Abstract
In many species, only one oocyte is specified among a group of interconnected germline sister cells. In Drosophila melanogaster, 16 interconnected cells form a germline cyst, where one cell differentiates into an oocyte, while the rest become nurse cells that supply the oocyte with mRNAs, proteins, and organelles through intercellular cytoplasmic bridges named ring canals via microtubule-based transport. In this study, we find that a microtubule polymerase Mini spindles (Msps), the Drosophila homolog of XMAP215, is essential for maintenance of the oocyte specification. mRNA encoding Msps is transported and concentrated in the oocyte by dynein-dependent transport along microtubules. Translated Msps stimulates microtubule polymerization in the oocyte, causing more microtubule plus ends to grow from the oocyte through the ring canals into nurse cells, further enhancing nurse cell-to-oocyte transport by dynein. Knockdown of msps blocks the oocyte growth and causes gradual loss of oocyte determinants. Thus, the Msps-dynein duo creates a positive feedback loop, ensuring oocyte fate maintenance by promoting high microtubule polymerization activity in the oocyte, and enhancing dynein-dependent nurse cell-to-oocyte transport.
| Original language | English (US) |
|---|---|
| Article number | e2303376120 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 120 |
| Issue number | 39 |
| DOIs | |
| State | Published - 2023 |
Funding
ACKNOWLEDGMENTS. We thank many colleagues who generously contributed reagents for this work: Dr. Steve Rogers (UNC at Chapel Hill), Dr. Antoine Guichet (CNRS, Institut Jacques Monod), Dr. David Glover (Caltech), Dr. Yu-Chiun Wang (RIKEN Center for Biosystems Dynamics Research, Japan), Dr. Graydon Gonsalvez (Augusta University), Dr. Timothy Megraw (Florida State University), Dr. Jordan Raff (University of Oxford), Dr. Zhao Zhang (Duke University School of Medicine), Dr. Paul Schedl (Princeton University), Dr. Scott Hawley (Stowers Institute), and Bloomington Drosophila Stock Center (supported by NIH grant P40OD018537) for fly stocks. The Orb 4H8 monoclonal antibody developed by Dr. Paul D. Schedl\u2019s group at Princeton University was obtained from the Developmental Studies Hybridoma Bank, created by the NICHD of the NIH and maintained at the University of Iowa. We thank Northwestern Center for Advanced Microscopy & Nikon Imaging Center for imaging assistance and Northwestern Sanger Sequencing Facility for sequencing services. We thank all the Gelfand laboratory members for their support, discussion, and suggestions. Research reported in this study was supported by the National Institute of General Medical Sciences grant R35GM131752 to V.I.G.
Keywords
- Drosophila
- cell fate
- dynein
- microtubule
- oocyte
ASJC Scopus subject areas
- General