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. 1990 May 25;18(10):2939–2946. doi: 10.1093/nar/18.10.2939

Tissue-specific expression, hormonal regulation and 5'-flanking gene region of the rat Clara cell 10 kDa protein: comparison to rabbit uteroglobin.

G Hagen 1, M Wolf 1, S L Katyal 1, G Singh 1, M Beato 1, G Suske 1
PMCID: PMC330822  PMID: 2349092

Abstract

The amino acid sequence of rat Clara Cell 10 kDa secretory protein (CC10) shows 55% identity to rabbit uteroglobin. In order to define the relationship between rat CC10 and rabbit uteroglobin in detail, the tissue-specific expression and hormonal regulation of rat CC10 mRNA was analyzed. We report that like rabbit uteroglobin, rat CC10 mRNA is expressed in lung and esophagus, as well as in uteri of estrogen- and progesterone-treated females. Expression of CC10 mRNA in lung is regulated by glucocorticoids. The similarity in expression pattern of rat CC10 mRNA and rabbit uteroglobin mRNA is reflected by a striking similarity in the 5'-flanking regions of the two genes. Despite this overall similarity, two regions of 0.3 kb and 2.1 kb are absent in the rat CC10 upstream gene region. The larger region includes a cluster of hormone receptor binding sites, believed to be responsible for differential regulation of rabbit uteroglobin by glucocorticoids and progesterone. Thus, while the sequence identities in the coding and 5'-flanking regions point towards a common ancestor for the uteroglobin and CC10 gene, later events (deletions/insertions) might have caused species-specific differences in their regulation.

