Snail Chirality: The Unwinding

Maderspacher, Florian

doi:10.1016/j.cub.2016.02.008

Cited by 9 publications

(7 citation statements)

References 18 publications

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“…Due to the helical nature of actin, both myosins ( Lebreton et al, 2018 ) and formins ( Mizuno et al, 2011 ; Jégou et al, 2013 ) can twist actin filaments while they respectively pull or polymerize them, and therefore both are potential sources of molecular torques. Interestingly, myosins as well as formins are also required for numerous cellular and organismal chiral processes ( Tee et al, 2015 ; Davison et al, 2016 ; Kuroda et al, 2016 ; Hozumi et al, 2006 ; Maderspacher, 2016 ; Spéder et al, 2006 ; Chougule et al, 2020 ). Future work will be required to identify the molecular source of torque generation in the actomyosin layer, as well as its organization principles that ensure a consistent handedness of the emerging torques and chiral cortical flows.…”

Section: Discussionmentioning

confidence: 99%

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early Caenorhabditis elegans development

Pimpale

Middelkoop

Mietke

et al. 2020

eLife

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Proper positioning of cells is essential for many aspects of development. Daughter cell positions can be specified via orienting the cell division axis during cytokinesis. Rotatory actomyosin flows during division have been implied in specifying and reorienting the cell division axis, but how general such reorientation events are, and how they are controlled, remains unclear. We followed the first nine divisions of Caenorhabditis elegans embryo development and demonstrate that chiral counter-rotating flows arise systematically in early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify a mechanism by which chiral counter-rotating actomyosin flows arise in the AB lineage only, and show that they drive lineage-specific spindle skew and cell reorientation events. In conclusion, our work sheds light on the physical processes that underlie chiral morphogenesis in early development.

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Section: Discussionmentioning

confidence: 99%

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early Caenorhabditis elegans development

Pimpale

Middelkoop

Mietke

et al. 2020

eLife

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“…Direct identification of the common genetic changes that serve as precursors to the evolution of a feature in related lineages would, of course, be the strongest line of evidence (Blount et al 2018). Unfortunately, the genetics underpinning gastropod shell morphology are not yet well understood (Liu et al 2013; Jackson and Degnan 2016; Kocot et al 2016; Maderspacher 2016), and fossils are not amenable to such analyses. An associative approach is frequently taken, in which frequent development of a feature within closely related lineages is considered suggestive of parallelism (Gould 2002; Vermeij 2005).…”

Section: Introductionmentioning

confidence: 99%

Convergence, parallelism, and function of extreme parietal callus in diverse groups of Cenozoic Gastropoda

et al. 2020

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We use scanning electron microscopy imaging to examine the shell microstructure of fossil and living species in five families of caenogastropods (Strombidae, Volutidae, Olividae, Pseudolividae, and Ancillariidae) to determine whether parallel or convergent evolution is responsible for the development of a unique caenogastropod trait, the extreme parietal callus (EPC). The EPC is defined as a substantial thickening of both the spire callus and the callus on the ventral shell surface such that it covers 50% or more of the surface. Caenogastropods as a whole construct the EPC convergently, using a variety of low-density, poorly organized microstructures that are otherwise uncommon in caenogastropod non-callus shell construction. Within clades, however, we see evidence for parallelism in decreased regulation in both the shell and callus microstructure. Low-density and poorly ordered microstructure—such as used for the EPC—uses less organic scaffolding and is less energetically expensive than normal shell microstructure. This suggests the EPC functions to rapidly and inexpensively increase shell thickness and overall body size. Tests of functional ecology suggest that the EPC might function both to defend against crushing predation through increased body size and dissipation of forces while aiding in shell orientation of highly mobile gastropods. These interpretations hinge on the current phylogenetic placement of caenogastropod families, emphasizing the essential contribution of phylogeny when interpreting homoplasy.

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“…actomyosin regulators, nucleators and cross-linkers) localise in a pattern similar to myosin, and many of these affect the chirality of actomyosin flows in the polarising one-cell embryo, we cannot exclude that other force generators provide the active torque needed for chiral counter-rotating flows. Interestingly, like myosins [41], diaphanous-like formins are known to generate torque at the molecular level [57,58] and are required for numerous cellular [59] and organismal chiral processes [60][61][62]. Future work will be needed to first identify the molecular torque generator and to subsequently unravel the molecular mechanism underlying active torque generation.…”

Section: Discussionmentioning

confidence: 99%

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early development

Pimpale

Middelkoop

Mietke

et al. 2019

Preprint

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Proper positioning of cells is important for many aspects of embryonic development, tissue homeostasis, and regeneration. A simple mechanism by which cell positions can be specified is via orienting the cell division axis. This axis is specified at the onset of cytokinesis, but can be reoriented as cytokinesis proceeds.Rotatory actomyosin flows have been implied in specifying and reorienting the cell division axis in certain cases, but how general such reorientation events are, and how they are controlled, remains unclear. In this study, we set out to address these questions by investigating early Caenorhabditis elegans development.In particular, we determined which of the early embryonic cell divisions exhibit chiral counter-rotating actomyosin flows, and which do not. We follow the first nine divisions of the early embryo, and discover that chiral counter-rotating flows arise systematically in the early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify specific properties of the actomyosin cortex in the symmetric AB lineage divisions that favor chiral counter-rotating actomyosin flows of the two halves of the dividing cell. Finally, we show that these counter-rotations are the driving force of both the AB lineage spindle skew and cell reorientation events. In conclusion, we here have shed light on the physical basis of lineage-specific actomyosin-based processes that drive chiral morphogenesis during development.Proper positioning of cells is instrumental for many aspects of early embryonic development [1][2][3]. One way to achieve proper cell positioning is via migration [4,5]. Another way by which cell positions can be specified is via the orientation of the cell division axis [6][7][8]. Since the orientation of the mitotic spindle dictates the cell division axis, the orientation of the mitotic spindle at cleavage is instrumental for determining daughter cell positions [9][10][11][12]. This axis can be set at the beginning of cytokinesis, by assembling the mitotic spindle in the correct orientation from the start, or during cytokinesis by reorientation of the mitotic spindle [13][14][15][16][17][18] While several studies highlight the mechanisms that determine the initial orientation of the mitotic spindle at the onset of cytokinesis [15-17, 19, 20] the mechanisms controlling reorientation remain not very well understood. We here set out to investigate cell repositioning during cytokinesis in the early development of the C. elegans nematode. The fully grown hermaphrodite worm consists of exactly 959 somatic cells that are essentially invariant both in terms of position and lineage [21][22][23][24]. Development is deterministic from the start: the one-cell embryo undergoes an asymmetric cell division that gives rise to the AB (somatic) lineage and the P lineage [22,25]. While the anterior daughter cell, AB, undergoes a symmetric cell division into ABa and ABp, the posterior daughter cell, P 1 , divides asymmetrically into...

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Snail Chirality: The Unwinding

Abstract: Most snails are coiled clockwise, but in some species rare genetic variants with reverse coiling occur. Now, a molecular determinant of coiling direction has been identified, the cytoskeletal regulator formin.

Cited by 9 publications

References 18 publications

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early Caenorhabditis elegans development

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early Caenorhabditis elegans development

Convergence, parallelism, and function of extreme parietal callus in diverse groups of Cenozoic Gastropoda

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early development

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