Dynamic microtubules at the vegetal cortex predict the embryonic axis in zebrafish

Development (Cambridge)

Volumn 139, Issue 19, 2012, Pages 3644-3652

  Tran, Long Duc ^a,b   Hino, Hiromu ^c   Quach, Helen ^a   Lim, Shimin ^a,d   Shindo, Asako ^e   Mimori Kiyosue, Yuko ^f   Mione, Marina ^g   Ueno, Naoto ^e   Winkler, Christoph ^b   Hibi, Masahiko ^c,f   Sampath, Karuna ^a,b,d  

^a TEMASEK LIFE SCIENCES LABORATORY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NAGOYA UNIVERSITY   (Japan)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^f RIKEN Center for Biosystems Dynamics Research   (Japan)

^g KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Cortical rotation; Dorsoventral patterning; Embryonic axes; Microtubule dynamics; Polarity; wnt8a RNA; Zebrafish

Indexed keywords

CALCIUM ION; WNT8A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTODERM; BRAIN CORTEX; CALCIUM SIGNALING; CELL DIVISION; CONTROLLED STUDY; EMBRYO AXIS; FERTILIZATION; HUMAN; IN VIVO STUDY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MICROARRAY; RNA TRANSLATION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLASTODERM; BODY PATTERNING; CALCIUM SIGNALING; CEREBRAL CORTEX; EMBRYO, NONMAMMALIAN; FEMALE; FERTILIZATION; FORECASTING; GREEN FLUORESCENT PROTEINS; MALE; MICROTUBULES; SPERM-OVUM INTERACTIONS; XENOPUS; ZEBRAFISH;

ANIMALIA; DANIO RERIO;

EID: 84865855454     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.082362     Document Type: Article

References (70)

1. Abraham, V. C., Miller, A. L. and Fluck, R. A. (1995). Microtubule arrays during ooplasmic segregation in the medaka fish egg (Oryzias latipes). Biol. Bull. 188, 136-145.
2. Brendza, R. P., Serbus, L. R., Duffy, J. B. and Saxton, W. M. (2000). A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289, 2120-2122.
3. Bullock, S. L. and Ish-Horowicz, D. (2001). Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature 414, 611-616.
4. Cha, B. J., Koppetsch, B. S. and Theurkauf, W. E. (2001). In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106, 35-46.
5. Clavert, J. (1962). Symmetrization of the egg of vertebrates. Adv. Morphol. 2, 27-60.
6. Delanoue, R. and Davis, I. (2005). Dynein anchors its mRNA cargo after apical transport in the Drosophila blastoderm embryo. Cell 122, 97-106.
7. Dettlaff, T. A. (1962). Cortical changes in acipenserid eggs during fertilization and artificial activation. J. Embryol. Exp. Morphol. 10, 1-26.
8. Dougan, S. T., Warga, R. M., Kane, D. A., Schier, A. F. and Talbot, W. S. (2003). The role of the zebrafish nodal-related genes squint and cyclops in patterning of mesendoderm. Development 130, 1837-1851.
9. Du, S., Draper, B. W., Mione, M., Moens, C. B. and Bruce, A. (2012). Differential regulation of epiboly initiation and progression by zebrafish Eomesodermin A. Dev. Biol. 362, 11-23.
10. Elinson, R. P. and Rowning, B. (1988). A transient array of parallel microtubules in frog eggs: potential tracks for a cytoplasmic rotation that specifies the dorsoventral axis. Dev. Biol. 128, 185-197.
11. Elinson, R. P. and Pasceri, P. (1989). Two UV-sensitive targets in dorsoanterior specification of frog embryos. Development 106, 511-518.
12. Elinson, R. P. and Palecek, J. (1993). Independence of two microtubule systems in fertilized frog eggs: the sperm aster and the vegetal parallel array. Dev. Genes Evol. 202, 224-232.
13. Elinson, R. P. and Ninomiya, H. (2003). Parallel microtubules and other conserved elements of dorsal axial specification in the direct developing frog, Eleutherodactylus coqui. Dev. Genes Evol. 213, 28-34.
14. Emelyanov, A., Gao, Y., Naqvi, N. I. and Parinov, S. (2006). Trans-kingdom transposition of the maize dissociation element. Genetics 174, 1095-1104
15. Gerhart, J. (2004). Symmetry breaking in the egg of xenopus. In Gastrulation: From Cells to Embryos (ed. C. D. Stern), pp. 341-351. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
16. Gerhart, J., Ubbels, G., Black, S., Hara, K. and Kirschner, M. (1981). A reinvestigation of the role of the grey crescent in axis formation in Senopus laevis. Nature 292, 511-516.
17. Gerhart, J., Danilchik, M., Doniach, T., Roberts, S., Rowning, B. and Stewart, R. (1989). Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107 Suppl., 37-51.
18. Gilligan, P. C., Kumari, P., Lim, S., Cheong, A., Chang, A. and Sampath, K. (2011). Conservation defines functional motifs in the squint/nodal-related 1 RNA dorsal localization element. Nucleic Acids Res. 39, 3340-3349.
19. Glotzer, J. B., Saffrich, R., Glotzer, M. and Ephrussi, A. (1997). Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes. Curr. Biol. 7, 326-337
20. Gore, A. V. and Sampath, K. (2002). Localization of transcripts of the zebrafish morphogen Squint is dependent on egg activation and the microtubule cytoskeleton. Mech. Dev. 112, 153-156.
21. Gore, A. V., Maegawa, S., Cheong, A., Gilligan, P. C., Weinberg, E. S. and Sampath, K. (2005). The zebrafish dorsal axis is apparent at the four-cell stage. Nature 438, 1030-1035.
22. Guzik, B. W. and Goldstein, L. S. (2004). Microtubule-dependent transport in neurons: steps towards an understanding of regulation, function and dysfunction. Curr. Opin. Cell Biol. 16, 443-450.
23. Hart, N. H. and Donovan, M. (1983). Fine-structure of the chorion and site of sperm entry in the egg of Brachydanio. J. Exp. Zool. 227, 277-296.
24. Houliston, E. and Elinson, R. P. (1991). Patterns of microtubule polymerization relating to cortical rotation in Xenopus laevis eggs. Development 112, 107-117.
25. Hsu, H. J., Liang, M. R., Chen, C. T. and Chung, B. C. (2006). Pregnenolone stabilizes microtubules and promotes zebrafish embryonic cell movement. Nature 439, 480-483.
26. Jesuthasan, S. and Strahle, U. (1997). Dynamic microtubules and specification of the zebrafish embryonic axis. Curr. Biol. 7, 31-42.
27. Johnson, A. D. and Krieg, P. A. (1994). Pxex, a vector for efficient expression of cloned sequences in xenopus embryos. Gene 147, 223-226.
28. Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N. and Mishina, M. (2004). A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 7, 133-144
29. Lachnit, M., Kur, E. and Driever, W. (2008). Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos. Dev. Biol. 315, 1-17.
30. Lall, S., Francis-Lang, H., Flament, A., Norvell, A., Schupbach, T. and IshHorowicz, D. (1999). Squid hnRNP protein promotes apical cytoplasmic transport and localization of Drosophila pair-rule transcripts. Cell 98, 171-180
31. Lecuyer, E., Yoshida, H., Parthasarathy, N., Alm, C., Babak, T., Cerovina, T., Hughes, T. R., Tomancak, P. and Krause, H. M. (2007). Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187.
32. Lee, H. X., Ambrosio, A. L., Reversade, B. and De Robertis, E. M. (2006). Embryonic dorsal-ventral signaling: secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell 124, 147-159.
33. Lee, K. W., Webb, S. E. and Miller, A. L. (1999). A wave of free cytosolic calcium traverses zebrafish eggs on activation. Dev. Biol. 214, 168-180.
34. Leung, C. F., Webb, S. E. and Miller, A. L. (1998). Calcium transients accompany ooplasmic segregation in zebrafish embryos. Dev. Growth Differ. 40, 313-326
35. Lim, S., Kumari, P., Gilligan, P., Quach, H. N., Mathavan, S. and Sampath, K. (2012). Dorsal activity of maternal squint is mediated by a non-coding function of the RNA. Development 139, 2903-2915.
36. Lin, K., Wang, S., Julius, M. A., Kitajewski, J., Moos, M., Jr and Luyten, F. P. (1997). The cysteine-rich frizzled domain of Frzb-1 is required and sufficient for modulation of Wnt signaling. Proc. Natl. Acad. Sci. USA 94, 11196-11200.
37. Lu, F. I., Thisse, C. and Thisse, B. (2011). Identification and mechanism of regulation of the zebrafish dorsal determinant. Proc. Natl. Acad. Sci. USA 108, 15876-15880.
38. Mei, W., Lee, K. W., Marlow, F. L., Miller, A. L. and Mullins, M. C. (2009). hnRNP I is required to generate the Ca2+ signal that causes egg activation in zebrafish. Development 136, 3007-3017.
39. Meijering, E., Dzyubachyk, O. and Smal, I. (2012). Methods for cell and particle tracking. Methods Enzymol. 504, 183-200.
40. Mii, Y. and Taira, M. (2009). Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 136, 4083-4088.
41. Miller, J. R., Rowning, B. A., Larabell, C. A., Yang-Snyder, J. A., Bates, R. L. and Moon, R. T. (1999). Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. J. Cell Biol. 146, 427-437.
42. Mimori-Kiyosue, Y., Shiina, N. and Tsukita, S. (2000). The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10, 865-868.
43. Munoz, A., Blu, T. and Unser, M. (2001). Least-squares image resizing using finite differences. IEEE Trans. Image Process 10, 1365-1378.
44. Nojima, H., Rothhamel, S., Shimizu, T., Kim, C. H., Yonemura, S., Marlow, F. L. and Hibi, M. (2010). Syntabulin, a motor protein linker, controls dorsal determination. Development 137, 923-933.
45. Onichtchouk, D., Aduroja, K., Belting, H. G., Gnugge, L. and Driever, W. (2003). Transgene driving GFP expression from the promoter of the zona pellucida gene zpc is expressed in oocytes and provides an early marker for gonad differentiation in zebrafish. Dev. Dyn. 228, 393-404.
46. Peng, G. and Westerfield, M. (2006). Lhx5 promotes forebrain development and activates transcription of secreted Wnt antagonists. Development 133, 3191-3200.
47. Pera, E. M. and De Robertis, E. M. (2000). A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1. Mech. Dev. 96, 183-195.
48. Ploper, D., Lee, H. X. and De Robertis, E. M. (2011). Dorsal-ventral patterning: Crescent is a dorsally secreted Frizzled-related protein that competitively inhibits Tolloid proteases. Dev. Biol. 352, 317-328.
49. Pokrywka, N. J. and Stephenson, E. C. (1991). Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 113, 55-66
50. Pokrywka, N. J. and Stephenson, E. C. (1995). Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167, 363-370.
51. Riechmann, V. and Ephrussi, A. (2001). Axis formation during Drosophila oogenesis. Curr. Opin. Genet. Dev. 11, 374-383.
52. Rowning, B. A., Wells, J., Wu, M., Gerhart, J. C., Moon, R. T. and Larabell, C. A. (1997). Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs. Proc. Natl. Acad. Sci. USA 94, 1224-1229.
53. Schnorrer, F., Bohmann, K. and Nusslein-Volhard, C. (2000). The molecular motor dynein is involved in targeting swallow and bicoid RNA to the anterior pole of Drosophila oocytes. Nat. Cell Biol. 2, 185-190.
54. Solnica-Krezel, L. and Driever, W. (1994). Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120, 2443-2455.
55. Steinhauer, J. and Kalderon, D. (2006). Microtubule polarity and axis formation in the Drosophila oocyte. Dev. Dyn. 235, 1455-1468.
56. Stepanova, T., Slemmer, J., Hoogenraad, C. C., Lansbergen, G., Dortland, B., De Zeeuw, C. I., Grosveld, F., van Cappellen, G., Akhmanova, A. and Galjart, N. (2003). Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655-2664.
57. Strahle, U. and Jesuthasan, S. (1993). Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119, 909-919.
58. Streisinger, G., Walker, C., Dower, N., Knauber, D. and Singer, F. (1981). Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291, 293-296.
59. Takesono, A., Moger, J., Faroq, S., Cartwright, E., Dawid, I. B., Wilson, S. W. and Kudoh, T. (2012). Solute carrier family 3 member 2 (Slc3a2) controls yolk syncytial layer (YSL) formation by regulating microtubule networks in the zebrafish embryo. Proc. Natl. Acad. Sci. USA 109, 3371-3376.
60. Tendeng, C. and Houart, C. (2006). Cloning and embryonic expression of five distinct sfrp genes in the zebrafish Danio rerio. Gene Expr. Patterns 6, 761-771
61. Topczewski, J. and Solnica-Krezel, L. (1999). Cytoskeletal dynamics of the zebrafish embryo. Methods Cell Biol. 59, 205-226.
62. Vincent, J. P., Oster, G. F. and Gerhart, J. C. (1986). Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. Dev. Biol. 113, 484-500.
63. Wagner, D. S., Dosch, R., Mintzer, K. A., Wiemelt, A. P. and Mullins, M. C. (2004). Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev. Cell 6, 781-790.
64. Wang, S., Krinks, M., Lin, K., Luyten, F. P. and Moos, M., Jr (1997). Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757-766.
65. Weaver, C., Farr, G. H., 3rd, Pan, W., Rowning, B. A., Wang, J., Mao, J., Wu, D., Li, L., Larabell, C. A. and Kimelman, D. (2003). GBP binds kinesin light chain and translocates during cortical rotation in Xenopus eggs. Development 130, 5425-5436.
66. Weil, T. T., Forrest, K. M. and Gavis, E. R. (2006). Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev. Cell 11, 251-262
67. Westerfield, M. (2007). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 5th Edition: University of Oregon Press
68. Westfall, T. A., Hjertos, B. and Slusarski, D. C. (2003). Requirement for intracellular calcium modulation in zebrafish dorsal-ventral patterning. Dev. Biol. 259, 380-391.
69. Wilkie, G. S. and Davis, I. (2001). Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105, 209-219.
70. Zimyanin, V. L., Belaya, K., Pecreaux, J., Gilchrist, M. J., Clark, A., Davis, I. and St Johnston, D. (2008). In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134, 843-853.