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Molecular Nature of Spemann's Organizer: the Role of the Xenopus

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Molecular Nature of Spemann's Organizer: the Role of the Xenopus Cell, Vol. 67, 111 I-1 120, December 20, 1991, Copyright 0 1991 by Cell Press Molecular Nature of Spemann’s Organizer: the Role of the Xenopus Homeobox Gene goosecoid Ken W. Y. Cho,’ Bruce Biumberg, dorsal cells of the embryo (Gimiich and Gerhart, 1984; Herbert Steinbeisser, and Eddy M. Lh? Robertis Gimlich, 1988) the so-called Nieuwkoop center (Gerhart Molecular Biology institute et al., 1989). Experiments involving coculture of tissue and Department of Biological Chemistry fragments suggest that cells from the Nieuwkoop center University of California release diffusible signals that in turn induce Spemann’s Los Angeles, California 90024-l 737 organizer activity in the overlying marginal zone ceils (Nieuwkoop, 1973). One of the most important recent advances in Xenopus Summary embryology is the discovery that peptide growth factors mediate mesoderm induction. Factors related to basic fi- This study analyzer, the function of the homeobox gene brobiast growth factor (bFGF) can induce ventral meso- goosecold in Xenopus development. First, we find that derm (blood, mesothelium, mesenchyme, and some mus- gooaecoid mFiNA distribution closely mimics the ex- cle), while growth factors of the TGF-8 family, in particular pected localization of organizer tissue in normal em- activin (also called XTC-MIF), are very potent dorsal meso- bryos as well as in those treated with LiCi and UV light. derm inducers (prechordal mesoderm, notochord, and Second, goosecoid mRNA accumulation is induced muscle) (Slack et al., 1989; Smith et al., 1989; Green and by activin, even in the absence of protein synthesis. Smith, 1990). Uncommitted ceils from the animal cap (top) it is not affected by bFGF and is @passed by retinoic region of Xenopus biastulae acquire Spemann’s organizer acid. Lastly, microinjection of goosecoid mRNA into the activity when incubated with activin, inducing secondary ventral side of Xenopus embryos, where goosecold is axes including head, trunk, and tail after transplantation normally absent, ieads to the formation of an additional into host embryos (Cooke et al., 1987; Fluiz i Altaba and complete body axis, including head structures and Melton, 1989). Furthermore, microinjection of activin abundant notochordai tissue. The results suggest that mRNA into cleaving Xenopus embryos can also induce the goosecoid homeodomain protein plays a central role secondary axes (Thomsen et al., 1990). Thus, in molecular in executing Spemann’s organizer phenomenon. terms the organizer is currently thought to be induced as a result of the release of a dorsal growth factor by the introduction Nieuwkoop center blastomeres. This growth factor would then act upon the overlying cells of the marginal zone, The “organizer” experiment (Spemann and Mangold, inducing them to become organizer tissue. 1924) is one of the best known in biology, but its molecular At the late blastula stage, the organizer is located in basis remains largely unknown. if the region where gastru- a patch of cells encompassing 80° of arc of the dorsal lation starts in an amphibian embryo, called the dorsal lip marginal zone, which gives rise to head and notochordal of the blastopore, is transplanted into the opposite (ventral) (anterodorsal) mesoderm and determines the site where side of a host embryo, an entire new body axis results. The gastruiation starts. Since this tissue displays great powers transplanted tissue, whose normal fate is to become head of regulation after experimental manipulation, it has been (“prechordal”) mesoderm and notochord, is able to recruit termed the “organizer field” (Spemann, 1938) or “primary cellsfrom theventral sideof theembryo, “organizing”them organization field” (Cooke, 1972). Examples of these regu- into axial structures such as somites and neural tube (re- latory properties include the following. First, a dorsal lip viewed by Spemann, 1938; Hamburger, 1988). can be divided into several fragments, each of which can This ability of the organizer region to initiate a cascade induce a secondary axis. Second, surgical removal of half of cell-cell interactions stimulated a large body of research an organizer results in entirely normal embryos (Stewart employing the transplantation methods of experimental and Gerhart, 1990), while removal of more than this embryology; in recent years most of this research has been amount results in tadpoles with progressively more severe carried out with Xenopus laevis. The formation of the orga- anterior deficiencies. Third, if an organizer is transplanted nizer can be traced back to the moment of fertilization. closer than 80“ of arc to the site of the host’s dorsal lip, a The egg is initially radially