New horizons at the caudal embryos: coordinated urogenital/reproductive organ formation by growth factor signaling

Suzuki, Kentaro; Economides, Aris N.; Yanagita, Motoko; Graf, Daniel; Yamada, Gen

doi:10.1016/j.gde.2009.08.004

Cited by 17 publications

(18 citation statements)

References 66 publications

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“…However, the possibility remains that an imperforate anus induced by elevated RA may be homologous in amphioxus and vertebrates in the sense that RA signaling is transmitted via comparable gene networks to elicit similar changes in downstream effector genes determining cell morphology and adhesion. Developmental genetic studies in vertebrates have indicated some genes that are key components in directing hindgut morphogenesis (Ramalho‐Santos et al ; Nakata et al ; Suzuki et al ). For example in the mouse, when RA is elevated prior to opening of the anus, there is downregulation of Shh and BMP4 , genes required for anus formation and normally expressed in the cloacal epithelium and underlying mesenchyme, respectively (Sasaki et al ).…”

Section: Discussionmentioning

confidence: 99%

Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death

Koop

Holland

Setiamarga

et al. 2011

Evolution and Development

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The vitamin A derived morphogen retinoic acid (RA) is known to function in the regulation of tissue proliferation and differentiation. Here, we show that exogenous RA applied to late larvae of the invertebrate chordate amphioxus can reverse some differentiated states. Although treatment with the RA antagonist BMS009 has no obvious effect on late larvae of amphioxus, administration of excess RA alters the morphology of the posterior end of the body. The anus closes over, and gut contents accumulate in the hindgut. In addition, the larval tail fin regresses, although little apoptosis takes place. This fin normally consists of columnar epidermal cells, each characterized by a ciliary rootlet running all the way from an apical centriole to the base of the cell and likely contributing substantial cytoskeletal support. After a few days of RA treatment, the rootlet becomes disrupted, and the cell shape changes from columnar to cuboidal. Transmission electron microscopy (TEM) shows fragments of the rootlet in the basal cytoplasm of the cuboidal cell. A major component of the ciliary rootlet in amphioxus is the protein Rootletin, which is encoded by a single AmphiRootletin gene. This gene is highly expressed in the tail epithelial cells of control larvae, but becomes downregulated after about a day of RA treatment, and the breakup of the ciliary rootlet soon follows. The effect of excess RA on these epidermal cells of the larval tail in amphioxus is unlike posterior regression in developing zebrafish, where elevated RA signaling alters connective tissues of mesodermal origin. In contrast, however, the RA-induced closure of the amphioxus anus has parallels in the RA-induced caudal regression syndrome of mammals.

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Section: Discussionmentioning

confidence: 99%

Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death

Koop

Holland

Setiamarga

et al. 2011

Evolution and Development

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“…While the cells of the vertebrate limb bud arise through an epithelial-to-mesenchymal transition (EMT) of an epithelial lateral plate mesoderm (LPM) population lining the coelomic cavity 11 , the developmental origin of external genitalia in vertebrates is still unclear. We developed a lenti-viral lineage tracing approach (see Methods), to systematically follow the two sources previously proposed, the LPM and tail bud 10 , 12 , 13 , in three amniote species, mouse, chicken and anole. Injections into the coelom of embryonic day 9.5 (E9.5) mouse embryos label cells surrounding the coelom as well as the developing hindlimb ( Fig.…”

mentioning

confidence: 99%

A relative shift in cloacal location repositions external genitalia in amniote evolution

Tschopp

Sherratt

Sanger

et al. 2014

Nature

101

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The move of vertebrates to a terrestrial lifestyle required major adaptations in their locomotory apparatus and reproductive organs. While the fin-to-limb transition has received considerable attention1,2, little is known about the developmental and evolutionary origins of external genitalia. Similarities in gene expression have been interpreted as a potential evolutionary link between the two anatomical structures3-6, yet without providing any underlying developmental mechanism. Here, we have reexamined this question using micro-Computed Tomography (μCT), lineage tracing in three amniote clades and RNA-Seq transcriptional profiling. We show that the developmental origin of external genitalia has shifted through evolution, and in some taxa limbs and genitals share a common primordium. In squamates, the genitalia develop directly from the budding hindlimbs, or the remnants thereof, whereas in mice the genital tubercle originates from the ventral and tail bud mesenchyme. The recruitment of different cell populations for genital outgrowth follows a change in the relative position of the cloaca, the genitalia organizing center. Ectopic grafting of the cloaca demonstrates the conserved ability of different mesenchymal cells to respond to these genitalia-inducing signals. Our results support a limb-like developmental origin of external genitalia as the ancestral condition. Moreover, it suggests that a change in the relative position of the cloacal signaling center during evolution has led to an altered developmental route of external genitalia in mammals, while preserving parts of the ancestral limb molecular circuitry due to a common evolutionary origin.

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“…These findings indicate the existence of developmental programs for the coordinated organogenesis of urogenital/reproductive tissues based on growth factor function and crosstalk. [6] Interestingly, structures that are developmentally separate from these caudal elements such as the brain, proximal spine and spinal cord, are generally spared by CRS. The consequences of the disruption after the maturation of spinal cord's caudal portion ensue after the 4 th week of gestation are different.…”

Section: Discussionmentioning

confidence: 99%

Scoliotic deformity and asymptomatic cervical syrinx in a 9 year old with caudal regression syndrome

et al. 2012

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New horizons at the caudal embryos: coordinated urogenital/reproductive organ formation by growth factor signaling

Cited by 17 publications

References 66 publications

Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death

Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death

A relative shift in cloacal location repositions external genitalia in amniote evolution

Scoliotic deformity and asymptomatic cervical syrinx in a 9 year old with caudal regression syndrome

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