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Selected References

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  1. Beier H. M. Uteroglobin: a hormone-sensitive endometrial protein involved in blastocyst development. Biochim Biophys Acta. 1968 Jun 26;160(2):289–291. doi: 10.1016/0005-2795(68)90108-6. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  3. Boyd M. R. Evidence for the Clara cell as a site of cytochrome P450-dependent mixed-function oxidase activity in lung. Nature. 1977 Oct 20;269(5630):713–715. doi: 10.1038/269713a0. [DOI] [PubMed] [Google Scholar]
  4. Bullock D. W. Progesterone induction of messenger RNA and protein synthesis in rabbit uterus. Ann N Y Acad Sci. 1977 Mar 11;286:260–272. doi: 10.1111/j.1749-6632.1977.tb29422.x. [DOI] [PubMed] [Google Scholar]
  5. Bullock D. W., Willen G. F. Regulation of a specific uterine protein by estrogen and progesterone in ovariectomized rabbits. Proc Soc Exp Biol Med. 1974 May;146(1):294–298. doi: 10.3181/00379727-146-38091. [DOI] [PubMed] [Google Scholar]
  6. Cato A. C., Geisse S., Wenz M., Westphal H. M., Beato M. The nucleotide sequences recognized by the glucocorticoid receptor in the rabbit uteroglobin gene region are located far upstream from the initiation of transcription. EMBO J. 1984 Dec 1;3(12):2771–2778. doi: 10.1002/j.1460-2075.1984.tb02208.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. Devereux T. R. Alveolar type II and Clara cells: isolation and xenobiotic metabolism. Environ Health Perspect. 1984 Jun;56:95–101. doi: 10.1289/ehp.845695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fernández-Renau D., Lombardero M., Nieto A. Glucocorticoid-dependent uteroglobin synthesis and uteroglobulin mRNA levels in rabbit lung explants cultured in vitro. Eur J Biochem. 1984 Nov 2;144(3):523–527. doi: 10.1111/j.1432-1033.1984.tb08497.x. [DOI] [PubMed] [Google Scholar]
  10. Fung Y. K., Lewis W. G., Crittenden L. B., Kung H. J. Activation of the cellular oncogene c-erbB by LTR insertion: molecular basis for induction of erythroblastosis by avian leukosis virus. Cell. 1983 Jun;33(2):357–368. doi: 10.1016/0092-8674(83)90417-8. [DOI] [PubMed] [Google Scholar]
  11. Georgiev G. P. Mobile genetic elements in animal cells and their biological significance. Eur J Biochem. 1984 Dec 3;145(2):203–220. doi: 10.1111/j.1432-1033.1984.tb08541.x. [DOI] [PubMed] [Google Scholar]
  12. Gillner M., Lund J., Cambillau C., Alexandersson M., Hurtig U., Bergman A., Klasson-Wehler E., Gustafsson J. A. The binding of methylsulfonyl-polychloro-biphenyls to uteroglobin. J Steroid Biochem. 1988 Jul;31(1):27–33. doi: 10.1016/0022-4731(88)90201-4. [DOI] [PubMed] [Google Scholar]
  13. Grossberger D. Minipreps of DNA from bacteriophage lambda. Nucleic Acids Res. 1987 Aug 25;15(16):6737–6737. doi: 10.1093/nar/15.16.6737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jagadeeswaran P., Forget B. G., Weissman S. M. Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts? Cell. 1981 Oct;26(2 Pt 2):141–142. doi: 10.1016/0092-8674(81)90296-8. [DOI] [PubMed] [Google Scholar]
  15. Jantzen K., Fritton H. P., Igo-Kemenes T., Espel E., Janich S., Cato A. C., Mugele K., Beato M. Partial overlapping of binding sequences for steroid hormone receptors and DNaseI hypersensitive sites in the rabbit uteroglobin gene region. Nucleic Acids Res. 1987 Jun 11;15(11):4535–4552. doi: 10.1093/nar/15.11.4535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
  17. Kay E., Feigelson M. An estrogen modulated protein in rabbit oviducal fluid. Biochim Biophys Acta. 1972 Jul 21;271(2):436–441. doi: 10.1016/0005-2795(72)90219-x. [DOI] [PubMed] [Google Scholar]
  18. Kirchner C., Schroer H. G. Uterine secretion-like proteins in the seminal plasma of the rabbit. J Reprod Fertil. 1976 Jul;47(2):325–330. doi: 10.1530/jrf.0.0470325. [DOI] [PubMed] [Google Scholar]
  19. Krayev A. S., Markusheva T. V., Kramerov D. A., Ryskov A. P., Skryabin K. G., Bayev A. A., Georgiev G. P. Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B2 sequencing. Nucleic Acids Res. 1982 Dec 11;10(23):7461–7475. doi: 10.1093/nar/10.23.7461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lund J., Nordlund L., Gustafsson J. A. Partial purification of a binding protein for polychlorinated biphenyls from rat lung cytosol: physicochemical and immunochemical characterization. Biochemistry. 1988 Oct 4;27(20):7895–7901. doi: 10.1021/bi00420a047. [DOI] [PubMed] [Google Scholar]
