Gradient in cytoplasmic pressure in the germline cells controls overlying epithelial cell morphogenesis

Lamiré, Laurie-Anne; Milani, Pascale; Runel, Gaël; Kiss, Annamária; Arias, Leticia; Vergier, Blandine; Das, Pradeep; Cluet, David; Boudaoud, Arezki; Grammont, Muriel

doi:10.1101/440438

Cited by 5 publications

(15 citation statements)

References 97 publications

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“…2F). By also accounting for natural cell-to-cell variability in effective cell surface tension (34), the proposed model successfully captures experimentally observed complex transport patterns along the 16-cell tree. For example, our data show the L4 NC transiently increasing in size during NC dumping, which can occur if the L3 cell to which it is connected shrinks sufficiently such that it becomes smaller than the L4 cell.…”

Section: Resultsmentioning

confidence: 88%

Dynamics of hydraulic and contractile wave-mediated fluid transport duringDrosophilaoogenesis

Alsous

Romeo

Jackson

et al. 2020

Preprint

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29Interactions in which individuals benefit others at a cost to themselves are rife within the 30 animal kingdom 1 , from stalk cells in slime mold fruiting bodies 2 to social insect colonies where 31 sterile workers live for the queen 3 . The development of an egg cell occurs within similarly self-32 sacrificing communes. Across species, oocytes develop within cysts alongside nurse-like germ 33 cells; a key juncture in oogenesis occurs when these sister cells transport their cytoplasm to the 34 oocyte prior to fertilization 4,5 . As a result, the oocyte grows as its sister cells regress and die 6 . 35 Long observed in insects, recent work shows that development of the mammalian egg cell occurs 36 through similar intercellular transport processes 7,8 . Although critical for fertility and embryonic 37 life, the biological and physical mechanisms underlying such altruistic fluid transport remain 38 poorly understood, owing to a lack of time-resolved quantitative data. Here, we combined ex vivo 39 live imaging of germline cysts with mathematical modeling to investigate the dynamics and 40 mechanisms that enable directional and complete cytoplasmic transport in Drosophila 41 melanogaster egg chambers. We discovered that during 'nurse cell dumping', most cytoplasm is 42 transported into the oocyte independently of changes in myosin-II contractility, with dynamics 43 predicted by Young-Laplace's law, suggesting pressure-driven transport induced by baseline cell 44 surface tension. A minimal flow network model inspired by the famous two-balloon experiment 45 correctly predicts transport directionality and time scale. Long thought to trigger transport 46 through 'squeezing' 9,10 , increased actomyosin contractility is required only once cell volume is 47 reduced by ~75%, in the form of cell peristaltic contractile waves that permit continued flow. Our 48 work thus demonstrates how biological and physical mechanisms cooperate to enable proper cell 49 and tissue level behaviours during a conserved act of cytoplasmic transport in early development. 50 51 Main text 52The Drosophila oocyte develops within an egg chamber, a multicellular structure that comprises a 53 germline cyst of 16 cells that are interconnected through intercellular bridges called ring canals and 54 covered by an epithelium (Fig. 1a) [11][12][13] . After the oocyte grows to ~50% of the egg chamber's volume, all 55 15 sister germ cells, called nurse cells, transport the entirety of their contents directionally into the oocyte 56 in a process called 'nurse cell (NC) dumping'; with a diameter of ~10 µm, ring canals are large enough to 57 permit passage of most cytoplasmic contents ( Fig. 1b; Extended Data Fig. 1a; Supplementary Video 1) 14 . 58 It is thought that NC dumping is driven by global cortical contractile forces generated through interactions 59 of non-muscle myosin II (myosin) with actin filaments (henceforth actomyosin), i.e. through an increase in 60 pressure, cytoplasm is 'squeezed' out of the NCs and into the oocyte 9,10 . While mutants in ...

