Cargando…
Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans
The oocytes of most sexually reproducing animals arrest in meiotic prophase I. Oocyte growth, which occurs during this period of arrest, enables oocytes to acquire the cytoplasmic components needed to produce healthy progeny and to gain competence to complete meiosis. In the nematode Caenorhabditis...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Genetics Society of America
2014
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4256769/ https://www.ncbi.nlm.nih.gov/pubmed/25261697 http://dx.doi.org/10.1534/genetics.114.168823 |
_version_ | 1782347631049048064 |
---|---|
author | Spike, Caroline A. Coetzee, Donna Nishi, Yuichi Guven-Ozkan, Tugba Oldenbroek, Marieke Yamamoto, Ikuko Lin, Rueyling Greenstein, David |
author_facet | Spike, Caroline A. Coetzee, Donna Nishi, Yuichi Guven-Ozkan, Tugba Oldenbroek, Marieke Yamamoto, Ikuko Lin, Rueyling Greenstein, David |
author_sort | Spike, Caroline A. |
collection | PubMed |
description | The oocytes of most sexually reproducing animals arrest in meiotic prophase I. Oocyte growth, which occurs during this period of arrest, enables oocytes to acquire the cytoplasmic components needed to produce healthy progeny and to gain competence to complete meiosis. In the nematode Caenorhabditis elegans, the major sperm protein hormone promotes meiotic resumption (also called meiotic maturation) and the cytoplasmic flows that drive oocyte growth. Prior work established that two related TIS11 zinc-finger RNA-binding proteins, OMA-1 and OMA-2, are redundantly required for normal oocyte growth and meiotic maturation. We affinity purified OMA-1 and identified associated mRNAs and proteins using genome-wide expression data and mass spectrometry, respectively. As a class, mRNAs enriched in OMA-1 ribonucleoprotein particles (OMA RNPs) have reproductive functions. Several of these mRNAs were tested and found to be targets of OMA-1/2-mediated translational repression, dependent on sequences in their 3′-untranslated regions (3′-UTRs). Consistent with a major role for OMA-1 and OMA-2 in regulating translation, OMA-1-associated proteins include translational repressors and activators, and some of these proteins bind directly to OMA-1 in yeast two-hybrid assays, including OMA-2. We show that the highly conserved TRIM-NHL protein LIN-41 is an OMA-1-associated protein, which also represses the translation of several OMA-1/2 target mRNAs. In the accompanying article in this issue, we show that LIN-41 prevents meiotic maturation and promotes oocyte growth in opposition to OMA-1/2. Taken together, these data support a model in which the conserved regulators of mRNA translation LIN-41 and OMA-1/2 coordinately control oocyte growth and the proper spatial and temporal execution of the meiotic maturation decision. |
format | Online Article Text |
id | pubmed-4256769 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | Genetics Society of America |
record_format | MEDLINE/PubMed |
spelling | pubmed-42567692014-12-08 Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans Spike, Caroline A. Coetzee, Donna Nishi, Yuichi Guven-Ozkan, Tugba Oldenbroek, Marieke Yamamoto, Ikuko Lin, Rueyling Greenstein, David Genetics Investigations The oocytes of most sexually reproducing animals arrest in meiotic prophase I. Oocyte growth, which occurs during this period of arrest, enables oocytes to acquire the cytoplasmic components needed to produce healthy progeny and to gain competence to complete meiosis. In the nematode Caenorhabditis elegans, the major sperm protein hormone promotes meiotic resumption (also called meiotic maturation) and the cytoplasmic flows that drive oocyte growth. Prior work established that two related TIS11 zinc-finger RNA-binding proteins, OMA-1 and OMA-2, are redundantly required for normal oocyte growth and meiotic maturation. We affinity purified OMA-1 and identified associated mRNAs and proteins using genome-wide expression data and mass spectrometry, respectively. As a class, mRNAs enriched in OMA-1 ribonucleoprotein particles (OMA RNPs) have reproductive functions. Several of these mRNAs were tested and found to be targets of OMA-1/2-mediated translational repression, dependent on sequences in their 3′-untranslated regions (3′-UTRs). Consistent with a major role for OMA-1 and OMA-2 in regulating translation, OMA-1-associated proteins include translational repressors and activators, and some of these proteins bind directly to OMA-1 in yeast two-hybrid assays, including OMA-2. We show that the highly conserved TRIM-NHL protein LIN-41 is an OMA-1-associated protein, which also represses the translation of several OMA-1/2 target mRNAs. In the accompanying article in this issue, we show that LIN-41 prevents meiotic maturation and promotes oocyte growth in opposition to OMA-1/2. Taken together, these data support a model in which the conserved regulators of mRNA translation LIN-41 and OMA-1/2 coordinately control oocyte growth and the proper spatial and temporal execution of the meiotic maturation decision. Genetics Society of America 2014-12 2014-09-26 /pmc/articles/PMC4256769/ /pubmed/25261697 http://dx.doi.org/10.1534/genetics.114.168823 Text en Copyright © 2014 by the Genetics Society of America Available freely online through the author-supported open access option. |
spellingShingle | Investigations Spike, Caroline A. Coetzee, Donna Nishi, Yuichi Guven-Ozkan, Tugba Oldenbroek, Marieke Yamamoto, Ikuko Lin, Rueyling Greenstein, David Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title | Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title_full | Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title_fullStr | Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title_full_unstemmed | Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title_short | Translational Control of the Oogenic Program by Components of OMA Ribonucleoprotein Particles in Caenorhabditis elegans |
title_sort | translational control of the oogenic program by components of oma ribonucleoprotein particles in caenorhabditis elegans |
topic | Investigations |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4256769/ https://www.ncbi.nlm.nih.gov/pubmed/25261697 http://dx.doi.org/10.1534/genetics.114.168823 |
work_keys_str_mv | AT spikecarolinea translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT coetzeedonna translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT nishiyuichi translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT guvenozkantugba translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT oldenbroekmarieke translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT yamamotoikuko translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT linrueyling translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans AT greensteindavid translationalcontroloftheoogenicprogrambycomponentsofomaribonucleoproteinparticlesincaenorhabditiselegans |