  21. López de Haro M. S., Alvarez L., Nieto A. Testosterone induces the expression of the uteroglobin gene in rabbit epididymis. Biochem J. 1988 Mar 15;250(3):647–651. doi: 10.1042/bj2500647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. López de Haro M. S., Nieto A. Glucocorticoids induce the expression of the uteroglobin gene in rabbit foetal lung explants cultured in vitro. Biochem J. 1985 Jan 1;225(1):255–258. doi: 10.1042/bj2250255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Menne C., Suske G., Arnemann J., Wenz M., Cato A. C., Beato M. Isolation and structure of the gene for the progesterone-inducible protein uteroglobin. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4853–4857. doi: 10.1073/pnas.79.16.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Müller H., Beato M. RNA synthesis in rabbit endometrial nuclei. Hormonal regulation of transcription of the uteroglobin gene. Eur J Biochem. 1980 Nov;112(2):235–241. doi: 10.1111/j.1432-1033.1980.tb07199.x. [DOI] [PubMed] [Google Scholar]
  25. Neel B. G., Gasic G. P., Rogler C. E., Skalka A. M., Ju G., Hishinuma F., Papas T., Astrin S. M., Hayward W. S. Molecular analysis of the c-myc locus in normal tissue and in avian leukosis virus-induced lymphomas. J Virol. 1982 Oct;44(1):158–166. doi: 10.1128/jvi.44.1.158-166.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nieto A., Lombardero M. Uteroglobin-like antigens in species of Lagomorpha. Comp Biochem Physiol B. 1982;71(3):511–514. doi: 10.1016/0305-0491(82)90417-5. [DOI] [PubMed] [Google Scholar]
  27. Nieto A., Ponstingl H., Beato M. Purification and quaternary structure of the hormonally induced protein uteroglobin. Arch Biochem Biophys. 1977 Apr 15;180(1):82–92. doi: 10.1016/0003-9861(77)90011-x. [DOI] [PubMed] [Google Scholar]
  28. Noske I. G., Feigelson M. Immunological evidence of uteroglobin (blastokinin) in the male reproductive tract and in nonreproductive ductal tissues and their secretions. Biol Reprod. 1976 Dec;15(5):704–713. doi: 10.1095/biolreprod15.5.704. [DOI] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Singh G., Katyal S. L. An immunologic study of the secretory products of rat Clara cells. J Histochem Cytochem. 1984 Jan;32(1):49–54. doi: 10.1177/32.1.6418790. [DOI] [PubMed] [Google Scholar]
  31. Singh G., Katyal S. L., Brown W. E., Phillips S., Kennedy A. L., Anthony J., Squeglia N. Amino-acid and cDNA nucleotide sequences of human Clara cell 10 kDa protein. Biochim Biophys Acta. 1988 Sep 7;950(3):329–337. doi: 10.1016/0167-4781(88)90129-7. [DOI] [PubMed] [Google Scholar]
  32. Singh G., Singal S., Katyal S. L., Brown W. E., Gottron S. A. Isolation and amino acid composition of the isotypes of a rat Clara cell specific protein. Exp Lung Res. 1987;13(3):299–309. doi: 10.3109/01902148709069595. [DOI] [PubMed] [Google Scholar]
  33. Singh G., Singh J., Katyal S. L., Brown W. E., Kramps J. A., Paradis I. L., Dauber J. H., Macpherson T. A., Squeglia N. Identification, cellular localization, isolation, and characterization of human Clara cell-specific 10 KD protein. J Histochem Cytochem. 1988 Jan;36(1):73–80. doi: 10.1177/36.1.3275712. [DOI] [PubMed] [Google Scholar]
  34. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  35. Stavenhagen J. B., Robins D. M. An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene. Cell. 1988 Oct 21;55(2):247–254. doi: 10.1016/0092-8674(88)90047-5. [DOI] [PubMed] [Google Scholar]
  36. Strähle U., Klock G., Schütz G. A DNA sequence of 15 base pairs is sufficient to mediate both glucocorticoid and progesterone induction of gene expression. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7871–7875. doi: 10.1073/pnas.84.22.7871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Suske G., Wenz M., Cato A. C., Beato M. The uteroglobin gene region: hormonal regulation, repetitive elements and complete nucleotide sequence of the gene. Nucleic Acids Res. 1983 Apr 25;11(8):2257–2271. doi: 10.1093/nar/11.8.2257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Torkkeli T., Krusius T., Jänne O. Uterine and lung uteroglobins in the rabbit. Two similar proteins with differential hormonal regulation. Biochim Biophys Acta. 1978 Dec 18;544(3):578–592. doi: 10.1016/0304-4165(78)90332-x. [DOI] [PubMed] [Google Scholar]
  39. Watanabe H., Imai T., Sharp P. A., Handa H. Identification of two transcription factors that bind to specific elements in the promoter of the adenovirus early-region 4. Mol Cell Biol. 1988 Mar;8(3):1290–1300. doi: 10.1128/mcb.8.3.1290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]

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