The transmembrane protein Macroglobulin complement-related is essential for septate junction formation and epithelial barrier function in Drosophila

Development (Cambridge)

Volumn 141, Issue 4, 2014, Pages 899-908

  Bätz, Tilmann ^a   Förster, Dominique ^a,b   Luschnig, Stefan ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Alpha 2 macroglobulin; CD109; Complement; Drosophila melanogaster; Epithelial barrier; Innate immunity; Septate junction; Thioester proteins

Indexed keywords

ALPHA 2 MACROGLOBULIN; FODRIN; GENOMIC DNA; LOW DENSITY LIPOPROTEIN RECEPTOR; MACROGLOBULIN COMPLEMENT RELATED; MESSENGER RNA; UNCLASSIFIED DRUG; UVOMORULIN;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; BLASTODERM; CELL COUNT; CELL JUNCTION; CELL MEMBRANE; CELL SHAPE; CELL SURFACE; CELLULAR DISTRIBUTION; DROSOPHILA MELANOGASTER; DROSOPHILA STRAIN; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; EPITHELIUM CELL; GENE LOCUS; GERM CELL; IMAGE ANALYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INNATE IMMUNITY; MEMBRANE FORMATION; MICROSCOPY; MISSENSE MUTATION; MOLECULAR BIOLOGY; MOLECULAR WEIGHT; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; SALIVARY GLAND; STOP CODON; TISSUE CULTURE; TRACHEA MUCOSA;

ALPHA-2-MACROGLOBULIN; CD109; COMPLEMENT; DROSOPHILA MELANOGASTER; EPITHELIAL BARRIER; INNATE IMMUNITY; SEPTATE JUNCTION; THIOESTER PROTEINS;

ANIMALS; CYTOKINES; DROSOPHILA; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNITY, INNATE; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; INTERCELLULAR JUNCTIONS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; OLIGONUCLEOTIDES; SERPINS;

EID: 84893269348     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.102160     Document Type: Article

References (59)

