Abstract

One of the most studied phosphoinositides is phosphatidylinositol 4,5-bisphosphate (PIP2), which localizes to the plasma membrane, nuclear speckles, small foci in the nucleoplasm, and to the nucleolus in mammalian cells. Here, we show that PIP2 also localizes to the nucleus in prophase I, during the gametogenesis of C. elegans hermaphrodite. The depletion of PIP2 by type I PIP kinase (PPK-1) kinase RNA interference results in an altered chromosome structure and leads to various defects during meiotic progression. We observed a decreased brood size and aneuploidy in progeny, defects in synapsis, and crossover formation. The altered chromosome structure is reflected in the increased transcription activity of a tightly regulated process in prophase I. To elucidate the involvement of PIP2 in the processes during the C. elegans development, we identified the PIP2-binding partners, leucine-rich repeat (LRR-1) protein and proteasome subunit beta 4 (PBS-4), pointing to its involvement in the ubiquitin–proteasome pathway.

Highlights

  • Meiotic division is a specific process of gametogenesis, where the DNA from the maternal cell replicates and divides in two turns of cell division, into new haploid germ cells

  • Indirect immunofluorescence using an anti-PIP2 antibody showed the localization of PIP2 in the C. elegans germ cells

  • It is known that PPK-1 is a PIP2 synthesizing enzyme, the depletion of PIP2 is possible via the knockdown of PPK-1 [31]

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Summary

Introduction

Meiotic division is a specific process of gametogenesis, where the DNA from the maternal cell replicates and divides in two turns of cell division, into new haploid germ cells. In Caenorhabditis elegans, this includes the pairing of homologous chromosomes, which occurs during the leptotene and zygotene stages of prophase I (transition zone of the germ line). During this highly dynamic process, the two homologous copies of each chromosome find each other within the nucleus through an active search process that enables the chromosomes to distinguish the “self versus non-self” and to assume a side-by-side alignment [1]. The process of pairing is coupled with a synaptonemal complex assembly between the formation of homologs and crossovers (COs), which provides sufficient tension to align the chromosomes on the spindle. DNA transcription in germ cells is tightly regulated and represents ~21% of the transcription of all known C. elegans genes [5], mostly expressing only the proteins involved in or regulating the meiotic progression

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