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Coupled oscillators coordinate collective germline growth

Doherty, Caroline A. and Diegmiller, Rocky and Kapasiawala, Manisha and Gavis, Elizabeth R. and Shvartsman, Stanislav Y. (2021) Coupled oscillators coordinate collective germline growth. Developmental Cell, 56 (6). 860-870.e8. ISSN 1534-5807. https://resolver.caltech.edu/CaltechAUTHORS:20210429-132054379

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.devcel.2021.02.015DOIArticle
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.
Funders:
Funding AgencyGrant Number
NIHR01 GM134204
NIHR35 GM126967
NIH Postdoctoral FellowshipF31 HD098835
NIH Predoctoral FellowshipT32 GM007388
Subject Keywords:Drosophila oogenesis; endoreplication; Dacapo; cyclin E; coupled oscillators; nonlinear dynamics; germline cyst
Issue or Number:6
Record Number:CaltechAUTHORS:20210429-132054379
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210429-132054379
Official Citation:Caroline A. Doherty, Rocky Diegmiller, Manisha Kapasiawala, Elizabeth R. Gavis, Stanislav Y. Shvartsman, Coupled oscillators coordinate collective germline growth, Developmental Cell, Volume 56, Issue 6, 2021, Pages 860-870.e8, ISSN 1534-5807, https://doi.org/10.1016/j.devcel.2021.02.015.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108877
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:29 Apr 2021 20:42
Last Modified:29 Apr 2021 20:42

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