Molecular to organismal chirality is induced by the conserved myosin 1D

Lebreton, Gaëlle; Géminard, Charles; Lapraz, François; Pyrpassopoulos, Serapion; Cerezo, Delphine; Spéder, Pauline; Ostap, E. Michael; Noselli, Stéphane

doi:10.1126/science.aat8642

Cited by 121 publications

(134 citation statements)

References 30 publications

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“…Thus, the target gene(s) of Da encodes a protein that presumably has some relationship with MyoID biochemically. Although this part of the pathway remains unknown at this point, one possibility is that the Emc‐Da cascade influences the activity of MyoID to promote F ‐actin gliding in a counterclockwise path, as observed in vitro (Lebreton et al, ).…”

Section: Discussionmentioning

confidence: 95%

E and ID proteins regulate cell chirality and left–right asymmetric development in Drosophila

et al. 2019

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How left–right (LR) asymmetric forms in the animal body is a fundamental problem in Developmental Biology. Although the mechanisms for LR asymmetry are well studied in some species, they are still poorly understood in invertebrates. We previously showed that the intrinsic LR asymmetry of cells (designated as cell chirality) drives LR asymmetric development in the Drosophila embryonic hindgut, although the machinery of the cell chirality formation remains elusive. Here, we found that the Drosophila homologue of the Id gene, extra macrochaetae (emc), is required for the normal LR asymmetric morphogenesis of this organ. Id proteins, including Emc, are known to interact with and inhibit E‐box‐binding proteins (E proteins), such as Drosophila Daughterless (Da). We found that the suppression of da by wild‐type emc was essential for cell chirality formation and for normal LR asymmetric development of the embryonic hindgut. Myosin ID (MyoID), which encodes the Drosophila Myosin ID protein, is known to regulate cell chirality. We further showed that Emc‐Da regulates cell chirality formation, in which Emc functions upstream of or parallel to MyoID. Abnormal Id‐E protein regulation is involved in various human diseases. Our results suggest that defects in cell shape may contribute to the pathogenesis of such diseases.

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Section: Discussionmentioning

confidence: 95%

E and ID proteins regulate cell chirality and left–right asymmetric development in Drosophila

et al. 2019

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“…This effect was robust to the use of either left or right‐handed control groups, and thus was a specific property of RHLD subjects in this data set, rather than left‐handedness in general. We speculate that functional language laterality may be grounded in an evolutionarily ancient mechanism of inducing organ‐intrinsic left‐right morphogenesis, which can be traced back to the ancestral bilateria, and which arises from fundamental aspects of cellular biology and mechanics . Developmental studies will be needed to assess whether cellular chirality is transiently present before asymmetric embryonic development of the mammalian brain.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, the typical form of human brain functional laterality may instead originate from a genetic‐developmental mechanism that is brain‐intrinsic. Recent studies in Drosophila have showed that cellular chirality induces left‐right asymmetry of individual organs in an organ‐intrinsic manner, without being induced by the ciliary‐nodal pathway . In these mechanisms, chirality is a transient property of whole cell morphology at key points in embryonic development .…”

Section: Introductionmentioning

confidence: 99%

“…[24][25][26][27] In these mechanisms, chirality is a transient property of whole cell morphology at key points in embryonic development. 24 A role of actin-related genes in establishing cellular chirality has been observed in both invertebrate (Drosophila, snail) [24][25][26][27] and vertebrate models (cultured cells, frog, zebrafish), 24,28,29 suggesting that this mechanism is important to establish left-right organ asymmetry across bilaterian groups. Apart from the cilia-related nodal signaling pathway, cellular chirality is the only biological mechanism that has been shown to give rise to organ asymmetry in multicellular animals, of which we are aware.…”

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confidence: 99%

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Genome sequencing for rightward hemispheric language dominance

Carrión-Castillo

Haegen

Tzourio‐Mazoyer

et al. 2019

Genes Brain and Behavior

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Most people have left‐hemisphere dominance for various aspects of language processing, but only roughly 1% of the adult population has atypically reversed, rightward hemispheric language dominance (RHLD). The genetic‐developmental program that underlies leftward language laterality is unknown, as are the causes of atypical variation. We performed an exploratory whole‐genome‐sequencing study, with the hypothesis that strongly penetrant, rare genetic mutations might sometimes be involved in RHLD. This was by analogy with situs inversus of the visceral organs (left‐right mirror reversal of the heart, lungs and so on), which is sometimes due to monogenic mutations. The genomes of 33 subjects with RHLD were sequenced and analyzed with reference to large population‐genetic data sets, as well as 34 subjects (14 left‐handed) with typical language laterality. The sample was powered to detect rare, highly penetrant, monogenic effects if they would be present in at least 10 of the 33 RHLD cases and no controls, but no individual genes had mutations in more than five RHLD cases while being un‐mutated in controls. A hypothesis derived from invertebrate mechanisms of left‐right axis formation led to the detection of an increased mutation load, in RHLD subjects, within genes involved with the actin cytoskeleton. The latter finding offers a first, tentative insight into molecular genetic influences on hemispheric language dominance.

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“…Richard Goldschmidt called them “hopeful monsters” (Piternick, ) to stress their potential as progenitors of new species, assuming they confer an adaptive benefit (Diogo, Guinard, & Diaz, ). Saltations of this sort may have founded a few taxa (Lebreton et al, ), but they surely did not play the kind of cardinal role that Bateson and Goldschmidt envisioned (Dietrich, ; Theissen, ).…”

Section: Introductionmentioning

confidence: 99%

Reflections on Bateson's rule: Solving an old riddle about why extra legs are mirror‐symmetric

Held

Sessions

2019

J Exp Zool Pt B

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William Bateson was an obsessive observer of animal oddities, and at some point in his herculean survey of museum collections leading up to his monumental 1894 monograph (Materials for the study of variation), he noticed a peculiar trend among the preserved specimens (mainly insects) that possessed extra legs: multiple legs that branched from the same socket tended to be mirror images of their adjacent neighbors. He did not know why. These symmetry relationships have come to be known as Bateson's rule, and they have defied a satisfactory explanation for 125 years. In the past few decades, tantalizing clues have emerged from various lines of investigation, and those lines have converged on a possible solution. An attempt is made here to fit all of those clues together to form a coherent picture of the etiology. Two case studies have proven to be pivotal: a fly mutant whose extra legs are caused by patches of dying cells and a frog syndrome whose extra legs are caused by a parasitic flatworm. The conclusion reached is that the extra legs of insects and vertebrates obey Bateson's rule for the same reason, but that reason has nothing to do with the specific molecules in their signaling pathways. Rather, it is an emergent property of the circuitry of the pathways and their polarized alignments along the limb axes. A parade of theoretical models have tried and failed to crack this mystery in the past, and they are reviewed here as part of the narrative.

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Molecular to organismal chirality is induced by the conserved myosin 1D

Cited by 121 publications

References 30 publications

E and ID proteins regulate cell chirality and left–right asymmetric development in Drosophila

E and ID proteins regulate cell chirality and left–right asymmetric development in Drosophila

Genome sequencing for rightward hemispheric language dominance

Reflections on Bateson's rule: Solving an old riddle about why extra legs are mirror‐symmetric

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