Left–right asymmetric morphogenesis of the anterior midgut depends on the activation of a non-muscle myosin II in Drosophila

Okumura, Takashi; Fujiwara, Hiroo; Taniguchi, Kiichiro; Kuroda, Junpei; Nakazawa, Naotaka; Nakamura, Mitsutoshi; Hatori, Ryo; Ishio, Akira; Maeda, Reo; Matsuno, Kenji

doi:10.1016/j.ydbio.2010.05.501

Cited by 17 publications

(32 citation statements)

References 76 publications

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“…3D,E; and data not shown). Rotation of the gut in connection with loop formation (Okumura et al, 2010) results in stretching of the TARMs and bilateral asymmetry of their left and right anchoring sites ( Fig. 3F,F′; supplementary material Fig.…”

Section: T2mentioning

confidence: 99%

“…TARMs also establish intimate topological relations with cephalic branches of the trachea in their trajectory from thoracic lateral epidermis/exoskeleton to specific regions of the midgut. Rotation of the gut at the end of embryogenesis (Okumura et al, 2010) results in stretching and bilateral asymmetry of the left and right TARMs. This suggests that TARMs have elastic properties, as already indicated by their transient deformation upon interaction with the MT tip cell (Weavers and Skaer, 2013).…”

Section: Ams and Tarms And The Anatomical Organization Of The Larvamentioning

confidence: 99%

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An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

et al. 2014

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The T-box transcription factor Tbx1 and the LIM-homeodomain transcription factor Islet1 are key components in regulatory circuits that generate myogenic and cardiogenic lineage diversity in chordates. We show here that Org-1 and Tup, the Drosophila orthologs of Tbx1 and Islet1, are co-expressed and required for formation of the heart-associated alary muscles (AMs) in the abdomen. The same holds true for lineage-related muscles in the thorax that have not been described previously, which we name thoracic alary-related muscles (TARMs). Lineage analyses identified the progenitor cell for each AM and TARM. Three-dimensional highresolution analyses indicate that AMs and TARMs connect the exoskeleton to the aorta/heart and to different regions of the midgut, respectively, and surround-specific tracheal branches, pointing to an architectural role in the internal anatomy of the larva. Org-1 controls tup expression in the AM/TARM lineage by direct binding to two regulatory sites within an AM/TARM-specific cis-regulatory module, tupAME. The contributions of Org-1 and Tup to the specification of Drosophila AMs and TARMs provide new insights into the transcriptional control of Drosophila larval muscle diversification and highlight new parallels with gene regulatory networks involved in the specification of cardiopharyngeal mesodermal derivatives in chordates.

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Section: T2mentioning

confidence: 99%

Section: Ams and Tarms And The Anatomical Organization Of The Larvamentioning

confidence: 99%

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

et al. 2014

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“…We previously found that the first indication of LR symmetric morphogenesis in the AMG is observed as the LR asymmetric rearrangement of CVMU cells (Taniguchi et al, 2007b;Okumura et al, 2010). These rearrangements can be monitored by measuring the major axial angle of the nuclei in the CVMU cells to the midline of the AMG.…”

Section: 2mentioning

confidence: 99%

“…Several mutations that affect the laterality of some of these organs have been identified (Adá m et al, 2003;Hozumi et al, 2006;Spé der et al, 2006;Maeda et al, 2007;Taniguchi et al, 2007b;Okumura et al, 2010). For example, during metamorphosis in male Drosophila melanogaster, the external genitalia undergo a 360-degree clockwise (dextral) rotation, which causes the spermiduct to loop around the hindgut in a dextral direction (Gleichauf, 1936).…”

Section: Introductionmentioning

confidence: 99%

Canonical Wnt signaling in the visceral muscle is required for left–right asymmetric development of the Drosophila midgut

Kuroda

Nakamura

Yoshida

et al. 2012

Mechanisms of Development

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Many animals develop left-right (LR) asymmetry in their internal organs. The mechanisms of LR asymmetric development are evolutionarily divergent, and are poorly understood in invertebrates. Therefore, we studied the genetic pathway of LR asymmetric development in Drosophila. Drosophila has several organs that show directional and stereotypic LR asymmetry, including the embryonic gut, which is the first organ to develop LR asymmetry during Drosophila development. In this study, we found that genes encoding components of the Wnt-signaling pathway are required for LR asymmetric development of the anterior part of the embryonic midgut (AMG). frizzled 2 (fz2) and Wnt4, which encode a receptor and ligand of Wnt signaling, respectively, were required for the LR asymmetric development of the AMG. arrow (arr), an ortholog of the mammalian gene encoding low-density lipoprotein receptor-related protein 5/6, which is a co-receptor of the Wnt-signaling pathway, was also essential for LR asymmetric development of the AMG. These results are the first demonstration that Wnt signaling contributes to LR asymmetric development in invertebrates, as it does in vertebrates. The AMG consists of visceral muscle and an epithelial tube. Our genetic analyses revealed that Wnt signaling in the visceral muscle but not the epithelium of the midgut is required for the AMG to develop its normal laterality. Furthermore, fz2 and Wnt4 were expressed in the visceral muscles of the midgut. Consistent with these results, we observed that the LR asymmetric rearrangement of the visceral muscle cells, the first visible asymmetry of the developing AMG, did not occur in embryos lacking Wnt4 expression. Our results also suggest that canonical Wnt/β-catenin signaling, but not non-canonical Wnt signaling, is responsible for the LR asymmetric development of the AMG. Canonical Wnt/β-catenin signaling is reported to have important roles in LR asymmetric development in zebrafish. Thus, the contribution of canonical Wnt/β-catenin signaling to LR asymmetric development may be an evolutionarily conserved feature between vertebrates and invertebrates.

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“…55,56 Furthermore, a recent study has also shown that non-muscle myosin II is required for the l-r asymmetric development of the embryonic anterior midgut in Drosophila. 57 Thus, forces from actomyosin seem to represent a central aspect of l-r patterning in both worms and flies.…”

Section: O N O T D I S T R I B U T Ementioning

confidence: 99%

Left-right patterning in the C. elegans embryo

Pohl

2011

Communicative & Integrative Biology

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Left–right asymmetric morphogenesis of the anterior midgut depends on the activation of a non-muscle myosin II in Drosophila

Cited by 17 publications

References 76 publications

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

Canonical Wnt signaling in the visceral muscle is required for left–right asymmetric development of the Drosophila midgut

Left-right patterning in the C. elegans embryo

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