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Link to original content: https://pubmed.ncbi.nlm.nih.gov/33214282
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. 2020 Nov 20;370(6519):987-990.
doi: 10.1126/science.aaz4741.

Tissue topography steers migrating Drosophila border cells

Wei Dai #  1 , Xiaoran Guo #  1 , Yuansheng Cao  2 , James A Mondo  1 , Joseph P Campanale  1 , Brandon J Montell  3 , Haley Burrous  1 , Sebastian Streichan  4 , Nir Gov  5 , Wouter-Jan Rappel  2 , Denise J Montell  6
Affiliations

Tissue topography steers migrating Drosophila border cells

Wei Dai et al. Science. .

Abstract

Moving cells can sense and respond to physical features of the microenvironment; however, in vivo, the significance of tissue topography is mostly unknown. Here, we used Drosophila border cells, an established model for in vivo cell migration, to study how chemical and physical information influences path selection. Although chemical cues were thought to be sufficient, live imaging, genetics, modeling, and simulations show that microtopography is also important. Chemoattractants promote predominantly posterior movement, whereas tissue architecture presents orthogonal information, a path of least resistance concentrated near the center of the egg chamber. E-cadherin supplies a permissive haptotactic cue. Our results provide insight into how cells integrate and prioritize topographical, adhesive, and chemoattractant cues to choose one path among many.

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Conflict of interest statement

Competing Interests: The authors declare no competing interests.

Figures

Fig. 1.
Fig. 1.. Medial migration not primarily controlled by chemoattraction
(A) Lateral views of egg chambers showing border cell migration between nurse cells to the oocyte. Dashed lines in (A) indicate cross sections shown in (B). (C) HA-tagged endogenous Keren schematic. (D) Anti-HA-stained living egg chamber. (E) HA-Keren quantification. Dots, locations on path. (F) Quantification of border cell position. Each dot indicates one cluster. ****, P < 0.0001 (Mann-Whitney test). (G and H) Rainbow views of border cell migration in control or with ectopic UAS-PVF1. Scale bars, 20 μm.
Fig. 2.
Fig. 2.. E-cadherin, a permissive medial traction cue
(A to C)Images of control, nurse-cell E-cadherin knockdown (KD), or mosaic nurse-cell overexpression (OE). (D) Quantification of migration. Letters a and b designate significantly different groups (P < 0.01, Kruskal-Wallist test). (E and F) Still images from movies showing border cells pull on nurse-cell junctures in a control egg chamber (E) and the absence of deflection in an E-cadherin knockdown egg chamber (F). (G) Traces of nurse-cell membrane deflections. (H) Quantification of maximum deflections. (**, P < 0.01 Mann-Whitney test). Scale bars, 20 μm.
Fig. 3.
Fig. 3.. Centrally enriched multiple-nurse-cell junctures
(A to C) 3D reconstructions of nurse-cell contacts. Dashed lines in (A) indicate cross sections in (B). (D) Heat map showing distributions of three- (left) or more-than-three- (right) cell junctures as a function of mediolateral position. (E) Schematic representation of protrusion into nurse-cell junctures. (F) Extracellular spaces filled with fluorescent dextran in wild-type. (G) Quantification of the extracellular juncture volume. Values from the 3D model (red) (see the supplementary text, section ST1) and the experimental data (blue). (H) Percentage side protrusions extending to two-cell or three-cell junctures as a fraction of total side protrusions. **, P <0.01 (paired t test). Scale bars, 20 μm.
Fig. 4.
Fig. 4.. Multiple-cell junctures steer cells
(A) Representative simulated trajectories through the wild-type geometry shown in Fig. 3A. (B) Quantification of 99 simulations. (C) Cross-sections showing border cell and nurse-cell positions relative to the egg-chamber center. (D) Representative simulated trajectory. (E) Comparison of the distance from the border cell centroid to the egg-chamber center versus the nearest three-cell juncture. ***, P < 0.001 (paired t-test). Scale bars, 20 μm.
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