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2. Multicellular actomyosin cables in epithelia under external anisotropic stress

Author

Spencer, Meryl A, Lopez-Gay, Jesus, Nunley, Hayden, Bellaïche, Yohanns, and Lubensky, David K

Subjects
Quantitative Biology - Tissues and Organs
Abstract

The alignment of cell-cell junctions and associated cortical actomyosin across multiple cells to form supracellular cables in an epithelium is an example of the long range tissue organization that drives morphogenesis. Here we demonstrate that the ability of tissues to assemble these parallel cables depends on the initial packing topology of the cells in the epithelium. Using a computational vertex model we develop two methods of measuring a disordered tissue's favorability to forming cables under an external stress. These measures quantify the deformation of cells and the distribution of tension in the tissue under stress. Using these measures we show that passive stress-induced cell flow reduces a tissue's ability to form cables, whereas oriented divisions create a packing which can sustain multiple parallel cables. These measures are applied to a region of the the Drosophila demonstrating a shift to a more cable-friendly packing after a wave of oriented divisions in the region.

Published
2018

3. Mechanical state, material properties and continuous description of an epithelial tissue

Author

Bonnet, Isabelle, Marcq, Philippe, Bosveld, Floris, Fetler, Luc, Bellaiche, Yohanns, and Graner, Francois

Subjects
Quantitative Biology - Cell Behavior, Physics - Biological Physics
Abstract

During development, epithelial tissues undergo extensive morphogenesis based on coordinated changes of cell shape and position over time. Continuum mechanics describes tissue mechanical state and shape changes in terms of strain and stress. It accounts for individual cell properties using only a few spatially averaged material parameters. To determine the mechanical state and parameters in the Drosophila pupa dorsal thorax epithelium, we sever in vivo the adherens junctions around a disk-shaped domain comprising typically hundred cells. This enables a direct measurement of the strain along different orientations at once. The amplitude and anisotropy of the strain increase during development. We also measure the stress to viscosity ratio and similarly find an increase in amplitude and anisotropy. The relaxation time is of order of ten seconds. We propose a space-time, continuous model of the relaxation. Good agreement with experimental data validates the description of the epithelial domain as a continuous, linear, visco-elastic material. We discuss the relevant time and length scales. Another material parameter, the ratio of external friction to internal viscosity, is estimated by fitting the initial velocity profile. Together, our results contribute to quantify forces and displacements, and their time evolution during morphogenesis., Comment: To appear in J R Soc Lond Interface

Published
2012

4. Epithelial apoptotic pattern emerges from global and local regulation by cell apical area

Author

Cachoux, Victoire M.L., primary, Balakireva, Maria, additional, Gracia, Mélanie, additional, Bosveld, Floris, additional, López-Gay, Jesús M., additional, Maugarny, Aude, additional, Gaugué, Isabelle, additional, di Pietro, Florencia, additional, Rigaud, Stéphane U., additional, Noiret, Lorette, additional, Guirao, Boris, additional, and Bellaïche, Yohanns, additional

Published
2023
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5. Systematic analysis of RhoGEF/GAP localizations uncovers regulators of mechanosensing and junction formation during epithelial cell division

Author

di Pietro, Florencia, primary, Osswald, Mariana, additional, De las Heras, José M., additional, Cristo, Inês, additional, López-Gay, Jesús, additional, Wang, Zhimin, additional, Pelletier, Stéphane, additional, Gaugué, Isabelle, additional, Leroy, Adrien, additional, Martin, Charlotte, additional, Morais-de-Sá, Eurico, additional, and Bellaïche, Yohanns, additional

Published
2023
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8. Rapid and robust optogenetic control of gene expression in Drosophila

Author

di Pietro, Florencia, primary, Herszterg, Sophie, additional, Huang, Anqi, additional, Bosveld, Floris, additional, Alexandre, Cyrille, additional, Sancéré, Lucas, additional, Pelletier, Stéphane, additional, Joudat, Amina, additional, Kapoor, Varun, additional, Vincent, Jean-Paul, additional, and Bellaïche, Yohanns, additional

Published
2021
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14. Applying mechanical forces on Drosophilatissues in vivousing the StretchCo, a 3D-printable device

Author

Gracia, Mélanie, Lefèvre, Bénédicte M., Güell Alonso, Raquel, Cachoux, Victoire, Balakireva, Maria, Guirao, Boris, Cuvelier, Damien, Bardin, Allison J., and Bellaïche, Yohanns

Abstract

Applying mechanical forces to tissues helps to understand morphogenesis and homeostasis. Additionally, recording the dynamics of living tissues under mechanical constraints is needed to explore tissue biomechanics. Here, we present a protocol to 3D-print a StretchCo device and use it to apply uniaxial mechanical stress on the Drosophilapupal dorsal thorax epithelium. We describe steps for 3D printing, polydimethylsiloxane (PDMS) strip cutting, and glue preparation. We detail procedures for PDMS strip mounting, tissue compaction, and live imaging upon force application. For additional details on the use and execution of this protocol, please refer to Cachoux et al. (2023)1from which the StretchCo machine has been derived.