1. Banerjee, S., Sousa, A. D. and Bhat, M. A. (2006). Organization and function of septate junctions: an evolutionary perspective. Cell Biochem. Biophys. 46, 65-77.
2. Banerjee, S., Bainton, R. J., Mayer, N., Beckstead, R. and Bhat, M. A. (2008). Septate junctions are required for ommatidial integrity and blood-eye barrier function in Drosophila. Dev. Biol. 317, 585-599.
3. Baumgartner, S., Littleton, J. T., Broadie, K., Bhat, M. A., Harbecke, R., Lengyel, J. A., Chiquet-Ehrismann, R., Prokop, A. and Bellen, H. J. (1996). A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87, 1059-1068.
4. Behr, M., Riedel, D. and Schuh, R. (2003). The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev. Cell 5, 611-620.
5. Beitel, G. J. and Krasnow, M. A. (2000). Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127, 3271-3282.
6. Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M. et al. (2004). The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761-781.
7. Bilder, D. and Perrimon, N. (2000). Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403, 676-680.
8. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
9. Blandin, S. and Levashina, E. A. (2004). Thioester-containing proteins and insect immunity. Mol. Immunol. 40, 903-908.
10. Blandin, S. A., Marois, E. and Levashina, E. A. (2008). Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe 3, 364-374.
11. Bonnay, F., Cohen-Berros, E., Hoffmann, M., Kim, S. Y., Boulianne, G. L., Hoffmann, J. A., Matt, N. and Reichhart, J. M. (2013). big bang gene modulates gut immune tolerance in Drosophila. Proc. Natl. Acad. Sci. USA 110, 2957-2962.
12. Borth, W. (1992). Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J. 6, 3345-3353.
13. Bou Aoun, R., Hetru, C., Troxler, L., Doucet, D., Ferrandon, D. and Matt, N. (2011). Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J. Innate Immun. 3, 52-64.
14. Buszczak, M., Paterno, S., Lighthouse, D., Bachman, J., Planck, J., Owen, S., Skora, A. D., Nystul, T. G., Ohlstein, B., Allen, A. et al. (2007). The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics175, 1505-1531.
15. Carlson, S. D., Juang, J. L., Hilgers, S. L. and Garment, M. B. (2000). Blood barriers of the insect. Annu. Rev. Entomol. 45, 151-174.
16. Caussinus, E., Colombelli, J. and Affolter, M. (2008). Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr. Biol. 18, 1727-1734.
17. Caussinus, E., Kanca, O. and Affolter, M. (2011). Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat. Struct. Mol. Biol. 19, 117-121.
18. Caviglia, S. and Luschnig, S. (2013). The ETS domain transcriptional repressor Anterior open inhibits MAP kinase and Wingless signaling to couple tracheal cell fate with branch identity. Development 140, 1240-1249.
19. de Navas, L., Foronda, D., Suzanne, M. and Sánchez-Herrero, E. (2006). A simple and efficient method to identify replacements of P-lacZ by P-Gal4 lines allows obtaining Gal4 insertions in the bithorax complex of Drosophila. Mech. Dev. 123, 860-867.
20. Fehon, R. G., Dawson, I. A. and Artavanis-Tsakonas, S. (1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545-557.
21. Förster, D., Armbruster, K. and Luschnig, S. (2010). Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr. Biol. 20, 62-68.
22. Furuse, M. and Tsukita, S. (2006). Claudins in occluding junctions of humans and flies. Trends Cell Biol. 16, 181-188.
23. Genova, J. L. and Fehon, R. G. (2003). Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J. Cell Biol. 161, 979-989.
24. Gupta, A. P. and Han, S. S. (1988). Arthropod immune system. III. Septate junctions in the hemocytic capsule of the german cockroach, Blattella germanica. Tissue Cell 20, 629-634.
25. Hasegawa, M., Hagiwara, S., Sato, T., Jijiwa, M., Murakumo, Y., Maeda, M., Moritani, S., Ichihara, S. and Takahashi, M. (2007). CD109, a new marker for myoepithelial cells of mammary, salivary, and lacrimal glands and prostate basal cells. Pathol. Int. 57, 245-250.
26. Hemphälä, J., Uv, A., Cantera, R., Bray, S. and Samakovlis, C. (2003). Grainy head controls apical membrane growth and tube elongation in response to Branchless/FGF signalling. Development 130, 249-258.
27. Hijazi, A., Masson, W., Augé, B., Waltzer, L., Haenlin, M. and Roch, F. (2009). boudin is required for septate junction organisation in Drosophila and codes for a diffusible protein of the Ly6 superfamily. Development 136, 2199-2209.
28. Hortsch, M. and Margolis, B. (2003). Septate and paranodal junctions: kissing cousins. Trends Cell Biol. 13, 557-561.
29. Ile, K. E., Tripathy, R., Goldfinger, V. and Renault, A. D. (2012). Wunen, a Drosophila lipid phosphate phosphatase, is required for septate junction-mediated barrier function. Development 139, 2535-2546.
30. Jaspers, M. H., Nolde, K., Behr, M., Joo, S. H., Plessmann, U., Nikolov, M., Urlaub, H. and Schuh, R. (2012). The claudin Megatrachea protein complex. J. Biol. Chem.287, 36756-36765.
