Control of Gliotactin localization and levels by tyrosine phosphorylation and endocytosis is necessary for survival of polarized epithelia

Journal of Cell Science

Volumn 123, Issue 23, 2010, Pages 4052-4062

  Padash Barmchi, Mojgan ^a   Browne, Kristen ^a   Sturgeon, Kendra ^a   Jusiak, Barbara ^a   Auld, Vanessa J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Drosophila; Endocytosis; JNK; Septate junction; Tricellular junction; Tyrosine phosphorylation

Indexed keywords

GLIOTACTIN; NEUROLIGIN; STRESS ACTIVATED PROTEIN KINASE; TYROSINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL JUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

AMINO ACID MOTIFS; ANIMALS; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; DROSOPHILA; ENDOCYTOSIS; ENDOSOMES; EPITHELIAL CELLS; INTERCELLULAR JUNCTIONS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT;

EID: 78649737037     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.066605     Document Type: Article

References (53)

1. Ahmadian, G., Ju, W., Liu, L., Wyszynski, M., Lee, S. H., Dunah, A. W., Taghibiglou, C., Wang, Y., Lu, J., Wong, T. P. et al. (2004). Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD. EMBO J. 23, 1040-1050.
2. Auld, V. J., Fetter, R. D., Broadie, K. and Goodman, C. S. (1995). Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 81, 757-767.
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. Behrens, J., Vakaet, L., Friis, R., Winterhager, E., Van Roy, F., Mareel, M. M. and Birchmeier, W. (1993). Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature- sensitive v-SRC gene. J. Cell Biol. 120, 757-766.
5. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
6. Cantarelli, V. V., Kodama, T., Nijstad, N., Abolghait, S. K., Nada, S., Okada, M., Iida, T. and Honda, T. (2007). Tyrosine phosphorylation controls cortactin binding to two enterohaemorrhagic Escherichia coli effectors: Tir and EspFu/TccP. Cell. Microbiol. 9, 1782-1795.
7. Chen, W. L., Lin, C. T., Lo, H. F., Lee, J. W., Tu, I. H. and Hu, F. R. (2007). The role of protein tyrosine phosphorylation in the cell-cell interactions, junctional permeability and cell cycle control in post-confluent bovine corneal endothelial cells. Exp. Eye. Res. 85, 259-269.
8. Cuevas, B. D., Lu, Y., Mao, M., Zhang, J., LaPushin, R., Siminovitch, K. and Mills, G. B. (2001). Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 27455-27461.
9. Dupre, S., Volland, C. and Haguenauer-Tsapis, R. (2001). Membrane transport: ubiquitylation in endosomal sorting. Curr. Biol. 11, R932-R934.
10. Fan, Y. and Bergmann, A. (2008). Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell! Trends Cell Biol. 18, 467-473.
11. 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.
12. Fristrom, D. K. (1982). Septate junctions in imaginal disks of Drosophila: a model for the redistribution of septa during cell rearrangement. J. Cell Biol. 94, 77-87.
13. 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.
14. Gilbert, M. M. and Auld, V. J. (2005). Evolution of clams (cholinesterase-like adhesion molecules): structure and function during development. Front. Biosci. 10, 2177-2192.
15. Gilbert, M., Smith, J., Roskams, A. J. and Auld, V. J. (2001). Neuroligin 3 is a vertebrate gliotactin expressed in the olfactory ensheathing glia, a growth-promoting class of macroglia. Glia 34, 151-164.
16. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
17. Huh, J. R., Guo, M. and Hay, B. A. (2004). Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14, 1262-1266.
18. Ivanov, A. I., Nusrat, A. and Parkos, C. A. (2005). Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. BioEssays 27, 356-365.
19. Jekely, G. and Rorth, P. (2003). Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168.
20. Katzmann, D. J., Babst, M. and Emr, S. D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
21. Kirchner, J., Gross, S., Bennett, D. and Alphey, L. (2007). The nonmuscle myosin phosphatase PP1beta (flapwing) negatively regulates Jun N-terminal kinase in wing imaginal discs of Drosophila. Genetics 175, 1741-1749.
22. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G. and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
23. Marois, E., Mahmoud, A. and Eaton, S. (2006). The endocytic pathway and formation of the Wingless morphogen gradient. Development 133, 307-317.
24. Martin, F. A., Perez-Garijo, A. and Morata, G. (2008). Apoptosis in Drosophila: compensatory proliferation and undead cells. Int. J. Dev. Biol. 53, 1341-1437.