Published
2024
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18. Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis

Author

Edwards-Jorquera, Sandra Sofía, Bosveld, Floris, Bellaïche, Yohanns, Lennon-Duménil, Ana-María, Glavic, Álvaro, Markova, Olga, Guirao, Boris, Martin, Charlotte, Wang, Zhimin, Pierre, Anaëlle, Balakireva, Maria, Gaugue, Isabelle, Ainslie, Anna, Christophorou, Nicolas, Lubensky, David, Minc, Nicolas, Universidad de Chile, Génétique et Biologie du Développement, Centre National de la Recherche Scientifique (CNRS)-Institut Curie [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC), Institut Curie [Paris], Universidad de Chile = University of Chile [Santiago] (UCHILE), Université de Bordeaux (UB), Institut Jacques Monod (IJM (UMR_7592)), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Department of Physics [Ann Arbor], University of Michigan [Ann Arbor], University of Michigan System-University of Michigan System, CePoDro ANR, MorphoDro ERC Advanced, ARC (SL220130607097), Curie Mayent-Rothschild, Labex DEEP, NSF DMR1056456, ICAM, Centre National de la Recherche Scientifique (CNRS)-Institut Curie-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC), Department of Physics, and Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut Curie [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, 0301 basic medicine, Cell division, [SDV]Life Sciences [q-bio], Morphogenesis, Mitosis, Cell Cycle Proteins, Nerve Tissue Proteins, GTP-Binding Protein alpha Subunits, Gi-Go, Biology, Drosophila-melanogaster, Microtubules, Cell junction, Article, Epithelium, 03 medical and health sciences, 0302 clinical medicine, Divisions, Cell polarity, Animals, Drosophila Proteins, Cell Shape, Interphase, [SDV.BDD]Life Sciences [q-bio]/Development Biology, ComputingMilieux_MISCELLANEOUS, Guanine Nucleotide Dissociation Inhibitors, Multidisciplinary, Cleavage plane, Tissue, Polarity pathway, Protein, Mitotic spindle, Cell Polarity, Membrane Proteins, Epithelial Cells, Spindle apparatus, Cell biology, Regulates spindle orientation, Drosophila melanogaster, Intercellular Junctions, 030104 developmental biology, Localization, Female, Astral microtubules, Cell Division, 030217 neurology & neurosurgery
Abstract

International audience; The orientation of cell division along the long axis of the interphase cell--the century-old Hertwig's rule--has profound roles in tissue proliferation, morphogenesis, architecture and mechanics. In epithelial tissues, the shape of the interphase cell is influenced by cell adhesion, mechanical stress, neighbour topology, and planar polarity pathways. At mitosis, epithelial cells usually adopt a rounded shape to ensure faithful chromosome segregation and to promote morphogenesis. The mechanisms underlying interphase cell shape sensing in tissues are therefore unknown. Here we show that in Drosophila epithelia, tricellular junctions (TCJs) localize force generators, pulling on astral microtubules and orienting cell division via the Dynein-associated protein Mud independently of the classical Pins/Gαi pathway. Moreover, as cells round up during mitosis, TCJs serve as spatial landmarks, encoding information about interphase cell shape anisotropy to orient division in the rounded mitotic cell. Finally, experimental and simulation data show that shape and mechanical strain sensing by the TCJs emerge from a general geometric property of TCJ distributions in epithelial tissues. Thus, in addition to their function as epithelial barrier structures, TCJs serve as polarity cues promoting geometry and mechanical sensing in epithelial tissues.

Published
2016

23. Erratum: Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis

Author

Bosveld, Floris, primary, Markova, Olga, additional, Guirao, Boris, additional, Martin, Charlotte, additional, Wang, Zhimin, additional, Pierre, Anaëlle, additional, Balakireva, Maria, additional, Gaugue, Isabelle, additional, Ainslie, Anna, additional, Christophorou, Nicolas, additional, Lubensky, David K., additional, Minc, Nicolas, additional, and Bellaïche, Yohanns, additional

Published
2016
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26. Tricellular junction proteins promote disentanglement of daughter and neighbour cells during epithelial cytokinesis.

