Lethal giant larvae 2 regulates development of the ciliated organ Kupffer's vesicle

Development (Cambridge)

Volumn 140, Issue 7, 2013, Pages 1550-1559

  Tay, Hwee Goon ^a   Schulze, Sabrina K ^b   Compagnon, Julien ^c   Foley, Fiona C ^a   Heisenberg, Carl Philipp ^c   Yost, H Joseph ^d   Abdelilah Seyfried, Salim ^b   Amack, Jeffrey D ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cilia; Left right asymmetry; Lethal giant larvae 2; Lumenogenesis; Rab11a; Zebrafish

Indexed keywords

PROTEIN LETHAL GIANT LARVAE 2; RAB11 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; GENE INTERACTION; IMMUNOFLUORESCENCE; INNER EAR; KIDNEY; KUPFFER CELL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PRONEPHROS; TIME LAPSE IMAGING; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CELL POLARITY; CILIA; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KUPFFER CELLS; LARVA; MORPHOGENESIS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84875061446     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.087130     Document Type: Article

References (65)

1. Alexander, J. and Stainier, D. Y. (1999). A molecular pathway leading to endoderm formation in zebrafish. Curr. Biol. 9, 1147-1157.
2. Amack, J. D., Wang, X. and Yost, H. J. (2007). Two T-box genes play independent and cooperative roles to regulate morphogenesis of ciliated Kupffer's vesicle in zebrafish. Dev. Biol. 310, 196-210.
3. Atwood, S. X. and Prehoda, K. E. (2009). aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr.Biol. 19, 723-729.
4. Betschinger, J., Mechtler, K. and Knoblich, J. A. (2003). The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422, 326-330.
5. Betschinger, J., Eisenhaber, F. and Knoblich, J. A. (2005). Phosphorylation- induced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae. Curr. Biol. 15, 276-282.
6. Bisgrove, B. W., Essner, J. J. and Yost, H. J. (1999). Regulation of midline development by antagonism of lefty and nodal signaling. Development 126, 3253-3262.
7. Bryant, D. M., Datta, A., Rodríguez-Fraticelli, A. E., Peränen, J., MartínBelmonte, F. and Mostov, K. E. (2010). A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035-1045.
8. Clark, B. S., Winter, M., Cohen, A. R. and Link, B. A. (2011). Generation of Rabbased transgenic lines for in vivo studies of endosome biology in zebrafish. Dev. Dyn. 240, 2452-2465.
9. Cooper, M. S. and D'Amico, L. A. (1996). A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 180, 184-198.
10. Das, A. and Guo, W. (2011). Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 21, 383-386.
11. Datta, A., Bryant, D. M. and Mostov, K. E. (2011). Molecular regulation of lumen morphogenesis. Curr. Biol. 21, R126-R136.
12. Desclozeaux, M., Venturato, J., Wylie, F. G., Kay, J. G., Joseph, S. R., Le, H. T. and Stow, J. L. (2008). Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am. J. Physiol. Cell Physiol. 295, C545-C556.
13. Dodd, M. E., Hatzold, J., Mathias, J. R., Walters, K. B., Bennin, D. A., Rhodes, J., Kanki, J. P., Look, A. T., Hammerschmidt, M. and Huttenlocher, A. (2009). The ENTH domain protein Clint1 is required for epidermal homeostasis in zebrafish. Development 136, 2591-2600.
14. Essner, J. J., Branford, W. W., Zhang, J. and Yost, H. J. (2000). Mesendoderm and left-right brain, heart and gut development are differentially regulated by pitx2 isoforms. Development 127, 1081-1093.
15. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. and Yost, H. J. (2005). Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132, 1247-1260.
16. Ferrante, M. I., Romio, L., Castro, S., Collins, J. E., Goulding, D. A., Stemple, D. L., Woolf, A. S. and Wilson, S. W. (2009). Convergent extension movements and ciliary function are mediated by ofd1, a zebrafish orthologue of the human oral-facial-digital type 1 syndrome gene. Hum. Mol. Genet. 18, 289-303.
17. Fogelgren, B., Lin, S. Y., Zuo, X., Jaffe, K. M., Park, K. M., Reichert, R. J., Bell, P. D., Burdine, R. D. and Lipschutz, J. H. (2011). The exocyst protein Sec10 interacts with Polycystin-2 and knockdown causes PKD-phenotypes. PLoS Genet. 7, e1001361.
18. Gangar, A., Rossi, G., Andreeva, A., Hales, R. and Brennwald, P. (2005). Structurally conserved interaction of Lgl family with SNAREs is critical to their cellular function. Curr. Biol. 15, 1136-1142.
