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A Nonneural Epithelial Domain of Embryonic Cranial Neural Folds Gives Rise to Ectomesenchyme

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A Nonneural Epithelial Domain of Embryonic Cranial Neural Folds Gives Rise to Ectomesenchyme A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme Marie Anne Breau*†, Thomas Pietri*‡, Marc P. Stemmler§, Jean Paul Thiery*¶, and James A. Weston‡ʈ *Centre National de la Recherche Scientifique, Unite Mixte de Recherche 144, Institut Curie, 26 Rue d’Ulm, 75248 Paris Cedex 05, France; §Department of Molecular Embryology, Max Planck-Institute of Immunobiology, Stuebeweg 51, D-79108 Freiburg, Germany; and ‡Institute of Neuroscience, University of Oregon, Eugene, OR 97403-1254 Edited by Igor B. Dawid, National Institutes of Health, Bethesda, MD, and approved March 26, 2008 (received for review November 30, 2007) The neural crest is generally believed to be the embryonic source define the general location of an epithelial domain in the murine of skeletogenic mesenchyme (ectomesenchyme) in the vertebrate cranial NFs from which some EM originates. head and other derivatives, including pigment cells and neurons and glia of the peripheral nervous system. Although classical Results transplantation experiments leading to this conclusion assumed Cre-Recombinase Is Expressed in Lateral Neural Fold Epithelium Be- that embryonic neural folds were homogeneous epithelia, we fore EMT in Ht-PA-Cre Transgenic Embryos. In transgenic mouse reported that embryonic cranial neural folds contain spatially and embryos expressing Cre-recombinase (Cre) under the control phenotypically distinct domains, including a lateral nonneural of the human tissue plasminogen activator promoter (Ht-PA- domain with cells that coexpress E-cadherin and PDGFR␣ and a Cre/R26R), cells exhibiting ␤-galactosidase (␤-gal) activity thickened mediodorsal neuroepithelial domain where these pro- appear precociously in BA, frontonasal process, and periocular teins are reduced or absent. We now show that Wnt1-Cre is mesenchyme before any marked cells appear in cranial NF expressed in the lateral nonneural epithelium of rostral neural epithelium (Fig. 1). To reconcile this early appearance of folds and that cells coexpressing Cre-recombinase and PDGFR␣ labeled mesenchyme with its presumed NC origin, it was delaminate precociously from some of this nonneural epithelium. suggested (11) that some crest cells might disperse before the We also show that ectomesenchymal cells exhibit ␤-galactosidase transgenic marker was activated. In early [embryonic days activity in embryos heterozygous for an Ecad-lacZ reporter knock- (E)8.0–E8.5] transgenic embryos, however, we observed Cre in allele. We conclude that a lateral nonneural domain of the neural protein in cell nuclei both in the nonneural epithelium of the fold epithelium, which we call ‘‘metablast,’’ is a source of ecto- cranial NFs and in underlying mesenchyme (Fig. 2). Therefore, mesenchyme distinct from the neural crest. We suggest that closer we conclude that Cre-expression precedes or at least is coin- analysis of the origin of ectomesenchyme might help to under- cident with the delamination of labeled cells from the non- stand (i) the molecular-genetic regulation of development of both neural epithelium. These results are consistent with the neural crest and ectomesenchyme lineages; (ii) the early develop- prediction in ref. 5 that at least some EM originates preco- mental origin of skeletogenic and connective tissue mesenchyme in ciously from a source other than NC. the vertebrate head; and (iii) the presumed origin of head and branchial arch skeletal and connective tissue structures during Wnt1-Cre Is Expressed in NonNeural Epithelium of Embryonic Cranial vertebrate evolution. Neural Folds. Previous cell labeling studies, using Wnt1-Cre transgenic embryos report that both BA mesenchyme and trunk cranial neural crest ͉ EMT ͉ metablast ͉ PDGFR␣ NC derivatives express ␤-gal in E9.5 and older Wnt1-Cre/R26R transgenic embryos (11, 12). Because Wnt1 is generally assumed n vertebrate embryos, dorsal neural epithelium of the neural to be expressed only in dorsal neural tissue (13, 14), it is widely Itube (NT) undergoes an epithelium-to-mesenchyme transition regarded as a definitive marker for NC-derived cells (e.g., ref. (EMT) (1) to produce neural crest (NC) cells. These cells then 15). When we examined Cre expression in the NFs of E8 (4–7 disperse in embryonic interstitial spaces and eventually give rise somite) transgenic embryos carrying Wnt1-Cre, we confirmed to pigment cells and neurons and glia of the peripheral nervous that Cre-immunoreactive (IR) cells are present in the dorsal systems (PNS). At cranial levels of amphibian, avian and mam- neural epithelium of the NFs at and caudal to the Vagal axial malian embryos, the cells derived from neural fold (NF) epi- level [data not shown; see supporting information (SI) Fig. S1]. thelium also give rise to these derivatives. In addition, however, However, in the