Author

Zhimin Wang, Bosveld, Floris, and Bellaïche, Yohanns

Subjects
CELL junctions, EPITHELIAL cells, CYTOKINESIS
Abstract

In epithelial tissue, new cell-cell junctions are formed upon cytokinesis. To understand junction formation during cytokinesis, we explored de novo formation of tricellular septate junctions (TCJs) in Drosophila epithelium. We found that upon midbody formation, the membranes of the two daughter cells and of the neighbouring cells located below the adherens junction (AJ) remain entangled in a 4-cell structure apposed to the midbody. The septate junction protein Discs-Large and components of the TCJ, Gliotactin and Anakonda accumulate in this 4-cell structure. Subsequently, a basal movement of the midbody parallels the detachment of the neighbouring cell membranes from the midbody, the disengagement of the daughter cells from their neighbours and the reorganisation of TCJs between the two daughter cells and their neighbouring cells. While the movement of midbody is independent of the Alix and Shrub abscission regulators, the loss of Gliotactin or Anakonda function impedes both the resolution of the connection between the daughterneighbour cells and midbody movement. TCJ proteins therefore control an additional step of cytokinesis necessary for the disentanglement of the daughter cells from their neighbours during cytokinesis. [ABSTRACT FROM AUTHOR]

Published
2018
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41. Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo

Author

Orgogozo, Virginie, Schweisguth, François, and Bellaïche, Yohanns

Abstract

The stereotyped pattern of the Drosophila embryonic peripheral nervous system (PNS) makes it an ideal system to use to identify mutations affecting cell polarity during asymmetric cell division. However, the characterisation of such mutations requires a detailed description of the polarity of the asymmetric divisions in the sensory organ lineages. We describe the pattern of cell divisions generating the vp1-vp4a mono-innervated external sense (es) organs. Each sensory organ precursor (SOP) cell follows a series of four asymmetric cell divisions that generate the four es organs cells (the socket, shaft, sheath cells and the es neurone) together with one multidendritic (md) neurone. This lineage is distinct from any of the previously proposed es lineages. Strikingly, the stereotyped pattern of cell divisions in this lineage is identical to those described for the embryonic chordotonal organ lineage and for the adult thoracic bristle lineage. Our analysis reveals that the vp2-vp4a SOP cells divide with a planar polarity to generate a dorsal pIIa cell and a ventral pIIb cell. The pIIb cell next divides with an apical-basal polarity to generate a basal daughter cell that differentiates as an md neurone. We found that Inscuteable specifically accumulated at the apical pole of the dividing pIIb cell and regulated the polarity of the pIIb division. This study establishes for the first time the function of Inscuteable in the PNS, and provides the basis for studying the mechanisms controlling planar and apical-basal cell polarities in the embryonic sensory organ lineages.

Published
2001
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42. Neither the homeodomain nor the activation domain of Bicoid is specifically required for its down-regulation by the Torso receptor tyrosine kinase cascade

Author

Bellaïche, Yohanns, Bandyopadhyay, Rupa, Desplan, Claude, and Dostatni, Nathalie

Abstract

Bicoid (Bcd) is a maternal morphogen responsible for patterning the head and thorax of the Drosophila embryo. Correct specification of head structure, however, requires the activity of the Torso receptor tyrosine kinase cascade, which also represses expression of Bcd targets at the most anterior tip of the embryo. Here, we investigate the role of both the homeodomain (HD) and the activation domain of Bcd in the anterior repression of its targets. When a Bcd mutant protein whose HD has been replaced by the Gal4 DNA-binding domain is expressed in early embryos, a reporter gene driven by Gal4 DNA-binding sites is first activated in an anterior domain and then repressed from the anterior pole. The down-regulation of Bcd-Gal4 activity requires torso function but does not depend on endogenous bcd activity, indicating that the Bcd protein alone and none of its targets is required to mediate the effect of torso. Functional analysis of a chimeric protein, whose activation domain has been replaced by a generic activation domain, indicates that the activation domain of Bcd is also not specifically required for its downregulation by Torso. We propose that Torso does not affect the ability of Bcd to bind DNA, but instead directs modification of Bcd or of a potential Bcd co-factor, which renders the Bcd protein unable to activate transcription.