19. Gao, C., Wang, G., Amack, J. D. and Mitchell, D. R. (2010). Oda16/Wdr69 is essential for axonemal dynein assembly and ciliary motility during zebrafish embryogenesis. Dev. Dyn. 239, 2190-2197.
20. Gateff, E. (1978). Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200, 1448-1459.
21. Grosshans, B. L., Andreeva, A., Gangar, A., Niessen, S., Yates, J. R., 3rd, Brennwald, P. and Novick, P. (2006). The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J. Cell Biol. 172, 55-66.
22. Haga, Y., Dominique, V. J., 3rd and Du, S. J. (2009). Analyzing notochord segmentation and intervertebral disc formation using the twhh:gfp transgenic zebrafish model. Transgenic Res. 18, 669-683.
23. Hava, D., Forster, U., Matsuda, M., Cui, S., Link, B. A., Eichhorst, J., Wiesner, B., Chitnis, A. and Abdelilah-Seyfried, S. (2009). Apical membrane maturation and cellular rosette formation during morphogenesis of the zebrafish lateral line. J. Cell Sci. 122, 687-695.
24. Huang, C. J., Tu, C. T., Hsiao, C. D., Hsieh, F. J. and Tsai, H. J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
25. Ishikawa, H. and Marshall, W. F. (2011). Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12, 222-234.
26. Kane, D. A., McFarland, K. N. and Warga, R. M. (2005). Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 132, 1105-1116.
27. Kaplan, N. A., Liu, X. and Tolwinski, N. S. (2009). Epithelial polarity: interactions between junctions and apical-basal machinery. Genetics 183, 897-904.
28. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
29. Klezovitch, O., Fernandez, T. E., Tapscott, S. J. and Vasioukhin, V. (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev. 18, 559-571.
30. Knödler, A., Feng, S., Zhang, J., Zhang, X., Das, A., Peränen, J. and Guo, W. (2010). Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl. Acad. Sci. USA 107, 6346-6351.
31. Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schier, A. F. and Drummond, I. A. (2005). Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921.
32. Krauss, S., Concordet, J. P. and Ingham, P. W. (1993). A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444.
33. Lehman, K., Rossi, G., Adamo, J. E. and Brennwald, P. (1999). Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J. Cell Biol. 146, 125-140.
34. Lock, J. G. and Stow, J. L. (2005). Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin. Mol. Biol. Cell 16, 1744-1755.
35. Long, S., Ahmad, N. and Rebagliati, M. (2003). The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130, 2303-2316.
36. Matsui, T., Thitamadee, S., Murata, T., Kakinuma, H., Nabetani, T., Hirabayashi, Y., Hirate, Y., Okamoto, H. and Bessho, Y. (2011). Canopy1, a positive feedback regulator of FGF signaling, controls progenitor cell clustering during Kupffer's vesicle organogenesis. Proc. Natl. Acad. Sci. USA 108, 9881-9886.
37. Melby, A. E., Warga, R. M. and Kimmel, C. B. (1996). Specification of cell fates at the dorsal margin of the zebrafish gastrula. Development 122, 2225-2237.
38. Müsch, A., Cohen, D., Yeaman, C., Nelson, W. J., Rodriguez-Boulan, E. and Brennwald, P. J. (2002). Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol. Biol. Cell 13, 158-168.
39. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998). Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95, 829-837.
40. Okada, Y., Takeda, S., Tanaka, Y., Izpisúa Belmonte, J. C. and Hirokawa, N. (2005). Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121, 633-644.
41. Oteíza, P., Köppen, M., Concha, M. L. and Heisenberg, C. P. (2008). Origin and shaping of the laterality organ in zebrafish. Development 135, 2807-2813.
42. Oteiza, P., Köppen, M., Krieg, M., Pulgar, E., Farias, C., Melo, C., Preibisch, S., Müller, D., Tada, M., Hartel, S. et al. (2010). Planar cell polarity signaling regulates cell adhesion properties in progenitors of the zebrafish laterality organ. Development 137, 3459-3468.
43. Oztan, A., Silvis, M., Weisz, O. A., Bradbury, N. A., Hsu, S. C., Goldenring, J. R., Yeaman, C. and Apodaca, G. (2007). Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol. Biol. Cell 18, 3978-3992.
