An unconventional myosin in Drosophila reverses the default handedness in visceral organs

Hozumi, Shunya; Maeda, Reo; Taniguchi, Kiichiro; Kanai, Maiko; Shirakabe, Syuichi; Sasamura, Takeshi; Spéder, Pauline; Noselli, Stéphane; Aigaki, Toshiro; Murakami, Ryutaro; Matsuno, Kenji

doi:10.1038/nature04625

Cited by 199 publications

(336 citation statements)

References 29 publications

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“…LR asymmetry is established in some animals during early developmental stages, long before cilia are present or in some cases, with no cilia present at all; these include snails (Meshcheryakov and Beloussov, 1975;Shibazaki et al, 2004), sea urchin (Kitazawa and Amemiya, 2007), Drosophila (Hozumi et al, 2006;Coutelis et al, 2008), Arabidopsis (Hashimoto, 2002;Thitamadee et al, 2002;Abe et al, 2004), and C. elegans (Priess, 1994;Hutter and Schnabel, 1995), for example. Other animals establish the LR axis later in development, when thousands of cells are present, but also without using cilia.…”

Section: Many Phyla Establish Lr Asymmetry Without Ciliary Flowsmentioning

confidence: 99%

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

Vandenberg

Levin

2010

Developmental Dynamics

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Consistent laterality is a crucial aspect of embryonic development, physiology, and behavior. While strides have been made in understanding unilaterally expressed genes and the asymmetries of organogenesis, early mechanisms are still poorly understood. One popular model centers on the structure and function of motile cilia and subsequent chiral extracellular fluid flow during gastrulation. Alternative models focus on intracellular roles of the cytoskeleton in driving asymmetries of physiological signals or asymmetric chromatid segregation, at much earlier stages. All three models trace the origin of asymmetry back to the chirality of cytoskeletal organizing centers, but significant controversy exists about how this intracellular chirality is amplified onto cell fields. Analysis of specific predictions of each model and crucial recent data on new mutants suggest that ciliary function may not be a broadly conserved, initiating event in left-right patterning. Many questions about embryonic left-right asymmetry remain open, offering fascinating avenues for further research in cell, developmental, and evolutionary biology. Developmental Dynamics 239:3131-3146,

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Section: Many Phyla Establish Lr Asymmetry Without Ciliary Flowsmentioning

confidence: 99%

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

Vandenberg

Levin

2010

Developmental Dynamics

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“…The use of isolated F-actin binding domains from proteins such as moesin or fimbrim [Edwards et al, 1997;Sheahan et al, 2004] has the potential to overcome this problem, but in general, the properties of a given F-actin binding protein or domain used for in vivo F-actin labeling have not been characterized with respect to their effects on F-actin stability. Further, in some cases, such constructs have been reported to alter actin-dependent processes in vivo [Hozumi et al, 2006].…”

Section: Introductionmentioning

confidence: 99%

Versatile fluorescent probes for actin filaments based on the actin‐binding domain of utrophin

Burkel

Dassow

Bement

2007

Cell Motil. Cytoskeleton

448

485

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Actin filaments (F-actin) are protein polymers that undergo rapid assembly and disassembly and control an enormous variety of cellular processes ranging from force production to regulation of signal transduction. Consequently, imaging of F-actin has become an increasingly important goal for biologists seeking to understand how cells and tissues function. However, most of the available means for imaging F-actin in living cells suffer from one or more biological or experimental shortcomings. Here we describe fluorescent F-actin probes based on the calponin homology domain of utrophin (Utr-CH), which binds F-actin without stabilizing it in vitro. We show that these probes faithfully report the distribution of F-actin in living and fixed cells, distinguish between stable and dynamic F-actin, and have no obvious effects on processes that depend critically on the balance of actin assembly and disassembly.

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“…These findings indicate that Myo95E 1 and Myo95E 2 are null alleles of Myo95E. We used the Myo95E 1 allele in subsequent studies, because it had a larger deletion than Myo95E 2 ( Figure 1C).Myo31DF or Myo61F homozygous mutant flies were previously reported to be viable and fertile (Hozumi et al 2006;Speder et al 2006;Hegan et al 2007). Our finding that the Myo61F 1 or Myo95E 1 homozygotes were also viable and fertile (data not shown) combined with the earlier data suggests that all class I myosins are dispensable for survival in Drosophila, if their functions are disrupted separately.…”

mentioning

confidence: 99%

“…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%

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

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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An unconventional myosin in Drosophila reverses the default handedness in visceral organs

Cited by 199 publications

References 29 publications

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

Versatile fluorescent probes for actin filaments based on the actin‐binding domain of utrophin

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

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