Control of E-cadherin apical localisation and morphogenesis by a SOAP-1/AP-1/clathrin pathway in C. elegans epidermal cells

Development (Cambridge)

Volumn 142, Issue 9, 2015, Pages 1684-1694

  Gillard, Ghislain ^a,b   Shafaq Zadah, Massiullah ^a,b,c   Nicolle, Opheĺie ^a,b   Damaj, Raghida ^a,b   Pećreáux, Jacques ^a,b   Michaux, Greǵoire ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c CNRS UMR3666   (France)

Author keywords

AP 1; Caenorhabditis elegans; E cadherin; Epithelial polarity; Membrane traffic

Indexed keywords

CLATHRIN; PROTEIN; SOAP 1 PROTEIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; UVOMORULIN; ARMADILLO DOMAIN PROTEIN; CADHERIN; CAENORHABDITIS ELEGANS PROTEIN; SOAP-1 PROTEIN, C ELEGANS;

ACTIN FILAMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPIDERMIS CELL; GENE IDENTIFICATION; IN VIVO STUDY; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE; ANIMAL; CELL ADHESION; CELL POLARITY; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; EMBRYOLOGY; EPIDERMIS; METABOLISM; PHYSIOLOGY;

CAENORHABDITIS ELEGANS;

ANIMALS; ARMADILLO DOMAIN PROTEINS; CADHERINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION; CELL POLARITY; CLATHRIN; EMBRYONIC DEVELOPMENT; EPIDERMIS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; RNA INTERFERENCE; TRANSCRIPTION FACTOR AP-1;

EID: 84928599109     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.118216     Document Type: Article

References (66)

