Tup/Islet1 integrates time and position to specify muscle identity in <i>Drosophila</i>

Boukhatmi, Hadi; Frendo, Jean-Louis; Enriquez, Jonathan; Crozatier, Michèle; Dubois, L.; Víncent, Alaín

doi:10.1242/dev.083410

Cited by 26 publications

(51 citation statements)

References 68 publications

(104 reference statements)

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“…Tup is also expressed in AMs, in addition to the heart and the dorsal DA1, DA2, DO1 and DO2 muscles (Tao et al, 2007;Boukhatmi et al, 2012), dorsal ectoderm, amnioserosa and precursor cells of the pharynx (Thor and Thomas, 1997;Ashe et al, 2000). Expression of the org-1-HN39-lacZ (org-1-lacZ) reporter recapitulates org-1 expression in the somatic musculature (Schaub et al, 2012), while both IsletH-GFP and tupF4-GFP, two overlapping reporter constructs, reproduce tup expression in AMs (Tao et al, 2007;Boukhatmi et al, 2012).…”

Section: Resultsmentioning

confidence: 99%

“…Staining embryos at that stage for Tup and rp298(duf)-lacZ, a marker of muscle PCs and FCs (Nose et al, 1998), identified the four PCs at the origin of the DA1, DO2, DO1 and DA2 dorsal muscles, plus another cell located several cell diameters posterior to the DA2/AMP PC (Boukhatmi et al, 2012). Double staining for Org-1 and IsletH-GFP shows that this cell is the AM progenitor and is segmentally repeated along the posterior/anterior segmental border ( Fig.…”

Section: Am and Tarm Lineage Analysesmentioning

confidence: 99%

“…The absence of AMs in thoracic segments correlates with the anterior aorta ending at the T2/T3 boundary, and bending ventrally to form a funnel-shaped outflow tract that is anchored by the heart-anchoring cells and cardiac outflow muscles (Zmojdzian et al, 2008). We recently found that both Org-1 (Optomotor-blind-related-gene-1), which is the ortholog of the vertebrate T-box factor Tbx1, and Tailup (Tup), the ortholog of the LIM-homeodomain factor Islet1, are expressed in AMs, and we devised reporter genes that allow the embryonic development of these muscles to be followed (Schaub et al, 2012;Tao et al, 2007;Boukhatmi et al, 2012).…”

Section: Introductionmentioning

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: Resultsmentioning

confidence: 99%

Section: Am and Tarm Lineage Analysesmentioning

confidence: 99%

Section: Introductionmentioning

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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“…FCs dictate the number of cell fusion events that take place, leading to a characteristic number of nuclei for each muscle in the pattern . These fusing nuclei adopt the transcriptional profile of the original FC nucleus (Bourgouin et al 1992;D'Alessio and Frasch 1996;Ruiz-Gomez et al 1997;Jagla et al 1998;Keller et al 1998;Nose et al 1998;Crozatier and Vincent 1999;Knirr et al 1999;Duan et al 2007;Muller et al 2010;Carrasco-Rando et al 2011;Boukhatmi et al 2012;Schaub et al 2012), which determines the specific morphological features of each muscle fiber.The identity of each FC, and its capacity to confer this identify on the resulting muscle fiber, is determined by expression of a unique combination of transcription factors in FCs (Baylies et al 1998;Frasch 1999;Beckett and Baylies 2007;Tixier et al 2010). Correspondingly, the loss or misexpression of these identity transcription factors (iTFs) can affect the formation and morphology of the specific muscles in which they are expressed.…”

