Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion

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

Volumn 107, Issue 4, 2010, Pages 1425-1430

  Zhang, Jingjing ^a   Piontek, Jörg ^b   Wolburg, Hartwig ^c   Piehl, Christian ^b   Liss, Martin ^a,b   Otten, Cécile ^a   Christ, Annabel ^a   Willnow, Thomas E ^a   Blasig, Ingolf E ^b   Abdelilah Seyfried, Salim ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Brain morphogenesis; Cell polarity; Lumen formation; Na+,K+ ATPase; Tight junctions

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CLAUDIN 5; CLAUDIN 5A; LANTHANUM; LANTHANUM NITRATE; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN VENTRICLE; EMBRYO; ENZYME ACTIVITY; MORPHOGENESIS; MOUSE; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TIGHT JUNCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; MICE; MICROSCOPY, ELECTRON; MUTATION; NEUROEPITHELIAL CELLS; TIGHT JUNCTIONS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 76549090463     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911996107     Document Type: Article

References (34)

1. Lowery LA, Sive H (2005) Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 132:2057-2067.
2. Jeong JY, et al. (2008) Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res Bull 75:619-628.
3. Bill BR, et al. (2008) Development and Notch signaling requirements of the zebrafish choroid plexus. PLoS One 3:e3114.
4. García-Lecea M, Kondrychyn I, Fong SH, Ye ZR, Korzh V (2008) In vivo analysis of choroid plexus morphogenesis in zebrafish. PLoS One 3:e3090.
5. Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181-188.
6. Furuse M, Moriwaki K (2009) The role of claudin-based tight junctions in morphogenesis. Ann N Y Acad Sci 1165:58-61.
7. Bagnat M, Cheung ID, Mostov KE, Stainier DY (2007) Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol 9:954-960.
8. Moriwaki K, Tsukita S, Furuse M (2007) Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos. Dev Biol 312: 509-522.
9. Kollmar R, Nakamura SK, Kappler JA, Hudspeth AJ (2001) Expression and phylogeny of claudins in vertebrate primordia. Proc Natl Acad Sci USA 98:10196-10201.
10. Loh YH, Christoffels A, Brenner S, Hunziker W, Venkatesh B (2004) Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res 14: 1248-1257.
11. Nitta T, et al. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161:653-660.
12. Nasevicius A, Ekker SC (2000) Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26:216-220.
13. Horne-Badovinac S, et al. (2001) Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr Biol 11:1492-1502.
14. Whittembury G, Rawlins FA (1971) Evidence of a paracellular pathway for ion flow in the kidney proximal tubule. Electromicroscopic demonstration of lanthanum precipitate in the tight junction. Pflugers Arch 330:302-309.
15. Wolburg H, et al. (2008) Epithelial and endothelial barriers in the olfactory region of the nasal cavity of the rat. Histochem Cell Biol 130:127-140.
16. Piontek J, et al. (2008) Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 22:146-158.
17. Krause G, et al. (2008) Structure and function of claudins. Biochim Biophys Acta 1778: 631-645.
18. Wen H, Watry DD, Marcondes MC, Fox HS (2004) Selective decrease in paracellular conductance of tight junctions: Role of the first extracellular domain of claudin-5. Mol Cell Biol 24:8408-8417.
19. Robu ME, et al. (2007) p53 activation by knockdown technologies. PLoS Genet 3:e78.
20. Bit-Avragim N, et al. (2008) Divergent polarization mechanisms during vertebrate epithelial development mediated by the Crumbs complex protein Nagie oko. J Cell Sci 121:2503-2510.
21. Malicki J, Driever W (1999) oko meduzy mutations affect neuronal patterning in the zebrafish retina and reveal cell-cell interactions of the retinal neuroepithelial sheet. Development 126:1235-1246.
22. Omori Y, Malicki J (2006) oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol 16:945-957.
23. Wei X, Malicki J (2002) nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet 31:150-157.
24. Itoh M, et al. (1993) The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 121:491-502.
25. Drummond IA, et al. (1998) Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125:4655-4667.
26. Schlüter MA, et al. (2009) Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol Biol Cell 20:4652-4663.
27. Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648-677.
28. Abuazza G, et al. (2006) Claudins 6, 9, and 13 are developmentally expressed renal tight junction proteins. Am J Physiol Renal Physiol 291:F1132-F1141.
29. Shu X, et al. (2003) Na,K-ATPase is essential for embryonic heart development in the zebrafish. Development 130:6165-6173.
30. Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203-1215.
31. Trinh LA, Stainier DY (2004) Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev Cell 6:371-382.
32. Blasig IE, et al. (2006) On the self-association potential of transmembrane tight junction proteins. Cell Mol Life Sci 63:505-514.
33. Blasig IE, Mertsch K, Haseloff RF (2002) Nitronyl nitroxides, a novel group of protective agents against oxidative stress in endothelial cells forming the blood-brain barrier. Neuropharmacology 43:1006-1014.
34. Hammes A, et al. (2001) Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 106:319-329.