1. Achilleos, A., Wehman, A. M. and Nance, J. (2010). PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 137, 1833-1842.
2. Apodaca, G., Gallo, L. I. and Bryant, D. M. (2012). Role of membrane traffic in the generation of epithelial cell asymmetry. Nat. Cell Biol. 14, 1235-1243.
3. Balklava, Z., Pant, S., Fares, H. and Grant, B. D. (2007). Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9, 1066-1073.
4. Baust, T., Czupalla, C., Krause, E., Bourel-Bonnet, L. and Hoflack, B. (2006). Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc. Natl. Acad. Sci. USA 103, 3159-3164.
5. Bembenek, J. N., White, J. G. and Zheng, Y. (2010). A role for separase in the regulation of RAB-11-positive vesicles at the cleavage furrow and midbody. Curr. Biol. 20, 259-264.
6. Blankenship, J. T., Fuller, M. T. and Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120, 3099-3110.
7. Bolte, S. and Cordelières, F. P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
8. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
9. Chisholm, A. D. and Hardin, J. (2005). Epidermal morphogenesis. In WormBook, pp. 1-22.
10. Costa, M., Raich, W., Agbunag, C., Leung, B., Hardin, J. and Priess, J. R. (1998). A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141, 297-308.
11. Deborde, S., Perret, E., Gravotta, D., Deora, A., Salvarezza, S., Schreiner, R. and Rodriguez-Boulan, E. (2008). Clathrin is a key regulator of basolateral polarity. Nature 452, 719-723.
12. Diogon, M., Wissler, F., Quintin, S., Nagamatsu, Y., Sookhareea, S., Landmann, F., Hutter, H., Vitale, N. and Labouesse, M. (2007). The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis. Development 134, 2469-2479.
13. Dwyer, N. D., Adler, C. E., Crump, J. G., L’Etoile, N. D. and Bargmann, C. I. (2001). Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31, 277-287.
14. Fernańdez, G. E. and Payne, G. S. (2006). Laa1p, a conserved AP-1 accessory protein important for AP-1 localization in yeast. Mol. Biol. Cell 17, 3304-3317.
15. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
16. Francis, R. and Waterston, R. H. (1991). Muscle cell attachment in Caenorhabditis elegans. J. Cell Biol. 114, 465-479.
17. Fujita, Y., Krause, G., Scheffner, M., Zechner, D., Leddy, H. E. M., Behrens, J., Sommer, T. and Birchmeier, W. (2002). Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4, 222-231.
18. Gally, C., Wissler, F., Zahreddine, H., Quintin, S., Landmann, F. and Labouesse, M. (2009). Myosin II regulation during C. elegans embryonic elongation: LET-502/ ROCK, MRCK-1 and PAK-1, three kinases with different roles. Development 136, 3109-3119.
19. Georgiou, M., Marinari, E., Burden, J. and Baum, B. (2008). Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr. Biol. 18, 1631-1638.
20. Gonzalez, R. C. and Woods, R. E. (2002). Digital Image Processing. Upper Saddle River, NJ: Prentice Hall.
21. Harris, K. P. and Tepass, U. (2008). Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J. Cell Biol. 183, 1129-1143.
22. Ivanov, A. I. and Naydenov, N. G. (2013). Dynamics and regulation of epithelial adherens junctions: recent discoveries and controversies. Int. Rev. Cell Mol. Biol. 303, 27-99.
23. Kamath, R. S. and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
24. Kapur, J. N., Sahoo, P. K. and Wong, A. K. C. (1985). A new method for gray-level picture thresholding using the entropy of the histogram. Comput. Vis. Graph. Image Process. 29, 273-285.
25. Köppen, M., Simske, J. S., Sims, P. A., Firestein, B. L., Hall, D. H., Radice, A. D., Rongo, C. and Hardin, J. D. (2001). Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3, 983-991.
26. Labbe, J.-C., Pacquelet, A., Marty, T. and Gotta, M. (2006). A genomewide screen for suppressors of par-2 uncovers potential regulators of PAR protein-dependent cell polarity in Caenorhabditis elegans. Genetics 174, 285-295.
27. Langevin, J., Morgan, M. J., Rossé, C., Racine, V., Sibarita, J.-B., Aresta, S., Murthy, M., Schwarz, T., Camonis, J. and Bellaïche, Y. (2005). Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 9, 365-376.
28. Le Bras, S., Rondanino, C., Kriegel-Taki, G., Dussert, A. and Le Borgne, R. (2012). Genetic identification of intracellular trafficking regulators involved in Notch-dependent binary cell fate acquisition following asymmetric cell division. J. Cell Sci. 125, 4886-4901.
29. Legouis, R., Gansmuller, A., Sookhareea, S., Bosher, J. M., Baillie, D. L. and Labouesse, M. (2000). LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat. Cell Biol. 2, 415-422.
30. Leibfried, A., Fricke, R., Morgan, M. J., Bogdan, S. and Bellaiche, Y. (2008). Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr. Biol. 18, 1639-1648.
31. Leung, B., Hermann, G. J. and Priess, J. R. (1999). Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216, 114-134.
32. Levayer, R. and Lecuit, T. (2013). Oscillation and polarity of E-cadherin asymmetries control actomyosin flow patterns during morphogenesis. Dev. Cell 26, 162-175.
33. Levayer, R., Pelissier-Monier, A. and Lecuit, T. (2011). Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529-540.
34. Lieǵeois, S., Benedetto, A., Garnier, J.-M., Schwab, Y. and Labouesse, M. (2006). The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173, 949-961.
35. Ling, K., Bairstow, S. F., Carbonara, C., Turbin, D. A., Huntsman, D. G. and Anderson, R. A. (2007). Type I gamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J. Cell Biol. 176, 343-353.
