A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis

Martin ET, Blatt P, Ngyuen E, Lahr R, Selvam S, Yoon HAM, Pocchiari T, Emtenani S, Siekhaus DE, Berman A, Fuchs G, Rangan P. 2022. A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis. Developmental Cell. 57(7), 883–900.e10.


Journal Article | Published | English

Scopus indexed
Author
Martin, Elliot T.; Blatt, Patrick; Ngyuen, Elaine; Lahr, Roni; Selvam, Sangeetha; Yoon, Hyun Ah M.; Pocchiari, Tyler; Emtenani, ShamsiISTA ; Siekhaus, Daria EISTA ; Berman, Andrea; Fuchs, Gabriele; Rangan, Prashanth
All
Department
Abstract
Ribosomal defects perturb stem cell differentiation, causing diseases called ribosomopathies. How ribosome levels control stem cell differentiation is not fully known. Here, we discovered three RNA helicases are required for ribosome biogenesis and for Drosophila oogenesis. Loss of these helicases, which we named Aramis, Athos and Porthos, lead to aberrant stabilization of p53, cell cycle arrest and stalled GSC differentiation. Unexpectedly, Aramis is required for efficient translation of a cohort of mRNAs containing a 5’-Terminal-Oligo-Pyrimidine (TOP)-motif, including mRNAs that encode ribosomal proteins and a conserved p53 inhibitor, Novel Nucleolar protein 1 (Non1). The TOP-motif co-regulates the translation of growth-related mRNAs in mammals. As in mammals, the La-related protein co-regulates the translation of TOP-motif containing RNAs during Drosophila oogenesis. Thus, a previously unappreciated TOP-motif in Drosophila responds to reduced ribosome biogenesis to co-regulate the translation of ribosomal proteins and a p53 repressor, thus coupling ribosome biogenesis to GSC differentiation.
Publishing Year
Date Published
2022-04-11
Journal Title
Developmental Cell
Acknowledgement
We are grateful to all members of the Rangan and Fuchs labs for their discussion and comments on the manuscript. We also thanks Dr. Sammons, Dr. Marlow, Life Science Editors, for their thoughts and comments the manuscript Additionally, we thank the Bloomington Stock Center, the Vienna Drosophila Resource Center, the BDGP Gene Disruption Project, and Flybase for fly stocks, reagents, and other resources. P.R. is funded by the NIH/NIGMS (R01GM111779-06 and RO1GM135628-01), G.F. is funded by NSF MCB-2047629 and NIH RO3 AI144839, D.E.S. was funded by Marie Curie CIG 334077/IRTIM and the Austrian Science Fund (FWF) grant ASI_FWF01_P29638S, and A.B is funded by NIH R01GM116889 and American Cancer Society RSG-17-197-01-RMC.
Volume
57
Issue
7
Page
883-900.e10
ISSN
eISSN
IST-REx-ID

Cite this

Martin ET, Blatt P, Ngyuen E, et al. A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis. Developmental Cell. 2022;57(7):883-900.e10. doi:10.1016/j.devcel.2022.03.005
Martin, E. T., Blatt, P., Ngyuen, E., Lahr, R., Selvam, S., Yoon, H. A. M., … Rangan, P. (2022). A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis. Developmental Cell. Elsevier. https://doi.org/10.1016/j.devcel.2022.03.005
Martin, Elliot T., Patrick Blatt, Elaine Ngyuen, Roni Lahr, Sangeetha Selvam, Hyun Ah M. Yoon, Tyler Pocchiari, et al. “A Translation Control Module Coordinates Germline Stem Cell Differentiation with Ribosome Biogenesis during Drosophila Oogenesis.” Developmental Cell. Elsevier, 2022. https://doi.org/10.1016/j.devcel.2022.03.005.
E. T. Martin et al., “A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis,” Developmental Cell, vol. 57, no. 7. Elsevier, p. 883–900.e10, 2022.
Martin ET, Blatt P, Ngyuen E, Lahr R, Selvam S, Yoon HAM, Pocchiari T, Emtenani S, Siekhaus DE, Berman A, Fuchs G, Rangan P. 2022. A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during Drosophila oogenesis. Developmental Cell. 57(7), 883–900.e10.
Martin, Elliot T., et al. “A Translation Control Module Coordinates Germline Stem Cell Differentiation with Ribosome Biogenesis during Drosophila Oogenesis.” Developmental Cell, vol. 57, no. 7, Elsevier, 2022, p. 883–900.e10, doi:10.1016/j.devcel.2022.03.005.
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