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Regulation of Paraxis Expression and Somite Formation by Ectoderm- and Neural Tube-Derived Signals

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Regulation of Paraxis Expression and Somite Formation by Ectoderm- and Neural Tube-Derived Signals DEVELOPMENTAL BIOLOGY 185, 229±243 (1997) ARTICLE NO. DB978561 Regulation of paraxis Expression and Somite Formation by Ectoderm- and Neural Tube-Derived Signals DrazÏen SÏosÏicÂ,* Beate Brand-Saberi,² Corina Schmidt,² Bodo Christ,² and Eric N. Olson*,1 *Hamon Center for Basic Cancer Research, The University of Texas, Southwestern Medical Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235-9148; and ²Institute of Anatomy, University of Freiburg, P.O. Box 111, 79001 Freiburg i. Brsg., Germany During vertebrate embryogenesis, the paraxial mesoderm becomes segmented into somites, which form as paired epithelial spheres with a periodicity that re¯ects the segmental organization of the embryo. As a somite matures, the ventral region gives rise to a mesenchymal cell population, the sclerotome, that forms the axial skeleton. The dorsal region of the somite remains epithelial and is called dermomyotome. The dermomyotome gives rise to the trunk and limb muscle and to the dermis of the back. Epaxial and hypaxial muscle precursors can be attributed to distinct somitic compartments which are laid down prior to overt somite differentiation. Inductive signals from the neural tube, notochord, and overlying ectoderm have been shown to be required for patterning of the somites into these different compartments. Paraxis is a basic helix± loop±helix transcription factor expressed in the unsegmented paraxial mesoderm and throughout epithelial somites before becoming restricted to epithelial cells of the dermomyotome. To determine whether paraxis might be a target for inductive signals that in¯uence somite patterning, we examined the in¯uence of axial structures and surface ectoderm on paraxis expression by performing microsurgical operations on chick embryos. These studies revealed two distinct phases of paraxis expression, an early phase in the paraxial mesoderm that is dependent on signals from the ectoderm and independent of the neural tube, and a later phase that is supported by redundant signals from the ectoderm and neural tube. Under experimental conditions in which paraxis failed to be expressed, cells from the paraxial mesoderm failed to epithelialize and somites were not formed. We also performed an RT-PCR analysis of combined tissue explants in vitro and con®rmed that surface ectoderm is suf®cient to induce paraxis expression in segmental plate mesoderm. These results demonstrate that somite formation requires signals from adjacent cell types and that the paraxis gene is a target for the signal transduc- tion pathways that regulate somitogenesis. q 1997 Academic Press INTRODUCTION mation have been documented in detail, little is known of the transcriptional mechanisms that control somite forma- Somites are segmental units of the paraxial mesoderm tion and patterning. that form in a rostral-to-caudal progression during verte- Immediately after they bud off from the segmental plate, brate embryogenesis. The reiterative arrangement of so- somites appear as paired epithelial spheres that surround a mites along the rostrocaudal axis re¯ects the segmental or- loose aggregate of mesenchymal cells. As somites mature, ganization of the vertebrate embryo and imposes segmental they undergo a series of morphological and molecular patterning on the axial skeleton, the intrinsic back muscu- changes that culminate with the formation of three somitic lature, the peripheral nervous system, and the vasculature. compartments, the dermatome, myotome, and sclerotome While the morphological events associated with somite for- (reviewed in Keynes and Stern, 1988; Christ and Ordahl, 1995; Brand-Saberi et al., 1996). Initially, the ventral region Sequence data from this article have been deposited with the of the newly formed somite undergoes an epithelial-to-mes- EMBL/GenBank Data Libraries under Accession No. U76665. enchymal transition, giving rise to the sclerotome, the ori- 1 To whom correspondence should be addressed. Fax: (214)648- gin of the axial skeleton. The remaining epithelial sheet in 1196. E-mail: [email protected]. the dorsal somite, referred to as the dermomyotome and 0012-1606/97 $25.00 Copyright q 1997 by Academic Press All rights of reproduction in any form reserved. 