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The CPEB Protein Orb2 Has Multiple Functions during Spermatogenesis in Drosophila melanogaster

Xu, Shuwa and Hafer, Nathaniel and Agunwamba, Blessing and Schedl, Paul (2012) The CPEB Protein Orb2 Has Multiple Functions during Spermatogenesis in Drosophila melanogaster. PLoS Genetics, 8 (11). Art. No. e1003079. ISSN 1553-7390. http://resolver.caltech.edu/CaltechAUTHORS:20130320-101550398

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Abstract

Cytoplasmic Polyadenylation Element Binding (CPEB) proteins are translational regulators that can either activate or repress translation depending on the target mRNA and the specific biological context. There are two CPEB subfamilies and most animals have one or more genes from each. Drosophila has a single CPEB gene, orb and orb2, from each subfamily. orb expression is only detected at high levels in the germline and has critical functions in oogenesis but not spermatogenesis. By contrast, orb2 is broadly expressed in the soma; and previous studies have revealed important functions in asymmetric cell division, viability, motor function, learning, and memory. Here we show that orb2 is also expressed in the adult male germline and that it has essential functions in programming the progression of spermatogenesis from meiosis through differentiation. Like the translational regulators boule (bol) and off-schedule (ofs), orb2 is required for meiosis and orb2 mutant spermatocytes undergo a prolonged arrest during the meiotic G2-M transition. However, orb2 differs from boule and off-schedule in that this arrest occurs at a later step in meiotic progression after the synthesis of the meiotic regulator twine. orb2 is also required for the orderly differentiation of the spermatids after meiosis is complete. The differentiation defects in orb2 mutants include abnormal elongation of the spermatid flagellar axonemes, a failure in individualization and improper post-meiotic gene expression. Amongst the orb2 differentiation targets are orb and two other mRNAs, which are transcribed post-meiotically and localized to the tip of the flagellar axonemes. Additionally, analysis of a partial loss of function orb2 mutant suggests that the orb2 differentiation phenotypes are independent of the earlier arrest in meiosis.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pgen.1003079 DOIUNSPECIFIED
http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1003079PublisherUNSPECIFIED
Additional Information:© 2012 Xu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received July 10, 2012; Accepted September 27, 2012; Published November 29, 2012. Funding: This work was initially supported by NIH GM05937 until the grant was terminated in 2008. Subsequent support came from GM043432. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We would like to thank the lab members for their support and technical help. We also would like to thank Dr. Steven Wasserman for the generous provision of Boule antibody; Dr. Minx Fuller, Dr. Catherine Baker, and Dr. Steve DiNardo for generous provision of flies and helpful discussions; Dr. Kathryn Miller for MyosinVI antibody; Bloomington Stock center for mutant flies; HSDB for monoclonal antibodies; J. Goodhouse for assistance with confocal microscopy; Gordon Gray for fly food. We thank the Princeton Drosophila community for sharing reagents. Author Contributions: Conceived and designed the experiments: SX NH PS. Performed the experiments: SX NH BA. Analyzed the data: SX NH BA PS. Contributed reagents/materials/analysis tools: SX NH BA. Wrote the paper: SX PS.
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Funding AgencyGrant Number
NIHGM05937
NIHGM043432
Record Number:CaltechAUTHORS:20130320-101550398
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20130320-101550398
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:37574
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:25 Mar 2013 23:08
Last Modified:25 Mar 2013 23:08

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