Abstract
In Xenopus, Dishevelled (Xdsh) signaling is required for both neural tube closure and neural convergent extension, but the connection between these two morphogenetic processes remains unclear. Indeed normal neurulation requires several different cell polarity decisions, any of which may require Xdsh signaling. In this paper we address two issues: (1) which aspects of normal neurulation require Xdsh function; and (2) what role convergent extension plays in the closure of the neural tube. We show that Xdsh signaling is not required for neural fold elevation, medial movement or fusion. Disruption of Xdsh signaling therefore provides a specific tool for uncoupling convergent extension from other processes of neurulation. Using disruption of Xdsh signaling, we demonstrate that convergent extension is crucial to tube closure. Targeted injection revealed that Xdsh function was required specifically in the midline for normal neural tube closure. We suggest that the inherent movement of the neural folds can accomplish only a finite amount of medial progress and that convergent extension of the midline is necessary to reduce the distance between the nascent neural folds, allowing them to meet and fuse. Similar results with Xenopus strabismus implicate the planar cell polarity (PCP) signaling cascade in neural convergent extension and tube closure. Together, these data demonstrate that PCP-mediated convergent extension movements are crucial to proper vertebrate neurulation.
References
71
Referenced
279
-
Alvarez, I. S. and Schoenwolf, G. C. (1992). Expansion of surface epithelium provides the major extrinsic force for bending of the neural plate. J. Exp. Zool.261,340-348.
(
10.1002/jez.1402610313
) -
Appel, B., Fritz, A., Westerfield, M., Grunwald, D. J., Eisen,J. S. and Riley, B. B. (1999). Delta-mediated specification of midline cell fates in zebrafish embryos. Curr. Biol.9,247-256.
(
10.1016/S0960-9822(99)80113-4
) -
Bang, A. G., Papalopulu, N., Goulding, M. D. and Kintner, C.(1999). Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm.Dev. Biol.212,366-380.
(
10.1006/dbio.1999.9319
) -
Bellaiche, Y., Gho, M., Kaltschmidt, J. A., Brand, A. H. and Schweisguth, F. (2001). Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat. Cell Biol.3, 50-57.
(
10.1038/35050558
) -
Botto, L. D., Moore, C. A., Khoury, M. J. and Erickson, J. D. (1999). Neural-tube defects. New Engl. J. Med.341,1509-1519.
(
10.1056/NEJM199911113412006
) -
Bronner-Fraser, M. and Fraser, S. E. (1997). Differentiation of the vertebrate neural tube. Curr. Opin. Cell Biol.9,885-891.
(
10.1016/S0955-0674(97)80092-0
) -
Brouns, M. R., Matheson, S. F., Hu, K. Q., Delalle, I.,Caviness, V. S., Silver, J., Bronson, R. T. and Settleman, J.(2000). The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development.Development127,4891-4903.
(
10.1242/dev.127.22.4891
) -
Brun, R. B. and Garson, J. A. (1983). Neurulation in the Mexican salamander (Ambystoma mexicanum): a drug study and cell shape analysis of the epidermis and the neural plate. J. Embryol. Exp. Morphol.74,275-295.
(
10.1242/dev.74.1.275
) -
Burnside, M. B. and Jacobson, A. G. (1968). Analysis of morphogenetic movements in the neural plate of the newt Taricha torosa. Dev. Biol.18,537-552.
(
10.1016/0012-1606(68)90025-0
) -
Cooper, M. T. and Bray, S. J. (1999). Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye.Nature397,526-530.
(
10.1038/17395
) -
Copp, A. J., Checiu, I. and Henson, J. N.(1994). Developmental basis of severe neural tube defects in the loop-tail (Lp) mutant mouse: use of microsatellite DNA markers to identify embryonic genotype. Dev. Biol.165, 20-29.
(
10.1006/dbio.1994.1230
) -
Darken, R. S., Scola, A. M., Rakeman, A. S., Das, G., Mlodzik,M. and Wilson, P. A. (2002). The planar polarity gene strabismus regulates convergent extension movements in Xenopus.EMBO J.21,976-985.
(
10.1093/emboj/21.5.976
) -
Davidson, L. A. and Keller, R. E. (1999). Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension.Development126,4547-4556.
(
10.1242/dev.126.20.4547
) -
de la Torre, J. R., Hopker, V. H., Ming, G. L., Poo, M. M.,Tessier-Lavigne, M., Hemmati-Brivanlou, A. and Holt, C. E.(1997). Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron19,1211-1224.
(
10.1016/S0896-6273(00)80413-4
) -
Domingo, C. and Keller, R. (1995). Induction of notochord cell intercalation behavior and differentiation by progressive signals in the gastrula of Xenopus laevis. Development121,3311-3321.
(
10.1242/dev.121.10.3311
) -
Elul, T. and Keller, R. (2000). Monopolar protrusive activity: a new morphogenic cell behavior in the neural plate dependent on vertical interactions with the mesoderm in Xenopus.Dev. Biol.224,3-19.
(
10.1006/dbio.2000.9746
) -
Fanto, M. and Mlodzik, M. (1999). Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature397,523-526.
(
10.1038/17389
) -
Fetka, I., Doederlein, G. and Bouwmeester, T.(2000). Neuroectodermal specification and regionalization of the Spemann organizer in Xenopus. Mech. Dev.93, 49-58.
(
10.1016/S0925-4773(00)00265-3
) -
George, T. M. and Speer, M. C. (2000). Genetic and embryological approaches to studies of neural tube defects: a critical review. NTD Collaborative Group. Neurol. Res.22,117-122.
(
10.1080/01616412.2000.11741046
) -
Gerrelli, D. and Copp, A. J. (1997). Failure of neural tube closure in the loop-tail (Lp) mutant mouse: analysis of the embryonic mechanism. Dev. Brain Res.102,217-224.
(
10.1016/S0165-3806(97)00099-0
) -
Goto, T. and Keller, R. (2002). The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev. Biol.247,165-181.
(
10.1006/dbio.2002.0673
) -
Greene, N. D., Gerrelli, D., van Straaten, H. W. and Copp, A. J. (1998). Abnormalities of floor plate, notochord and somite differentiation in the loop-tail (Lp) mouse: a model of severe neural tube defects. Mech. Dev.73,59-72.
(
10.1016/S0925-4773(98)00029-X
) - Hamblet, N. S., Lijam, N., Ruiz-Lozano, P., Wang, J., Yang, Y.,Chien, K. R., Sussuman, D. J. and Wynshaw-Boris, A. (2002). Dishevelled-2 is essential for cardiac outflow tract development, somite segmentation and neural tube clsoure. Development129,5827-5838.
-
Harris, M. J. (2001). Why are the genes that cause risk of human neural tube defects so hard to find?Teratology63,165-166.
(
10.1002/tera.1030
) -
Harris, M. J. and Juriloff, D. M. (1999). Mini-review: toward understanding mechanisms of genetic neural tube defects in mice. Teratology60,292-305.
(
10.1002/(SICI)1096-9926(199911)60:5<292::AID-TERA10>3.0.CO;2-6
) -
Hirose, G. and Jacobson, M. (1979). Clonal organization of the central nervous system of the frog. I. Clones stemming from individual blastomeres of the 16-cell and earlier stages. Dev. Biol.71,191-202.
(
10.1016/0012-1606(79)90163-5
) -
Holmberg, J., Clarke, D. L. and Frisen, J.(2000). Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature408,203-206.
(
10.1038/35041577
) - Jacobson, A. G. (1978). Some forces that shape the nervous system. Zoon6, 13-21.
-
Jacobson, A. G. (1984). Further evidence that formation of the neural tube requires elongation of the nervous system.J. Exp. Zool.230,23-28.
(
10.1002/jez.1402300105
) -
Jacobson, A. G. and Gordon, R. (1976). Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. J. Exp. Zool.197,191-246.
(
10.1002/jez.1401970205
) - Jacobson, C.-O. and Jacobson, A. (1973). Studies on the morphogenetic movements during neural tube closure in amphibia.Zoon1,17-21.
-
Keller, R., Davidson, L., Edlund, A., Elul, T., Ezin, M., Shook,D. and Skoglund, P. (2000). Mechanisms of convergence and extension by cell intercalation. Philos. Trans. R. Soc. Lond. B Biol. Sci.355,897-922.
(
10.1098/rstb.2000.0626
) -
Keller, R., Shih, J. and Sater, A. (1992). The cellular basis of the convergence and extension of the Xenopus neural plate.Dev. Dyn.193,199-217.
(
10.1002/aja.1001930302
) -
Kibar, Z., Vogan, K. J., Groulx, N., Justice, M. J., Underhill,D. A. and Gros, P. (2001). Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet.28,251-255.
(
10.1038/90081
) -
Kirillova, I., Novikova, I., Auge, J., Audollent, S., Esnault,D., Encha-Razavi, F., Lazjuk, G., Attie-Bitach, T. and Vekemans, M.(2000). Expression of the sonic hedgehog gene in human embryos with neural tube defects. Teratology61,347-354.