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Section: Resultsmentioning

confidence: 88%

Dynamics of hydraulic and contractile wave-mediated fluid transport duringDrosophilaoogenesis

Alsous

Romeo

Jackson

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…In spite of these simplifications our theory bring several generic, robust and experimentally testable predictions. In particular, we expect our theory to be relevant, beyond lumenogenesis, to describe the hydraulic cell coarsening phenomena underlying Drosophila and C. elegans oogenesis (35,37,38). Our theory demonstrates that lumen coarsening exhibits a generic dynamic scaling behavior.…”

Section: Discussionmentioning

confidence: 99%

“…Such important topological differences may explain why baso-lateral cavities, in contrast to their apical counterparts, appear systematically pressurized, as they need to grow against adhesive contacts; it may also explain why tissues with multiple apical lumens may fail to spontaneously resolve into a single cavity (33). Hydraulic and osmotic flows are more and more recog- nized as essential determinants of embryo and tissue shaping (8,32,(34)(35)(36)(37)(38). However only a few physical models describe the interplay between cell mechanics, osmotic effects and fluid flow in morphogenesis (39)(40)(41)(42) and in previous models, osmolarity is most generally considered spatially homogeneous.…”

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confidence: 99%

A hydro-osmotic coarsening theory of biological cavity formation

Verge-Serandour

Turlier

2020

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The blastocoel is a fluid-filled cavity characterizing early embryos at blastula stage. It is commonly described as the result of cell division patterning, but in tightly compacted embryos the mechanism underlying its emergence remains unclear. Based on experimental observations, we discuss an alternative physical model by which a single cavity forms by growth and coarsening of myriad of micrometric lumens interconnected through the intercellular space. Considering explicitly ion and fluid exchanges, we find that cavity formation is primarily controlled by hydraulic fluxes, with a minor influence of osmotic heterogeneities on the dynamics. Performing extensive numerical simulations on 1-dimensional chains of lumens, we show that coarsening is self-similar with a dynamic scaling exponent reminiscent of dewetting films over a large range of ion and water permeability values. Adding active pumping of ions to account for lumen growth largely enriches the dynamics: it prevents from collective collapse and leads to the emergence of a novel coalescence-dominated regime exhibiting a distinct scaling law. Finally, we prove that a spatial bias in pumping may be sufficient to position the final cavity, delineating hence a novel mode of symmetry breaking for tissue patterning. Providing generic testable predictions our hydro-osmotic coarsening theory highlights the essential roles of hydraulic and osmotic flows in development, with expected applications in early embryogenesis and lumenogenesis.

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“…The radius of curvature of a spherical interface is inversely proportional to the difference in pressure between the two sides of the interface. Thus, to analyse NC cytoplasmic pressure, we determined the radius of curvature of the posterior membrane of NCs, by measuring -in 2D optical sections-the radius of the circle fitting this membrane, as described in (Lamire et al, 2020), Figure S8A, B, E, n>12 per position). In agreement with previous results (Lamire et al, 2020), we found a gradient of cytoplasmic pressure decreasing from anterior to posterior in early S9 control egg chambers (Figure S8E).…”

Section: Bm Stiffness Influences Nc Cortical Tensionmentioning

confidence: 99%

Constriction forces imposed by basement membranes regulate developmental cell migration

Martín-Bermudo

López

Kabanova

2022

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The basement membrane (BM) is a specialized extracellular matrix, which underlies or encase developing tissues. Mechanical properties of encasing BMs have been shown to profoundly influence the shaping of associated tissues. Here, we use the migration of the border cells (BCs) of the Drosophila egg chamber to unravel a new role of encasing BMs in developmental cell migration. BCs move between a group of cells, the nurse cells (NCs), that are enclosed by a monolayer of follicle cells (FCs), enveloped in turn by a BM, the follicle BM. We show that increasing or reducing the stiffness of the follicle BM, by altering laminins or Coll IV levels, conversely affects BC migration speed and alters migration mode and dynamics. Follicle BM stiffness also controls pairwise NC and FC cortical tension. We propose that constriction forces imposed by the follicle BM influence NC and FC cortical tension, which, in turn, regulate BC migration. Encasing BMs emerge as key players in the regulation of collective cell migration during morphogenesis.

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Gradient in cytoplasmic pressure in the germline cells controls overlying epithelial cell morphogenesis

Cited by 5 publications

References 97 publications

Dynamics of hydraulic and contractile wave-mediated fluid transport duringDrosophilaoogenesis

Dynamics of hydraulic and contractile wave-mediated fluid transport duringDrosophilaoogenesis

A hydro-osmotic coarsening theory of biological cavity formation

Constriction forces imposed by basement membranes regulate developmental cell migration

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