Coupled oscillators coordinate collective germline growth
Abstract
Developing oocytes need large supplies of macromolecules and organelles. A conserved strategy for accumulating these products is to pool resources of oocyte-associated germline nurse cells. In Drosophila, these cells grow more than 100-fold to boost their biosynthetic capacity. No previously known mechanism explains how nurse cells coordinate growth collectively. Here, we report a cell cycle-regulating mechanism that depends on bidirectional communication between the oocyte and nurse cells, revealing the oocyte as a critical regulator of germline cyst growth. Transcripts encoding the cyclin-dependent kinase inhibitor, Dacapo, are synthesized by the nurse cells and actively localized to the oocyte. Retrograde movement of the oocyte-synthesized Dacapo protein to the nurse cells generates a network of coupled oscillators that controls the cell cycle of the nurse cells to regulate cyst growth. We propose that bidirectional nurse cell-oocyte communication establishes a growth-sensing feedback mechanism that regulates the quantity of maternal resources loaded into the oocyte.
Additional Information
© 2021 Elsevier. Received 1 May 2020, Revised 3 December 2020, Accepted 16 February 2021, Available online 8 March 2021. We thank G. Laevsky for expert microscopy assistance, P. Schedl, T. Schüpbach, N. Martin, and J. Imran Alsous for discussions and comments on the manuscript, A. Spradling, C. Tarnita, F. Duncan, and M. Golubitsky, I. Ruvinsky, B. Shao, for helpful discussions, R. Marmion for advice on transgenic fly design, L. Yang for supplying purified sfGFP, and J. von Stetina and C. Taber for assistance in developing the method of DNA quantification. Cartoons were created with BioRender. This work was supported by NIH grant R01 GM134204 to S.Y.S., NIH grant R35 GM126967 to E.R.G., NIH F31 HD098835 to R.D. C.A.D. was supported by training grant T32 GM007388. Author contributions. C.A.D., E.R.G., and S.Y.S. conceived and designed the study. C.A.D. and M.K. performed experiments and analyzed data. R.D. and S.Y.S. developed the mathematical model with insight from M.K., C.A.D., R.D., E.R.G., and S.Y.S. wrote the manuscript. These authors declare no competing interests.Attached Files
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Supplemental Material - 1-s2.0-S1534580721001556-mmc2.xlsx
Supplemental Material - 1-s2.0-S1534580721001556-mmc4.mp4
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Additional details
- Eprint ID
- 108877
- DOI
- 10.1016/j.devcel.2021.02.015
- Resolver ID
- CaltechAUTHORS:20210429-132054379
- R01 GM134204
- NIH
- R35 GM126967
- NIH
- F31 HD098835
- NIH Postdoctoral Fellowship
- T32 GM007388
- NIH Predoctoral Fellowship
- Created
-
2021-04-29Created from EPrint's datestamp field
- Updated
-
2021-11-16Created from EPrint's last_modified field