DE-Cadherin regulates unconventional Myosin ID and Myosin IC in <i>Drosophila</i> left-right asymmetry establishment

Petzoldt, Astrid G.; Coutelis, Jean-Baptiste; Géminard, Charles; Spéder, Pauline; Cerezo, Delphine; Noselli, Stéphane

doi:10.1242/jcs.112862

Cited by 16 publications

(50 citation statements)

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“…The overexpression of Myo61F in wild-type embryos results in LR inversion of the embryonic pmg and hg and the male genitalia (Hozumi et al 2006(Hozumi et al , 2008Petzoldt et al 2012). We also reported that the ubiquitous overexpression of Myo31DF reverses the LR asymmetry of the fg and amg, whereas the Myo31DF loss-of-function mutant does not show LR inversion in these organs (Hozumi et al 2006).…”

Section: Lr Asymmetric Development Of the Embryonic Gut Does Not Invomentioning

confidence: 53%

“…This result suggests that the sinistral activity of Myo61F was independent of Myo31DF. This finding prompted us to reconsider the previously proposed model suggesting that Myo61F does not have intrinsic sinistral activity, but rather acts as a negative regulator of Myo31DF (Hozumi et al 2006;Petzoldt et al 2012). However, despite the strong sinistral activity of overexpressed Myo61F, there was no detectable effect of the Myo61F loss-of-function mutation, even in combination with Myo31DF and/or Myo95E mutations, on the LR asymmetric development of the embryonic gut ( Figure 3F).…”

Section: Lr Asymmetric Development Of the Embryonic Gut Does Not Invomentioning

confidence: 80%

“…These results demonstrated that class I myosins are not essential for survival itself, but are required for optimal hatching and survival rates, and thus are important mediators in Drosophila, at least under our experimental conditions. Differential expression of Myo31DF, Myo61F, and Myo95E during embryogenesis Myo31DF and Myo61F mRNAs and their protein products are detected in the gut epithelium and genital disc (Morgan et al 1995;Hozumi et al 2006;Speder et al 2006;Petzoldt et al 2012). To gain insight into the tissue-specific roles and functional redundancy of the three class I myosins in the LR asymmetric development of the embryonic gut, we analyzed their expression in embryos, using in situ hybridization.…”

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confidence: 99%

“…Myo31DF is involved in the development of left-right (LR) asymmetry (Hozumi et al 2006;Speder et al 2006), and its loss leads to the LR inversion of several organs, including the embryonic gut, male genital plate, spermiduct, and testes (Hozumi et al 2006;Speder et al 2006). Myo61F is required for maintenance of the enterocyte brush border structure, as determined genetically (Hegan et al 2007), while its roles in LR asymmetric development are mostly based on overexpression and RNA interference experiments (Hozumi et al 2006(Hozumi et al , 2008Petzoldt et al 2012). Myo61F overexpression antagonizes Myo31DF's function, leading to LR inversion of the embryonic gut and the male genitalia (Hozumi et al 2008;Petzoldt et al 2012), and a model was proposed suggesting that overexpressed Myo61F prevents the binding of Myo31DF to adherens junction components, leading to impaired LR rotation of the male genitalia (Petzoldt et al 2012).…”

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confidence: 99%

“…Myo61F is required for maintenance of the enterocyte brush border structure, as determined genetically (Hegan et al 2007), while its roles in LR asymmetric development are mostly based on overexpression and RNA interference experiments (Hozumi et al 2006(Hozumi et al , 2008Petzoldt et al 2012). Myo61F overexpression antagonizes Myo31DF's function, leading to LR inversion of the embryonic gut and the male genitalia (Hozumi et al 2008;Petzoldt et al 2012), and a model was proposed suggesting that overexpressed Myo61F prevents the binding of Myo31DF to adherens junction components, leading to impaired LR rotation of the male genitalia (Petzoldt et al 2012). In contrast, no studies of Myo95E have been reported.…”

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confidence: 99%

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Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development in Drosophila

