The occludin and ZO-1 complex, defined by small angle X-ray scattering and NMR, has implications for modulating tight junction permeability

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 27, 2012, Pages 10855-10860

  Tash, Brian R ^a,c   Bewley, Maria C ^a   Russo, Mariano ^a   Keil, Jason M ^a   Griffin, Kathleen A ^a   Sundstrom, Jeffrey M ^b   Antonetti, David A ^a   Tian, Fang ^a   Flanagan, John M ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Calmodulin; Membrane associated guanylate kinase; Tricellulin

Indexed keywords

OCCLUDIN; PROTEIN ZO1;

ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; TIGHT JUNCTION; X RAY CRYSTALLOGRAPHY;

ACIDS; CALMODULIN; CELL MEMBRANE PERMEABILITY; ESCHERICHIA COLI; GUANYLATE KINASE; HUMANS; MEMBRANE PROTEINS; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SCATTERING, RADIATION; SOLUTIONS; TIGHT JUNCTIONS;

EID: 84863566207     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1121390109     Document Type: Article

References (40)

1. Van Itallie CM, Anderson JM (2004) The molecular physiology of tight junction pores. Physiology (Bethesda) 19:331-338. (Pubitemid 39636080)
2. Forster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130:55-70.
3. Edelblum KL, Turner JR (2009) The tight junction in inflammatory disease: Communication breakdown. Curr Opin Pharmacol 9:715-720.
4. Fanning AS, Mitic LL, Anderson JM (1999) Transmembrane proteins in the tight junction barrier. J Am Soc Nephrol 10:1337-1345. (Pubitemid 29247001)
5. Mitic LL, Van Itallie CM, Anderson JM (2000) 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.
6. Sanchez-Pulido L, Martin-Belmonte F, Valencia A, Alonso MA (2002) MARVEL: A conserved domain involved in membrane apposition events. Trends Biochem Sci 27:599-601. (Pubitemid 35435304)
7. Sundstrom JM, et al. (2009) Identification and analysis of occludin phosphosites: A combined mass spectrometry and bioinformatics approach. J Proteome Res 8:808-817.
8. Marchiando AM, et al. (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189:111-126.
9. Van Itallie CM, Fanning AS, Holmes J, Anderson JM (2010) Occludin is required for cytokine-induced regulation of tight junction barriers. J Cell Sci 123:2844-2852.
10. Murakami T, Felinski EA, Antonetti DA (2009) Occludin phosphorylation and ubiquitination regulate tight junction trafficking and vascular endothelial growth factorinduced permeability. J Biol Chem 284:21036-21046.
11. Balda MS, et al. (1996) 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. (Pubitemid 26278226)
12. FuruseM, et al. (1994) Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J Cell Biol 127:1617-1626. (Pubitemid 24380900)
13. Nusrat A, et al. (2000) The coiled-coil domain of occludin can act to organize structural and functional elements of the epithelial tight junction. J Biol Chem 275:29816-29822. (Pubitemid 32043866)
14. Fanning AS, Anderson JM(2009) Zonula occludens-1 and -2 are cytosolic scaffolds that regulate the assembly of cellular junctions. Ann NY Acad Sci 1165:113-120.
15. Bauer H, Zweimueller-Mayer J, Steinbacher P, Lametschwandtner A, Bauer HC (2010) The dual role of zonula occludens (ZO) proteins. J Biomed Biotechnol 2010:402593, 10.1155/2010/402593.
16. Li Y, Fanning AS, Anderson JM, Lavie A (2005) Structure of the conserved cytoplasmic C-terminal domain of occludin: Identification of the ZO-1 binding surface. J Mol Biol 352:151-164. (Pubitemid 41213309)
17. Muller SL, et al. (2005) The tight junction protein occludin and the adherens junction protein alpha-catenin share a common interaction mechanism with ZO-1. J Biol Chem 280:3747-3756. (Pubitemid 40223843)
