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The Dorsal Neural Tube Organizes the Dermamyotome and Induces Axial Myocytes in the Avian Embryo

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The Dorsal Neural Tube Organizes the Dermamyotome and Induces Axial Myocytes in the Avian Embryo Development 122, 231-241 (1996) 231 Printed in Great Britain © The Company of Biologists Limited 1996 DEV3253 The dorsal neural tube organizes the dermamyotome and induces axial myocytes in the avian embryo Martha S. Spence1, Joseph Yip2 and Carol A. Erickson1,* 1Section of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA 2Department of Neurobiology, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15261, USA *Author for correspondence (e-mail: [email protected]) SUMMARY Somites, like all axial structures, display dorsoventral reported previously to induce sclerotome. Thus, we have polarity. The dorsal portion of the somite forms the der- demonstrated that in the context of the embryonic envi- mamyotome, which gives rise to the dermis and axial mus- ronment, a dorsalizing signal from the dorsal neural tube culature, whereas the ventromedial somite disperses to can compete with the diffusible ventralizing signal from the generate the sclerotome, which later comprises the notochord. vertebrae and intervertebral discs. Although the neural In contrast to dorsal neural tube, pieces of ventral neural tube and notochord are known to regulate some aspects of tube, dorsal ectoderm or neural crest cells, all of which this dorsoventral pattern, the precise tissues that initially have been postulated to control dermamyotome formation specify the dermamyotome, and later the myotome from it, or to induce myogenesis, either fail to do so or provoke only have been controversial. Indeed, dorsal and ventral neural minimal inductive responses in any of our assays. However, tube, notochord, ectoderm and neural crest cells have all complicating the issue, we find consistent with previous been proposed to influence dermamyotome formation or to studies that following ablation of the entire neural tube, regulate myocyte differentiation. In this report we describe dermamyotome formation still proceeds adjacent to the a series of experimental manipulations in the chick embryo dorsal ectoderm. Together these results suggest that, to show that dermamyotome formation is regulated by although dorsal ectoderm may be less potent than the interactions with the dorsal neural tube. First, we demon- dorsal neural tube in inducing dermamyotome, it does strate that when a neural tube is rotated 180° around its nonetheless possess some dermamyotomal-inducing dorsoventral axis, a secondary dermamyotome is induced activity. from what would normally have developed as sclerotome. Based on our data and that of others, we propose a model Second, if we ablate the dorsal neural tube, dermamy- for somite dorsoventral patterning in which competing dif- otomes are absent in the majority of embryos. Third, if we fusible signals from the dorsal neural tube and from the graft pieces of dorsal neural tube into a ventral position notochord/floorplate specify dermamyotome and sclero- between the notochord and ventral somite, a derma- tome, respectively. In our model, the positioning of the myotome develops from the sclerotome that is proximate dermamyotome dorsally is due to the absence or reduced to the graft, and myocytes differentiate. In addition, we also levels of the notochord-derived ventralizing signals, as well show that myogenesis can be regulated by the dorsal neural as to the presence of dominant dorsalizing signals. These tube because when pieces of dorsal neural tube and unseg- dorsal signals are possibly localized and amplified by mented paraxial mesoderm are combined in tissue culture, binding to the basal lamina of the ectoderm, where they can myocytes differentiate, whereas mesoderm cultures alone signal the underlying somite, and may also be produced by do not produce myocytes autonomously. In all of the exper- the ectoderm as well. imental perturbations in vivo, the dorsal neural tube induced dorsal structures from the mesoderm in the Key words: dermamyotome, myogenesis, neural tube, somites, avian presence of notochord and floorplate, which have been embryo INTRODUCTION lack obvious morphological polarity (Bellairs, 1963; Christ et al., 1972; Mestres and Hinrichsen, 1976). Within a few hours, The paraxial mesoderm first arises by ingressing through the however, morphogenetic movements generate regional histo- primitive streak to form a uniform band of tissue that flanks logical differences along the dorsal-ventral axis of each somite the neural tube. Although initially unsegmented, the paraxial (Mestres and Hinrichsen, 1976; reviewed by Stern et al., 1988; mesoderm soon becomes partitioned in an anterior-to-posterior Ordahl, 1993). Cells comprising the ventromedial portion of wave to form the somites, which