Cell sorting, cell tension and morphogenesis. Morphogenesis: Big Questions
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1 Cell sorting, cell tension and morphogenesis Morphogenesis: Big Questions How are tissues formed from populations of cells? How are organs constructed from tissues? How do organs form in particular locations, and how do migrating cells reach their destinations? How do organs and their cells grow, and how is their growth coordinated throughout development? How do organs achieve polarity? 1
2 Cell organization in the embryo Epithelial cells: tightly connected to one another in sheets or tubes. Mesenchymal cells: unconnected to one another; operating as independent units. Morphogenesis is brought about by changes in cellular processes within these two types of arrangements: the direction and number of cell divisions cell shape changes cell movement cell growth cell death changes in the composition of the cell membrane and/or secreted factors Townes & Holtfreter (1955): Differential cell affinity and self-organization Combination of cells from 3-germ layers (isolated shortly after neural tube formation) become spatially segregated: each cell type sorts out into its own region, reflecting their embryonic position. Ectoderm inner surface has affinity f o r m e s o d e r m b u t r e p e l s endoderm. Mesoderm has affinity for both ecto and endoderm. Selective affinity imparts positional information. 2
3 Steinberg (1964): differential adhesion hypothesis (DAH) Self-sorting (hystotypic aggregation) behavior of cell aggregates is mechanistically equivalent to liquid surface tension, specifically the spontaneous separation of immiscible liquids (water vs. oil). Adhesive forces between aggregated cells play the same role during cell sorting than intermolecular attractive (cohesive) forces play in liquid surface tension. In cell sorting assays the cells with the strongest homotypic interaction (more cohesive) will be sorted to the center, while the less cohesive ones will remain outside. Hierarchy of cell sorting by decreasing surface tension Mesoderm>Endoderm>Ectoderm 3
4 Harris: differential surface contraction (DSC) Main critiques to DAH: 1. Cell-cell adhesions are more than just close range attraction as cells can be held together by forces that are different from the ones than originally brought them together. 2. Loss of cell adhesion is not just the reverse thermodynamically than forming an adhesion. 3. Liquids droplets are closed thermodynamic systems while live cells generate energy capable of altering cell position and adhesion. 4. Cell-cell adhesion are concentrated at small foci, therefore increase adhesion does not require an increase of intercellular contact area (same if decreasing adhesion). Alternative: cortical tension (surface contractions) generated by the cell at the interphase between cell membrane and the surrounding environment could drive cell sorting. Assays for testing cell sorting/surface tension Mixed cell aggregates Juxtaposed mixed cell aggregates Single cell aggregates Self-sorting Engulfment Flatten Green (2008) Nat Cell Biol 10:
5 Measuring cell adhesion/deformability by AFM Adhesiveness Cortical tension Green (2008) Nat Cell Biol 10:
6 Measuring adhesion of germ-layer progenitors Force to pull cells appart: AdM>AdEn>AdEc Cell shape/size Cadherin-dependant adhesion Nodal-TGFβ signaling modulates cortical tension Ectoderm progenitors: 54.5+/-8.6 µn/m Ectoderm+activin*: /- 8.6 µn/m * mesendoderm inducer 6
7 Measuring cell-cortex tension Force to deform cell surface: CtEc>CtM>CtEn Phase Phalloidin/pMLC Cortical tension: myosin II-dependant Pair-wise sorting assays: ectoderm in the middle Time course of cluster formation Meso Ecto +EDTA Adhesion Ecto Ecto/Meso Cytochalasin D Blebbistatin Dominant negative ROCK Cortical tension Ecto 7
8 Cell Potts Model Cell behavior driven by energy minimization: total energy of an aggregate depends on the interfacial tension between cell-cell and cell-surface interfaces. Factors controlling cell-cell interfacial tension: - adhesion (J) - cortex elasticity/tension (T) Adhesion values (experimental): - Homotypic: J endo >J meso >J ecto - Heterotypic: J ecto.meso =J ecto,endo =J ecto, (ecto homotypic) - Cell-media= zero Cortical tension: - cell cortex: homogeneous (simulated/non-polarized) T c ecto >T c meso > T c endo - cell-medium: (experimental values/polarized) T c ecto/medium >T c meso/medium > T c endo/medium - cell-cell: equal for all progenitors Simulation of cell sorting: DSC wins over DAH? Central position correlates with higher cortical tension not adhesion Equilibrium Phalloidin /differential Ct at cellmedia interface Straighter surface ecto Reduced Ct Ecto k: interfacial tension at cell-cell (γcc)or cell-media (γcm)interface l: α, β angles between cells at the surface of homotypic aggregates 8
9 Morphogenetic behavior in vivo MZ-oep: maternal-zygotic one-eye pinhead mutant, consisting mainly of ectodermal progenitors. b. ecto-transplant: loose cluster in epiblast. c,d. meso/ endo transplant: segregated into a compact cluster (meso) or disperse (endo) between yolk/epiblast. in vivo sorting different from in vitro. Model h-j: simulation including strong adhesion interaction between ecto- EVL and meso-yolk (source of TGFβ signaling); similar to in vitro germlayer sorting. Yolk, EVL, Ecto,Meso Interaction with epithelia breaks sorting rules? Self-aggregation driven by forces along the surface of cell aggregates can be modeled by either adhesion (DAH), tension (DSC) or both. Strong adhesive interaction with epithelia can reduce cell surface tension within an aggregate (i.e. mesoderm elongation as it is surrounded by epithelia) Experimental evidence: Ectoderm aggregates: control (no treatment) or over expressing M-PAC*: Result: Control ectoderm inside, M-PAC outside Wrapping aggregates with control ectoderm (non-treated): Result: Control ectoderm outside, M-PAC inside Wrapping aggregates with M-PAC ectoderm: Result: Control ectoderm inside, M-PAC outside *protocadherin that reduces cadherin-dependent adhesion 9
10 Summary Differences in actomyosin-dependent cell-cortex tension play a role in germ layer progenitor sorting. Cell sort according to their aggregate surface tension, i.e. the aggregate with the lower surface tension surrounds the one with the higher surface tension. Aggregate surface tension characterizes the tendency of the global cell aggregate area to decrease. Aggregate surface tension is higher at the interface between cell-media(γ CM ); which is controlled by cortical actomyosin tension only; and lower at the cell-cell (γ C-C ) interface; which is the result of cortical tension minus adhesion at the interface. For cell-cortex tension to increase aggregate surface tension and influence cell sorting; it must be higher at the cell-media interface than at the cell-cell interface. Cell-cell adhesion increases aggregate surface tension by reducing cell-cell tension. Both differential adhesion and interface-specific cortex tension are important to explain sorting behavior in vitro and in vivo. 10
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