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Actomyosin contractility regulators stabilize the cytoplasmic bridge between the two primordial germ cells during Caenorhabditis elegans embryogenesis.

ABSTRACT: Stable cytoplasmic bridges arise from failed cytokinesis, the last step of cell division, and are a key feature of syncytial architectures in the germline of most metazoans. Whereas the Caenorhabditiselegans germline is syncytial, its formation remains poorly understood. We found that the germline precursor blastomere, P4 , fails cytokinesis, leaving a stable cytoplasmic bridge between the two daughter cells, Z2 and Z3 Depletion of several regulators of actomyosin contractility resulted in a regression of the membrane partition between Z2 and Z3, indicating that they are required to stabilize the cytoplasmic bridge. Epistatic analysis revealed a pathway in which Rho regulators promote accumulation of the noncannonical anillin ANI-2 at the stable cytoplasmic bridge, which in turns promotes the accumulation of the nonmuscle myosin II NMY-2 and the midbody component CYK-7 at the bridge, in part by limiting the accumulation of canonical anillin ANI-1. Our results uncover key steps in C. elegans germline formation and define a set of conserved regulators that are enriched at the primordial germ cell cytoplasmic bridge to ensure its stability during embryonic development.

SUBMITTER: Goupil E

PROVIDER: S-EPMC5739295 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Actomyosin contractility regulators stabilize the cytoplasmic bridge between the two primordial germ cells during Caenorhabditis elegans embryogenesis.

Goupil Eugénie E Amini Rana R Hall David H DH Labbé Jean-Claude JC

Molecular biology of the cell 20171026 26

Stable cytoplasmic bridges arise from failed cytokinesis, the last step of cell division, and are a key feature of syncytial architectures in the germline of most metazoans. Whereas the Caenorhabditiselegans germline is syncytial, its formation remains poorly understood. We found that the germline precursor blastomere, P4 , fails cytokinesis, leaving a stable cytoplasmic bridge between the two daughter cells, Z2 and Z3 De ...[more]

PMID: 29074566

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Project description:Mitochondria harbor an independent genome, called mitochondrial DNA (mtDNA), which contains essential metabolic genes. Although mtDNA mutations occur at high frequency, they are inherited infrequently, indicating that germline mechanisms limit their accumulation. To determine how germline mtDNA is regulated, we examined the control of mtDNA quantity and quality in C. elegans primordial germ cells (PGCs). We show that PGCs combine strategies to generate a low point in mtDNA number by segregating mitochondria into lobe-like protrusions that are cannibalized by adjacent cells, and by concurrently eliminating mitochondria through autophagy, reducing overall mtDNA content twofold. As PGCs exit quiescence and divide, mtDNAs replicate to maintain a set point of ~200 mtDNAs per germline stem cell. Whereas cannibalism and autophagy eliminate mtDNAs stochastically, we show that the kinase PTEN-induced kinase 1 (PINK1), operating independently of Parkin and autophagy, preferentially reduces the fraction of mutant mtDNAs. Thus, PGCs employ parallel mechanisms to control both the quantity and quality of the founding population of germline mtDNAs. eLife digest Mitochondria are the powerhouses of every cell in our bodies. These tiny structures convert energy from the food we eat into a form that cells are able to use. As well as being a separate organ-like structure within our cells, mitochondria even have their own DNA. Mitochondrial DNA contains genes for a small number of special enzymes that allow it to extract energy from food. In contrast, the rest of our cells’ DNA is stored in another structure called the nucleus. Mitochondrial and nuclear DNA are also inherited differently. We inherit nuclear DNA from both our mother and father, but mitochondrial DNA is only passed down from our mothers. During reproduction, maternal DNA (including mitochondrial DNA) comes from the egg cell, which combines with sperm to produce offspring. Defects, or mutations, in mitochondrial genes often lead to mitochondrial diseases. These have a severe impact on health, especially during the very first stages of life. The lineage of precursor cells that gives rise to egg cells is thought to protect itself from mitochondrial mutations, but how it does this is still unclear. Schwartz et al. therefore set out to determine what molecular mechanisms preserve the integrity of mitochondrial DNA from one generation to the next. To address this question, C. elegans roundworms were used, as they are easy to manipulate genetically, and since they are small and transparent, their cells – as well as their mitochondria – are also easily viewed under a microscope. Tracking mitochondria in the worms’ egg precursor cells (also called primordial germ cells, or PGCs) revealed that PGCs actively removed excess mitochondria. The PGCs did this either by internally breaking down mitochondria themselves, or by moving them into protruding lobe-like structures which surrounding cells then engulfed and ‘digested’. Further genetic studies revealed that the PGCs also directly regulated the quality of mitochondrial DNA via a mechanism dependent on the protein PINK1. In worms lacking PINK1, mutant mitochondrial DNA remained in the PGCs at high levels, whereas normal worms successfully reduced the mutant DNA. Thus, the PGCs used parallel mechanisms to control both the quantity and quality of mitochondria passed to the next generation. These results contribute to our understanding of how organisms safeguard their offspring from inheriting mutant mitochondrial DNA. In the future, Schwartz et al. hope that this knowledge will help us treat inherited mitochondrial diseases in humans.

Dataset Information

Actomyosin contractility regulators stabilize the cytoplasmic bridge between the two primordial germ cells during Caenorhabditis elegans embryogenesis.

Publications

Actomyosin contractility regulators stabilize the cytoplasmic bridge between the two primordial germ cells during <i>Caenorhabditis elegans</i> embryogenesis.

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