25. Martin-Blanco, E., Gampel, A., Ring, J., Virdee, K., Kirov, N., Tolkovsky, A. M. and Martinez-Arias, A. (1998). puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12, 557-570.
26. Martin-Blanco, E., Pastor-Pareja, J. C. and Garcia-Bellido, A. (2000). JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc. Natl. Acad. Sci. USA 97, 7888-7893.
27. Mattila, J., Omelyanchuk, L., Kyttala, S., Turunen, H. and Nokkala, S. (2005). Role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila melanogaster wing imaginal disc. Int. J. Dev. Biol. 49, 391-399.
28. McCawley, L. J. and Matrisian, L. M. (2000). Matrix metalloproteinases: multifunctional contributors to tumor progression. Mol. Med. Today 6, 149-156.
29. McEwen, D. G. and Peifer, M. (2005). Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 132, 3935-3946.
30. Meyer, T. N., Hunt, J., Schwesinger, C. and Denker, B. M. (2003). Galpha12 regulates epithelial cell junctions through Src tyrosine kinases. Am. J. Physiol. Cell Physiol. 285, C1281-C1293.
31. Noirot-Timothee, C., Graf, F. and Noirot, C. (1982). The specialization of septate junctions in regions of tricellular junctions. II. Pleated septate junctions. J. Ultrastruct. Res. 78, 152-165.
32. Oda, H., Uemura, T., Harada, Y., Iwai, Y. and Takeichi, M. (1994). A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165, 716-726.
33. Page-McCaw, A., Serano, J., Sante, J. M. and Rubin, G. M. (2003). Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development. Dev. Cell 4, 95-106.
34. Parnas, D., Haghighi, A. P., Fetter, R. D., Kim, S. W. and Goodman, C. S. (2001). Regulation of postsynaptic structure and protein localization by the Rho-type guanine exchange factor dPix. Neuron 32, 415-424.
35. + ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130, 4963-4974.
36. Perez-Garijo, A., Martin, F. A. and Morata, G. (2004). Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131, 5591-5598.
37. Perez-Garijo, A., Shlevkov, E. and Morata, G. (2009). The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc. Development 136, 1169-1177.
38. Piper, R. C. and Luzio, J. P. (2007). Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr. Opin. Cell Biol. 19, 459-465.
39. Purdy, G. E. and Russell, D. G. (2007). Ubiquitin trafficking to the lysosome: keeping the house tidy and getting rid of unwanted guests. Autophagy 3, 399-401.
40. Raiborg, C. and Stenmark, H. (2009). The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452.
41. Raiborg, C., Bache, K. G., Gillooly, D. J., Madshus, I. H., Stang, E. and Stenmark, H. (2002). Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394-398.
42. Ryoo, H. D., Gorenc, T. and Steller, H. (2004). Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell 7, 491-501.
43. Schulte, J., Tepass, U. and Auld, V. J. (2003). Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J. Cell Biol. 161, 991-1000.
44. Schulte, J., Charish, K., Que, J., Ravn, S., MacKinnon, C. and Auld, V. J. (2006). Gliotactin and Discs large form a protein complex at the tricellular junction of polarized epithelial cells in Drosophila. J. Cell Sci. 119, 4391-4401.
45. Takeda, H., Nagafuchi, A., Yonemura, S., Tsukita, S., Behrens, J., Birchmeier, W. and Tsukita, S. (1995). V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J. Cell Biol. 131, 1839-1847.
46. Tanos, B. and Pendergast, A. M. (2006). Abl tyrosine kinase regulates endocytosis of the epidermal growth factor receptor. J. Biol. Chem. 281, 32714-32723.
47. Tapia, C., Kutzner, H., Mentzel, T., Savic, S., Baumhoer, D. and Glatz, K. (2006). Two mitosis-specific antibodies, MPM-2 and phosphoHistoneH3 (Ser28), allow rapid and precise determination of mitotic activity. Am. J. Surg. Pathol. 30, 83-89.
48. Teleman, A. A. and Cohen, S. M. (2000). Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103, 971-980.
49. Tsukita, S., Furuse, M. and Itoh, M. (2001). Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293.
50. Uhlirova, M. and Bohmann, D. (2006). JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 25, 5294-5304.
51. Venema, D. R., Zeev-Ben-Mordehai, T. and Auld, V. J. (2004). Transient apical polarization of Gliotactin and Coracle is required for parallel alignment of wing hairs in Drosophila. Dev. Biol. 275, 301-314.
52. Wucherpfennig, T., Wilsch-Brauninger, M. and Gonzalez-Gaitan, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161, 609-624.
53. Yu, S. Y., Yoo, S. J., Yang, L., Zapata, C., Srinivasan, A., Hay, B. A. and Baker, N. E. (2002). A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129, 3269-3278.