fore- and midbrain NFs of these embryos, most avian and mammalian cranial NFs, like the NFs at all axial levels Cre-IR was observed in the nonneural (E-cad-IR) epithelium of amphibian embryos, give rise to some connective tissue cells and skeletogenic mesenchyme [‘‘ectomesenchyme’’ (EM)]. It is generally believed that the NC produces EM and that the crest Author contributions: J.P.T. and J.A.W. contributed equally to this work; J.A.W. designed at trunk axial levels of avian and mammalian embryos has lost research; M.A.B., T.P., and M.P.S. performed research; T.P. and M.P.S. contributed new reagents/analytic tools; M.A.B., T.P., M.P.S., J.P.T., and J.A.W. analyzed data; and M.A.B. the ability to do so (ref. 2; see also refs. 3 and 4). and J.A.W. wrote the paper. However, Weston et al. (5) have challenged this idea, noting The authors declare no conflict of interest. that mouse cranial NF epithelium is heterogeneous and that a This article is a PNAS Direct Submission. sharp boundary exists between lateral E-cadherinϩ (Ecadϩ) Freely available online through the PNAS open access option. nonneural epithelium and the thickened E-cadϪ neural epithe- † lium (NE) in the dorsomedial ridge (see also refs. 6 and 7). Present address: Division of Developmental Neurobiology, National Institute for Medical ϩ Research, Mill Hill, London NW7 1AA, United Kingdom. Moreover, a subpopulation of E-cad cells in the lateral non- ¶ ␣ To whom correspondence may be addressed at the present address: Institute of Molecular neural epithelium coexpresses PDGFR , which is a well estab- and Cell Biology, Agency for Science, Technology, and Research, 61 Biopolis Drive, Singa- lished marker of mesenchyme and connective tissue in somites pore 138673. E-mail: [email protected]. and in the head and branchial arches (BA) (8–10). They sug- ʈTo whom correspondence may be addressed. E-mail: [email protected]. ϩ ϩ gested that EM arises from this PDGFR␣ /E-cad NF epithe- This article contains supporting information online at www.pnas.org/cgi/content/full/ lium in vivo. Our present results support the idea that the source 0711344105/DCSupplemental. of EM is not restricted to the dorsal NE and have allowed us to © 2008 by The National Academy of Sciences of the USA 7750–7755 ͉ PNAS ͉ June 3, 2008 ͉ vol. 105 ͉ no. 22 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711344105 Downloaded by guest on October 2, 2021 endogenous E-cad expression patterns (17). These embryos reveal that ␤-gal is, or had recently been active in both nonneural epithelium of cranial NFs and in underlying EM cells (see Fig. 5 A–H and Fig. S2). We infer that these mesenchyme cells must have originated in the nonneural epithelium. In addition, how- ever, we occasionally observed a few labeled cells within neural epithelium of E.8.5 Ecad-lacZ knockin embryos (data not shown, but see Discussion), suggesting that these cells also originate from the E-cadϩ (nonneural) epithelium. Cells Derived from Nonneural Epithelium also Coexpress PDGFR␣. BA mesenchyme persistently expresses PDGFR␣ϩ, and requires its function for normal development of EM derivatives (8–10). Therefore, if EM originated from nonneural epithelium (see refs. 5 and 10), we would expect that (i) some cells in the NF epithelium of Wnt1Ϫ and Ht-PA-Cre transgenic embryos would express both PDGFR␣ and Cre, (ii) some of these PDGFR␣ϩ cells would also coexpress E-cad, and (iii) ␤-gal-expressing cells in Ecad-lacZ knockin embryos would express PDGFR␣. These predictions were verified: Cre/PDGFR␣ double-positive cells were present in both the nonneural epithelium of NFs and in Fig. 1. ␤-galactosidaseϩ mesenchymal cells appear precociously in the underlying mesenchyme of E8 Ht-PA-Cre (Fig. 4 A–D) and branchial arches. (A–C) X-Gal staining of E8-E8.5 Ht-PA-Cre/ROSA26 embryos Wnt1-Cre (Fig. 4 E–H) embryos. Likewise, labeled nonneural at the 4-somite (A), 8-somite (B), and 10-somite (C) stages. (D) High magnifi- epithelium and mesenchyme in Ecad-lacZ knockin embryos cation of outlined region in C, showing ␤-galϩ epithelial cells lateral to the coexpressed PDGFR␣ (Fig. 5 G and I). Thus, it seems likely that dorsal ridge of the NF. Labeled cells are present in the BA (white arrowheads), ␣ϩ in the frontonasal process (red arrowhead), and around the optic pit (black skeletogenic (PDGFR ) mesenchymal cells delaminate from arrowheads) before any marked cells are present in the NE. The dorsal ridge this nonneural domain of the NF. of NE, comprising the mediodorsal domain of the NF (the NC), is indicated by dashed lines. Discussion A Lateral Nonneural Domain of Cranial Neural Folds Produces Ecto- mesenchyme. Our results have allowed us to map the general lateral to the dorsal ridges and in underlying mesenchymal cells location of a lateral nonneural epithelial domain in the rostral (Fig. 3). These results contradict the notion that Wnt1-Cre-IR NF of early murine embryos (Fig. 6A, green shading) that cells arise solely from dorsal neural epithelium in these early produces ectomesenchyme.
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