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. 1989 Jul;9(7):3132–3135. doi: 10.1128/mcb.9.7.3132

Developmental regulation of hypomethylation of delta-crystallin genes in chicken embryo lens cells.

C H Sullivan 1, J T Norman 1, T Borrás 1, R M Grainger 1
PMCID: PMC362788  PMID: 2779557

Abstract

Sequences in the two delta-crystallin genes become hypomethylated when they are expressed in the chick lens. This system is particularly advantageous for studying temporal changes in hypomethylation, since lens tissue can be isolated at all developmental stages. In previous work we have shown that most HpaII sites become hypomethylated within the delta 1-crystallin gene long after delta-crystallin gene activation. One site is hypomethylated when crystallin mRNA begins to be synthesized at high levels at 50 h; we show here that this site maps to the 3' end (intron 15) of the delta 1-crystallin gene. In addition, we have examined the methylation status of HpaII and HhaI sites found near the 5' end of the delta 1-crystallin gene. Two HhaI sites adjacent to a viral core enhancer sequence in intron 2 are also first hypomethylated at 50 h. These findings point to regions of the delta 1 gene that should be investigated further for functional significance in regulating delta-crystallin transcription.

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Selected References

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

  1. Agata K., Yasuda K., Okada T. S. Gene coding for a lens-specific protein, delta-crystallin, is transcribed in nonlens tissues of chicken embryos. Dev Biol. 1983 Nov;100(1):222–226. doi: 10.1016/0012-1606(83)90214-2. [DOI] [PubMed] [Google Scholar]
  2. Bird A. P., Southern E. M. Use of restriction enzymes to study eukaryotic DNA methylation: I. The methylation pattern in ribosomal DNA from Xenopus laevis. J Mol Biol. 1978 Jan 5;118(1):27–47. doi: 10.1016/0022-2836(78)90242-5. [DOI] [PubMed] [Google Scholar]
  3. Borrás T., Nickerson J. M., Chepelinsky A. B., Piatigorsky J. Structural and functional evidence for differential promoter activity of the two linked delta-crystallin genes in the chicken. EMBO J. 1985 Feb;4(2):445–452. doi: 10.1002/j.1460-2075.1985.tb03649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Borrás T., Peterson C. A., Piatigorsky J. Evidence for positive and negative regulation in the promoter of the chicken delta 1-crystallin gene. Dev Biol. 1988 May;127(1):209–219. doi: 10.1016/0012-1606(88)90202-3. [DOI] [PubMed] [Google Scholar]
  5. Choi O. R., Engel J. D. A 3' enhancer is required for temporal and tissue-specific transcriptional activation of the chicken adult beta-globin gene. Nature. 1986 Oct 23;323(6090):731–734. doi: 10.1038/323731a0. [DOI] [PubMed] [Google Scholar]
  6. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Errington L. H., Cooper D. N., Clayton R. M. The pattern of DNA methylation in the delta-crystallin genes in transdifferentiating neural retina cultures. Differentiation. 1983;24(1):33–38. doi: 10.1111/j.1432-0436.1983.tb01299.x. [DOI] [PubMed] [Google Scholar]
  8. Grainger R. M., Hazard-Leonards R. M., Samaha F., Hougan L. M., Lesk M. R., Thomsen G. H. Is hypomethylation linked to activation of delta-crystallin genes during lens development? Nature. 1983 Nov 3;306(5938):88–91. doi: 10.1038/306088a0. [DOI] [PubMed] [Google Scholar]
  9. Hayashi S., Goto K., Okada T. S., Kondoh H. Lens-specific enhancer in the third intron regulates expression of the chicken delta 1-crystallin gene. Genes Dev. 1987 Oct;1(8):818–828. doi: 10.1101/gad.1.8.818. [DOI] [PubMed] [Google Scholar]
  10. Jones R. E., DeFeo D., Piatigorsky J. Transcription and site-specific hypomethylation of the delta-crystallin genes in the embryonic chicken lens. J Biol Chem. 1981 Aug 10;256(15):8172–8176. [PubMed] [Google Scholar]
  11. Kelley D. E., Pollok B. A., Atchison M. L., Perry R. P. The coupling between enhancer activity and hypomethylation of kappa immunoglobulin genes is developmentally regulated. Mol Cell Biol. 1988 Feb;8(2):930–937. doi: 10.1128/mcb.8.2.930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Nickerson J. M., Wawrousek E. F., Borras T., Hawkins J. W., Norman B. L., Filpula D. R., Nagle J. W., Ally A. H., Piatigorsky J. Sequence of the chicken delta 2 crystallin gene and its intergenic spacer. Extreme homology with the delta 1 crystallin gene. J Biol Chem. 1986 Jan 15;261(2):552–557. [PubMed] [Google Scholar]
  13. Nickerson J. M., Wawrousek E. F., Hawkins J. W., Wakil A. S., Wistow G. J., Thomas G., Norman B. L., Piatigorsky J. The complete sequence of the chicken delta 1 crystallin gene and its 5' flanking region. J Biol Chem. 1985 Aug 5;260(16):9100–9105. [PubMed] [Google Scholar]
  14. O'RAHILLY R., MEYER D. B. The early development of the eye in the chick Gallus domesticus (stages 8 to 25). Acta Anat (Basel) 1959;36(1-2):20–58. doi: 10.1159/000141425. [DOI] [PubMed] [Google Scholar]
  15. Ohno M., Sakamoto H., Yasuda K., Okada T. S., Shimura Y. Nucleotide sequence of a chicken delta-crystallin gene. Nucleic Acids Res. 1985 Mar 11;13(5):1593–1606. doi: 10.1093/nar/13.5.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Parker D. S., Wawrousek E. F., Piatigorsky J. Expression of the delta-crystallin genes in the embryonic chicken lens. Dev Biol. 1988 Apr;126(2):375–381. doi: 10.1016/0012-1606(88)90147-9. [DOI] [PubMed] [Google Scholar]
  17. Piatigorsky J. Delta crystallins and their nucleic acids. Mol Cell Biochem. 1984;59(1-2):33–56. doi: 10.1007/BF00231304. [DOI] [PubMed] [Google Scholar]
  18. Piatigorsky J., O'Brien W. E., Norman B. L., Kalumuck K., Wistow G. J., Borras T., Nickerson J. M., Wawrousek E. F. Gene sharing by delta-crystallin and argininosuccinate lyase. Proc Natl Acad Sci U S A. 1988 May;85(10):3479–3483. doi: 10.1073/pnas.85.10.3479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shinohara T., Piatigorsky J. Quantitation of delta-crystallin messenger RNA during lens induction in chick embryos. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2808–2812. doi: 10.1073/pnas.73.8.2808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sullivan C. H., Grainger R. M. Delta-crystallin genes become hypomethylated in postmitotic lens cells during chicken development. Proc Natl Acad Sci U S A. 1987 Jan;84(2):329–333. doi: 10.1073/pnas.84.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Trainor C. D., Stamler S. J., Engel J. D. Erythroid-specific transcription of the chicken histone H5 gene is directed by a 3' enhancer. 1987 Aug 27-Sep 2Nature. 328(6133):827–830. doi: 10.1038/328827a0. [DOI] [PubMed] [Google Scholar]
  22. Wawrousek E. F., Nickerson J. M., Piatigorsky J. Two delta-crystallin polypeptides are derived from a cloned delta 1-crystallin cDNA. FEBS Lett. 1986 Sep 15;205(2):235–240. doi: 10.1016/0014-5793(86)80904-8. [DOI] [PubMed] [Google Scholar]
  23. Weiher H., König M., Gruss P. Multiple point mutations affecting the simian virus 40 enhancer. Science. 1983 Feb 11;219(4585):626–631. doi: 10.1126/science.6297005. [DOI] [PubMed] [Google Scholar]
  24. Wistow G., Piatigorsky J. Recruitment of enzymes as lens structural proteins. Science. 1987 Jun 19;236(4808):1554–1556. doi: 10.1126/science.3589669. [DOI] [PubMed] [Google Scholar]

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