The TRIM-NHL Protein LIN-41 and the OMA RNA-Binding Proteins Antagonistically Control the Prophase-to-Metaphase Transition and Growth of Caenorhabditis elegans Oocytes

Abstract

In many animals, oocytes enter meiosis early in their development but arrest in meiotic prophase I. Oocyte growth, which occurs during this arrest period, enables the acquisition of meiotic competence and the capacity to produce healthy progeny. Meiotic resumption, or meiotic maturation, involves the transition to metaphase I (M phase) and is regulated by intercellular signaling and cyclin-dependent kinase activation. Premature meiotic maturation would be predicted to diminish fertility as the timing of this event, which normally occurs after oocyte growth is complete, is crucial. In the accompanying article in this issue, we identify the highly conserved TRIM-NHL protein LIN-41 as a translational repressor that copurifies with OMA-1 and OMA-2, RNA-binding proteins redundantly required for normal oocyte growth and meiotic maturation. In this article, we show that LIN-41 enables the production of high-quality oocytes and plays an essential role in controlling and coordinating oocyte growth and meiotic maturation. lin-41 null mutants display a striking defect that is specific to oogenesis: pachytene-stage cells cellularize prematurely and fail to progress to diplotene. Instead, these cells activate CDK-1, enter M phase, assemble spindles, and attempt to segregate chromosomes. Translational derepression of the CDK-1 activator CDC-25.3 appears to contribute to premature M-phase entry in lin-41 mutant oocytes. Genetic and phenotypic analyses indicate that LIN-41 and OMA-1/2 exhibit an antagonistic relationship, and we suggest that translational regulation by these proteins could be important for controlling and coordinating oocyte growth and meiotic maturation.

Meiosis

“…In lin-41 mutants pachytene cells prematurely cellularize, diplotene does not occur, and oocytes prematurely enter M phase. This premature M phase entry is elicited in part by translational derepression of a CDK-1 inhibitor (Spike et al, 2014: PMID 25261698). For further reading on oocyte maturation and oocyte release from prophase arrest, please see Control of oocyte meiotic maturation and fertilization, http://dx.doi.org/10.1895/wormbook.1.53.1, as well as (Kim et al, 2013: PMID 22872481).…”

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

“…SS615 pgl-1(bn101) unc-24(e138) IV; pgl-3(bn104) dpy-11(e224) V, SS712 ife-1(bn127) III, WM300 alg-4(ok1041) III; alg-3(tm1155) IV, JK1403 fog-3(q470)/unc-13(e1091) lin-11(n566) I, CB3844 fem-3(e2006) IV and TH206 [ pgl-1p::PGL-1::TY1::EGFP::3xFLAG(92C12)::pgl-1 3′ UTR + Cbr-unc-119(+)] I. DG3913 lin-41(tn1541[GFP::tev::s::LIN-41]) I was kindly provided by David Greenstein (Spike et al, 2014). RNAi P-granule RNAi (simultaneously targeting pgl-1, pgl-3, glh-1 and glh-4) has been described previously (Updike et al, 2014).…”

Depletion of cdc‐25.3, a Caenorhabditis elegans orthologue of cdc25, increases physiological germline apoptosis

“…Then, the distribution of germ nuclei containing different numbers of RAD-51 foci in the respective zones was plotted for both N2 and cdc-25.3(ok358) mutant hermaphrodites (Fig. Nevertheless, the brood size of cdc-25.3(ok358) mutants was only 16% lower than that of N2 hermaphrodites as previously reported [43], and the embryonic lethality in cdc-25.3(ok358) mutants was merely 2.9-fold higher than that in N2 under physiological conditions (Fig. We found that the number of RAD-51 foci per germ nucleus was higher in cdc-25.3(ok358) mutant hermaphrodite gonads than in N2 hermaphrodite gonads through the pachytene zones ( Fig.…”