18. Schmidt A, Utepbergenov DI, Krause G, Blasig IE (2001) Use of surface plasmon resonance for real-time analysis of the interaction of ZO-1 and occludin. Biochem Biophys Res Commun 288:1194-1199. (Pubitemid 33131727)
19. Schmidt A, et al. (2004) Occludin binds to the SH3-hinge-GuK unit of zonula occludens protein 1: Potential mechanism of tight junction regulation. Cell Mol Life Sci 61:1354-1365. (Pubitemid 38822424)
20. Lye MF, Fanning AS, Su Y, Anderson JM, Lavie A (2010) Insights into regulated ligand binding sites from the structure of ZO-1 Src homology 3-guanylate kinase module. J Biol Chem 285:13907-13917.
21. Nomme J, et al. (2011) The Src homology 3 domain is required for junctional adhesion molecule binding to the third PDZ domain of the scaffolding protein ZO-1. J Biol Chem 286:43352-43360.
22. Pan L, Chen J, Yu J, Yu H, Zhang M (2011) The structure of the PDZ3-SH3-GuK tandem of ZO-1 suggests a supramodular organization of the MAGUK family scaffold protein core. J Biol Chem 286:40069-40074.
23. Engelman DM, Moore PB (1975) Determination of quaternary structure by small angle neutron scattering. Annu Rev Biophys Bioeng 4:219-241.
24. Petoukhov MV, Svergun DI (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J 89:1237-1250. (Pubitemid 41099005)
25. Fanning AS, Lye MF, Anderson JM, Lavie A (2007) Domain swapping within PDZ2 is responsible for dimerization of ZO proteins. J Biol Chem 282:37710-37716.
26. Salzmann M, Wider G, Pervushin K, Senn H, Wuthrich K (1999) TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins. J Am Chem Soc 121:844-848.
27. Salzmann M, Pervushin K, Wider G, Senn H, Wuthrich K (1998) TROSY in triple-resonance experiments: New perspectives for sequential NMR assignment of large proteins. Proc Natl Acad Sci USA 95:13585-13590. (Pubitemid 28523015)
28. Takahashi H, Nakanishi T, Kami K, Arata Y, Shimada I (2000) A novel NMR method for determining the interfaces of large protein-protein complexes. Nat Struct Biol 7:220-223. (Pubitemid 30140768)
29. Fanning AS, et al. (2007) The unique-5 and -6 motifs of ZO-1 regulate tight junction strand localization and scaffolding properties. Mol Biol Cell 18:721-731. (Pubitemid 46399480)
30. Reese ML, Dakoji S, Bredt DS, Dotsch V (2007) The guanylate kinase domain of the MAGUK PSD-95 binds dynamically to a conserved motif in MAP1a. Nat Struct Mol Biol 14:155-163.
31. Zhu J, et al. (2011) Guanylate kinase domains of the MAGUK family scaffold proteins as specific phospho-protein-binding modules. EMBO J 30:4986-4997.
32. Raleigh DR, et al. (2010) Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21:1200-1213.
33. Riazuddin S, et al. (2006) Tricellulin is a tight-junction protein necessary for hearing. Am J Hum Genet 79:1040-1051. (Pubitemid 44853475)
34. Balda MS, Anderson JM, Matter K (1996) The SH3 domain of the tight junction protein ZO-1 binds to a serine protein kinase that phosphorylates a region C-terminal to this domain. FEBS Lett 399:326-332. (Pubitemid 26426876)
35. Elias BC, et al. (2009) Phosphorylation of Tyr-398 and Tyr-402 in occludin prevents its interaction with ZO-1 and destabilizes its assembly at the tight junctions. J Biol Chem 284:1559-1569.
36. Kale G, Naren AP, Sheth P, Rao RK (2003) Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2, and ZO-3. Biochem Biophys Res Commun 302:324-329. (Pubitemid 36397924)
37. Raleigh DR, et al. (2011) Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J Cell Biol 193:565-582.
38. Rao RK, Basuroy S, Rao VU, Karnaky KJ, Jr, Gupta A (2002) Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J 368:471-481. (Pubitemid 35454525)
39. Du D, et al. (2010) The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev Cell 18:52-63.
40. Yamamoto M, et al. (2008) Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial cells. Am J Pathol 172:521-533. (Pubitemid 351282037)