudins regulate the interactions between occludin, tricellulin and marvelD3, which, inversely, modulate claudin oligomerization. J Cell Sci 126, 554-564.
7. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM (1998). The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273, 29745-29753.
8. Fanning AS, Van Itallie CM, Anderson JM (2012). Zonula occludens-1 and -2 regulate apical cell structure and the zonula adherens cytoskeleton in polarized epithelia. Mol Biol Cell 23, 577-590.
9. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S (1993). Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123, 1777-1788.
10. Furuse M, Sasaki H, Fujimoto K, Tsukita S (1998). A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143, 391-401.
11. Furuse M, Sasaki H, Tsukita S (1999). Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cel Biol 147, 891-903.
12. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, et al (2015). A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat Methods 12, 244-250.
13. Gunzel D, Yu AS (2013). Claudins and the modulation of tight junction permeability. Physiol Rev 93, 525-569.
14. Gustafsson MG (2000). Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198, 82-87.
15. Kenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S (2005). Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171, 939-945.
16. Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999). Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147, 1351-1363.
17. Ivanov AI, Parkos CA, Nusrat A (2010). Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol 177, 512-524.
18. Kojima T, Sawada N, Yamamoto M, Kokai Y, Mori M, Mochizuki Y (1999). Disruption of circumferential actin filament causes disappearance of occludin from the cell borders of rat hepatocytes in primary culture without distinct changes of tight junction strands. Cell Struct Funct 24, 11-17.
19. Koval M (2013). Differential pathways of claudin oligomerization and integration into tight junctions. Tissue Barriers 1, e24518.
20. Madara JL, Barenberg D, Carlson S (1986). Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: further evidence that the cytoskeleton may influence paracellular permeability and junctional charge selectivity. J Cell Biol 102, 2125-2136.
21. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, et al (1998). Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142, 117-127.
22. Meza I, Ibarra G, Sabanero M, Martinez-Palomo A, Cereijido M (1980). Occluding junctions and cytoskeletal components in a cultured transporting epithelium. J Cell Biol 87, 746-754.
23. Nomme J, Antanasijevic A, Caffrey M, Van Itallie CM, Anderson JM, Fanning AS, Lavie A (2015). Structural basis of a key factor regulating the affinity between the zonula occludens first PDZ domain and claudins. J Biol Chem 290, 16595-16606.
24. Piontek J, Winkler L, Wolburg H, Muller SL, Zuleger N, Piehl C, Wiesner B, Krause G, Blasig IE (2008). Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 22, 146-158.
25. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013). Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8, 2281-2308.
26. Rodgers LS, Beam MT, Anderson JM, Fanning AS (2013). Epithelial barrier assembly requires coordinated activity of multiple domains of the tight junction protein ZO-1. J Cell Sci 126, 1565-1575.
27. Rodgers LS, Fanning AS (2011). Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton (Hoboken) 68, 653-660.
28. Ruffer C, Gerke V (2004). The C-terminal cytoplasmic tail of claudins 1 and 5 but not its PDZ-binding motif is required for apical localization at epithelial and endothelial tight junctions. Eur J Cell Biol 83, 135-144.
29. Sasaki H, Matsui C, Furuse K, Mimori-Kiyosue Y, Furuse M, Tsukita S (2003). Dynamic behavior of paired claudin strands within apposing plasma membranes. Proc Natl Acad Sci USA 100, 3971-3976.
30. Schermelleh L, Heintzmann R, Leonhardt H (2010). A guide to super-resolution fluorescence microscopy. J Cell Biol 190, 165-175.
31. Schlingmann B, Overgaard CE, Molina SA, Lynn KS, Mitchell LA, Dorsainvil White S, Mattheyses AL, Guidot DM, Capaldo CT, Koval M (2016). Regulation of claudin/zonula occludens-1 complexes by hetero-claudin interactions. Nat Commun 7, 12276.
32. Shen L, Turner JR (2005). Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16, 3919-3936.
33. Shen L, Weber CR, Turner JR (2008). The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J Cell Biol 181, 683-695.
34. Tokuda S, Higashi T, Furuse M (2014). ZO-1 knockout by TALEN-mediated gene targeting in MDCK cells: involvement of ZO-1 in the regulation of cytoskeleton and cell shape. PLoS One 9, e104994.
35. Umeda K, Ikenouchi J, Katahira-Tayama S, Furuse K, Sasaki H, Nakayama M, Matsui T, Tsukita S, Furuse M (2006). ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126, 741-754.
36. Van Itallie CM, Fanning AS, Anderson JM (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.
37. Van Itallie CM, Holmes J, Bridges A, Gookin JL, Coccaro MR, Proctor W, Colegio OR, Anderson JM (2008). The density of small tight junction pores varies among cell types and is increased by expression of claudin-2. J Cell Sci 121, 298-305.
38. Van Itallie CM, Tietgens AJ, Krystofiak E, Kachar B, Anderson JM (2015). A complex of ZO-1 and the BAR-domain protein TOCA-1 regulates actin assembly at the tight junction. Mol Biol Cell 26, 2769-2787.
39. Van Itallie CM, Tietgens AJ, LoGrande K, Aponte A, Gucek M, Anderson JM (2012). Phosphorylation of claudin-2 on serine 208 promotes membrane retention and reduces trafficking to lysosomes. J Cell Sci 125, 4902-4912.
40. Yamazaki Y, Umeda K, Wada M, Nada S, Okada M, Tsukita S (2008). ZO-1- and ZO-2-dependent integration of myosin-2 to epithelial zonula adherens. Mol Biol Cell 19, 3801-3811.
41. York AG, Parekh SH, Dalle Nogare D, Fischer RS, Temprine K, Mione M, Chitnis AB, Combs CA, Shroff H (2012). Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy. Nat Methods 9, 749-754.
42. Yu D, Marchiando AM, Weber CR, Raleigh DR, Wang Y, Shen L, Turner JR (2010). MLCK-dependent exchange and actin binding region-dependent anchoring of ZO-1 regulate tight junction barrier function. Proc Natl Acad Sci USA 107, 8237-8241.