Role of paraxial mesoderm in limb/flank regionalization of the trunk lateral plate

Noro, Miyuki; Yuguchi, Hiroki; Sato, T.; Tsuihiji, Takanobu; Yonei‐Tamura, Sayuri; Yokoyama, Hitoshi; Wakamatsu, Yoshio; Tamura, Koji

doi:10.1002/dvdy.22666

Cited by 11 publications

(9 citation statements)

References 60 publications

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“…Chick embryos were processed for whole‐mount in situ hybridization as described previously (Yonei et al, ), using antisense RNA probes for chick Fgf8 , a reliable marker for the AER (Ohuchi et al, ). To detect apoptosis in the limb bud, whole‐mount TUNEL was performed as described previously (Noro et al, ). For Nile Blue staining, another method of detecting apoptosis, a 1:10,000 dilution of Nile Blue in PBS was injected into a cavity of the amnioserosa membrane, and the embryos were incubated for 30 min at 38°C.…”

Section: Methodsmentioning

confidence: 99%

Altered developmental events in the anterior region of the chick forelimb give rise to avian‐specific digit loss

Nomura

Yokoyama

Tamura

2014

Developmental Dynamics

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Background: Avian forelimb (wing) contains only three digits, and the three-digit formation in the bird forelimb is one of the avian-specific limb characteristics that have been evolutionarily inherited from the common ancestral form in dinosaurs. Despite many studies on digit formation in the chick limb bud, the developmental mechanisms giving rise to the three-digit forelimb in birds have not been completely clarified. Results: To identify which cell populations of the early limb bud contribute to digit formation in the late limb bud, fate maps of the early fore-and hindlimb buds were prepared. Based on these fate maps, we found that the digit-forming region in the forelimb bud is narrower than that in the hindlimb bud, suggesting that some developmental mechanisms on the anterior-most region lead to a reduced number of digits in the forelimb. We also found temporal differences in the onset of appearance of the ANZ (anterior necrotic zone) as well as differences in the position of the anterior edge of the AER. Conclusions: Forelimb-specific events in the anterior limb bud are possible developmental mechanisms that might generate the different cell fates in the fore-and hindlimb buds, regulating the number of digits in birds. Developmental Dynamics 243:741-752,

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Section: Methodsmentioning

confidence: 99%

Altered developmental events in the anterior region of the chick forelimb give rise to avian‐specific digit loss

Nomura

Yokoyama

Tamura

2014

Developmental Dynamics

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“…Before this stage, development of a wing only results if medial (dorsal) presomitic mesoderm is included in the transplants from the wing‐forming level (Kieny, ; Noro et al. ). This has been interpreted as being due to the presomitic mesoderm producing a limb‐induction signal.…”

Section: Determination Of Lateral Plate Mesoderm To Form a Limbmentioning

confidence: 99%

How the embryo makes a limb: determination, polarity and identity

Tickle

2015

Journal of Anatomy

109

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The vertebrate limb with its complex anatomy develops from a small bud of undifferentiated mesoderm cells encased in ectoderm. The bud has its own intrinsic polarity and can develop autonomously into a limb without reference to the rest of the embryo. In this review, recent advances are integrated with classical embryology, carried out mainly in chick embryos, to present an overview of how the embryo makes a limb bud. We will focus on how mesoderm cells in precise locations in the embryo become determined to form a limb and express the key transcription factors Tbx4 (leg/hindlimb) or Tbx5 (wing/forelimb). These Tbx transcription factors have equivalent functions in the control of bud formation by initiating a signalling cascade involving Wnts and fibroblast growth factors (FGFs) and by regulating recruitment of mesenchymal cells from the coelomic epithelium into the bud. The mesoderm that will form limb buds and the polarity of the buds is determined with respect to both anteroposterior and dorso-ventral axes of the body. The position in which a bud develops along the antero-posterior axis of the body will also determine its identity -wing/forelimb or leg/hindlimb. Hox gene activity, under the influence of retinoic acid signalling, is directly linked with the initiation of Tbx5 gene expression in the region along the antero-posterior axis of the body that will form wings/forelimbs and determines antero-posterior polarity of the buds. In contrast, Tbx4 expression in the regions that will form legs/hindlimbs is regulated by the homeoprotein Pitx1 and there is no evidence that Hox genes determine antero-posterior polarity of the buds. Bone morphogenetic protein (BMP) signalling determines the region along the dorso-ventral axis of the body in which both wings/forelimbs and legs/hindlimbs develop and dorso-ventral polarity of the buds. The polarity of the buds leads to the establishment of signalling regions -the dorsal and ventral ectoderm, producing Wnts and BMPs, respectively, the apical ectodermal ridge producing fibroblast growth factors and the polarizing region, Sonic hedgehog (Shh). These signals are the same in both wings/forelimbs and legs/hindlimbs and control growth and pattern formation by providing the mesoderm cells of the limb bud as it develops with positional information. The precise anatomy of the limb depends on the mesoderm cells in the developing bud interpreting positional information according to their identity -determined by Pitx1 in hindlimbs -and genotype. The competence to form a limb extends along the entire antero-posterior axis of the trunk -with Hox gene activity inhibiting the formation of forelimbs in the interlimb region -and also along the dorso-ventral axis.

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“…Noro et al. () showed that the regionalisation of the presomitic mesoderm along the embryonic axis by the Hox code is responsible for the specification of the limb and flank fields in the chick embryo (Noro et al. ).…”

Section: Developmentmentioning

confidence: 99%

“…() showed that the regionalisation of the presomitic mesoderm along the embryonic axis by the Hox code is responsible for the specification of the limb and flank fields in the chick embryo (Noro et al. ). Through transplant and ablation experiments it was shown that the presomitic mesoderm adjacent to the prospective limb field is permissive to the development of a limb field and affects the size of the limb field while the paraxial mesoderm adjacent to the flank suppresses limb bud development (Noro et al.…”

Section: Developmentmentioning

confidence: 99%

“…Through transplant and ablation experiments it was shown that the presomitic mesoderm adjacent to the prospective limb field is permissive to the development of a limb field and affects the size of the limb field while the paraxial mesoderm adjacent to the flank suppresses limb bud development (Noro et al. ). In addition, it has been suggested that Hox transcription factors may be responsible for the restricted patterns of Tbx4 (Minguillon et al.…”

Section: Developmentmentioning

confidence: 99%

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The evolutionary history of the development of the pelvic fin/hindlimb

2012

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SummaryThe arms and legs of man are evolutionarily derived from the paired fins of primitive jawed fish. Few evolutionary changes have attracted as much attention as the origin of tetrapod limbs from the paired fins of ancestral fish. The hindlimbs of tetrapods are derived from the pelvic fins of ancestral fish. These evolutionary origins can be seen in the examination of shared gene and protein expression patterns during the development of pelvic fins and tetrapod hindlimbs. The pelvic fins of fish express key limb positioning, limb bud induction and limb outgrowth genes in a similar manner to that seen in hindlimb development of higher vertebrates. We are now at a point where many of the key players in the development of pelvic fins and vertebrate hindlimbs have been identified and we can now readily examine and compare mechanisms between species. This is yielding fascinating insights into how the developmental programme has altered during evolution and how that relates to anatomical change. The role of pelvic fins has also drastically changed over evolutionary history, from playing a minor role during swimming to developing into robust weight-bearing limbs. In addition, the pelvic fins/hindlimbs have been lost repeatedly in diverse species over evolutionary time. Here we review the evolution of pelvic fins and hindlimbs within the context of the changes in anatomical structure and the molecular mechanisms involved.

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Role of paraxial mesoderm in limb/flank regionalization of the trunk lateral plate

Cited by 11 publications

References 60 publications

Altered developmental events in the anterior region of the chick forelimb give rise to avian‐specific digit loss

Altered developmental events in the anterior region of the chick forelimb give rise to avian‐specific digit loss

How the embryo makes a limb: determination, polarity and identity

The evolutionary history of the development of the pelvic fin/hindlimb

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