Coupled oscillators coordinate collective germline growth

Caroline A. Doherty, Rocky Diegmiller, Manisha Kapasiawala, Elizabeth R. Gavis, Stanislav Y. Shvartsman

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

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. Doherty et al. uncover a mechanism whereby oocyte-mediated cell cycle regulation controls the collective growth of supporting nurse cells within the Drosophila ovarian cyst. This mechanism fits the framework of coupled oscillators that undergo synchronization and has widespread implications for other similar dynamical systems in biology.

Original languageEnglish (US)
Pages (from-to)860-870.e8
JournalDevelopmental cell
Volume56
Issue number6
DOIs
StatePublished - Mar 22 2021

All Science Journal Classification (ASJC) codes

  • General Biochemistry, Genetics and Molecular Biology
  • Molecular Biology
  • Cell Biology
  • Developmental Biology

Keywords

  • Dacapo
  • Drosophila oogenesis
  • coupled oscillators
  • cyclin E
  • endoreplication
  • germline cyst
  • nonlinear dynamics

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