Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans

Gibert, M. Alsina; Starck, Joëlle; Beguet, B.

doi:10.1111/j.1768-322x.1984.tb00254.x

Cited by 62 publications

(41 citation statements)

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“…If germline CGH-1/CAR-1 foci are involved in storage or translational regulation but not degradation of maternal mRNA, it could explain why they increase in intensity and appear in the gonad core in parallel with newly synthesized mRNA (Fig. 3A,J) (Gibert et al, 1984;Navarro and Blackwell, 2005;Navarro et al, 2001;Schisa et al, 2001), and why physical association between CGH-1 orthologs and the mRNA decapping/degradation machinery has not been detected in the metazoan germline (Table 1).…”

Section: Discussionmentioning

confidence: 99%

A conserved RNA-protein complex component involved in physiological germline apoptosis regulation inC. elegans

2005

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Two conserved features of oogenesis are the accumulation of translationally quiescent mRNA, and a high rate of stage-specific apoptosis. Little is understood about the function of this cell death. In C. elegans, apoptosis occurring through a specific 'physiological' pathway normally claims about half of all developing oocytes. The frequency of this germ cell death is dramatically increased by a lack of the RNA helicase CGH-1, orthologs of which are involved in translational control in oocytes and decapping-dependent mRNA degradation in yeast processing (P) bodies. Here, we describe a predicted RNAbinding protein, CAR-1, that associates with CGH-1 and Y-box proteins within a conserved germline RNA-protein (RNP) complex, and in cytoplasmic particles in the gonad and early embryo. The CGH-1/CAR-1 interaction is conserved in Drosophila oocytes. When car-1 expression is depleted by RNA interference (RNAi), physiological apoptosis is increased, brood size is modestly reduced, and early embryonic cytokinesis is abnormal. Surprisingly, if apoptosis is prevented car-1(RNAi) animals are characterized by a progressive oogenesis defect that leads rapidly to gonad failure. Elevated germ cell death similarly compensates for lack of the translational regulator CPB-3 (CPEB), orthologs of which function together with CGH-1 in diverse organisms. We conclude that CAR-1 is of critical importance for oogenesis, that the association between CAR-1 and CGH-1 has been conserved, and that the regulation of physiological germ cell apoptosis is specifically influenced by certain functions of the CGH-1/CAR-1 RNP complex. We propose that this cell death pathway facilitates the formation of functional oocytes, possibly by monitoring specific cytoplasmic events during oogenesis.

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Section: Discussionmentioning

confidence: 99%

A conserved RNA-protein complex component involved in physiological germline apoptosis regulation inC. elegans

2005

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“…These results provide a mechanistic explanation for previous observations on the distribution of RNA in the gonad. Labeled-uridine incorporation showed that nascent RNA (largely rRNA) first appears in pachytene nuclei, and subsequently accumulates in the gonad core before appearing in oocyte cytoplasm (Gibert et al, 1984;Schisa et al, 2001;Starck, 1977). Because materials are transported from numerous pachytene-stage nuclei into single, enlarging oocytes, the pachytene-stage nuclei can be considered a nurse cell population.…”

Section: Discussionmentioning

confidence: 99%

“…elegans gonads do not contain morphologically distinct nurse cells, and none of the germline nuclei appear to be highly polyploid when stained for DNA (Hirsh et al, 1976) (our unpublished data). Prior to oogenesis, most germ cells appear to be highly active transcriptionally, producing RNA that accumulates in the gonad core (Gibert et al, 1984;Starck, 1977). As the transcriptionally quiescent oocytes enlarge, they presumably incorporate core cytoplasm that they, or other germ cells, synthesized during earlier developmental stages and deposited in the core.…”

Section: Introductionmentioning

confidence: 99%

Actin-dependent cytoplasmic streaming inC. elegansoogenesis

2007

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*Oocytes in the C. elegans gonad enlarge rapidly. During the stage of enlargement, they are transcriptionally quiescent, and it is not understood how they acquire large quantities of materials such as mRNA and protein. Enlarging oocytes are connected via cytoplasmic bridges to a large, younger population of transcriptionally active germ cells at various stages of mitosis and meiosis. We show here that there is a general streaming of gonad cytoplasm towards and into the enlarging oocytes, originating primarily from pachytene-stage germ cells. Because previous studies suggested that most or all of the pachytene germ cells have the potential to differentiate into oocytes, the pachytene cells appear to function transiently as nurse cells. Somatic gonadal cells that surround the germ cells do not appear essential for streaming. Instead, materials appear to be pulled into oocytes by forces generated either in, or adjacent to, the enlarging oocytes themselves. Streaming appears to be driven by the actomyosin cytoskeleton, although we show that populations of both microfilaments and microtubules are oriented in the direction of flow. Our study shows that oocyte enlargement in C. elegans differs significantly from that in Drosophila, where a small number of specialized nurse cells expel their contents into the enlarging oocyte.

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“…Two uORFs are boxed, and the ATG of the GNA-2 ORF is in bold and underlined. mosomes become highly condensed in late-stage oocytes (diakinesis), almost no de novo RNA synthesis occurs (Gibert et al 1984;Schisa et al 2001) and RNA polymerase II becomes inactive (Kelly et al 2002). Therefore, most maternal transcripts, including GLD-1 targets rme-2, oma-1, and oma-2 mRNAs, are transcribed mainly in pachytene-stage germ cells in the distal region and transported into the common cytoplasmic core.…”

Section: Gna-2 Mrna Is a Naturally Occurring Target Of Nmd And Gld-1 mentioning

confidence: 99%

Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans

Schedl¹

2004

Genes Dev.

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Previously, we identified multiple in vivo mRNA targets of the maxi-KH/STAR domain protein GLD-1 by their ability to interact with GLD-1 in cytoplasmic extracts and, for all targets tested thus far, GLD-1 functions as a translational repressor. However, here we show that GLD-1 stabilizes the mRNAs of two targets, gna-2 (T23G11.2) and Y75B12B.1. gna-2 mRNA has two upstream open reading frames (uORF), resulting in two premature stop codons. We found that gna-2 mRNA is a naturally occurring mRNA target of nonsense-mediated mRNA decay (NMD) and that the binding of GLD-1 protects gna-2 mRNA from NMD, likely by repressing translation of the uORFs. Therefore, gna-2 mRNA comes under two posttranscriptional controls: (1) translation regulation by a specific translational repressor, GLD-1; and (2) uORF elicited regulation, mainly through NMD. As a result, these two posttranscriptional controls together provide precise temporal and spatial control of gene expression. Consistent with this novel mode of regulation, when GLD-1 mRNA targets acquire premature stop codon mutations, GLD-1 protects them from NMD. Analysis of several mRNA targets containing premature stop codons suggests that in translation repression, GLD-1 either represses ribosome assembly on the target mRNA, or subsequent ribosome elongation to the premature stop codon.[Keywords: Germ line; translation repression; upstream open reading frame; nonsense-mediated mRNA decay; gld-1; gna-2] Supplemental material is available at http://www.genesdev.org.

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Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans

Cited by 62 publications

References 0 publications

A conserved RNA-protein complex component involved in physiological germline apoptosis regulation inC. elegans

A conserved RNA-protein complex component involved in physiological germline apoptosis regulation inC. elegans

Actin-dependent cytoplasmic streaming inC. elegansoogenesis

Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans

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