Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1996 Apr 1;24(7):1360–1368. doi: 10.1093/nar/24.7.1360

Positive elements in the laminin gamma 1 gene synergize to activate high level transcription during cellular differentiation.

H S Chang 1, N B Kim 1, S L Phillips 1
PMCID: PMC145770  PMID: 8614642

Abstract

Transcription of the murine laminin gamma 1 gene is activated during retinoic acid/cAMP induced differentiation of F9 embryonal carcinoma cells. Positive transcription control elements associated with two DNase I hypersensitive regions in the large first intron of the gene have been identified which confer a differentiation response on the laminin gamma 1 promoter. However, the kinetics of transcriptional activation suggest each DNA region interacts with transcription factors appearing at different times during differentiation. Synergy between the two regions in cis causes high level activation.

Full Text

The Full Text of this article is available as a PDF (151.5 KB).

Selected References

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

  1. Amasino R. M. Acceleration of nucleic acid hybridization rate by polyethylene glycol. Anal Biochem. 1986 Feb 1;152(2):304–307. doi: 10.1016/0003-2697(86)90413-6. [DOI] [PubMed] [Google Scholar]
  2. Berstine E. G., Hooper M. L., Grandchamp S., Ephrussi B. Alkaline phosphatase activity in mouse teratoma. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3899–3903. doi: 10.1073/pnas.70.12.3899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brasier A. R., Tate J. E., Habener J. F. Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines. Biotechniques. 1989 Nov-Dec;7(10):1116–1122. [PubMed] [Google Scholar]
  4. Burbelo P. D., Bruggeman L. A., Gabriel G. C., Klotman P. E., Yamada Y. Characterization of a cis-acting element required for efficient transcriptional activation of the collagen IV enhancer. J Biol Chem. 1991 Nov 25;266(33):22297–22302. [PubMed] [Google Scholar]
  5. Burbelo P. D., Horikoshi S., Yamada Y. DNA methylation and collagen IV gene expression in F9 teratocarcinoma cells. J Biol Chem. 1990 Mar 25;265(9):4839–4843. [PubMed] [Google Scholar]
  6. Burbelo P. D., Martin G. R., Yamada Y. Alpha 1(IV) and alpha 2(IV) collagen genes are regulated by a bidirectional promoter and a shared enhancer. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9679–9682. doi: 10.1073/pnas.85.24.9679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlin B. E., Durkin M. E., Bender B., Jaffe R., Chung A. E. Synthesis of laminin and entactin by F9 cells induced with retinoic acid and dibutyryl cyclic AMP. J Biol Chem. 1983 Jun 25;258(12):7729–7737. [PubMed] [Google Scholar]
  8. Chakravarti S., Hassell J. R., Phillips S. L. Perlecan gene expression precedes laminin gene expression during differentiation of F9 embryonal carcinoma cells. Dev Dyn. 1993 Jun;197(2):107–114. doi: 10.1002/aja.1001970204. [DOI] [PubMed] [Google Scholar]
  9. Chen C. A., Okayama H. Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques. 1988 Jul-Aug;6(7):632–638. [PubMed] [Google Scholar]
  10. Chomczynski P., Qasba P. K. Alkaline transfer of DNA to plastic membrane. Biochem Biophys Res Commun. 1984 Jul 18;122(1):340–344. doi: 10.1016/0006-291x(84)90480-7. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Cooper A. R., Taylor A., Hogan B. L. Changes in the rate of laminin and entactin synthesis in F9 embryonal carcinoma cells treated with retinoic acid and cyclic amp. Dev Biol. 1983 Oct;99(2):510–516. doi: 10.1016/0012-1606(83)90300-7. [DOI] [PubMed] [Google Scholar]
  13. Darrow A. L., Rickles R. J., Strickland S. Maintenance and use of F9 teratocarcinoma cells. Methods Enzymol. 1990;190:110–117. doi: 10.1016/0076-6879(90)90015-s. [DOI] [PubMed] [Google Scholar]
  14. Durkin M. E., Bartos B. B., Liu S. H., Phillips S. L., Chung A. E. Primary structure of the mouse laminin B2 chain and comparison with laminin B1. Biochemistry. 1988 Jul 12;27(14):5198–5204. doi: 10.1021/bi00414a038. [DOI] [PubMed] [Google Scholar]
  15. Durkin M. E., Phillips S. L., Chung A. E. Control of laminin synthesis during differentiation of F9 embryonal carcinoma cells. A study using cDNA clones complementary to the mRNA species for the A, B1 and B2 subunits. Differentiation. 1986;32(3):260–266. doi: 10.1111/j.1432-0436.1986.tb00582.x. [DOI] [PubMed] [Google Scholar]
  16. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  17. Grosveld F., van Assendelft G. B., Greaves D. R., Kollias G. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell. 1987 Dec 24;51(6):975–985. doi: 10.1016/0092-8674(87)90584-8. [DOI] [PubMed] [Google Scholar]