et al. 2015

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The class I myosin genes are conserved in diverse organisms, and their gene products are involved in actin dynamics, endocytosis, and signal transduction. Drosophila melanogaster has three class I myosin genes, Myosin 31DF (Myo31DF), Myosin 61F (Myo61F), and Myosin 95E (Myo95E). Myo31DF, Myo61F, and Myo95E belong to the Myosin ID, Myosin IC, and Myosin IB families, respectively. Previous loss-of-function analyses of Myo31DF and Myo61F revealed important roles in left-right (LR) asymmetric development and enterocyte maintenance, respectively. However, it was difficult to elucidate their roles in vivo, because of potential redundant activities. Here we generated class I myosin double and triple mutants to address this issue. We found that the triple mutant was viable and fertile, indicating that all three class I myosins were dispensable for survival. A loss-of-function analysis revealed further that Myo31DF and Myo61F, but not Myo95E, had redundant functions in promoting the dextral LR asymmetric development of the male genitalia. Myo61F overexpression is known to antagonize the dextral activity of Myo31DF in various Drosophila organs. Thus, the LR-reversing activity of overexpressed Myo61F may not reflect its physiological function. The endogenous activity of Myo61F in promoting dextral LR asymmetric development was observed in the male genitalia, but not the embryonic gut, another LR asymmetric organ. Thus, Myo61F and Myo31DF, but not Myo95E, play tissue-specific, redundant roles in LR asymmetric development. Our studies also revealed differential colocalization of the class I myosins with filamentous (F)-actin in the brush border of intestinal enterocytes.KEYWORDS myosin I; Myosin 31DF; Myosin 61F; Myosin 95E; left-right asymmetry T HE class I myosin genes encode myosin heavy chains, which are conserved in phylogenetically diverse organisms (Sellers 2000;Krendel and Mooseker 2005). The class I myosins are nonfilamentous, actin-based motor proteins and were the first discovered unconventional myosin proteins. These myosins are involved in a variety of cellular processes, such as cell migration, cell adhesion, and cell growth, through their regulation of actin dynamics, endocytosis, and signal transduction (Osherov and May 2000;Krendel and Mooseker 2005;Kim and Flavell 2008;McConnell and Tyska 2010).The structure of the myosin I heavy chains is evolutionarily conserved and composed of head (or motor), neck, and tail domains ( Figure 1A) (Coluccio 1997;Barylko et al. 2000). The head domain binds to filamentous (F)-actin and adenosine triphosphate (ATP), a common feature of myosin proteins ( Figure 1A) (Mermall et al. 1998); the neck domain possesses one or more IQ motifs, which directly interact with calmodulin or calmodulin-related myosin light chains (Coluccio 1997;Barylko et al. 2000), and the tail domains are divided into short and long types. Short tails contain a single tail homology 1 (TH1) domain, which is rich in basic residues and thought to interact with plasma membranes (Coluccio 1997;Barylko...

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Section: Lr Asymmetric Development Of the Embryonic Gut Does Not Invomentioning

confidence: 53%

Section: Lr Asymmetric Development Of the Embryonic Gut Does Not Invomentioning

confidence: 80%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development in Drosophila

et al. 2015

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Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

Namigai

Kenny

Shimeld

2014

Genesis

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Directional left/right (LR) asymmetries, in which there are consistent, heritable differences in morphology between the left and right sides of bilaterally symmetrical organisms, are found in animals across the Bilateria. For many years, we have lacked evidence for shared mechanisms underlying their development. This led to the supposition that the mechanisms driving establishment of LR asymmetries, and consequently the asymmetries themselves, had evolved separately in the three major Superphyla that constitute the Bilateria. The recent discovery that the transforming growth factor-beta (TGF-B) ligand Nodal plays a role in the regulation of LR asymmetry in both Deuterostomia and Lophotrochozoa has reignited debate in this field, as it suggests that at least this aspect of the development of the LR axis is conserved. In this review, we discuss evidence for shared mechanisms of LR asymmetry establishment across the bilaterian tree of life and consider how these mechanisms might have diverged across the Metazoa over the last 500 million years or so of evolution. As well as the likelihood that Nodal is an ancestral mechanism for regulating LR asymmetry, we reemphasize cytoskeletal architecture as a potential shared mechanism underlying symmetry breaking. However, convergent evolution remains a distinct possibility and study of a wider diversity of species will be needed to distinguish between conserved and lineage-specific mechanisms. genesis 52:458-470,

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The myosin ID pathway and left–right asymmetry in Drosophila

Géminard

González-Morales

Coutelis

et al. 2014

Genesis

Self Cite

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Summary: Drosophila is a classical model to study body patterning, however left-right (L/R) asymmetry had remained unexplored, until recently. The discovery of the conserved myosin ID gene as a major determinant of L/R asymmetry has revealed a novel L/R pathway involving the actin cytoskeleton and the adherens junction. In this process, the HOX gene Abdominal-B plays a major role through the control of myosin ID expression and therefore symmetry breaking. In this review, we present organs and markers showing L/R asymmetry in Drosophila and discuss our current understanding of the underlying molecular genetic mechanisms. Drosophila represents a valuable model system revealing novel strategies to establish L/R asymmetry in invertebrates and providing an evolutionary perspective to the problem of laterality in bilateria. genesis 52:471-480,

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DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment

Cited by 16 publications

References 1 publication

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development in Drosophila

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development in Drosophila

Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

The myosin ID pathway and left–right asymmetry in Drosophila

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