229 AID DB 8561 / 6x23$$$181 05-07-97 11:44:50 dba 230 SÏ osÏic et al. FIG. 1. Deduced primary amino acid sequence of chicken paraxis protein and its homology with mouse paraxis. (A) Nucleotide sequence of chicken paraxis cDNA and deduced amino acid sequence of paraxis protein. The bHLH region is indicated in bold. (B) Homology between chicken and mouse paraxis proteins. The bHLH region is underlined. later the dermotome, gives rise to the myotome at its crani- the ventrolateral body wall (Christ et al., 1974, 1977, 1983; omedial edge (Kaehn et al., 1988; Christ and Ordahl, 1995). Chevallier et al., 1977; Ordahl and Le Douarin, 1992). The myotome consists of a layer of postmitotic, differenti- Cells surrounding the somites play important roles in ated skeletal muscle cells that form the back muscles (for speci®ying and patterning of different somitic cell lineages. a review, see Christ et al., 1990). The lateral part of the Sclerotome differentiation occurs in response to the se- dermomyotome gives rise to the muscles of the limb and creted morphogen sonic hedgehog, which is produced by FIG. 2. Expression of paraxis transcripts during chick embryogenesis. Paraxis mRNA was detected by whole-mount in situ hybridization. (A) HH stage 5 chick gastrula. Paraxis mRNA is present in prospective segmental plate mesoderm (arrows). (B) Stage 7 embryo. Paraxis is expressed in the rostral end of the segmental plate and in newly formed somites. (C) HH stage 11 embryo (12 somites), ventral view. Paraxis transcripts are found in the segmental plate and somites. (D) Higher magni®cation of the embryo shown in (C). The rostrocaudal gradient of paraxis expression can be observed with highest expression in the segmental plate and lowest in the rostral-most somites. (E) HH stage 19 chick embryo. Paraxis is expressed in all somites and in the segmental plate. (F) Higher magni®cation of the embryo shown in (E). The most recently formed somites show uniform expression of paraxis. More mature somites show highest expression in the mediocaudal quadrant, while the rostral-most somites express paraxis predominantly at their rostral and caudal edges. Arrows in (F) indicate paraxis expression at the rostral and caudal edges of the somite. The arrowhead in (F) points to precursors of tongue muscle. Staining in the head in (E) and (F) is background. Abbreviations: ps, primitive streak; s, somite; sp, segmental plate; nt, neural tube. Copyright q 1997 by Academic Press. All rights of reproduction in any form reserved. AID DB 8561 / 6x23$$$181 05-07-97 11:44:50 dba Regulation of paraxis Expression and Somite Formation 231 Copyright q 1997 by Academic Press. All rights of reproduction in any form reserved. AID DB 8561 / 6x23$$8561 05-07-97 11:44:50 dba 232 SÏ osÏic et al. hybridization. (A) Schematic in situ Transverse sections of HH stages 11 and 16 chick embryos showing paraxis expression detected by FIG. 3. illustration of cross-sections throughshown HH in stage (B), 11 (C), andparaxial and 16 mesoderm. (D), embryos. (C) respectively. As The (B)an lines somites Section anterior designated through mature, paraxis the B, somite rostral expression Cmyotome. that end Abbreviations: is and has nt, of lost D neural differentiated the in in tube; segmental themyotome; into this no, s, sclerotome, plate. panel notochord; dermatome, Paraxis sclerotome; but i, indicate d, myotome, intermediate mRNA persists the is mesoderm; dermatome; in and planes so, found m, the sclerotome. of somatic throughout myotome. dermomyotome. mesoderm; section the Paraxis (D) sp, entire Section expression splanchnic mesoderm; through is dm, dermo- restricted to the dermatome and Copyright q 1997 by Academic Press. All rights of reproduction in any form reserved. AID DB 8561 / 6x23$$8561 05-07-97 11:44:50 dba Regulation of paraxis Expression and Somite Formation 233 the notochord and ventral neural tube (Brand-Saberi et al., expression of paraxis during chick embryogenesis. We show 1993; Pourquie et al., 1993; Fan and Tessier-Lavigne, 1994; that there are two distinct phases of paraxis expression in Johnson et al., 1994; Fan et al., 1995; Ebensperger et al., paraxial mesoderm and developing somites. The initial ex- 1995). Induction of muscle gene expression in the myotome pression of paraxis in unsegmented paraxial mesoderm is has also been shown to be in¯uenced by signals from the dependent on the surface ectoderm and independent of the notochord and the dorsal neural tube (Rong et al., 1990, neural tube, whereas the later expression of paraxis in the 1992; Buf®nger and Stockdale, 1994, 1995; MuÈnsterberg and dermomyotome appears to be dependent on redundant sig- Lassar, 1995; Stern and Hauschka, 1995; Pownall et al., nals from the neural tube and surface ectoderm. In regions 1996; Spense et al., 1996; Amthor et al., 1996). Members of of manipulated chick embryos in which paraxis was not the wingless family of growth factors (Wnts), which are expressed, the paraxial mesoderm failed to epithelialize, re- secreted by the dorsal neural tube, and sonic hedgehog ap- sulting in the absence of epithelial somites and the dermo- pear to mediate the effects of axial organs on myotome myotome. These results demonstrate the importance of cel- development (Stern et al., 1995; MuÈ nsterberg et al., 1995). lular signaling for somitogenesis and are consistent with Myogenic cells of the ventrolateral portion of the dermomy- the notion that the paraxis gene is a target for redundant otome, which form the lateral muscle cell lineage, appear signaling pathways from the ectoderm and neural tube that to be in¯uenced by different signals than the medial lineage control somite formation and epithelialization of the para- (Gamel et al., 1995; Pourquie et al., 1995). Bone morphogen- xial mesoderm. etic protein-4 (BMP-4), which is expressed in the lateral mesoderm, inhibits differentiation of the lateral myogenic lineage (Pourquie et al., 1996).
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