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confidence: 99%

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confidence: 99%

Muscle Cell Fate Choice Requires the T-Box Transcription Factor Midline in Drosophila

et al. 2015

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Drosophila Midline (Mid) is an ortholog of vertebrate Tbx20, which plays roles in the developing heart, migrating cranial motor neurons, and endothelial cells. Mid functions in cell-fate specification and differentiation of tissues that include the ectoderm, cardioblasts, neuroblasts, and egg chambers; however, a role in the somatic musculature has not been described. We identified mid in genetic and molecular screens for factors contributing to somatic muscle morphogenesis. Mid is expressed in founder cells (FCs) for several muscle fibers, and functions cooperatively with the T-box protein H15 in lateral oblique muscle 1 and the segment border muscle. Mid is particularly important for the specification and development of the lateral transverse (LT) muscles LT3 and LT4, which arise by asymmetric division of a single muscle progenitor. Mid is expressed in this progenitor and its two sibling FCs, but is maintained only in the LT4 FC. Both muscles were frequently missing in mid mutant embryos, and LT4-associated expression of the transcription factor Krüppel (Kr) was lost. When present, LT4 adopted an LT3-like morphology. Coordinately, mid misexpression caused LT3 to adopt an LT4-like morphology and was associated with ectopic Kr expression. From these data, we concluded that mid functions first in the progenitor to direct development of LT3 and LT4, and later in the FCs to influence whichever of these differentiation profiles is selected. Mid is the first T-box factor shown to influence LT3 and LT4 muscle identity and, along with the T-box protein Optomotor-blind-related-gene 1 (Org-1), is representative of a new class of transcription factors in muscle specification. KEYWORDS midline; Tbx20; founder cell; muscle identity; differentiation T HE body wall muscles of the Drosophila larva are composed of a stereotypic pattern that includes 30 unique muscle fibers (each a single myotube) per abdominal hemisegment (Bate 1990). These muscles form during embryogenesis, during which time they take on unique characteristics such as size, shape, pattern of innervation, and epidermal attachment Baylies et al. 1998;Frasch 1999;De Joussineau et al. 2012). The unique identity of each muscle fiber is conferred through overlapping signaling pathways and cell autonomous transcription factors that specify muscle progenitors Baylies et al. 1998;Frasch 1999;Tixier et al. 2010), which then undergo asymmetric cell division to generate founder cells (FCs) (Bate 1990;Carmena et al. 1998). A single FC initiates the formation of multinucleate syncytia by fusing with fusion competent myoblasts (FCMs) (Rochlin et al. 2010;Abmayr and Pavlath 2012). FCs dictate the number of cell fusion events that take place, leading to a characteristic number of nuclei for each muscle in the pattern . These fusing nuclei adopt the transcriptional profile of the original FC nucleus (Bourgouin et al. 1992;D'Alessio and Frasch 1996;Ruiz-Gomez et al. 1997;Jagla et al. 1998;Keller et al. 1998;Nose et al. 1998;Crozatier and Vincent 1999;Knirr et al. 1999;D...

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Chip/Ldb1 interacts with Tailup/islet1 to regulate cardiac gene expression in Drosophila

Werner¹,

Donow²,

Pandur³

2017

Genesis

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The LIM-homeodomain transcription factor Tailup (Tup) is a component of the complex cardiac transcriptional network governing specification and differentiation of cardiac cells in Drosophila. LIM-domain containing factors are known to interact with the adaptor molecule Chip/Ldb1 to form higher order protein complexes to regulate gene expression thereby determining a cell's developmental fate. However, with respect to Drosophila heart development, it has not been investigated yet, whether Chip and tup interact to regulate the generation of different cardiac cell types. Here we show that Chip is required for normal heart development and that it interacts with tup in this context. Particularly the number of Odd skipped-expressing pericardial cells depends on balanced amounts of Chip and Tup. Data from luciferase assays using Hand- and even-skipped reporter constructs in Drosophila S2 cells indicate that Chip and Tup act as a tetrameric complex on the regulatory regions of Hand and even-skipped (eve). Finally we have identified and verified five Tup binding sites in the eve mesodermal enhancer, which adds Tup as novel factor to directly regulate eve expression. Taken together this study provides novel findings regarding cardiac gene expression regulation in Drosophila.

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Tup/Islet1 integrates time and position to specify muscle identity in Drosophila

Cited by 26 publications

References 68 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

Muscle Cell Fate Choice Requires the T-Box Transcription Factor Midline in Drosophila

Chip/Ldb1 interacts with Tailup/islet1 to regulate cardiac gene expression in Drosophila

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