are epithelial in nature and the somite undergo an epithelial-to-mesenchymal transforma- 232 M. S. Spence, J. Yip and C. A. Erickson tion to form the sclerotome, which lies lateral to the neural tube that dorsal fate is a default pathway in the absence of a ven- and notochord (Hay, 1968). In contrast, cells in the dorsal tralizing signal from the neural tube and notochord (Pourquié portion of the somite maintain an epithelial organization and et al., 1993), and therefore that dorsal-specifying signals may constitute the transient dermamyotome. Cells at the cranial not be necessary at all. edge of the dermamyotome later give rise to the more ventrally To characterize the cellular interactions that signal situated myotome, while the remaining dermamyotome cells formation of the dermamyotome as well as specification of become dermatome (Kaehn et al., 1988; Tosney et al., 1994). myocytes, we have employed the techniques of experimental Although the derivatives of the somites (i.e. dermatome, embryology. Because most of our experiments attempt to myotome and sclerotome) are positioned with obvious dorsal- identify and characterize various signaling centers in the ventral polarity, such regionalization is not intrinsic to either context of the embryo, the environmental conditions and the unsegmented paraxial mesoderm or the most recently spatial organization of inducing and responding tissues are formed somites. This absence of regional specification at early close to normal, in contrast with previously employed tissue stages is revealed in experiments in which 180° rotation of the culture assays where these signals may be lost or altered. paraxial mesoderm or early somites has no effect on the sub- Results from a series of manipulations including dorsoventral sequent dorsal-ventral patterning (Aoyama and Asamoto, rotation of the neural tube, extirpation of the dorsal neural tube 1988). Similarly, when the dorsal half of an early somite is and grafting of putative inducing tissues ventrally adjacent to replaced with a ventral half, the grafted ventral tissue the sclerotome together support a model in which the dorsal undergoes normal myogenesis (Christ et al., 1992). These neural tube induces the formation of the dermamyotome. In studies suggest that dorsal-ventral pattern within each somite contrast, surface ectoderm, ventral neural tube and neural crest is established through interactions with surrounding axial cells appear to have only modest, direct signaling roles, or do structures during and subsequent to segmentation. not participate in the induction of the dermamyotome. Fur- Several axial tissues could potentially contribute to somite thermore, our study suggests that the signal emanating from patterning. For example, the neural tube and notochord are the dorsal neural tube is a diffusible molecule that can compete, known to play a role in the development of the sclerotome. Co- in the embryo, with the ventralizing signal from the notochord. cultures of somite with neural tube and notochord produce an abundance of cartilage, a sclerotome derivative (Lash et al., 1957; Lash, 1968; Kosher and Lash, 1975). Moreover, when a MATERIALS AND METHODS notochord is grafted ectopically to dorsal regions of the somite, the sclerotome expands at the expense of the dermamyotome Embryo culture (Pourquié et al., 1993; Bober et al., 1994; Goulding et al., White Leghorn chicken embryos were used for all in vivo manipula- 1994). Finally, early removal of the notochord enhances the tions (Avian Sciences Department, University of California-Davis or development of the dermamyotome and results in the absence Western Scientific, Sacramento, CA). Some embryos were treated and of sclerotome (van Stratten and Hekking, 1991; Rong et al., maintained in ovo. On the day before the operation, a small hole was 1992; Goulding et al., 1993, 1994). Recent studies reveal that cut into the egg shell above the embryo, the window sealed with cel- Sonic hedgehog is produced by the notochord and floor plate lophane tape and the egg returned to the incubator. Just prior to any at the correct time to induce sclerotome (Johnson et al., 1994) experimental manipulation, a drop of 0.02% neutral red in Locke’s saline was applied to the vitelline membrane to stain the embryo and and, furthermore, that heterologous cells expressing Sonic reveal the vitelline membrane, which was subsequently slit with a hedgehog can induce sclerotome formation, as assessed using tungsten needle to access the embryo. After surgery, the eggs were molecular markers, both in culture assays (Fan and Tessier- resealed and incubated at 38°C and 70% humidity until the embryos Lavigne, 1994) and in vivo (Johnson et al., 1994). were fixed. Unlike the sclerotome, candidate molecules that regulate the Alternatively, some embryos were cultured in vitro after surgery. formation of dermamyotome or
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