Development, Vol 116, Issue 4 887-899, Copyright © 1992 by Company of Biologists

JOURNAL ARTICLES

The epithelium of the dorsal marginal zone of Xenopus has organizer properties

J Shih and R Keller
Department of Molecular and Cell Biology, University of California, Berkeley, 94720.

We have investigated the properties of the epithelial layer of the dorsal marginal zone (DMZ) of the Xenopus laevis early gastrula and found that it has inductive properties similar to those of the entire Spemann organizer. When grafts of the epithelial layer of the DMZ of early gastrulae labelled with fluorescein dextran were transplanted to the ventral sides of unlabelled host embryos, they induced secondary axes composed of notochord, somites and posterior neural tube. The organizer epithelium rescued embryos ventralized by UV irradiation, inducing notochord, somites and posterior neural tube in these embryos, while over 90% of ventralized controls showed no such structures. Combinations of organizer epithelium and ventral marginal zone (VMZ) in explants of the early gastrula resulted in convergence, extension and differentiation of dorsal mesodermal tissues, whereas similar recombinants of nonorganizer epithelium and the VMZ did none of these things. In all cases, the axial structures forming in response to epithelial grafts were composed of labelled graft and unlabelled host cells, indicating an induction by the organizer epithelium of dorsal, axial morphogenesis and tissue differentiation among mesodermal cells that otherwise showed non-axial development. Serial sectioning and scanning electron microscopy of control grafts shows that the epithelial organizer effect occurs in the absence of contaminating deep cells adhering to the epithelial grafts. However, labelled organizer epithelium grafted to the superficial cell layer contributed cells to deep mesodermal tissues, and organizer epithelium developed into mesodermal tissues when deliberately grafted into the deep region. This shows that these prospective endodermal epithelial cells are able to contribute to mesodermal, mesenchymal tissues when they move or are moved into the deep environment. These results suggest that in normal development, the endodermal epithelium may influence some aspects of the cell motility underlying the mediolateral intercalation (see Shih, J. and Keller, R. (1992) Development 116, 901-914), as well as the tissue differentiation of mesodermal cells. These results have implications for the analysis of mesoderm induction and for analysis of variations in the differentiation and morphogenetic function of the marginal zone in different species of amphibians.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				P. Oteiza, M. Koppen, M. L. Concha, and C.-P. Heisenberg Origin and shaping of the laterality organ in zebrafish Development, August 15, 2008; 135(16): 2807 - 2813. [Abstract] [Full Text] [PDF]

				A. D. Chalmers, B. Strauss, and N. Papalopulu Oriented cell divisions asymmetrically segregate aPKC and generate cell fate diversity in the early Xenopus embryo Development, June 15, 2003; 130(12): 2657 - 2668. [Abstract] [Full Text] [PDF]

				L. A. Barlow Specification of pharyngeal endoderm is dependent on early signals from axial mesoderm Development, November 15, 2001; 128(22): 4573 - 4583. [Abstract] [Full Text] [PDF]

				A. Schier, S. Neuhauss, K. Helde, W. Talbot, and W Driever The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail Development, January 1, 1997; 124(2): 327 - 342. [Abstract] [PDF]

				C. Hansen, C. Marion, K Steele, S George, and W. Smith Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3 Development, January 1, 1997; 124(2): 483 - 492. [Abstract] [PDF]

				M Sakai The vegetal determinants required for the Spemann organizer move equatorially during the first cell cycle Development, July 1, 1996; 122(7): 2207 - 2214. [Abstract] [PDF]

				K. Kroll and E Amaya Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation Development, January 10, 1996; 122(10): 3173 - 3183. [Abstract] [PDF]

				J. Ramos, C. Whittaker, and D. DeSimone Integrin-dependent adhesive activity is spatially controlled by inductive signals at gastrulation Development, January 9, 1996; 122(9): 2873 - 2883. [Abstract] [PDF]

				J Shih and S. Fraser Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage Development, January 4, 1996; 122(4): 1313 - 1322. [Abstract] [PDF]

				M. Vodicka and J. Gerhart Blastomere derivation and domains of gene expression in the Spemann Organizer of Xenopus laevis Development, January 11, 1995; 121(11): 3505 - 3518. [Abstract] [PDF]

				K. Storey, M. Selleck, and C. Stern Neural induction and regionalisation by different subpopulations of cells in Hensen's node Development, January 2, 1995; 121(2): 417 - 428. [Abstract] [PDF]

				D. Bauer, S Huang, and S. Moody The cleavage stage origin of Spemann's Organizer: analysis of the movements of blastomere clones before and during gastrulation in Xenopus Development, January 5, 1994; 120(5): 1179 - 1189. [Abstract] [PDF]

				T Holowacz and R. Elinson Cortical cytoplasm, which induces dorsal axis formation in Xenopus, is inactivated by UV irradiation of the oocyte Development, January 9, 1993; 119(1): 277 - 285. [Abstract] [PDF]

				E. Davidson Later embryogenesis: regulatory circuitry in morphogenetic fields Development, January 7, 1993; 118(3): 665 - 690. [Abstract] [PDF]

				H Steinbeisser, E. De Robertis, M Ku, D. Kessler, and D. Melton Xenopus axis formation: induction of goosecoid by injected Xwnt-8 and activin mRNAs Development, January 6, 1993; 118(2): 499 - 507. [Abstract] [PDF]

				S. M. Purcell and R. Keller A different type of amphibian mesoderm morphogenesis in Ceratophrys ornata Development, January 1, 1993; 117(1): 307 - 317. [Abstract] [PDF]