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. 1995 Feb 15;306(Pt 1):225–234. doi: 10.1042/bj3060225

Tissue- and cell-specific expression of mouse xanthine oxidoreductase gene in vivo: regulation by bacterial lipopolysaccharide.

M Kurosaki 1, M Li Calzi 1, E Scanziani 1, E Garattini 1, M Terao 1
PMCID: PMC1136505  PMID: 7864814

Abstract

The expression of the xanthine oxidoreductase gene was studied in various mouse organs and tissues, under basal conditions and on treatment with bacterial lipopolysaccharide. Levels of xanthine oxidoreductase protein and mRNA were compared in order to understand the molecular mechanisms regulating the expression of this enzyme system. The highest amounts of xanthine oxidoreductase and the respective mRNA are observed in the duodenum and jejunum, where the protein is present in an unusual form because of a specific proteolytic cleavage of the primary translation product present in all locations. Under basal conditions, multiple tissue-specific mechanisms of xanthine oxidoreductase regulation are evident. Lipopolysaccharide increases enzyme activity in some, but not all tissues, mainly via modulation of the respective transcript, although translational and post-translational mechanisms are also active. In situ hybridization studies on tissue sections obtained from mice under control conditions or with lipopolysaccharide treatment demonstrate that xanthine oxidoreductase is present in hepatocytes, predominantly in the proximal tubules of the kidney, epithelial layer of the gastrointestinal mucosa, the alveolar compartment of the lung, the pulpar region of the spleen and the vascular component of the heart.