symmetrical, but sperm entry secondary axis is not induced and a normal embryo en- triggers a microtubule-driven rotation of the egg cortex. sues (Cooke, 1972). Fourth, if uncommitted embryonic This intracellular movement eventually leads to the forma- cells are transplanted into the dorsal lip region, they will tion of the body axis. The direction of this cortical rotation become incorporated into the organizer, adopting a noto- determines the position of the future dorsal lip, which usu- chordal cell fate (Spemann, 1938). Because it is the site ally forms opposite to the sperm entry point (Gerhart et al., where the body axis is initially formed, and because it 1989; Elinson and Kao, 1989). Blastomere transplantation has such interesting properties, the organizer field has experiments suggest that at the 32-cell stage the dorsal fascinated embryologists for almost 70 years. To under- information is located in the most vegetal (bottom) and stand what makes this region unique, however, it is first necessary to isolate the molecules that control its biologi- * Present address: Department of Developmental and Cell Biology, cal behavior. University of California, Irvine. California 92717. The starting point for the present investigation was pro- Cdl 1112 vided by a previous study in which a cDNA library from pore. The fate of these cells is to form mostly prechordal manually dissected Xenopus dorsal lips was screened (head) mesoderm and notochord in later development with an oligonucleotide probe specific for homeobox (Keller, 1978; Slack, 1991). However, neither the “bottle genes (Blumberg et al., 1991). We chose to start by study- cells” of Hamburger, located directly at the leading edge ing homeobox genes, because they have been shown to of the blastoporal invagination (arrow in Figure lD), nor mediate axis formation in Drosophila and vertebrates (re- the superficial layer of cells located directly above the lip viewed by Gehring, 1987; De Robertis et al., 1990; Kessel express goose&d mRNA. The fate of bottle cells is to and Gruss, 1990; Melton, 1991). This experiment resulted become pharyngeal endoderm, and the fate of superficial in the isolation of four types of homeoboxcontaining cells is to form the dorsal endoderm of the digestive tract cDNAs, all of which were found to be concentrated in the (Keller, 1975). The localization observed is consistent with dorsal lip by Northern blot analysis of dissected embryos. goosecoid being expressed in cells that give rise to head One cDNA, Xlab, was a labial homolog, and two others, and notochordal mesoderm. Xcadl and XcadP, were caudal homologs. The fourth type The in situ hybridizations indicate that the border of the of cDNA was the most interesting because it is expressed patch of goosecoid expression in the marginal zone is not earlier than the others and especially because it encodes sharply defined and tends to taper off at the edges (e.g., a protein that binds DNA in vitro with a specificity similar to Figures 1 B and 2A), but it is difficult to conclude whether that of the homeodomain of the Drosophila protein bicoid it is graded or not. The Drosophila homeodomain protein (Blumberg et al., 1991). The gene bicoid occupies a high bicoid, which mediates the first step in anteroposterioraxis place in the regulatory hierarchy leading to anteroposterior formation, forms a gradient in the anterior region of the fly axis formation in fruit flies (Driever and Nusslein-Volhard, embryo (Driever and Ntisslein-Volhard, 1988). In addition, 1988; Niisslein-Volhard, 1991). This Xenopus gene was vertebrate homeobox proteins are known to form gradi- named goosecoid (gsc) to reflect its similarity, in parts of ents of nuclear proteins in fields of differentiating cells the homeodomain, to the Drosophila genes gooseberry such as limbs or feather buds (reviewed by De Robertis and bicoid. et al., 1991). Homeoprotein gradients are best visualized The present study is concerned with the function of when the distribution of proteins is examined with specific goosecoid in Xenopus development. We find that the in antibodies rather than by in situ hybridization; it will there- situ distribution of goosecoid transcripts mimics the loca- fore be of interest to examine the distribution of goosecoid tion of the organizer field in normal and experimentally protein, particularly during mesoderm invagination, once manipulated embryos, that goose&d expression is a pri- a specific antiserum becomes available. mary response to activin induction, and that microinjection A time course of goosecoid expression by in situ hybrid- of its mRRA into the ventral blastomeres of the 4-cell em- ization (not shown) reveals that while it is not detectable bryo issuff icient to induce the formation of secondary body at mid-blastula, a localized patch of dorsal expression is axes at high frequency. The results
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