Checkpoint and physiological apoptosis in germ cells proceeds normally in spaceflown Caenorhabditis elegans

Abstract

It is important for human life in space to study the effects of environmental factors during spaceflight on a number of physiological phenomena. Apoptosis plays important roles in development and tissue homeostasis in metazoans. In this study, we have analyzed apoptotic activity in germ cells of the nematode C. elegans, following spacefight. Comparison of the number of cell corpses in wild type or ced-1 mutants, grown under either ground or spaceflight conditions, showed that both pachytene-checkpoint apoptosis and physiological apoptosis in germ cells occurred normally under spaceflight conditions. In addition, the expression levels of the checkpoint and apoptosis related genes are comparable between spaceflight and ground conditions. This is the first report documenting the occurrence of checkpoint apoptosis in the space environment and suggests that metazoans, including humans, would be able to eliminate cells that have failed to repair DNA lesions introduced by cosmic radiation during spaceflight.

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References

  1. 1.

    Nelson GA, Schubert WW, Kazarians GA, et al. Radiation effects in nematodes: Results from IML-1 experiments. Adv Space Res 1994; 14: 87–91.

    Article  Google Scholar 

  2. 2.

    Nelson GA, Schubert WW, Kazarians GA, Richards GF. Development and chromosome mechanics in nematodes: Results from IML-1. Adv Space Res 1994; 14: 209–214.

    Article  PubMed  Google Scholar 

  3. 3.

    Lu NC, Goetsch KM. Carbohydrate requirement of chemically defined medium. Nematologica 1993; 39: 303–331.

    Google Scholar 

  4. 4.

    Szewczyk NJ, Kozak E, Conley CA. Chemically defined medium and Caenorhabditis elegans. BMC Biotechnol 2003; 3: 19.

    Article  PubMed  Google Scholar 

  5. 5.

    Steller H. Mechanisms and genes of cellular suicide. Science 1995; 267: 1445–1449.

    PubMed  Google Scholar 

  6. 6.

    Vaux DL, Korsmeyer SJ. Cell death in development. Cell 1999; 96: 245–254.

    PubMed  Google Scholar 

  7. 7.

    Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980; 284: 555–556.

    PubMed  Google Scholar 

  8. 8.

    Wyllie AH, Kerr JFR, Currie AR. Cell death: The significance of apoptosis. Internat Rev Cytol 1980; 68: 251–306.

    Google Scholar 

  9. 9.

    Sulston JE, Horvitz HR. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 1977; 56: 110–156.

    Article  PubMed  Google Scholar 

  10. 10.

    Sulstone JE, Schierenberg E, White JG, Thomson N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983; 100: 64–119.

    Article  PubMed  Google Scholar 

  11. 11.

    Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999; 126: 1011–1022.

    PubMed  Google Scholar 

  12. 12.

    Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO. A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 2000; 5: 435–443.

    Article  PubMed  Google Scholar 

  13. 13.

    Aoki H, Sato S, Takanami T, et al.. Characterization of Ce-atl-1, an ATM-like gene from Caenorhabditis elegans.Mol Gen Genet 2000; 264: 119–126.

    Article  PubMed  Google Scholar 

  14. 14.

    Boulton SJ, Gartner A, Reboul J, et al.. Combined functional genomic maps of the C. elegans DNA damage response. Science 2002; 295: 127–131.

    Article  PubMed  Google Scholar 

  15. 15.

    Ellis RE, Jacobson DM, Horvitz HR. Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 1991; 129: 79–94.

    PubMed  Google Scholar 

  16. 16.

    Wu Y, Horvitz HR. The C. elegans cell corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 1998; 93: 951–960.

    Article  PubMed  Google Scholar 

  17. 17.

    Reddien PW, Horvitz HR. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol 2000; 2: 131–136.

    Article  PubMed  Google Scholar 

  18. 18.

    Zhou Z, Hartwieg E, Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 2001; 104: 43–56.

    Article  PubMed  Google Scholar 

  19. 19.

    Stergiou L, Hengartner M. Death and more: DNA damage response pathways in the nematode C. elegans. Cell death differ 2004; 11: 21–28.

    Article  PubMed  Google Scholar 

  20. 20.

    Lewis ML, Reynolds JL, Cubano LA, Hatton JP, Lawless BD, Piepmeier EH. Spaceflight alters microtubules and increases apoptosis in human lymphocytes (Jurkat). FASEB J 1998; 12: 1007–1018.

    PubMed  Google Scholar 

  21. 21.

    Cubano LA, Lewis ML. Fas/APO-1 protein is increased in spaceflown lymphocytes (Jurkat). Exp Gerontol 2000; 35: 389–400.

    Article  PubMed  Google Scholar 

  22. 22.

    Kumei Y, Morita S, Nakamura H, et al.. Coinduction of GTP cyclohydrolase I and inducible NO synthase in rat osteoblasts during space flight: Apoptotic and self-protective response? Ann N Y Acad Sci 2003; 10: 481–485.

    Article  Google Scholar 

  23. 23.

    Schatten H, Lewis ML, Chakrabarti A. Spaceflight and clinorotation cause cytoskeleton and mitochondria changes and increases in apoptosis in cultured cells. Acta Astronaut 2001; 49: 399–418.

    Article  PubMed  Google Scholar 

  24. 24.

    Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 1993; 362: 847–849.

    Article  PubMed  Google Scholar 

  25. 25.

    Ohnishi T, Inoue N, Matsumoto H, Omatsum T, Ohira Y, Nagaoka S. Cellular content of p53 protien in rat skin after exposure to the space environment. J Appl Physiol 1996; 81: 183–185.

    PubMed  Google Scholar 

  26. 26.

    Ohnishi T, Takahashi A, Wang X, Ohnishi K, Ohira Y, Nagaoka S. Accumulation of a tumor suppressor p53 protein in rat muscle during a space flight. Mutat Res 1999; 430: 271–274.

    PubMed  Google Scholar 

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Correspondence to A. Higashitani.

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Higashitani, A., Higashibata, A., Sasagawa, Y. et al. Checkpoint and physiological apoptosis in germ cells proceeds normally in spaceflown Caenorhabditis elegans. Apoptosis 10, 949–954 (2005). https://doi.org/10.1007/s10495-005-1323-3

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Keywords

  • ced-1
  • C. elegans
  • cell corpse
  • checkpoint
  • meiosis
  • pachytene
  • spaceflight