(
10.1002/(SICI)1096-9926(200005)61:5<347::AID-TERA6>3.0.CO;2-#
) -
Krasnow, R. E. and Adler, P. N. (1994). A single frizzled protein has a dual function in tissue polarity.Development120,1883-1893.
(
10.1242/dev.120.7.1883
) -
Lawson, A., Anderson, H. and Schoenwolf, G. C.(2001). Cellular mechanisms of neural fold formation and morphogenesis in the chick embryo. Anat. Rec.262,153-168.
(
10.1002/1097-0185(20010201)262:2<153::AID-AR1021>3.0.CO;2-W
) -
Layton, W. M., Jr and Smith, J. M. (1977). Craniomyeloschisis: a spontaneous mutation of the rat.Teratology15,171-177.
(
10.1002/tera.1420150207
) -
Manning, S. M., Jennings, R. and Madsen, J. R.(2000). Pathophysiology, prevention, and potential treatment of neural tube defects. Ment. Retard. Dev. Disabil. Res. Rev.6,6-14.
(
10.1002/(SICI)1098-2779(2000)6:1<6::AID-MRDD2>3.0.CO;2-B
) -
Marin-Padilla, M. (1966). Study of the vertebral column in human craniorhachischisis. Acta. Anat.63,32-48.
(
10.1159/000142778
) - Marsden, M. and DeSimone, D. W. (2001). Regulation of cell polarity, radial intercalation and epiboly in Xenopus:novel roles for integrin and fibronectin. Development128,3635-3647.
-
Mizuseki, K., Kishi, M., Matsui, M., Nakanishi, S. and Sasai,Y. (1998). Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development125,579-587.
(
10.1242/dev.125.4.579
) -
Moury, J. D. and Schoenwolf, G. C. (1995). Cooperative model of epithelial shaping and bending during avian neurulation:autonomous movements of the neural plate, autonomous movements of the epidermis, and interactions in the neural plate/epidermis transition zone.Dev. Dyn.204,323-337.
(
10.1002/aja.1002040310
) -
Murdoch, J. N., Doudney, K., Paternotte, C., Copp, A. J. and Stanier, P. (2001). Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum. Mol. Genet.10,2593-2601.
(
10.1093/hmg/10.22.2593
) -
Nakatsu, T., Uwabe, C. and Shiota, K. (2000). Neural tube closure in humans initiates at multiple sites: evidence from human embryos and implications for the pathogenesis of neural tube defects.Anat. Embryol.201,455-466.
(
10.1007/s004290050332
) -
Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P.(1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet.21,444-448.
(
10.1038/7788
) - Nieuwkoop, P. D. and Faber, J. (1994).Normal Table of Xenopus laevis (Daudin). New York:Garland.
-
Poznanski, A., Minsuk, S., Stathopoulos, D. and Keller, R.(1997). Epithelial cell wedging and neural trough formation are induced planarly in Xenopus, without persistent vertical interactions with mesoderm. Dev. Biol.189,256-269.
(
10.1006/dbio.1997.8678
) -
Rothbächer, U., Laurent, M. N., Deardorff, M. A., Klein, P. S., Cho, K. W. Y. and Fraser, S. E. (2000). Dishevelled phosphorylation, subcellular localization and homomerization regulate its role in early embryogenesis. EMBO J.19,1010-1022.
(
10.1093/emboj/19.5.1010
) -
Saraga-Babic, M., Sapunar, D. and Stefanovic, V.(1993). Histological features of axial structures during embryonic and fetal stages of human craniorachischisis. Acta Neuropathol.86,289-294.
(
10.1007/BF00304144
) -
Schoenwolf, G. C. and Alvarez, I. S. (1989). Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development106,427-439.
(
10.1242/dev.106.3.427
) - Schroeder, T. E. (1970). Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy.J. Embryol. Exp. Morphol.23,427-462.
-
Selman, G. G. (1958). The forces producing neural closure in amphibia. J. Embryol. Exp. Morphol.6, 448-465.
(
10.1242/dev.6.3.448
) -
Shih, J. and Keller, R. (1992). Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis.Development116,915-930.
(
10.1242/dev.116.4.915
) - Sive, H. L., Grainger, R. M. and Harland, R. M.(2000). Early Development of Xenopus laevis: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
-
Smith, J. L. and Schoenwolf, G. C. (1997). Neurulation: coming to closure. Trends Neurosci.20,510-517.
(
10.1016/S0166-2236(97)01121-1
) -
Smith, L. J. and Stein, K. F. (1962). Axial elongation in the mouse and its retardation in homozygous looptail mice.J. Embryol. Exp. Morphol.10, 73-87.
