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The Forkhead Genes, Foxc1 and Foxc2, Regulate Paraxial Versus Intermediate Mesoderm Cell Fate

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The Forkhead Genes, Foxc1 and Foxc2, Regulate Paraxial Versus Intermediate Mesoderm Cell Fate View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Developmental Biology 271 (2004) 176–189 www.elsevier.com/locate/ydbio The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate Bettina Wilm,a,1 Richard G. James,b Thomas M. Schultheiss,b and Brigid L.M. Hoganc,* a Department of Cell Biology, Vanderbilt University, Nashville, TN 37232, USA b Molecular Medicine Unit, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02215, USA c Department of Cell Biology, Duke University Medical Center, Durham, NC 27710, USA Received for publication 28 October 2003, revised 15 March 2004, accepted 22 March 2004 Available online 4 May 2004 Abstract During vertebrate embryogenesis, the newly formed mesoderm is allocated to the paraxial, intermediate, and lateral domains, each giving rise to different cell and tissue types. Here, we provide evidence that the forkhead genes, Foxc1 and Foxc2, play a role in the specification of mesoderm to paraxial versus intermediate fates. Mouse embryos lacking both Foxc1 and Foxc2 show expansion of intermediate mesoderm markers into the paraxial domain, lateralization of somite patterning, and ectopic and disorganized mesonephric tubules. In gain of function studies in the chick embryo, Foxc1 and Foxc2 negatively regulate intermediate mesoderm formation. By contrast, their misexpression in the prospective intermediate mesoderm appears to drive cells to acquire paraxial fate, as revealed by expression of the somite markers Pax7 and Paraxis. Taken together, the data indicate that Foxc1 and Foxc2 regulate the establishment of paraxial versus intermediate mesoderm cell fates in the vertebrate embryo. D 2004 Elsevier Inc. All rights reserved. Keywords: Forkhead genes; Paraxial mesoderm; Intermediate mesoderm; Fate commitment; Mouse embryo; Chick embryo Introduction intermediate mesoderm (precursors of the kidney and gonads) and lateral plate mesoderm (precursors of the body In the embryo of higher vertebrates (amniotes), the meso- wall and the limbs). The most posterior streak cells migrate derm is generated during gastrulation when cells delaminate caudally to generate extraembryonic mesoderm (James and from the epiblast and move through the primitive streak into Schultheiss, 2003; Parameswaran and Tam, 1995; Psychoyos the region between the endoderm and ectoderm. Several and Stern, 1996; Schoenwolf et al., 1992; Smith et al., 1994; mechanisms are known to control mesodermal cell fate, Wilson and Beddington, 1996; Yang et al., 2002). However, including the anterior–posterior level at which they traverse fate mapping experiments alone do not indicate when mes- the streak, and local signals from neighboring tissues. Fate odermal cells are irreversibly committed to different fates. mapping studies in the mouse and chick indicate that mes- Heterotopic grafting experiments have revealed that cells endoderm precursors in the most anterior streak contribute to within the streak are still developmentally labile (Garcia- the node, midline notochord, and head mesoderm. Cells that Martinez and Schoenwolf, 1992; Parameswaran and Tam, emerge behind the node give rise to the paraxial mesoderm 1995). In the case of paraxial mesoderm cells, it appears that (future somites) adjacent to the midline, while cells that irreversible commitment to somite fate is only achieved after emerge at more caudal levels give rise sequentially to cells have been incorporated into epithelial somites (Tam and Trainor, 1994). The fate of anterior intermediate mesoderm in the chick is determined by Hamburger–Hamilton (HH) stage * Corresponding author. Department of Cell Biology, Duke University 8–9, concomitant with onset of expression of the intermedi- Medical Center, Box 3709, Durham, NC 27710. Fax: +1-919-684-8592. E-mail address: [email protected] (B.L.M. Hogan). ate mesoderm specific transcription factors, Lhx1 and Pax2 1 Current address: Divison of Cardiovascular Medicine, Vanderbilt (James and Schultheiss, 2003). It is not yet known when the University, Nashville, TN 37232, USA. lateral mesoderm is irreversibly committed. 0012-1606/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2004.03.034 B. Wilm et al. / Developmental Biology 271 (2004) 176–189 177 A number of factors have been identified that function transcripts is graded along the mediolateral axis, with in local signaling networks to regulate early mesoderm highest levels closest to the midline (Kume et al., 2000; development. Among these are secreted molecules pro- Sasaki and Hogan, 1993). Consistent with these expres- duced in the node (Fgf4, Nodal, Shh, Noggin), the sion domains, embryos homozygous null for either Foxc1 notochord (Shh, Noggin), the primitive streak (Fgf4, or Foxc2, or compound heterozygotes, exhibit deficiencies Fgf8, Wnt3a), and the lateral plate mesoderm (Bmp4). in tissues derived from the paraxial mesoderm and head Wnt3a is required for the development of all but the most mesenchyme, while Foxc1 and Foxc2 compound null anterior paraxial mesoderm, because Wnt3a-null embryos embryos completely lack morphological somites (Iida et lack somites posterior to somite 5–7, and instead display al., 1997; Kume et al., 1998, 2001; Winnier et al., 1997). ectopic neural tissues on either side of the neural tube Furthermore, single null embryos and compound hetero- (Takada et al., 1994; Yoshikawa et al., 1997). A critical zygotes have supernumerary mesonephric tubules and role for FGF signaling in early mesoderm morphogenesis ectopic ureter buds, tissues derived from the intermediate and patterning has been demonstrated in both the mouse mesoderm, leading to later malformations of the urogen- (Ciruna and Rossant, 2001; Deng et al., 1994; Sun et al., ital tract (Kume et al., 2000). 1999; Yamaguchi et al., 1994) and chick (Yang et al., In this paper, we have investigated the role of Foxc1 2002). Finally, Bmp4 signaling appears to act as a and Foxc2 in the early mediolateral patterning of the lateralizing/ventralizing factor for mesoderm. For exam- mesoderm. We show that in the Foxc1; Foxc2 compound ple, in the chick embryo, cells expressing the Bmp4 homozygous-null embryos, the paraxial mesoderm is antagonist Noggin induce a paraxial mesoderm fate when respecified so that instead of forming somites, cells grafted into nascent lateral plate mesoderm. By contrast, express markers characteristic of intermediate mesoderm. ectopic expression of Bmp4 in the presomitic mesoderm Furthermore, Foxc1 and Foxc2 appear to act in a dose- results in the conversion of presumptive paraxial meso- dependent fashion, since progressive loss of functional derm to lateral plate mesoderm fate (Tonegawa and Foxc2 alleles is associated with increasing lateralization of Takahashi, 1998; Tonegawa et al., 1997). the paraxial and somitic mesoderm. The expanded inter- Local signaling also regulates the mediolateral patterning mediate mesoderm domain of Foxc1; Foxc2 compound of newly formed somites. Thus, dorsolateral dermomyotome mutants gives rise to disorganized aggregates of cells and ventromedial sclerotome identities are established by expressing markers for nephric duct and mesonephric coordinated signaling from the notochord and floorplate tubules. Finally, by ectopically expressing Foxc1 or Foxc2 (Shh), the roofplate and surface ectoderm (Bmp4, Wnts), in chick embryos, we provide functional evidence that and the lateral plate mesoderm (Bmp4) (Hirsinger et al., both genes are able to convert cells from an intermediate 1997; Johnson et al., 1994; Marcelle et al., 1997, 1999; to a paraxial cell fate. Pourquie et al., 1996; Reshef et al., 1998; Teillet et al., 1998; Watanabe et al., 1998). Furthermore, dorsal–ventral patterning of the dermomyotome results in the formation of Materials and methods medial and lateral domains that express different myogenic genes and display specific behaviors (reviewed in Bucking- Mutant mice and embryos ham, 2001 and Pownall et al., 2002). Among the transcriptional regulators expressed during Generation and genotyping of Foxc1; Foxc2 compound early mesoderm development are Foxf1 and the closely heterozygous mice were essentially as described (Kume et related Foxc1 and Foxc2, members of the family of al., 2001). Noon of the day of plug was E0.5. Compound forkhead/winged helix DNA binding proteins (Carlsson homozygous and heterozygous embryos were generated by and Mahlapuu, 2002). Foxf1 is expressed in mesoderm mating compound heterozygotes. Wild-type control embry- cells emerging from the primitive streak that will form os were pooled, and included embryos single heterozygous lateral plate and extraembryonic mesoderm (Mahlapuu et for either gene. Genotyping was performed on DNA from al., 2001; Peterson et al., 1997).InFoxf1-null mutant embryonic yolk sacs. At least two embryos of each geno- embryos, separation of the lateral mesoderm into splanch- type were used for expression analysis. Somite number was nic and somatic mesoderm is impaired, and splanchnic generally used for staging embryos. In the case of com- mesoderm appears to be converted into somatic mesoderm pound homozygous embryos, where no somites are formed, (Mahlapuu et al., 2001). Foxc1 and Foxc2 are expressed similar-sized littermates were used. in almost identical patterns in cells destined to form cephalic, paraxial, and intermediate mesoderm. Expression Foxc1 and Foxc2 overexpression constructs and is first seen at the presomite
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