44. Plant, P. J., Fawcett, J. P., Lin, D. C., Holdorf, A. D., Binns, K., Kulkarni, S. and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301-308.
45. Rebagliati, M. R., Toyama, R., Fricke, C., Haffter, P. and Dawid, I. B. (1998). Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry. Dev. Biol. 199, 261-272.
46. Reischauer, S., Levesque, M. P., Nüsslein-Volhard, C. and Sonawane, M. (2009). Lgl2 executes its function as a tumor suppressor by regulating ErbB signaling in the zebrafish epidermis. PLoS Genet. 5, e1000720.
47. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A. and Ekker, S. C. (2007). p53 activation by knockdown technologies. PLoS Genet. 3, e78.
48. Rodríguez-Fraticelli, A. E., Gálvez-Santisteban, M. and Martín-Belmonte, F. (2011). Divide and polarize: recent advances in the molecular mechanism regulating epithelial tubulogenesis. Curr. Opin. Cell Biol. 23, 638-646.
49. Sakaguchi, T., Kikuchi, Y., Kuroiwa, A., Takeda, H. and Stainier, D. Y. (2006). The yolk syncytial layer regulates myocardial migration by influencing extracellular matrix assembly in zebrafish. Development 133, 4063-4072.
50. Schweickert, A., Weber, T., Beyer, T., Vick, P., Bogusch, S., Feistel, K. and Blum, M. (2007). Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 17, 60-66.
51. Sharma, N., Berbari, N. F. and Yoder, B. K. (2008). Ciliary dysfunction in developmental abnormalities and diseases. Curr. Top. Dev. Biol. 85, 371-427.
52. Shewan, A. M., Maddugoda, M., Kraemer, A., Stehbens, S. J., Verma, S., Kovacs, E. M. and Yap, A. S. (2005). Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542.
53. Smutny, M., Cox, H. L., Leerberg, J. M., Kovacs, E. M., Conti, M. A., Ferguson, C., Hamilton, N. A., Parton, R. G., Adelstein, R. S. and Yap, A. S. (2010). Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat. Cell Biol. 12, 696-702.
54. Sonawane, M., Carpio, Y., Geisler, R., Schwarz, H., Maischein, H. M. and Nuesslein-Volhard, C. (2005). Zebrafish penner/lethal giant larvae 2 functions in hemidesmosome formation, maintenance of cellular morphology and growth regulation in the developing basal epidermis. Development 132, 3255-3265.
55. Sonawane, M., Martin-Maischein, H., Schwarz, H. and Nüsslein-Volhard, C. (2009). Lgl2 and E-cadherin act antagonistically to regulate hemidesmosome formation during epidermal development in zebrafish. Development 136, 1231-1240.
56. Sripathy, S., Lee, M. and Vasioukhin, V. (2011). Mammalian Llgl2 is necessary for proper branching morphogenesis during placental development. Mol. Cell.Biol. 31, 2920-2933.
57. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol.Cell Biol. 10, 513-525.
58. Strand, D., Jakobs, R., Merdes, G., Neumann, B., Kalmes, A., Heid, H. W., Husmann, I. and Mechler, B. M. (1994). The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol. 127, 1361-1373.
59. Tanentzapf, G. and Tepass, U. (2003). Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5, 46-52.
60. Wan, Q., Liu, J., Zheng, Z., Zhu, H., Chu, X., Dong, Z., Huang, S. and Du, Q. (2012). Regulation of myosin activation during cell-cell contact formation by Par3-Lgl antagonism -entosis without matrix detachment. Mol. Biol. Cell 23, 2076-2091.
61. Wang, G., Cadwallader, A. B., Jang, D. S., Tsang, M., Yost, H. J. and Amack, J. D. (2011a). The Rho kinase Rock2b establishes anteroposterior asymmetry of the ciliated Kupffer's vesicle in zebrafish. Development 138, 45-54.
62. Wang, T., Liu, Y., Xu, X. H., Deng, C. Y., Wu, K. Y., Zhu, J., Fu, X. Q., He, M. and Luo, Z. G. (2011b). Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev. Cell 21, 431-444.
63. Westlake, C. J., Baye, L. M., Nachury, M. V., Wright, K. J., Ervin, K. E., Phu, L., Chalouni, C., Beck, J. S., Kirkpatrick, D. S., Slusarski, D. C. et al. (2011). Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc. Natl. Acad. Sci. USA 108, 2759-2764.
64. Yu, X., Lau, D., Ng, C. P. and Roy, S. (2011). Cilia-driven fluid flow as an epigenetic cue for otolith biomineralization on sensory hair cells of the inner ear. Development 138, 487-494.
65. Zhang, X., Wang, P., Gangar, A., Zhang, J., Brennwald, P., TerBush, D. and Guo, W. (2005). Lethal giant larvae proteins interact with the exocyst complex and are involved in polarized exocytosis. J. Cell Biol. 170, 273-283.