Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1973 Jul;70(7):2096–2100. doi: 10.1073/pnas.70.7.2096

Segregation During Ascidian Embryogenesis of Egg Cytoplasmic Information for Tissue-Specific Enzyme Development

J R Whittaker 1,2
PMCID: PMC433673  PMID: 4198663

Abstract

Cleavage-arrested embryos of the ascidian Ciona intestinalis were able to differentiate two tissue-specific enzymes—muscle acetylcholinesterase (EC 3.1.1.7) and brain pigment cell tyrosinase (EC 1.10.3.1). Cytochalasin B, colchicine, Colcemid, and podophyllotoxin were used as cleavage inhibitors at early embryonic stages up to the 64-cell stage. Only certain cells in the cleavage-arrested embryos developed these histochemically detectable enzymes, and this ability followed the cell lineage patterns for the two tissues. This result implies the presence of specific positional information in the egg cytoplasm that is differentially segregated during cleavage. There were distinct and separate puromycin and actinomycin D sensitivity periods for the occurrence of each enzyme during development of both normal and cleavage-arrested embryos. The segregated information is apparently neither the enzyme proteins nor RNA templates for enzyme synthesis, but is probably concerned with activation of appropriate genes.

Keywords: morphogenetic substances, egg localizations, cytochalasin B, acetylcholinesterase, tyrosinase

Full text

PDF
2096

Images in this article

2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097
2097Image
on p.2097

Selected References

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

  1. Borisy G. G., Taylor E. W. The mechanism of action of colchicine. Binding of colchincine-3H to cellular protein. J Cell Biol. 1967 Aug;34(2):525–533. doi: 10.1083/jcb.34.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Crippa M., Gross P. R. Maternal and embryonic contributions to the functional messenger RNA of early development. Proc Natl Acad Sci U S A. 1969 Jan;62(1):120–127. doi: 10.1073/pnas.62.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. DURANTE M. Cholinesterase in the development of Ciona intestinalis (Ascidia). Experientia. 1956 Aug 15;12(8):307–308. doi: 10.1007/BF02159626. [DOI] [PubMed] [Google Scholar]
  4. Davidson E. H., Haslett G. W., Finney R. J., Allfrey V. G., Mirsky A. E. Evidence for prelocalization of cytoplasmic factors affecting gene activation in early embryogenesis. Proc Natl Acad Sci U S A. 1965 Sep;54(3):696–704. doi: 10.1073/pnas.54.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davidson E. H. Note on the control of gene expression during development. J Theor Biol. 1971 Jul;32(1):123–130. doi: 10.1016/0022-5193(71)90140-8. [DOI] [PubMed] [Google Scholar]
  6. GURDON J. B. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J Embryol Exp Morphol. 1962 Dec;10:622–640. [PubMed] [Google Scholar]
  7. KARNOVSKY M. J., ROOTS L. A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES. J Histochem Cytochem. 1964 Mar;12:219–221. doi: 10.1177/12.3.219. [DOI] [PubMed] [Google Scholar]
  8. Lambert C. C. Genetic transcription during the development and metamorphosis of the tunicate Ascidia callosa. Exp Cell Res. 1971 Jun;66(2):401–409. doi: 10.1016/0014-4827(71)90694-x. [DOI] [PubMed] [Google Scholar]
  9. Raff R. A., Colot H. V., Selvig S. E., Gross P. R. Oogenetic origin of messenger RNA for embryonic synthesis of microtubule proteins. Nature. 1972 Jan 28;235(5335):211–214. doi: 10.1038/235211a0. [DOI] [PubMed] [Google Scholar]
  10. Raven C. P. The distribution of special cytoplasmic differentiations of the egg during early cleavage in Limnaea stagnalis. Dev Biol. 1967 Nov;16(5):407–437. doi: 10.1016/0012-1606(67)90057-7. [DOI] [PubMed] [Google Scholar]
  11. Schroeder T. E. The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z Zellforsch Mikrosk Anat. 1970;109(4):431–449. [PubMed] [Google Scholar]
  12. Scudder C. L., Karczmar A. G. Histochemical studies of cholinesterases in Ciona intestinalis. Comp Biochem Physiol. 1966 Feb;17(2):553–558. doi: 10.1016/0010-406x(66)90586-x. [DOI] [PubMed] [Google Scholar]
  13. Smith K. D. Genetic control of macromolecular synthesis during development of an ascidian: Ascidia nigra. J Exp Zool. 1967 Apr;164(3):393–405. doi: 10.1002/jez.1401640309. [DOI] [PubMed] [Google Scholar]
  14. Whittaker J. R. An analysis of melanogenesis in differentiating pigment cells of ascidian embryos. Dev Biol. 1966 Aug;14(1):1–39. doi: 10.1016/0012-1606(66)90003-0. [DOI] [PubMed] [Google Scholar]
  15. Whittaker J. R. Biosynthesis of a thouracil pheomelanin in embryonic pigment cells exposed to thouracil. J Biol Chem. 1971 Oct 25;246(20):6217–6226. [PubMed] [Google Scholar]
  16. Whittaker J. R. Tyrosinase in the presumptive pigment cells of ascidian embryos: tyrosine accessibility may initiate melanin synthesis. Dev Biol. 1973 Feb;30(2):441–454. doi: 10.1016/0012-1606(73)90101-2. [DOI] [PubMed] [Google Scholar]
  17. Wilson L. Properties of colchicine binding protein from chick embryo brain. Interactions with vinca alkaloids and podophyllotoxin. Biochemistry. 1970 Dec 8;9(25):4999–5007. doi: 10.1021/bi00827a026. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES