Roles of Type I Myosins in Drosophila Handedness

Taniguchi, Kiichiro; Hozumi, Shunya; Maeda, Reo; Okumura, Takashi; Matsuno, Kenji

doi:10.4161/fly.5252

Cited by 6 publications

(8 citation statements)

References 25 publications

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“…On the other hand, the overexpression of Myo61F resulted in no rotation and partial sinistral rotational phenotypes in wild-type and Myo31DF K2 /+ flies, respectively ( Figure 4G). This result suggested that Myo31DF antagonizes the sinistral activity of Myo61F overexpression, as reported previously (Taniguchi et al 2007). However, our loss-of-function analysis of Myo31DF and Myo61F showed that these two myosins function redundantly in dextral rotation of the male genital disc.…”

Section: Functional Redundancy Of Myo61f and Myo31df In Establishing supporting

confidence: 89%

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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Section: Functional Redundancy Of Myo61f and Myo31df In Establishing supporting

confidence: 89%

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

et al. 2015

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“…These results suggest that the cortical actin cytoskeleton of eggs has an intrinsic chirality in Xenopus. Because this also holds true for D. mela-nogaster and snails, similar mechanisms may be involved in vertebrates and invertebrates (Taniguchi et al, 2007a). If actin cytoskeleton-dependent LR specification is conserved in vertebrates, as seems to be the case, it will be interesting to learn if this mechanism functions upstream of or in parallel to the nodal flow-dependent LR patterning.…”

Section: Short Perspectivesmentioning

confidence: 88%

“…This finding suggests that the conventional motor functions of Myo31DF are essential for LR-polarity determination (Hozumi et al, this issue). Furthermore, LR-polarity defects appear in the midgut and hindgut when genes encoding the dominant-negative forms of two GTPase family proteins, Rho1 and Rac1, which regulate the organization of actin filaments, are overexpressed (Hozumi et al, 2006;Taniguchi et al, 2007a). These results suggest that Myo31DF contributes to the determination of LR polarity through its interactions with the actin cytoskeleton.…”

Section: An Actin-based Motor Protein Myo31df Functions In the Devementioning

confidence: 96%

“…melanogaster has long been used as a model organism for genetic analyses, especially of developmental programs. However, only a few studies on the development of LR asymmetry in D. melanogaster have been pursued (reviewed in Taniguchi et al, 2007a;Coutelis et al, 2008), perhaps because LR asymmetry has been overlooked in anatomy without gathering explicit interest. In D. melanogaster, several internal organs, such as the gut (Ligoxygakis et al, 2001;Hayashi and Murakami, 2001;Baum, 2006), brain (Pascual et al, 2004), male genitalia (Á dá m et al, 2003), and spermiduct (Hozumi et al, 2006), exhibit genetically determined directional asymmetry.…”

Section: Lr Asymmetry In D Melanogastermentioning

confidence: 99%

“…Invertebrates are, however, probably more suitable for comparative approaches to the evolution of LR asymmetry, for the following reasons. In many invertebrates, including Drosophila melanogaster, snails, and Caenorhabditis elegans, mutations affecting LR asymmetry have been identified by forward genetics, and molecular genetic analyses of these mutants are in progress (Hobert et al, 2002;Hosoiri et al, 2003;Hozumi et al, 2006;Spéder et al, 2006;Taniguchi et al, 2007a). Efficient and comprehensive genetic studies on the mechanisms of asymmetry development can be performed using invertebrates, especially D. melanogaster (Hozumi et al, 2006;Spéder et al, 2006) and C. elegans (Bergmann et al, 2003;Poole and Hobert, 2006).…”

Section: Introductionmentioning

confidence: 99%

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The development and evolution of left‐right asymmetry in invertebrates: Lessons from Drosophila and snails

Okumura

Utsuno

Kuroda

et al. 2008

Developmental Dynamics

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The unique nature of body handedness, which is distinct from the anteroposterior and dorsoventral polarities, has been attracting growing interest in diverse biological disciplines. Recent research progress on the left-right asymmetry of animal development has focused new attention on the mechanisms underlying the development and evolution of invertebrate handedness. This exploratory review of currently available information illuminates the prospective value of Drosophila and pulmonate snails for innovative new research aimed at elucidating these mechanisms. For example, findings in Drosophila and snails suggest that an actin filament-dependent mechanism may be evolutionarily conserved in protostomes. The polarity conservation of primary asymmetry across most metazoan phyla, which visceral handedness represents, indicates developmental constraint and purifying selection as possible but unexplored mechanisms. Comparative studies using Drosophila and snails, which have the great advantages of using genetic and evolutionary approaches, will accelerate our understanding of the mechanisms governing the conservation and diversity of animal handedness. Developmental Dynamics 237: 3497-3515, 2008.

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Head region of unconventional myosin I family members is responsible for the organ‐specificity of their roles in left–right polarity in Drosophila

Hozumi

Maeda

Taniguchi-Kanai

et al. 2008

Developmental Dynamics

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In Drosophila, Myosin31DF (Myo31DF), encoding a Myosin ID protein, has crucial roles in left-right (LR) asymmetric development. Loss of Myo31DF function leads to laterality inversion for many organs, including the embryonic gut. Here, we found that Myo31DF was required before LR asymmetric morphogenesis in the hindgut, suggesting it functions in LR patterning instead of directly in hindgut morphological changes. Myosin61F (Myo61F) encodes another Myosin I, and Myo31DF or Myo61F overexpression reverses the laterality of different organs. Myo31DF and Myo61F have domains conserved in Myosin proteins, particularly in the proteins' head regions. We studied the roles of these domains in LR patterning using overexpression analysis. The Actin-binding and ATP-binding domains were essential for both proteins, but the IQ domains, binding sites for Myosin light chains, were required only by Myo31DF. Our results also suggest that the organ specificities of the Myo31DF and Myo61F activities depended on their head regions.

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Roles of Type I Myosins in Drosophila Handedness

Cited by 6 publications

References 25 publications

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

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

The development and evolution of left‐right asymmetry in invertebrates: Lessons from Drosophila and snails

Head region of unconventional myosin I family members is responsible for the organ‐specificity of their roles in left–right polarity in Drosophila

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