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  1. Akaike T., Ando M., Oda T., Doi T., Ijiri S., Araki S., Maeda H. Dependence on O2- generation by xanthine oxidase of pathogenesis of influenza virus infection in mice. J Clin Invest. 1990 Mar;85(3):739–745. doi: 10.1172/JCI114499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amaya Y., Yamazaki K., Sato M., Noda K., Nishino T., Nishino T. Proteolytic conversion of xanthine dehydrogenase from the NAD-dependent type to the O2-dependent type. Amino acid sequence of rat liver xanthine dehydrogenase and identification of the cleavage sites of the enzyme protein during irreversible conversion by trypsin. J Biol Chem. 1990 Aug 25;265(24):14170–14175. [PubMed] [Google Scholar]
  3. Brigham K. L., Meyrick B., Berry L. C., Jr, Repine J. E. Antioxidants protect cultured bovine lung endothelial cells from injury by endotoxin. J Appl Physiol (1985) 1987 Aug;63(2):840–850. doi: 10.1152/jappl.1987.63.2.840. [DOI] [PubMed] [Google Scholar]
  4. Carpani G., Racchi M., Ghezzi P., Terao M., Garattini E. Purification and characterization of mouse liver xanthine oxidase. Arch Biochem Biophys. 1990 Jun;279(2):237–241. doi: 10.1016/0003-9861(90)90487-j. [DOI] [PubMed] [Google Scholar]
  5. Cazzaniga G., Terao M., Lo Schiavo P., Galbiati F., Segalla F., Seldin M. F., Garattini E. Chromosomal mapping, isolation, and characterization of the mouse xanthine dehydrogenase gene. Genomics. 1994 Sep 15;23(2):390–402. doi: 10.1006/geno.1994.1515. [DOI] [PubMed] [Google Scholar]
  6. Corte E. D., Stirpe F. The regulation of rat liver xanthine oxidase. Involvement of thiol groups in the conversion of the enzyme activity from dehydrogenase (type D) into oxidase (type O) and purification of the enzyme. Biochem J. 1972 Feb;126(3):739–745. doi: 10.1042/bj1260739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duke E. J., Joyce P., Ryan J. P. Characterization of alternative molecular forms of xanthine oxidase in the mouse. Biochem J. 1973 Feb;131(2):187–190. doi: 10.1042/bj1310187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dupont G. P., Huecksteadt T. P., Marshall B. C., Ryan U. S., Michael J. R., Hoidal J. R. Regulation of xanthine dehydrogenase and xanthine oxidase activity and gene expression in cultured rat pulmonary endothelial cells. J Clin Invest. 1992 Jan;89(1):197–202. doi: 10.1172/JCI115563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Falciani F., Ghezzi P., Terao M., Cazzaniga G., Garattini E. Interferons induce xanthine dehydrogenase gene expression in L929 cells. Biochem J. 1992 Aug 1;285(Pt 3):1001–1008. doi: 10.1042/bj2851001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Falciani F., Terao M., Goldwurm S., Ronchi A., Gatti A., Minoia C., Li Calzi M., Salmona M., Cazzaniga G., Garattini E. Molybdenum(VI) salts convert the xanthine oxidoreductase apoprotein into the active enzyme in mouse L929 fibroblastic cells. Biochem J. 1994 Feb 15;298(Pt 1):69–77. doi: 10.1042/bj2980069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frederiks W. M., Marx F. A histochemical procedure for light microscopic demonstration of xanthine oxidase activity in unfixed cryostat sections using cerium ions and a semipermeable membrane technique. J Histochem Cytochem. 1993 May;41(5):667–670. doi: 10.1177/41.5.8468447. [DOI] [PubMed] [Google Scholar]
  12. Fridovich I. Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. J Biol Chem. 1970 Aug 25;245(16):4053–4057. [PubMed] [Google Scholar]
  13. Ghezzi P., Bianchi M., Mantovani A., Spreafico F., Salmona M. Enhanced xanthine oxidase activity in mice treated with interferon and interferon inducers. Biochem Biophys Res Commun. 1984 Feb 29;119(1):144–149. doi: 10.1016/0006-291x(84)91630-9. [DOI] [PubMed] [Google Scholar]
  14. Ibrahim B., Stoward P. J. The histochemical localization of xanthine oxidase. Histochem J. 1978 Sep;10(5):615–617. doi: 10.1007/BF01003142. [DOI] [PubMed] [Google Scholar]
  15. Jarasch E. D., Grund C., Bruder G., Heid H. W., Keenan T. W., Franke W. W. Localization of xanthine oxidase in mammary-gland epithelium and capillary endothelium. Cell. 1981 Jul;25(1):67–82. doi: 10.1016/0092-8674(81)90232-4. [DOI] [PubMed] [Google Scholar]
  16. Kooij A., Frederiks W. M., Gossrau R., Van Noorden C. J. Localization of xanthine oxidoreductase activity using the tissue protectant polyvinyl alcohol and final electron acceptor Tetranitro BT. J Histochem Cytochem. 1991 Jan;39(1):87–93. doi: 10.1177/39.1.1983876. [DOI] [PubMed] [Google Scholar]
  17. McCord J. M. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985 Jan 17;312(3):159–163. doi: 10.1056/NEJM198501173120305. [DOI] [PubMed] [Google Scholar]
  18. Meyuhas O., Perry R. P. Construction and identification of cDNA clones for mouse ribosomal proteins: application for the study of r-protein gene expression. Gene. 1980 Jul;10(2):113–129. doi: 10.1016/0378-1119(80)90129-8. [DOI] [PubMed] [Google Scholar]
  19. Mohamedali K. A., Guicherit O. M., Kellems R. E., Rudolph F. B. The highest levels of purine catabolic enzymes in mice are present in the proximal small intestine. J Biol Chem. 1993 Nov 5;268(31):23728–23733. [PubMed] [Google Scholar]
  20. Parks D. A., Granger D. N. Ischemia-induced vascular changes: role of xanthine oxidase and hydroxyl radicals. Am J Physiol. 1983 Aug;245(2):G285–G289. doi: 10.1152/ajpgi.1983.245.2.G285. [DOI] [PubMed] [Google Scholar]
  21. Rajagopalan K. V., Handler P. Purification and properties of chicken liver xanthine dehydrogenase. J Biol Chem. 1967 Sep 25;242(18):4097–4107. [PubMed] [Google Scholar]
  22. Reiners J. J., Jr, Pence B. C., Barcus M. C., Cantu A. R. 12-O-tetradecanoylphorbol-13-acetate-dependent induction of xanthine dehydrogenase and conversion to xanthine oxidase in murine epidermis. Cancer Res. 1987 Apr 1;47(7):1775–1779. [PubMed] [Google Scholar]
  23. Suzuki M., Grisham M. B., Granger D. N. Leukocyte-endothelial cell adhesive interactions: role of xanthine oxidase-derived oxidants. J Leukoc Biol. 1991 Nov;50(5):488–494. doi: 10.1002/jlb.50.5.488. [DOI] [PubMed] [Google Scholar]
  24. Terao J., Matsushita S. Quinone formation from benzo[a]pyrene by free radicals: effects of antioxidants. Free Radic Biol Med. 1988;4(4):205–208. doi: 10.1016/0891-5849(88)90040-8. [DOI] [PubMed] [Google Scholar]
  25. Terao M., Cazzaniga G., Ghezzi P., Bianchi M., Falciani F., Perani P., Garattini E. Molecular cloning of a cDNA coding for mouse liver xanthine dehydrogenase. Regulation of its transcript by interferons in vivo. Biochem J. 1992 May 1;283(Pt 3):863–870. doi: 10.1042/bj2830863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wallace J. L., Steel G., Whittle B. J., Lagente V., Vargaftig B. Evidence for platelet-activating factor as a mediator of endotoxin-induced gastrointestinal damage in the rat. Effects of three platelet-activating factor antagonists. Gastroenterology. 1987 Oct;93(4):765–773. doi: 10.1016/0016-5085(87)90438-0. [DOI] [PubMed] [Google Scholar]
  27. Wohlrab F., Seidler E. Zur Histochemie der Xanthin-Dehydrogenase. Acta Histochem. 1978;62(1):120–132. [PubMed] [Google Scholar]
  28. de Groot H., Littauer A. Reoxygenation injury in isolated hepatocytes: cell death precedes conversion of xanthine dehydrogenase to xanthine oxidase. Biochem Biophys Res Commun. 1988 Aug 30;155(1):278–282. doi: 10.1016/s0006-291x(88)81080-5. [DOI] [PubMed] [Google Scholar]

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