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. 1991 Mar 15;274(Pt 3):673–678. doi: 10.1042/bj2740673

Retinoic acid induces liver/bone/kidney-type alkaline phosphatase gene expression in F9 teratocarcinoma cells.

M Gianni 1, M Studer 1, G Carpani 1, M Terao 1, E Garattini 1
PMCID: PMC1149964  PMID: 1849403

Abstract

All-trans retinoic acid (RA) induces alkaline phosphatase (ALP) activity by 3-8-fold in murine F9 teratocarcinoma cells, in parallel with their differentiation towards primitive endoderm. The elevation of ALP activity is associated with increases in the amounts of liver/bone/kidney-type ALP protein and the respective transcript. These effects of RA are due to activation of ALP gene transcription rather than to an increase in the half-life of the mRNA. Induction of ALP mRNA does not require de novo protein synthesis, since it is not blocked by treatment with cycloheximide. Dibutyryl cyclic AMP, which is known to induce further differentiation of F9 cells from the primitive to the parietal endoderm, blocks the induction of ALP mRNA by RA.

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Selected References

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  1. Beato M. Gene regulation by steroid hormones. Cell. 1989 Feb 10;56(3):335–344. doi: 10.1016/0092-8674(89)90237-7. [DOI] [PubMed] [Google Scholar]
  2. Benbrook D., Lernhardt E., Pfahl M. A new retinoic acid receptor identified from a hepatocellular carcinoma. Nature. 1988 Jun 16;333(6174):669–672. doi: 10.1038/333669a0. [DOI] [PubMed] [Google Scholar]
  3. Berger J., Garattini E., Hua J. C., Udenfriend S. Cloning and sequencing of human intestinal alkaline phosphatase cDNA. Proc Natl Acad Sci U S A. 1987 Feb;84(3):695–698. doi: 10.1073/pnas.84.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Borregaard N., Miller L. J., Springer T. A. Chemoattractant-regulated mobilization of a novel intracellular compartment in human neutrophils. Science. 1987 Sep 4;237(4819):1204–1206. doi: 10.1126/science.3629236. [DOI] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  6. Brand N., Petkovich M., Krust A., Chambon P., de Thé H., Marchio A., Tiollais P., Dejean A. Identification of a second human retinoic acid receptor. Nature. 1988 Apr 28;332(6167):850–853. doi: 10.1038/332850a0. [DOI] [PubMed] [Google Scholar]
  7. Brown N. A., Stofko R. E., Uhler M. D. Induction of alkaline phosphatase in mouse L cells by overexpression of the catalytic subunit of cAMP-dependent protein kinase. J Biol Chem. 1990 Aug 5;265(22):13181–13189. [PubMed] [Google Scholar]
  8. CHIQUOINE A. D. The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec. 1954 Feb;118(2):135–146. doi: 10.1002/ar.1091180202. [DOI] [PubMed] [Google Scholar]
  9. Cope F. O., Wille J. J. Retinoid receptor antisense DNAs inhibit alkaline phosphatase induction and clonogenicity in malignant keratinocytes. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5590–5594. doi: 10.1073/pnas.86.14.5590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erickson L. A., Lawrence D. A., Loskutoff D. J. Reverse fibrin autography: a method to detect and partially characterize protease inhibitors after sodium dodecyl sulfate--polyacrylamide gel electrophoresis. Anal Biochem. 1984 Mar;137(2):454–463. doi: 10.1016/0003-2697(84)90113-1. [DOI] [PubMed] [Google Scholar]
  11. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 1988 May 13;240(4854):889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Garattini E., Hua J. C., Pan Y. C., Udenfriend S. Human liver alkaline phosphatase, purification and partial sequencing: homology with the placental isozyme. Arch Biochem Biophys. 1986 Mar;245(2):331–337. doi: 10.1016/0003-9861(86)90223-7. [DOI] [PubMed] [Google Scholar]
  14. Garattini E., Hua J. C., Udenfriend S. Cloning and sequencing of bovine kidney alkaline phosphatase cDNA. Gene. 1987;59(1):41–46. doi: 10.1016/0378-1119(87)90264-2. [DOI] [PubMed] [Google Scholar]
  15. Goldstein D. J., Rogers C. E., Harris H. Expression of alkaline phosphatase loci in mammalian tissues. Proc Natl Acad Sci U S A. 1980 May;77(5):2857–2860. doi: 10.1073/pnas.77.5.2857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  17. Hahnel A. C., Schultz G. A. Cloning and characterization of a cDNA encoding alkaline phosphatase in mouse embryonal carcinoma cells. Clin Chim Acta. 1990 Jan 15;186(2):171–174. doi: 10.1016/0009-8981(90)90034-p. [DOI] [PubMed] [Google Scholar]
  18. Hatch C. L., Bonner W. M. Sequence of cDNAs for mammalian H2A.Z, an evolutionarily diverged but highly conserved basal histone H2A isoprotein species. Nucleic Acids Res. 1988 Feb 11;16(3):1113–1124. doi: 10.1093/nar/16.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hogan B. L., Taylor A., Adamson E. Cell interactions modulate embryonal carcinoma cell differentiation into parietal or visceral endoderm. Nature. 1981 May 21;291(5812):235–237. doi: 10.1038/291235a0. [DOI] [PubMed] [Google Scholar]
  20. Hu L., Gudas L. J. Cyclic AMP analogs and retinoic acid influence the expression of retinoic acid receptor alpha, beta, and gamma mRNAs in F9 teratocarcinoma cells. Mol Cell Biol. 1990 Jan;10(1):391–396. doi: 10.1128/mcb.10.1.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kam W., Clauser E., Kim Y. S., Kan Y. W., Rutter W. J. Cloning, sequencing, and chromosomal localization of human term placental alkaline phosphatase cDNA. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8715–8719. doi: 10.1073/pnas.82.24.8715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Krust A., Kastner P., Petkovich M., Zelent A., Chambon P. A third human retinoic acid receptor, hRAR-gamma. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5310–5314. doi: 10.1073/pnas.86.14.5310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MINTZ B., RUSSELL E. S. Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool. 1957 Mar;134(2):207–237. doi: 10.1002/jez.1401340202. [DOI] [PubMed] [Google Scholar]
  24. Martin C. A., Ziegler L. M., Napoli J. L. Retinoic acid, dibutyryl-cAMP, and differentiation affect the expression of retinoic acid receptors in F9 cells. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4804–4808. doi: 10.1073/pnas.87.12.4804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Martin G. R. Teratocarcinomas and mammalian embryogenesis. Science. 1980 Aug 15;209(4458):768–776. doi: 10.1126/science.6250214. [DOI] [PubMed] [Google Scholar]
  26. Minty A. J., Caravatti M., Robert B., Cohen A., Daubas P., Weydert A., Gros F., Buckingham M. E. Mouse actin messenger RNAs. Construction and characterization of a recombinant plasmid molecule containing a complementary DNA transcript of mouse alpha-actin mRNA. J Biol Chem. 1981 Jan 25;256(2):1008–1014. [PubMed] [Google Scholar]
  27. Misumi Y., Tashiro K., Hattori M., Sakaki Y., Ikehara Y. Primary structure of rat liver alkaline phosphatase deduced from its cDNA. Biochem J. 1988 Feb 1;249(3):661–668. doi: 10.1042/bj2490661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Petkovich M., Brand N. J., Krust A., Chambon P. A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature. 1987 Dec 3;330(6147):444–450. doi: 10.1038/330444a0. [DOI] [PubMed] [Google Scholar]
  29. Rambaldi A., Terao M., Bettoni S., Tini M. L., Bassan R., Barbui T., Garattini E. Expression of leukocyte alkaline phosphatase gene in normal and leukemic cells: regulation of the transcript by granulocyte colony-stimulating factor. Blood. 1990 Dec 15;76(12):2565–2571. [PubMed] [Google Scholar]
  30. Rambaldi A., Young D. C., Griffin J. D. Expression of the M-CSF (CSF-1) gene by human monocytes. Blood. 1987 May;69(5):1409–1413. [PubMed] [Google Scholar]
  31. Seiler-Tuyns A., Birnstiel M. L. Structure and expression in L-cells of a cloned H4 histone gene of the mouse. J Mol Biol. 1981 Oct 5;151(4):607–625. doi: 10.1016/0022-2836(81)90426-5. [DOI] [PubMed] [Google Scholar]
  32. Stoner C. M., Gudas L. J. Mouse cellular retinoic acid binding protein: cloning, complementary DNA sequence, and messenger RNA expression during the retinoic acid-induced differentiation of F9 wild type and RA-3-10 mutant teratocarcinoma cells. Cancer Res. 1989 Mar 15;49(6):1497–1504. [PubMed] [Google Scholar]
  33. Strickland S., Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell. 1978 Oct;15(2):393–403. doi: 10.1016/0092-8674(78)90008-9. [DOI] [PubMed] [Google Scholar]
  34. Strickland S., Sawey M. J. Studies on the effect of retinoids on the differentiation of teratocarcinoma stem cells in vitro and in vivo. Dev Biol. 1980 Jul;78(1):76–85. doi: 10.1016/0012-1606(80)90319-x. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Sucov H. M., Murakami K. K., Evans R. M. Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5392–5396. doi: 10.1073/pnas.87.14.5392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tanaka Y., Tsuyuki M., Itaya-Hironaka A., Inada Y., Yoshihara K., Kamiya T. Retinoic acid-induced differentiation-specific, C-kinase-dependent phosphorylation of cytosolic 44 and 32 kDa proteins in HL-60 cells. Biochem Biophys Res Commun. 1990 May 16;168(3):1253–1260. doi: 10.1016/0006-291x(90)91163-m. [DOI] [PubMed] [Google Scholar]
  38. Terao M., Mintz B. Cloning and characterization of a cDNA coding for mouse placental alkaline phosphatase. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7051–7055. doi: 10.1073/pnas.84.20.7051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Terao M., Studer M., Gianní M., Garattini E. Isolation and characterization of the mouse liver/bone/kidney-type alkaline phosphatase gene. Biochem J. 1990 Jun 15;268(3):641–648. doi: 10.1042/bj2680641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Thaller C., Eichele G. Identification and spatial distribution of retinoids in the developing chick limb bud. Nature. 1987 Jun 18;327(6123):625–628. doi: 10.1038/327625a0. [DOI] [PubMed] [Google Scholar]
  41. Wang S. Y., Gudas L. J. Isolation of cDNA clones specific for collagen IV and laminin from mouse teratocarcinoma cells. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5880–5884. doi: 10.1073/pnas.80.19.5880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang S. Y., LaRosa G. J., Gudas L. J. Molecular cloning of gene sequences transcriptionally regulated by retinoic acid and dibutyryl cyclic AMP in cultured mouse teratocarcinoma cells. Dev Biol. 1985 Jan;107(1):75–86. doi: 10.1016/0012-1606(85)90377-x. [DOI] [PubMed] [Google Scholar]
  43. Weiss M. J., Henthorn P. S., Lafferty M. A., Slaughter C., Raducha M., Harris H. Isolation and characterization of a cDNA encoding a human liver/bone/kidney-type alkaline phosphatase. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7182–7186. doi: 10.1073/pnas.83.19.7182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wilcox F. H. Genetics of alkaline phosphatase of the small intestine of the house mouser (Mus musculus). Biochem Genet. 1983 Aug;21(7-8):641–652. doi: 10.1007/BF00498912. [DOI] [PubMed] [Google Scholar]
  45. Wu R. S., Tsai S., Bonner W. M. Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell. 1982 Dec;31(2 Pt 1):367–374. doi: 10.1016/0092-8674(82)90130-1. [DOI] [PubMed] [Google Scholar]
  46. Zackson S. L., Steinberg M. S. A molecular marker for cell guidance information in the axolotl embryo. Dev Biol. 1988 Jun;127(2):435–442. doi: 10.1016/0012-1606(88)90329-6. [DOI] [PubMed] [Google Scholar]
  47. de Thé H., Marchio A., Tiollais P., Dejean A. A novel steroid thyroid hormone receptor-related gene inappropriately expressed in human hepatocellular carcinoma. Nature. 1987 Dec 17;330(6149):667–670. doi: 10.1038/330667a0. [DOI] [PubMed] [Google Scholar]

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