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Apoptosis Maintains Oocyte Quality in Aging Caenorhabditis elegans Females

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PLoS Genetics

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      Abstract

      In women, oocytes arrest development at the end of prophase of meiosis I and remain quiescent for years. Over time, the quality and quantity of these oocytes decreases, resulting in fewer pregnancies and an increased occurrence of birth defects. We used the nematode Caenorhabditis elegans to study how oocyte quality is regulated during aging. To assay quality, we determine the fraction of oocytes that produce viable eggs after fertilization. Our results show that oocyte quality declines in aging nematodes, as in humans. This decline affects oocytes arrested in late prophase, waiting for a signal to mature, and also oocytes that develop later in life. Furthermore, mutations that block all cell deaths result in a severe, early decline in oocyte quality, and this effect increases with age. However, mutations that block only somatic cell deaths or DNA-damage–induced deaths do not lower oocyte quality. Two lines of evidence imply that most developmentally programmed germ cell deaths promote the proper allocation of resources among oocytes, rather than eliminate oocytes with damaged chromosomes. First, oocyte quality is lowered by mutations that do not prevent germ cell deaths but do block the engulfment and recycling of cell corpses. Second, the decrease in quality caused by apoptosis mutants is mirrored by a decrease in the size of many mature oocytes. We conclude that competition for resources is a serious problem in aging germ lines, and that apoptosis helps alleviate this problem.

      Author Summary

      As women age, the quality of their oocytes declines, causing the eggs they make to have a higher chance of producing a miscarriage or a child with birth defects. We used the roundworm C. elegans to study this problem. We show that oocyte quality declines in these small animals during aging, much as in mammals. Furthermore, our results show that the programmed deaths of many developing oocytes help maintain the quality of the oocytes that survive, resulting in better eggs. These cell deaths appear to regulate the way resources are allocated in the aging germ line. Since many oocytes die in humans as well as in nematodes, our studies point to the possibility of improving oocyte quality by manipulating cell death in the germ line.

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      Most cited references 72

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      The genetics of Caenorhabditis elegans.

      Methods are described for the isolation, complementation and mapping of mutants of Caenorhabditis elegans, a small free-living nematode worm. About 300 EMS-induced mutants affecting behavior and morphology have been characterized and about one hundred genes have been defined. Mutations in 77 of these alter the movement of the animal. Estimates of the induced mutation frequency of both the visible mutants and X chromosome lethals suggests that, just as in Drosophila, the genetic units in C. elegans are large.
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        We have found that mutations in the gene daf-2 can cause fertile, active, adult Caenorhabditis elegans hermaphrodites to live more than twice as long as wild type. This lifespan extension, the largest yet reported in any organism, requires the activity of a second gene, daf-16. Both genes also regulate formation of the dauer larva, a developmentally arrested larval form that is induced by crowding and starvation and is very long-lived. Our findings raise the possibility that the longevity of the dauer is not simply a consequence of its arrested growth, but instead results from a regulated lifespan extension mechanism that can be uncoupled from other aspects of dauer formation. daf-2 and daf-16 provide entry points into understanding how lifespan can be extended.
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          The embryonic cell lineage of the nematode Caenorhabditis elegans.

          The embryonic cell lineage of Caenorhabditis elegans has been traced from zygote to newly hatched larva, with the result that the entire cell lineage of this organism is now known. During embryogenesis 671 cells are generated; in the hermaphrodite 113 of these (in the male 111) undergo programmed death and the remainder either differentiate terminally or become postembryonic blast cells. The embryonic lineage is highly invariant, as are the fates of the cells to which it gives rise. In spite of the fixed relationship between cell ancestry and cell fate, the correlation between them lacks much obvious pattern. Thus, although most neurons arise from the embryonic ectoderm, some are produced by the mesoderm and a few are sisters to muscles; again, lineal boundaries do not necessarily coincide with functional boundaries. Nevertheless, cell ablation experiments (as well as previous cell isolation experiments) demonstrate substantial cell autonomy in at least some sections of embryogenesis. We conclude that the cell lineage itself, complex as it is, plays an important role in determining cell fate. We discuss the origin of the repeat units (partial segments) in the body wall, the generation of the various orders of symmetry, the analysis of the lineage in terms of sublineages, and evolutionary implications.
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            Author and article information

            Affiliations
            Department of Molecular Biology, UMDNJ School of Osteopathic Medicine, Stratford, New Jersey, United States of America
            Huntsman Cancer Institute, United States of America
            Author notes

            Conceived and designed the experiments: SA REE. Performed the experiments: SA REE. Analyzed the data: SA REE. Wrote the paper: SA REE.

            Contributors
            Role: Editor
            Journal
            PLoS Genet
            plos
            plosgen
            PLoS Genetics
            Public Library of Science (San Francisco, USA )
            1553-7390
            1553-7404
            December 2008
            December 2008
            5 December 2008
            : 4
            : 12
            2585808
            19057674
            08-PLGE-RA-0735R3
            10.1371/journal.pgen.1000295
            (Editor)
            Andux, Ellis. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
            Counts
            Pages: 13
            Categories
            Research Article
            Cell Biology/Cellular Death and Stress Responses
            Developmental Biology/Aging
            Developmental Biology/Developmental Molecular Mechanisms
            Developmental Biology/Germ Cells
            Genetics and Genomics/Animal Genetics

            Genetics

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