36. Lui, W. W. Y., Collins, B. M., Hirst, J., Motley, A., Millar, C., Schu, P., Owen, D. J. and Robinson, M. S. (2003). Binding partners for the COOH-terminal appendage domains of the GGAs and gamma-adaptin. Mol. Biol. Cell 14, 2385-2398.
37. Lynch, A. M. and Hardin, J. (2009). The assembly and maintenance of epithelial junctions in C. elegans. Front. Biosci. 14, 1414-1432.
38. Lynch, A. M., Grana, T., Cox-Paulson, E., Couthier, A., Cameron, M., Chin-Sang, I., Pettitt, J. and Hardin, J. (2012). A genome-wide functional screen shows MAGI-1 is an L1CAM-dependent stabilizer of apical junctions in C. elegans. Curr. Biol. 22, 1891-1899.
39. Michaux, G., Gansmuller, A., Hindelang, C. and Labouesse, M. (2000). CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr. Biol. 10, 1098-1107.
40. Montpetit, A., Côté, S., Brustein, E., Drouin, C. A., Lapointe, L., Boudreau, M., Meloche, C., Drouin, R., Hudson, T. J., Drapeau, P. et al. (2008). Disruption of AP1S1, causing a novel neurocutaneous syndrome, perturbs development of the skin and spinal cord. PLoS Genet. 4, e1000296.
41. Mullen, G. P., Rogalski, T. M., Bush, J. A., Gorji, P. R. and Moerman, D. G. (1999). Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol. Biol. Cell 10, 3205-3221.
42. Nance, J., Munro, E. M. and Priess, J. R. (2003). C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130, 5339-5350.
43. Palacios, F., Price, L., Schweitzer, J., Collard, J. G. and D’Souza-Schorey, C. (2001). An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
44. Patel, F. B., Bernadskaya, Y. Y., Chen, E., Jobanputra, A., Pooladi, Z., Freeman, K. L., Gally, C., Mohler, W. A. and Soto, M. C. (2008). The WAVE/SCAR complex promotes polarized cell movements and actin enrichment in epithelia during C. elegans embryogenesis. Dev. Biol. 324, 297-309.
45. Pettitt, J., Cox, E. A., Broadbent, I. D., Flett, A. and Hardin, J. (2003). The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J. Cell Biol. 162, 15-22.
46. Priess, J. R. and Hirsh, D. I. (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117, 156-173.
47. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167-174.
48. Sato, M., Grant, B. D., Harada, A. and Sato, K. (2008). Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J. Cell Sci. 121, 3177-3186.
49. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
50. Shafaq-Zadah, M., Brocard, L., Solari, F. and Michaux, G. (2012). AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development 139, 2061-2070.
51. Shaye, D. D. and Greenwald, I. (2011). OrthoList: a compendium of C. elegans genes with human orthologs. PLoS ONE 6, e20085.
52. Shaye, D. D., Casanova, J. and Llimargas, M. (2008). Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat. Cell Biol. 10, 964-970.
53. Shim, J., Sternberg, P. W. and Lee, J. (2000). Distinct and redundant functions of mu1 medium chains of the AP-1 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol. Biol. Cell 11, 2743-2756.
54. Simske, J. S., Köppen, M., Sims, P., Hodgkin, J., Yonkof, A. and Hardin, J. (2003). The cell junction protein VAB-9 regulates adhesion and epidermal morphology in C. elegans. Nat. Cell Biol. 5, 619-625.
55. Soto, M. C., Qadota, H., Kasuya, K., Inoue, M., Tsuboi, D., Mello, C. C. and Kaibuchi, K. (2002). The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16, 620-632.
56. St Johnston, D. and Ahringer, J. (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757-774.
57. Stetak, A. and Hajnal, A. (2011). The C. elegans MAGI-1 protein is a novel component of cell junctions that is required for junctional compartmentalization. Dev. Biol. 350, 24-31.
58. Sugiyama, Y., Nishimura, A. and Ohno, S. (2008). Symmetrically dividing cell specific division axes alteration observed in proteasome depleted C. elegans embryo. Mech. Dev. 125, 743-755.
59. Vincent, L. and Soille, P. (1991). Watersheds in digital spaces: an efficient algorithm based on immersion simulations. IEEE Trans. Pattern Anal. Mach. Intell. 13, 583-598.
60. Wang, Q., Chen, X.-W. and Margolis, B. (2007). PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol. Biol. Cell 18, 874-885.
61. Winter, J. F., Höpfner, S., Korn, K., Farnung, B. O., Bradshaw, C. R., Marsico, G., Volkmer, M., Habermann, B. and Zerial, M. (2012). Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11-recycling endosome positioning and apicobasal cell polarity. Nat. Cell Biol. 14, 666-676.
62. Xiong, X., Xu, Q., Huang, Y., Singh, R. D., Anderson, R., Leof, E., Hu, J. and Ling, K. (2012). An association between type Igamma PI4P 5-kinase and Exo70 directs E-cadherin clustering and epithelial polarization. Mol. Biol. Cell 23, 87-98.
63. Yochem, J., Tuck, S., Greenwald, I. and Han, M. (1999). A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 126, 597-606.
64. Zhang, H., Squirrell, J. M. and White, J. G. (2008). RAB-11 permissively regulates spindle alignment by modulating metaphase microtubule dynamics in Caenorhabditis elegans early embryos. Mol. Biol. Cell 19, 2553-2565.
65. Zhang, H., Abraham, N., Khan, L. A., Hall, D. H., Fleming, J. T. and Göbel, V. (2011). Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell Biol. 13, 1189-1201.
66. Zhang, H., Kim, A., Abraham, N., Khan, L. A., Hall, D. H., Fleming, J. T. and Gobel, V. (2012). Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 139, 2071-2083.