  18. Gudas L. J., Grippo J. F., Kim K. W., Larosa G. J., Stoner C. M. The regulation of the expression of genes encoding basement membrane proteins during the retinoic acid-associated differentiation of murine teratocarcinoma cells. Ann N Y Acad Sci. 1990;580:245–251. doi: 10.1111/j.1749-6632.1990.tb17933.x. [DOI] [PubMed] [Google Scholar]
  19. Hogan B. L., Cooper A. R., Kurkinen M. Incorporation into Reichert's membrane of laminin-like extracellular proteins synthesized by parietal endoderm cells of the mouse embryo. Dev Biol. 1980 Dec;80(2):289–300. doi: 10.1016/0012-1606(80)90405-4. [DOI] [PubMed] [Google Scholar]
  20. Kihara-Negishi F., Tsujita R., Negishi Y., Ariga H. BOX DNA: a novel regulatory element related to embryonal carcinoma cell differentiation. Mol Cell Biol. 1993 Dec;13(12):7747–7756. doi: 10.1128/mcb.13.12.7747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kleinman H. K., Ebihara I., Killen P. D., Sasaki M., Cannon F. B., Yamada Y., Martin G. R. Genes for basement membrane proteins are coordinately expressed in differentiating F9 cells but not in normal adult murine tissues. Dev Biol. 1987 Aug;122(2):373–378. doi: 10.1016/0012-1606(87)90302-2. [DOI] [PubMed] [Google Scholar]
  22. Liu J. K., Bergman Y., Zaret K. S. The mouse albumin promoter and a distal upstream site are simultaneously DNase I hypersensitive in liver chromatin and bind similar liver-abundant factors in vitro. Genes Dev. 1988 May;2(5):528–541. doi: 10.1101/gad.2.5.528. [DOI] [PubMed] [Google Scholar]
  23. Marotti K. R., Brown G. D., Strickland S. Two-stage hormonal control of type IV collagen mRNA levels during differentiation of F9 teratocarcinoma cells. Dev Biol. 1985 Mar;108(1):26–31. doi: 10.1016/0012-1606(85)90005-3. [DOI] [PubMed] [Google Scholar]
  24. Martinez-Hernandez A., Amenta P. S. The basement membrane in pathology. Lab Invest. 1983 Jun;48(6):656–677. [PubMed] [Google Scholar]
  25. Mason I. J., Taylor A., Williams J. G., Sage H., Hogan B. L. Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell 'culture shock' glycoprotein of Mr 43,000. EMBO J. 1986 Jul;5(7):1465–1472. doi: 10.1002/j.1460-2075.1986.tb04383.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nordeen S. K. Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques. 1988 May;6(5):454–458. [PubMed] [Google Scholar]
  27. Ogawa K., Burbelo P. D., Sasaki M., Yamada Y. The laminin B2 chain promoter contains unique repeat sequences and is active in transient transfection. J Biol Chem. 1988 Jun 15;263(17):8384–8389. [PubMed] [Google Scholar]
  28. Ruoslahti E. Integrins. J Clin Invest. 1991 Jan;87(1):1–5. doi: 10.1172/JCI114957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  30. Staudt L. M., Singh H., Sen R., Wirth T., Sharp P. A., Baltimore D. A lymphoid-specific protein binding to the octamer motif of immunoglobulin genes. Nature. 1986 Oct 16;323(6089):640–643. doi: 10.1038/323640a0. [DOI] [PubMed] [Google Scholar]
  31. Strickland S. Mouse teratocarcinoma cells: prospects for the study of embryogenesis and neoplasia. Cell. 1981 May;24(2):277–278. doi: 10.1016/0092-8674(81)90313-5. [DOI] [PubMed] [Google Scholar]
  32. Strickland S., Smith K. K., Marotti K. R. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell. 1980 Sep;21(2):347–355. doi: 10.1016/0092-8674(80)90471-7. [DOI] [PubMed] [Google Scholar]
  33. Tanaka S., Kaytes P., Kurkinen M. An enhancer for transcription of collagen IV genes is activated by F9 cell differentiation. J Biol Chem. 1993 Apr 25;268(12):8862–8870. [PubMed] [Google Scholar]
  34. Umesono K., Murakami K. K., Thompson C. C., Evans R. M. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell. 1991 Jun 28;65(7):1255–1266. doi: 10.1016/0092-8674(91)90020-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Vasios G. W., Gold J. D., Petkovich M., Chambon P., Gudas L. J. A retinoic acid-responsive element is present in the 5' flanking region of the laminin B1 gene. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9099–9103. doi: 10.1073/pnas.86.23.9099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vasios G., Mader S., Gold J. D., Leid M., Lutz Y., Gaub M. P., Chambon P., Gudas L. The late retinoic acid induction of laminin B1 gene transcription involves RAR binding to the responsive element. EMBO J. 1991 May;10(5):1149–1158. doi: 10.1002/j.1460-2075.1991.tb08055.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wang S. Y., Gudas L. J. Protein synthesis inhibitors prevent the induction of laminin B1, collagen IV (alpha 1), and other differentiation-specific mRNAs by retinoic acid in F9 teratocarcinoma cells. J Cell Physiol. 1988 Aug;136(2):305–311. doi: 10.1002/jcp.1041360213. [DOI] [PubMed] [Google Scholar]
  38. Wu C. Analysis of hypersensitive sites in chromatin. Methods Enzymol. 1989;170:269–289. doi: 10.1016/0076-6879(89)70052-5. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES