The Triple-Repeat Protein Anakonda Controls Epithelial Tricellular Junction Formation in Drosophila

Developmental Cell

Volumn 33, Issue 5, 2015, Pages 535-548

  Byri, Sunitha ^a   Misra, Tvisha ^e   Syed, Zulfeqhar A ^a   Bätz, Tilmann ^e   Shah, Jimit ^e   Boril, Lukas ^e   Glashauser, Jade ^e   Aegerter Wilmsen, Tinri ^e   Matzat, Till ^c,d   Moussian, Bernard ^b   Uv, Anne ^a   Luschnig, Stefan ^c,d,e  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d CiM   (Germany)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANAKONDA PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GLIOTACTIN; NERVE PROTEIN;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EPITHELIUM CELL; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRICELLULAR JUNCTION; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; DROSOPHILA MELANOGASTER; EPITHELIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT; TIGHT JUNCTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPITHELIUM; IMMUNOBLOTTING; INTERCELLULAR JUNCTIONS; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; REPETITIVE SEQUENCES, AMINO ACID; TIGHT JUNCTIONS;

EID: 84930574301     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.03.023     Document Type: Article

References (50)

1. Adam G., Delbrück M. Reduction of dimensionality in biological diffusion processes. Structural Chemistry and Molecular Biology 1968, W.H. Freeman and Co. A. Rich, N. Davidson (Eds.).
2. Auld V.J., Fetter R.D., Broadie K., Goodman C.S. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 1995, 81:757-767.
3. Banerjee S., Sousa A.D., Bhat M.A. Organization and function of septate junctions: an evolutionary perspective. Cell Biochem. Biophys. 2006, 46:65-77.
4. Banerjee S., Bainton R.J., Mayer N., Beckstead R., Bhat M.A. Septate junctions are required for ommatidial integrity and blood-eye barrier function in Drosophila. Dev. Biol. 2008, 317:585-599.
5. Bätz T., Förster D., Luschnig S. The transmembrane protein macroglobulin complement-related is essential for septate junction formation and epithelial barrier function in Drosophila. Development 2014, 141:899-908.
6. Behr M., Riedel D., Schuh R. The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev. Cell 2003, 5:611-620.
7. Bilder D., Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 2000, 403:676-680.
8. Bowdish D.M., Gordon S. Conserved domains of the class A scavenger receptors: evolution and function. Immunol. Rev. 2009, 227:19-31.
9. Burns A.R., Walker D.C., Brown E.S., Thurmon L.T., Bowden R.A., Keese C.R., Simon S.I., Entman M.L., Smith C.W. Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J.Immunol. 1997, 159:2893-2903.
10. Caviglia S., Luschnig S. The ETS domain transcriptional repressor Anterior open inhibits MAP kinase and Wingless signaling to couple tracheal cell fate with branch identity. Development 2013, 140:1240-1249.
11. Chakraborty P., William Buaas F., Sharma M., Smith B.E., Greenlee A.R., Eacker S.M., Braun R.E. Androgen-dependent sertoli cell tight junction remodeling is mediated by multiple tight junction components. Mol. Endocrinol. 2014, 28:1055-1072.
12. Förster D., Armbruster K., Luschnig S. Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr. Biol. 2010, 20:62-68.
13. Fristrom D.K. Septate junctions in imaginal disks of Drosophila: a model for the redistribution of septa during cell rearrangement. J.Cell Biol. 1982, 94:77-87.
14. Fukumatsu M., Ogawa M., Arakawa S., Suzuki M., Nakayama K., Shimizu S., Kim M., Mimuro H., Sasakawa C. Shigella targets epithelial tricellular junctions and uses a noncanonical clathrin-dependent endocytic pathway to spread between cells. Cell Host Microbe 2012, 11:325-336.
15. Furuse M., Tsukita S. Claudins in occluding junctions of humans and flies. Trends Cell Biol. 2006, 16:181-188.
16. Furuse M., Izumi Y., Oda Y., Higashi T., Iwamoto N. Molecular organization of tricellular tight junctions. Tissue Barriers 2014, 2:e28960.
17. Genova J.L., Fehon R.G. Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J.Cell Biol. 2003, 161:979-989.
18. Graf F., Noirot-Timothée C., Noirot C. The specialization of septate junctions in regions of tricellular junctions. I. Smooth septate junctions (=continuous junctions). J.Ultrastruct. Res. 1982, 78:136-151.
19. Higashi T., Tokuda S., Kitajiri S., Masuda S., Nakamura H., Oda Y., Furuse M. Analysis of the 'angulin' proteins LSR, ILDR1 and ILDR2-tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J.Cell Sci. 2013, 126:966-977.
20. Ikenouchi J., Furuse M., Furuse K., Sasaki H., Tsukita S., Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J.Cell Biol. 2005, 171:939-945.
21. Izumi Y., Yanagihashi Y., Furuse M. A novel protein complex, Mesh-Ssk, is required for septate junction formation in the Drosophila midgut. J.Cell Sci. 2012, 125:4923-4933.
22. Jaspers M.H., Nolde K., Behr M., Joo S.H., Plessmann U., Nikolov M., Urlaub H., Schuh R. The claudin Megatrachea protein complex. J.Biol. Chem. 2012, 287:36756-36765.
23. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
24. Krug S.M., Amasheh S., Richter J.F., Milatz S., Günzel D., Westphal J.K., Huber O., Schulzke J.D., Fromm M. Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol. Biol. Cell 2009, 20:3713-3724.
25. Lamb R.S., Ward R.E., Schweizer L., Fehon R.G. Drosophila coracle, a member of the protein 4.1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol. Biol. Cell 1998, 9:3505-3519.
26. Llimargas M., Strigini M., Katidou M., Karagogeos D., Casanova J. Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 2004, 131:181-190.
27. Lowe N., Rees J.S., Roote J., Ryder E., Armean I.M., Johnson G., Drummond E., Spriggs H., Drummond J., Magbanua J.P., et al. Analysis of the expression patterns, subcellular localisations and interaction partners of Drosophila proteins using a pigP protein trap library. Development 2014, 141:3994-4005. UK Drosophila Protein Trap Screening Consortium.
28. Masuda S., Oda Y., Sasaki H., Ikenouchi J., Higashi T., Akashi M., Nishi E., Furuse M. LSR defines cell corners for tricellular tight junction formation in epithelial cells. J.Cell Sci. 2011, 124:548-555.
29. Mechler B.M., McGinnis W., Gehring W.J. Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. EMBO J. 1985, 4:1551-1557.
30. Nakai K., Tanaka T., Murai T., Ohguro N., Tano Y., Miyasaka M. Invasive human pancreatic carcinoma cells adhere to endothelial tri-cellular corners and increase endothelial permeability. Cancer Sci. 2005, 96:766-773.
31. Noirot-Timothee C., Noirot C. Septate and scalariform junctions in arthropods. Int. Rev. Cytol. 1980, 63:97-140.
32. Noirot-Timothée C., Graf F., Noirot C. The specialization of septate junctions in regions of tricellular junctions. II. Pleated septate junctions. J.Ultrastruct. Res. 1982, 78:152-165.
33. Oda Y., Otani T., Ikenouchi J., Furuse M. Tricellulin regulates junctional tension of epithelial cells at tricellular contacts through Cdc42. J.Cell Sci. 2014, 127:4201-4212.
34. Oshima K., Fehon R.G. Analysis of protein dynamics within the septate junction reveals a highly stable core protein complex that does not include the basolateral polarity protein Discs large. J.Cell Sci. 2011, 124:2861-2871.
35. Padash-Barmchi M., Browne K., Sturgeon K., Jusiak B., Auld V.J. Control of Gliotactin localization and levels by tyrosine phosphorylation and endocytosis is necessary for survival of polarized epithelia. J.Cell Sci. 2010, 123:4052-4062.
36. Padash-Barmchi M., Charish K., Que J., Auld V.J. Gliotactin and Discs large are co-regulated to maintain epithelial integrity. J.Cell Sci. 2013, 126:1134-1143.
37. Paul S.M., Ternet M., Salvaterra P.M., Beitel G.J. The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 2003, 130:4963-4974.
38. Quiñones-Coello A.T., Petrella L.N., Ayers K., Melillo A., Mazzalupo S., Hudson A.M., Wang S., Castiblanco C., Buszczak M., Hoskins R.A., Cooley L. Exploring strategies for protein trapping in Drosophila. Genetics 2007, 175:1089-1104.
39. Riazuddin S., Ahmed Z.M., Fanning A.S., Lagziel A., Kitajiri S., Ramzan K., Khan S.N., Chattaraj P., Friedman P.L., Anderson J.M., et al. Tricellulin is a tight-junction protein necessary for hearing. Am. J. Hum. Genet. 2006, 79:1040-1051.
40. Richter P.H., Eigen M. Diffusion controlled reaction rates in spheroidal geometry. Application to repressor-operator association and membrane bound enzymes. Biophys. Chem. 1974, 2:255-263.
41. Schulte J., Tepass U., Auld V.J. Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J.Cell Biol. 2003, 161:991-1000.
42. Schulte J., Charish K., Que J., Ravn S., MacKinnon C., Auld V.J. Gliotactin and Discs large form a protein complex at the tricellular junction of polarized epithelial cells in Drosophila. J.Cell Sci. 2006, 119:4391-4401.
43. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95:5857-5864.
44. Snow P.M., Bieber A.J., Goodman C.S. Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell 1989, 59:313-323.
45. Staehelin L.A. Further observations on the fine structure of freeze-cleaved tight junctions. J.Cell Sci. 1973, 13:763-786.
46. Tepass U., Hartenstein V. The development of cellular junctions in the Drosophila embryo. Dev. Biol. 1994, 161:563-596.
47. Tiklová K., Senti K.A., Wang S., Gräslund A., Samakovlis C. Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila. Nat. Cell Biol. 2010, 12:1071-1077.
48. Whitlock K.E. Development of Drosophila wing sensory neurons in mutants with missing or modified cell surface molecules. Development 1993, 117:1251-1260.
49. Woods D.F., Bryant P.J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 1991, 66:451-464.
50. Wu V.M., Schulte J., Hirschi A., Tepass U., Beitel G.J. Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J.Cell Biol. 2004, 164:313-323.