Published
1996
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43. Slit-Robo signalling prevents sensory cells from crossing the midline in Drosophila

Author

Orgogozo, Virginie, Schweisguth, François, and Bellaïche, Yohanns

Subjects
*DROSOPHILA, *CELL migration, *CELL proliferation, *CELL growth
Abstract

Maintenance of bilateral symmetry throughout animal development requires that both left and right halves of the body follow nearly identical patterns of cell proliferation, differentiation, death and migration. During formation of the perfectly bilateral Drosophila larval peripheral nervous system (PNS), the sensory precursor cells of the ventral multidendritic neuron vmd1a originating from each hemisegment migrate away from the ventral midline. Our observations indicate that in slit mutant embryos, as well as in robo, robo2 double mutants, sensory precursor cells of the left and right vmd1a neurons aberrantly cluster at the midline and then the pair of vmd1a neurons migrate to their final position on the same side of the embryo. This results in disruption of PNS bilateral symmetry. Expression of slit at the midline rescues the slit mutant vmd1a phenotype, suggesting that midline-secreted Slit activates Robo/Robo2 signalling to control the migration of the vmd1a sensory precursor cells. Our study indicates that midline-secreted Slit prevents vmd1a sensory cells from crossing the midline and thereby maintains PNS bilateral symmetry during development. [Copyright &y& Elsevier]

Published
2004
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44. γ-Tubulin Ring Complexes and EB1 play antagonistic roles in microtubule dynamics and spindle positioning.

Author

Bouissou A, Vérollet C, de Forges H, Haren L, Bellaïche Y, Perez F, Merdes A, and Raynaud-Messina B

Subjects
Animals, Animals, Genetically Modified, Cells, Cultured, Drosophila, HeLa Cells, Humans, Multiprotein Complexes physiology, Microtubule-Associated Proteins physiology, Microtubules metabolism, Spindle Apparatus physiology, Tubulin physiology
Abstract

γ-Tubulin is critical for microtubule (MT) assembly and organization. In metazoa, this protein acts in multiprotein complexes called γ-Tubulin Ring Complexes (γ-TuRCs). While the subunits that constitute γ-Tubulin Small Complexes (γ-TuSCs), the core of the MT nucleation machinery, are essential, mutation of γ-TuRC-specific proteins in Drosophila causes sterility and morphological abnormalities via hitherto unidentified mechanisms. Here, we demonstrate a role of γ-TuRCs in controlling spindle orientation independent of MT nucleation activity, both in cultured cells and in vivo, and examine a potential function for γ-TuRCs on astral MTs. γ-TuRCs locate along the length of astral MTs, and depletion of γ-TuRC-specific proteins increases MT dynamics and causes the plus-end tracking protein EB1 to redistribute along MTs. Moreover, suppression of MT dynamics through drug treatment or EB1 down-regulation rescues spindle orientation defects induced by γ-TuRC depletion. Therefore, we propose a role for γ-TuRCs in regulating spindle positioning by controlling the stability of astral MTs.

Published
2014
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46. Drosophila E-cadherin regulates the orientation of asymmetric cell division in the sensory organ lineage.

Author

Le Borgne R, Bellaïche Y, and Schweisguth F

Subjects
Animals, Cadherins genetics, Cell Lineage, Drosophila anatomy & histology, Drosophila genetics, Fluorescent Antibody Technique, Genes, Dominant, Green Fluorescent Proteins, Luminescent Proteins genetics, Thorax, Cadherins physiology, Cell Division physiology, Drosophila cytology
Abstract

Background: Generation of cell-fate diversity in Metazoan depends in part on asymmetric cell divisions in which cell-fate determinants are asymmetrically distributed in the mother cell and unequally partitioned between daughter cells. The polarization of the mother cell is a prerequisite to the unequal segregation of cell-fate determinants. In the Drosophila bristle lineage, two distinct mechanisms are known to define the axis of polarity of the pI and pIIb cells. Frizzled (Fz) signaling regulates the planar orientation of the pI division, while Inscuteable (Insc) directs the apical-basal polarity of the pIIb cell. The orientation of the asymmetric division of the pIIa cell is identical to the one of its mother cell, the pI cell, but, in contrast, is regulated by an unknown Insc- and Fz-independent mechanism., Results: DE-Cadherin-Catenin complexes are shown to localize at the cell contact between the two cells born from the asymmetric division of the pI cell. The mitotic spindle of the dividing pIIa cell rotates to line up with asymmetrically localized DE-Cadherin-Catenin complexes. While a complete loss of DE-Cadherin function disrupts the apical-basal polarity of the epithelium, both a partial loss of DE-Cadherin function and expression of a dominant-negative form of DE-Cadherin affect the orientation of the pIIa division. Furthermore, expression of dominant-negative DE-Cadherin also affects the position of Partner of Inscuteable (Pins) and Bazooka, two asymmetrically localized proteins known to regulate cell polarity. These results show that asymmetrically distributed Cad regulates the orientation of asymmetric cell division., Conclusions: We describe a novel mechanism involving a specialized Cad-containing cortical region by which a daughter cell divides with the same orientation as its mother cell.

Published
2002
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