Somite Compartments in Amphioxus and Its Implications on the Evolution of the Vertebrate Skeletal Tissues

Mineralized skeletal tissues of vertebrates are an evolutionary novelty within the chordate lineage. While the progenitor cells that contribute to vertebrate skeletal tissues are known to have two embryonic origins, the mesoderm and neural crest, the evolutionary origin of their developmental process remains unclear. Using cephalochordate amphioxus as our model, we found that cells at the lateral wall of the amphioxus somite express SPARC (a crucial gene for tissue mineralization) and various collagen genes. During development, some of these cells expand medially to surround the axial structures, including the neural tube, notochord and gut, while others expand laterally and ventrally to underlie the epidermis. Eventually these cell populations are found closely associated with the collagenous matrix around the neural tube, notochord, and dorsal aorta, and also with the dense collagen sheets underneath the epidermis. Using known genetic markers for distinct vertebrate somite compartments, we showed that the lateral wall of amphioxus somite likely corresponds to the vertebrate dermomyotome and lateral plate mesoderm. Furthermore, we demonstrated a conserved role for BMP signaling pathway in somite patterning of both amphioxus and vertebrates. These results suggest that compartmentalized somites and their contribution to primitive skeletal tissues are ancient traits that date back to the chordate common ancestor. The finding of SPARC-expressing skeletal scaffold in amphioxus further supports previous hypothesis regarding SPARC gene family expansion in the elaboration of the vertebrate mineralized skeleton.

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Hippo signaling determines the number of venous pole cells that originate from the anterior lateral plate mesoderm in zebrafish

eLife ◽

10.7554/elife.29106 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 5

Author(s):

Hajime Fukui ◽

Takahiro Miyazaki ◽

Renee Wei-Yan Chow ◽

Hiroyuki Ishikawa ◽

Hiroyuki Nakajima ◽

...

Keyword(s):

Cell Number ◽

Bmp Signaling ◽

Hippo Signaling ◽

Lateral Plate Mesoderm ◽

Cardiomyocyte Proliferation ◽

Heart Tube ◽

Lateral Plate ◽

Large Tumor ◽

Developmental Potential ◽

Anterior Lateral Plate Mesoderm

The differentiation of the lateral plate mesoderm cells into heart field cells constitutes a critical step in the development of cardiac tissue and the genesis of functional cardiomyocytes. Hippo signaling controls cardiomyocyte proliferation, but the role of Hippo signaling during early cardiogenesis remains unclear. Here, we show that Hippo signaling regulates atrial cell number by specifying the developmental potential of cells within the anterior lateral plate mesoderm (ALPM), which are incorporated into the venous pole of the heart tube and ultimately into the atrium of the heart. We demonstrate that Hippo signaling acts through large tumor suppressor kinase 1/2 to modulate BMP signaling and the expression of hand2, a key transcription factor that is involved in the differentiation of atrial cardiomyocytes. Collectively, these results demonstrate that Hippo signaling defines venous pole cardiomyocyte number by modulating both the number and the identity of the ALPM cells that will populate the atrium of the heart.

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Multi-modal effects of BMP signaling on Nodal expression in the lateral plate mesoderm during left–right axis formation in the chick embryo

Developmental Biology ◽

10.1016/j.ydbio.2012.11.027 ◽

2013 ◽

Vol 374 (1) ◽

pp. 71-84 ◽

Cited By ~ 7

Author(s):

Kenjiro Katsu ◽

Norifumi Tatsumi ◽

Daisuke Niki ◽

Ken-ichi Yamamura ◽

Yuji Yokouchi

Keyword(s):

Chick Embryo ◽

Bmp Signaling ◽

Axis Formation ◽

Lateral Plate Mesoderm ◽

Lateral Plate

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BMP2 is a positive regulator of Nodal signaling during left-right axis formation in the chicken embryo

Development ◽

10.1242/dev.129.14.3421 ◽

2002 ◽

Vol 129 (14) ◽

pp. 3421-3429

Author(s):

Thomas Schlange ◽

Hans-Henning Arnold ◽

Thomas Brand

Keyword(s):

Bone Morphogenetic Proteins ◽

Target Genes ◽

Bmp Signaling ◽

Paraxial Mesoderm ◽

Axis Formation ◽

Nodal Signaling ◽

Lateral Plate Mesoderm ◽

Lateral Plate ◽

Positive Regulator ◽

The Right

A model of left-right axis formation in the chick involves inhibition of bone morphogenetic proteins by the antagonist Car as a mechanism of upregulating Nodal in the left lateral plate mesoderm. By contrast, expression of CFC, a competence factor, which is absolutely required for Nodal signaling in the lateral plate mesoderm is dependent on a functional BMP signaling pathway. We have therefore investigated the relationship between BMP and Nodal in further detail. We implanted BMP2 and Noggin-expressing cells into the left lateral plate and paraxial mesoderm and observed a strong upregulation of Nodal and its target genes Pitx2 and Nkx3.2. In addition Cfc, the Nodal type II receptor ActrIIa and Snr were found to depend on BMP signaling for their expression. Comparison of the expression domains of Nodal, Bmp2, Car and Cfc revealed co-expression of Nodal, Cfc and Bmp2, while Car and Nodal only partially overlapped. Ectopic application of BMP2, Nodal, and Car as well as combinations of this signaling molecules to the right lateral plate mesoderm revealed that BMP2 and Car need to synergize in order to specify left identity. We propose a novel model of left-right axis formation, which involves BMP as a positive regulator of Nodal signaling in the chick embryo.

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BMP signaling positively regulates Nodal expression during left right specification in the chick embryo

Development ◽

10.1242/dev.129.14.3431 ◽

2002 ◽

Vol 129 (14) ◽

pp. 3431-3440 ◽

Cited By ~ 2

Author(s):

M. Elisa Piedra ◽

Mana A. Ros

Keyword(s):

Bmp Signaling ◽

Lateral Plate Mesoderm ◽

Lateral Plate ◽

Positive Role ◽

Molecular Control ◽

Left And Right ◽

Left Right Asymmetry ◽

The Right ◽

Rapid Activation ◽

Positive Effect

Exogenous application of BMP to the lateral plate mesoderm (LPM) of chick embryos at the early somite stage had a positive effect on Nodal expression. BMP applications into the right LPM were followed by a rapid activation of Nodal, while applications into the left LPM resulted in expansion of the normal domain of Nodal expression. Conversely, blocking of BMP signaling by Noggin in the left LPM interfered with the activation of Nodal expression. These results support a positive role for endogenous BMP on Nodal expression in the LPM. We also report that BMP positively regulates the expression of Caronte, Snail and Cfc in both the left and right LPM. BMP-treated embryos had molecular impairment of the midline with downregulation of Lefty1, Brachyury and Shh but we also show that the midline defect was not sufficient to induce ectopic Nodal expression. We discuss our findings in the context of the known molecular control of the specification of left-right asymmetry.

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