Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1998 Jul 15;333(Pt 2):309–315. doi: 10.1042/bj3330309

Developmental effect of polyamine depletion in Caenorhabditis elegans.

M MacRae 1, D L Kramer 1, P Coffino 1
PMCID: PMC1219587  PMID: 9657970

Abstract

Ornithine decarboxylase (ODC) catalyses the conversion of ornithine to putrescine, an obligate precursor to the polyamines spermidine and spermine. We reported previously that homozygous odc-1 (pc13) worms have no detectable ODC activity. Despite their inability to make polyamines, these mutant worms appear normal, but with a slight reduction in total brood size, when grown in complex medium that presumably contains polyamines. We now show that when ODC-deficient worms are transferred to polyamine-free medium, they show a strong phenotype. odc-1 worms have two different fates, depending upon the developmental stage at which polyamines are removed. If the polyamines are removed at the L1 larval stage, the mutant animals develop into adult hermaphrodites that produce very few or no eggs. In contrast, if mutant larvae at the later L4 stage of development are transferred to polyamine-deficient medium, they develop and lay eggs normally. However, approx. 90% of the eggs yield embryos that, although well differentiated, arrest at early stage 3. Either maternal or zygotic expression of ODC provides partial rescue of embryonic lethality. Supplementing deficient medium with the polyamine spermidine allows ODC-deficient worms to develop as on complex medium. Together, these findings suggest that ODC activity is most critically required during oogenesis and embryogenesis and, furthermore, that exogenous polyamines can override the requirement for ODC activity.

Full Text

The Full Text of this article is available as a PDF (280.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Argon Y., Ward S. Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics. 1980 Oct;96(2):413–433. doi: 10.1093/genetics/96.2.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Davis R. H., Morris D. R., Coffino P. Sequestered end products and enzyme regulation: the case of ornithine decarboxylase. Microbiol Rev. 1992 Jun;56(2):280–290. doi: 10.1128/mr.56.2.280-290.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Deppe U., Schierenberg E., Cole T., Krieg C., Schmitt D., Yoder B., von Ehrenstein G. Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1978 Jan;75(1):376–380. doi: 10.1073/pnas.75.1.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fozard J. R., Part M. L., Prakash N. J., Grove J. Inhibition of murine embryonic development by alpha-difluoromethylornithine, an irreversible inhibitor of ornithine decarboxylase. Eur J Pharmacol. 1980 Aug 8;65(4):379–391. doi: 10.1016/0014-2999(80)90342-8. [DOI] [PubMed] [Google Scholar]
  5. Fozard J. R., Part M. L., Prakash N. J., Grove J., Schechter P. J., Sjoerdsma A., Koch-Weser J. L-Ornithine decarboxylase:an essential role in early mammalian embryogenesis. Science. 1980 May 2;208(4443):505–508. doi: 10.1126/science.6768132. [DOI] [PubMed] [Google Scholar]
  6. Halmekytö M., Hyttinen J. M., Sinervirta R., Utriainen M., Myöhänen S., Voipio H. M., Wahlfors J., Syrjänen S., Syrjänen K., Alhonen L. Transgenic mice aberrantly expressing human ornithine decarboxylase gene. J Biol Chem. 1991 Oct 15;266(29):19746–19751. [PubMed] [Google Scholar]
  7. Kemphues K. J., Priess J. R., Morton D. G., Cheng N. S. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell. 1988 Feb 12;52(3):311–320. doi: 10.1016/s0092-8674(88)80024-2. [DOI] [PubMed] [Google Scholar]
  8. Kramer D., Mett H., Evans A., Regenass U., Diegelman P., Porter C. W. Stable amplification of the S-adenosylmethionine decarboxylase gene in Chinese hamster ovary cells. J Biol Chem. 1995 Feb 3;270(5):2124–2132. doi: 10.1074/jbc.270.5.2124. [DOI] [PubMed] [Google Scholar]
  9. Löwkvist B., Heby O., Emanuelsson H. Essential role of the polyamines in early chick embryo development. J Embryol Exp Morphol. 1980 Dec;60:83–92. [PubMed] [Google Scholar]
  10. Macrae M., Coffino P. Complementation of a polyamine-deficient Escherichia coli mutant by expression of mouse ornithine decarboxylase. Mol Cell Biol. 1987 Jan;7(1):564–567. doi: 10.1128/mcb.7.1.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Macrae M., Plasterk R. H., Coffino P. The ornithine decarboxylase gene of Caenorhabditis elegans: cloning, mapping and mutagenesis. Genetics. 1995 Jun;140(2):517–525. doi: 10.1093/genetics/140.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McConlogue L., Coffino P. Ornithine decarboxylase in difluoromethylornithine-resistant mouse lymphoma cells. Two-dimensional gel analysis of synthesis and turnover. J Biol Chem. 1983 Jul 10;258(13):8384–8388. [PubMed] [Google Scholar]
  13. Pietilä M., Alhonen L., Halmekytö M., Kanter P., Jänne J., Porter C. W. Activation of polyamine catabolism profoundly alters tissue polyamine pools and affects hair growth and female fertility in transgenic mice overexpressing spermidine/spermine N1-acetyltransferase. J Biol Chem. 1997 Jul 25;272(30):18746–18751. doi: 10.1074/jbc.272.30.18746. [DOI] [PubMed] [Google Scholar]
  14. Sarhan S., Knodgen B., Seiler N. The gastrointestinal tract as polyamine source for tumor growth. Anticancer Res. 1989 Jan-Feb;9(1):215–223. [PubMed] [Google Scholar]
  15. Steglich C., Scheffler I. E. An ornithine decarboxylase-deficient mutant of Chinese hamster ovary cells. J Biol Chem. 1982 Apr 25;257(8):4603–4609. [PubMed] [Google Scholar]
  16. Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
  17. Tabor H., Tabor C. W., Cohn M. S., Hafner E. W. Streptomycin resistance (rpsL) produces an absolute requirement for polyamines for growth of an Escherichia coli strain unable to synthesize putrescine and spermidine [delta(speA-speB) delta specC]. J Bacteriol. 1981 Aug;147(2):702–704. doi: 10.1128/jb.147.2.702-704.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ward S., Argon Y., Nelson G. A. Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol. 1981 Oct;91(1):26–44. doi: 10.1083/jcb.91.1.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ward S., Miwa J. Characterization of temperature-sensitive, fertilization-defective mutants of the nematode caenorhabditis elegans. Genetics. 1978 Feb;88(2):285–303. doi: 10.1093/genetics/88.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES