Skip to main content
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
. 1988 Dec;85(23):8988–8992. doi: 10.1073/pnas.85.23.8988

Structure and nucleotide sequence of the rat intestinal vitamin D-dependent calcium binding protein gene.

J Krisinger 1, H Darwish 1, N Maeda 1, H F DeLuca 1
PMCID: PMC282647  PMID: 3194402

Abstract

The vitamin D-dependent intestinal calcium binding protein (ICaBP, 9 kDa) is under transcriptional regulation by 1,25-dihydroxyvitamin D3 [1,25-(OH)2D3], the hormonal active form of the vitamin. To study the mechanism of gene regulation by 1,25-(OH)2D3, we isolated the rat ICaBP gene by using a cDNA probe. Its nucleotide sequence revealed 3 exons separated by 2 introns within approximately 3 kilobases. The first exon represents only noncoding sequences, while the second and third encode the two calcium binding domains of the protein. The gene contains a 15-base-pair imperfect palindrome in the first intron that shows high homology to the estrogen-responsive element. This sequence may represent the vitamin D-responsive element involved in the regulation of the ICaBP gene. The second intron shows an 84-base-pair-long simple nucleotide repeat that implicates Z-DNA formation. Genomic Southern analysis shows that the rat gene is represented as a single copy.

Full text

PDF
8988

Images in this article

Selected References

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

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baudier J., Glasser N., Strid L., Brehier A., Thomasset M., Gerard D. Purification, calcium-binding properties, and conformational studies on a 28-kDa cholecalcin-like protein from bovine brain. J Biol Chem. 1985 Sep 5;260(19):10662–10670. [PubMed] [Google Scholar]
  3. Bredderman P. J., Wasserman R. H. Chemical composition, affinity for calcium, and some related properties of the vitamin D dependent calcium-binding protein. Biochemistry. 1974 Apr 9;13(8):1687–1694. doi: 10.1021/bi00705a021. [DOI] [PubMed] [Google Scholar]
  4. Bruns M. E., Fausto A., Avioli L. V. Placental calcium binding protein in rats. Apparent identity with vitamin D-dependent calcium binding protein from rat intestine. J Biol Chem. 1978 May 10;253(9):3186–3190. [PubMed] [Google Scholar]
  5. Calabretta B., Battini R., Kaczmarek L., de Riel J. K., Baserga R. Molecular cloning of the cDNA for a growth factor-inducible gene with strong homology to S-100, a calcium-binding protein. J Biol Chem. 1986 Sep 25;261(27):12628–12632. [PubMed] [Google Scholar]
  6. Christakos S., Bruns M. E., Mehra A. S., Rhoten W. B., Van Eldik L. J. Calmodulin and rat vitamin D-dependent calcium-binding proteins: biochemical and immunochemical comparison. Arch Biochem Biophys. 1984 May 15;231(1):38–47. doi: 10.1016/0003-9861(84)90360-6. [DOI] [PubMed] [Google Scholar]
  7. Craik C. S., Choo Q. L., Swift G. H., Quinto C., MacDonald R. J., Rutter W. J. Structure of two related rat pancreatic trypsin genes. J Biol Chem. 1984 Nov 25;259(22):14255–14264. [PubMed] [Google Scholar]
  8. Darwish H. M., Krisinger J., Strom M., DeLuca H. F. Molecular cloning of the cDNA and chromosomal gene for vitamin D-dependent calcium-binding protein of rat intestine. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6108–6111. doi: 10.1073/pnas.84.17.6108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davie M. Calcium-ion-binding activity in human small-intestinal mucosal cytosol. Purification of two proteins and interrelationship of calcium-binding fractions. Biochem J. 1981 Jul 1;197(1):55–65. doi: 10.1042/bj1970055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delorme A. C., Danan J. L., Acker M. G., Ripoche M. A., Mathieu H. In rat uterus 17 beta-estradiol stimulates a calcium-binding protein similar to the duodenal vitamin D-dependent calcium-binding protein. Endocrinology. 1983 Oct;113(4):1340–1347. doi: 10.1210/endo-113-4-1340. [DOI] [PubMed] [Google Scholar]
  11. Desplan C., Heidmann O., Lillie J. W., Auffray C., Thomasset M. Sequence of rat intestinal vitamin D-dependent calcium-binding protein derived from a cDNA clone. Evolutionary implications. J Biol Chem. 1983 Nov 25;258(22):13502–13505. [PubMed] [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Emori Y., Ohno S., Tobita M., Suzuki K. Gene structure of calcium-dependent protease retains the ancestral organization of the calcium-binding protein gene. FEBS Lett. 1986 Jan 6;194(2):249–252. doi: 10.1016/0014-5793(86)80094-1. [DOI] [PubMed] [Google Scholar]
  14. Ferrari S., Calabretta B., deRiel J. K., Battini R., Ghezzo F., Lauret E., Griffin C., Emanuel B. S., Gurrieri F., Baserga R. Structural and functional analysis of a growth-regulated gene, the human calcyclin. J Biol Chem. 1987 Jun 15;262(17):8325–8332. [PubMed] [Google Scholar]
  15. Fullmer C. S., Wasserman R. H. The amino acid sequence of bovine intestinal calcium-binding protein. J Biol Chem. 1981 Jun 10;256(11):5669–5674. [PubMed] [Google Scholar]
  16. Gilbert W. Genes-in-pieces revisited. Science. 1985 May 17;228(4701):823–824. doi: 10.1126/science.4001923. [DOI] [PubMed] [Google Scholar]
  17. Gross M. D., Nelsestuen G. L., Kumar R. Observations on the binding of lanthanides and calcium to vitamin D-dependent chick intestinal calcium-binding protein. Implications regarding calcium-binding protein function. J Biol Chem. 1987 May 15;262(14):6539–6545. [PubMed] [Google Scholar]
  18. Hofmann T., Kawakami M., Hitchman A. J., Harrison J. E., Dorrington K. J. The amino acid sequence of porcine intestinal calcium-binding protein. Can J Biochem. 1979 Jun;57(6):737–748. doi: 10.1139/o79-092. [DOI] [PubMed] [Google Scholar]
  19. Hunziker W. The 28-kDa vitamin D-dependent calcium-binding protein has a six-domain structure. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7578–7582. doi: 10.1073/pnas.83.20.7578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Karasawa M., Hosoi J., Hashiba H., Nose K., Tohyama C., Abe E., Suda T., Kuroki T. Regulation of metallothionein gene expression by 1 alpha,25-dihydroxyvitamin D3 in cultured cells and in mice. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8810–8813. doi: 10.1073/pnas.84.24.8810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kessler M. A., Lamm L., Jarnagin K., DeLuca H. F. 1,25-Dihydroxyvitamin D3-stimulated mRNAs in rat small intestine. Arch Biochem Biophys. 1986 Dec;251(2):403–412. doi: 10.1016/0003-9861(86)90346-2. [DOI] [PubMed] [Google Scholar]
  22. Kretsinger R. H. Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem. 1980;8(2):119–174. doi: 10.3109/10409238009105467. [DOI] [PubMed] [Google Scholar]
  23. Leonard W. J., Strauss A. W., Go M. F., Alpers D. H., Gordon J. I. Biosynthesis and compartmentalization of rat-intestinal vitamin-D-dependent calcium-binding protein. Eur J Biochem. 1984 Mar 15;139(3):561–571. doi: 10.1111/j.1432-1033.1984.tb08042.x. [DOI] [PubMed] [Google Scholar]
  24. MacManus J. P., Watson D. C., Yaguchi M. The purification and complete amino acid sequence of the 9000-Mr Ca2+-binding protein from rat placenta. Identity with the vitamin D-dependent intestinal Ca2+-binding protein. Biochem J. 1986 Apr 15;235(2):585–595. doi: 10.1042/bj2350585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Martinez E., Givel F., Wahli W. The estrogen-responsive element as an inducible enhancer: DNA sequence requirements and conversion to a glucocorticoid-responsive element. EMBO J. 1987 Dec 1;6(12):3719–3727. doi: 10.1002/j.1460-2075.1987.tb02706.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maurer R. A., Notides A. C. Identification of an estrogen-responsive element from the 5'-flanking region of the rat prolactin gene. Mol Cell Biol. 1987 Dec;7(12):4247–4254. doi: 10.1128/mcb.7.12.4247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Maurer R. A. Selective binding of the estradiol receptor to a region at least one kilobase upstream from the rat prolactin gene. DNA. 1985 Feb;4(1):1–9. doi: 10.1089/dna.1985.4.1. [DOI] [PubMed] [Google Scholar]
  28. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. McDonnell D. P., Mangelsdorf D. J., Pike J. W., Haussler M. R., O'Malley B. W. Molecular cloning of complementary DNA encoding the avian receptor for vitamin D. Science. 1987 Mar 6;235(4793):1214–1217. doi: 10.1126/science.3029866. [DOI] [PubMed] [Google Scholar]
  30. Moore D. D., Marks A. R., Buckley D. I., Kapler G., Payvar F., Goodman H. M. The first intron of the human growth hormone gene contains a binding site for glucocorticoid receptor. Proc Natl Acad Sci U S A. 1985 Feb;82(3):699–702. doi: 10.1073/pnas.82.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pansini A. R., Christakos S. Cell-free translational analysis of messenger ribonucleic acid coding for vitamin D-dependent rat renal calcium-binding protein. Endocrinology. 1985 Oct;117(4):1652–1660. doi: 10.1210/endo-117-4-1652. [DOI] [PubMed] [Google Scholar]
  32. Perret C., Lomri N., Gouhier N., Auffray C., Thomasset M. The rat vitamin-D-dependent calcium-binding protein (9-kDa CaBP) gene. Complete nucleotide sequence and structural organization. Eur J Biochem. 1988 Feb 15;172(1):43–51. doi: 10.1111/j.1432-1033.1988.tb13853.x. [DOI] [PubMed] [Google Scholar]
  33. Petropoulos C. J., Yaswen P., Panzica M., Fausto N. Methylation of the alphafetoprotein gene in cell populations isolated from rat livers during carcinogenesis. Nucleic Acids Res. 1985 Nov 25;13(22):8105–8118. doi: 10.1093/nar/13.22.8105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Prince C. W., Butler W. T. 1,25-Dihydroxyvitamin D3 regulates the biosynthesis of osteopontin, a bone-derived cell attachment protein, in clonal osteoblast-like osteosarcoma cells. Coll Relat Res. 1987 Sep;7(4):305–313. doi: 10.1016/s0174-173x(87)80036-5. [DOI] [PubMed] [Google Scholar]
  35. Rowe D. W., Kream B. E. Regulation of collagen synthesis in fetal rat calvaria by 1,25-dihydroxyvitamin D3. J Biol Chem. 1982 Jul 25;257(14):8009–8015. [PubMed] [Google Scholar]
  36. Scheidereit C., Westphal H. M., Carlson C., Bosshard H., Beato M. Molecular model of the interaction between the glucocorticoid receptor and the regulatory elements of inducible genes. DNA. 1986 Oct;5(5):383–391. doi: 10.1089/dna.1986.5.383. [DOI] [PubMed] [Google Scholar]
  37. Sharp P. A. Speculations on RNA splicing. Cell. 1981 Mar;23(3):643–646. doi: 10.1016/0092-8674(81)90425-6. [DOI] [PubMed] [Google Scholar]
  38. Silver J., Russell J., Sherwood L. M. Regulation by vitamin D metabolites of messenger ribonucleic acid for preproparathyroid hormone in isolated bovine parathyroid cells. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4270–4273. doi: 10.1073/pnas.82.12.4270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Simmen R. C., Tanaka T., Ts'ui K. F., Putkey J. A., Scott M. J., Lai E. C., Means A. R. The structural organization of the chicken calmodulin gene. J Biol Chem. 1985 Jan 25;260(2):907–912. [PubMed] [Google Scholar]
  40. Simpson R. U., Hsu T., Begley D. A., Mitchell B. S., Alizadeh B. N. Transcriptional regulation of the c-myc protooncogene by 1,25-dihydroxyvitamin D3 in HL-60 promyelocytic leukemia cells. J Biol Chem. 1987 Mar 25;262(9):4104–4108. [PubMed] [Google Scholar]
  41. Sogawa K., Gotoh O., Kawajiri K., Fujii-Kuriyama Y. Distinct organization of methylcholanthrene- and phenobarbital-inducible cytochrome P-450 genes in the rat. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5066–5070. doi: 10.1073/pnas.81.16.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Suda T., DeLuca H. F., Tanaka Y. Biological activity of 25-hydroxyergocalciferol in rats. J Nutr. 1970 Sep;100(9):1049–1052. doi: 10.1093/jn/100.9.1049. [DOI] [PubMed] [Google Scholar]
  43. Szebenyi D. M., Obendorf S. K., Moffat K. Structure of vitamin D-dependent calcium-binding protein from bovine intestine. Nature. 1981 Nov 26;294(5839):327–332. doi: 10.1038/294327a0. [DOI] [PubMed] [Google Scholar]
  44. Takagi T., Nojiri M., Konishi K., Maruyama K., Nonomura Y. Amino acid sequence of vitamin D-dependent calcium-binding protein from bovine cerebellum. FEBS Lett. 1986 May 26;201(1):41–45. doi: 10.1016/0014-5793(86)80567-1. [DOI] [PubMed] [Google Scholar]
  45. Thomasset M., Cuisinier-Gleizes P., Mathieu H., DeLuca H. F. Intestinal calcium-binding protein (CaBP) and bone calcium mobilization in response to 1,24(R),25-(OH)3D3. Comparative effects of 1,25-(OH)2D3 and 24(R),25-(OH)2D3 in rats. Mol Pharmacol. 1980 May;17(3):362–366. [PubMed] [Google Scholar]
  46. Thomasset M., Parkes C. O., Cuisinier-Gleizes P. Rat calcium-binding proteins: distribution, development, and vitamin D dependence. Am J Physiol. 1982 Dec;243(6):E483–E488. doi: 10.1152/ajpendo.1982.243.6.E483. [DOI] [PubMed] [Google Scholar]
  47. Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G., Rich A. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature. 1979 Dec 13;282(5740):680–686. doi: 10.1038/282680a0. [DOI] [PubMed] [Google Scholar]
  48. Wasserman R. H., Fullmer C. S. Calcium transport proteins, calcium absorption, and vitamin D. Annu Rev Physiol. 1983;45:375–390. doi: 10.1146/annurev.ph.45.030183.002111. [DOI] [PubMed] [Google Scholar]
  49. Yamamoto K. R., Alberts B. M. Steroid receptors: elements for modulation of eukaryotic transcription. Annu Rev Biochem. 1976;45:721–746. doi: 10.1146/annurev.bi.45.070176.003445. [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