(
10.1242/dev.10.1.73
) -
Sokol, S. Y. (1996). Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol.6,1456-1467.
(
10.1016/S0960-9822(96)00750-6
) -
Solter, M., Koster, M., Hollemann, T., Brey, A., Pieler, T. and Knochel, W. (1999). Characterization of a subfamily of related winged helix genes, XFD-12/12'/12' (XFLIP), during Xenopus embryogenesis. Mech. Dev.89,161-165.
(
10.1016/S0925-4773(99)00195-1
) -
Sun, T. Q., Lu, B., Feng, J. J., Reinhard, C., Jan, Y. N.,Fantl, W. J. and Williams, L. T. (2001). PAR-1 is a Dishevelled-associated kinase and a positive regulator of Wnt signalling.Nat. Cell Biol.3,628-636.
(
10.1038/35083016
) - Tada, M. and Smith, J. C. (2000). Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via dishevelled, but not through the canonical Wnt pathway.Development127,2227-2238.
-
Theisen, H., Purcell, J., Bennett, M., Kansagara, D., Syed, A. and Marsh, J. L. (1994). Dishevelled is required during wingless signaling to establish both cell polarity and cell identity.Development120,347-360.
(
10.1242/dev.120.2.347
) -
van Straaten, H. W., Jaskoll, T., Rousseau, A. M.,Terwindt-Rouwenhorst, E. A., Greenberg, G., Shankar, K. and Melnick, M.(1993). Raphe of the posterior neural tube in the chick embryo:its closure and reopening as studied in living embryos with a high definition light microscope. Dev. Dyn.198, 65-76.
(
10.1002/aja.1001980107
) -
van Straaten, H. W., Janssen, H. C., Peeters, M. C., Copp, A. J. and Hekking, J. W. (1996). Neural tube closure in the chick embryo is multiphasic. Dev. Dyn.207,309-318.
(
10.1002/(SICI)1097-0177(199611)207:3<309::AID-AJA8>3.0.CO;2-L
) -
Wallingford, J. B., Fraser, S. E. and Harland, R. M.(2002). Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell2, 695-706.
(
10.1016/S1534-5807(02)00197-1
) - Wallingford, J. B. and Harland, R. M. (2001). Xenopus dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis.Development128,2581-2592.
-
Wallingford, J. B., Rowning, B. A., Vogeli, K. M.,Rothbächer, U., Fraser, S. E. and Harland, R. M. (2000). Dishevelled controls cell polarity during Xenopus gastrulation.Nature405,81-85.
(
10.1038/35011077
) -
Wiggan, O. and Hamel, P. A. (2002). Pax3 regulates morphogenetic cell behavior in vitro coincident with activation of a PCP/non-canonical Wnt-signaling cascade. J. Cell Sci.115,531-541.
(
10.1242/jcs.115.3.531
) -
Wilson, D. B. and Wyatt, D. P. (1992). Abnormal elevation of the neural folds in the loop-tail mutant mouse. Acta Anat.143,89-95.
(
10.1159/000147234
) -
Zhang, J., Hagopian-Donaldson, S., Serbedzija, G., Elsemore, J.,Plehn-Dujowich, D., McMahon, A. P., Flavell, R. A. and Williams, T.(1996). Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature381,238-241.
(
10.1038/381238a0
) -
Zimmerman, K., Shih, J., Bars, J., Collazo, A. and Anderson, D. J. (1993). XASH-3, a novel Xenopus achaete-scute homolog,provides an early marker of planar neural induction and position along the mediolateral axis of the neural plate. Development119,221-232.
(
10.1242/dev.119.1.221
)
Dates
Type | When |
---|---|
Created | 22 years, 8 months ago (Dec. 16, 2002, 4:34 p.m.) |
Deposited | 1 year, 7 months ago (Jan. 8, 2024, 7:07 a.m.) |
Indexed | 4 weeks, 1 day ago (Aug. 6, 2025, 8:22 a.m.) |
Issued | 22 years, 8 months ago (Dec. 15, 2002) |
Published | 22 years, 8 months ago (Dec. 15, 2002) |
Published Print | 22 years, 8 months ago (Dec. 15, 2002) |
@article{Wallingford_2002, title={Neural tube closure requires Dishevelled-dependent convergent extension of the midline}, volume={129}, ISSN={0950-1991}, url={http://dx.doi.org/10.1242/dev.00123}, DOI={10.1242/dev.00123}, number={24}, journal={Development}, publisher={The Company of Biologists}, author={Wallingford, John B. and Harland, Richard M.}, year={2002}, month=dec, pages={5815–5825} }