31. Lagueux, M., Perrodou, E., Levashina, E. A., Capovilla, M. and Hoffmann, J. A. (2000). Constitutive expression of a complement-like protein in toll and JAK gain-offunction mutants of Drosophila. Proc. Natl. Acad. Sci. USA 97, 11427-11432.
32. Lamb, R. S., Ward, R. E., Schweizer, L. and Fehon, R. G. (1998). 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 9, 3505-3519.
33. Laprise, P., Paul, S. M., Boulanger, J., Robbins, R. M., Beitel, G. J. and Tepass, U. (2010). Epithelial polarity proteins regulate Drosophila tracheal tube size in parallel to the luminal matrix pathway. Curr. Biol. 20, 55-61.
34. Le, T., Liang, Z., Patel, H., Yu, M. H., Sivasubramaniam, G., Slovitt, M., Tanentzapf, G., Mohanty, N., Paul, S. M., Wu, V. M. et al. (2006). A new family of Drosophila balancer chromosomes with a w-dfd-GMR yellow fluorescent protein marker. Genetics 174, 2255-2257.
35. Levashina, E. A., Moita, L. F., Blandin, S., Vriend, G., Lagueux, M. and Kafatos, F. C. (2001). Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709-718.
36. Luschnig, S., Bätz, T., Armbruster, K. and Krasnow, M. A. (2006). serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 16, 186-194.
37. McIntyre, J. A., Pierce, C. W. and Karnovsky, M. J. (1976). The formation of septatelike junctional complexes between lymphoid cells in vitro. J. Immunol. 116, 1582-1586.
38. Nilton, A., Oshima, K., Zare, F., Byri, S., Nannmark, U., Nyberg, K. G., Fehon, R. G. and Uv, A. E. (2010). Crooked, coiled and crimpled are three Ly6-like proteins required for proper localization of septate junction components. Development 137, 2427-2437.
39. Nonaka, M. and Yoshizaki, F. (2004). Evolution of the complement system. Mol. Immunol. 40, 897-902.
40. Oda, H. and Tsukita, S. (1999). Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dalpha-catenin-GFP fusion protein. Dev. Genes Evol. 209, 218-225.
41. Oshima, K. and Fehon, R. G. (2011). 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. 124, 2861-2871.
42. Paul, S. M., Ternet, M., Salvaterra, P. M. and Beitel, G. J. (2003). The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130, 4963-4974.
43. Paul, S. M., Palladino, M. J. and Beitel, G. J. (2007). A pump-independent function of the Na, K-ATPase is required for epithelial junction function and tracheal tube-size control. Development 134, 147-155.
44. Russo, J., Dupas, S., Frey, F., Carton, Y. and Brehelin, M. (1996). Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 112, 135-142.
45. Shiga, Y., Tanaka-Matakatsu, M. and Hayashi, S. (1996). A nuclear GFP/ betagalactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38, 99-106.
46. Shin, K., Fogg, V. C. and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
47. Siebert, A. E., Jr (1979). Septate-like junctions between cells of the immune system in vivo. Cell Biol. Int. Rep. 3, 331-335.
48. Snow, P. M., Bieber, A. J. and Goodman, C. S. (1989). Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell 59, 313-323.
49. Stroschein-Stevenson, S. L., Foley, E., O'Farrell, P. H. and Johnson, A. D. (2006). Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 4, e4.
50. Syed, M. H., Krudewig, A., Engelen, D., Stork, T. and Klämbt, C. (2011). The CD59 family member Leaky/Coiled is required for the establishment of the blood-brain barrier in Drosophila. J. Neurosci. 31, 7876-7885.
51. Tepass, U. and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
52. Tiklová, K., Senti, K. A., Wang, S., Gräslund, A. and Samakovlis, C. (2010). Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila. Nat. Cell Biol. 12, 1071-1077.
53. Wang, S., Jayaram, S. A., Hemphälä, J., Senti, K. A., Tsarouhas, V., Jin, H. and Samakovlis, C. (2006). Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr. Biol. 16, 180-185.
54. Ward, R. E., IV, Lamb, R. S. and Fehon, R. G. (1998). A conserved functional domain of Drosophila coracle is required for localization at the septate junction and has membrane-organizing activity. J. Cell Biol. 140, 1463-1473.
55. Williams, M. J. (2009). The Drosophila cell adhesion molecule Neuroglian regulates Lissencephaly-1 localisation in circulating immunosurveillance cells. BMC Immunol.10, 17.
56. Woods, D. F. and Bryant, P. J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell66, 451-464.
57. Wu, V. M. and Beitel, G. J. (2004). A junctional problem of apical proportions: epithelial tube-size control by septate junctions in the Drosophila tracheal system. Curr. Opin. Cell Biol. 16, 493-499.
58. Wu, V. M., Schulte, J., Hirschi, A., Tepass, U. and Beitel, G. J. (2004). Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J. Cell Biol. 164, 313-323.
59. Zhang, L. and Ward, R. E., IV (2009). uninflatable encodes a novel ectodermal apical surface protein required for tracheal inflation in Drosophila. Dev. Biol. 336, 201-212.