Dihydroxy-, hydroxyspirolactone-, and dihydroxyspirolactone-urochlorins induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in the liver of mice

Chemical Research in Toxicology

Volumn 19, Issue 12, 2006, Pages 1660-1667

  Lim, Chang Kee ^a   Danton, Malcolm ^a   Clothier, Bruce ^b   Smith, Andrew G ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ACETIC ACID; CARBOXYLIC ACID DERIVATIVE; DIHYDROXYSPIROLACTONE; DIHYDROXYSPIROLACTONE UROCHLORIN DERIVATIVE; HYDROXYSPIROLACTONE; IRON; LACTONE DERIVATIVE; PROPIONIC ACID; PYRROLE DERIVATIVE; UROPORPHYRIN; UROPORPHYRINOGEN I; UROPORPHYRINOGEN III;

ANIMAL TISSUE; ARTICLE; CHEMICAL BOND; DECARBOXYLATION; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROXYLATION; ISOMER; MALE; MOUSE; NONHUMAN; OXIDATION; OXYGENATION; PORPHYRIA; PORPHYRIA CUTANEA TARDA; QUADRUPOLE MASS SPECTROMETRY; TIME OF FLIGHT MASS SPECTROMETRY;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; LIVER; MALE; MICE; MICE, INBRED C57BL; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPIRONOLACTONE; TANDEM MASS SPECTROMETRY; TETRACHLORODIBENZODIOXIN; UROPORPHYRINOGENS; UROPORPHYRINS;

EID: 33845755817     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx060212v     Document Type: Article

References (48)

1. Smith, A. G. (2003) Porphyria Caused by Chlorinated AH Receptor Ligands and Associated Mechanisms of Liver Injury and Cancer. In The Porphyrin Handbook, Medical Aspects of Porphyrins (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) Vol. 14, pp 169-210, Academic Press, San Diego, CA.
2. Egger, N. G., Goeger, D. E., Payne, D. A., Miskovsky, E. P., Weinman, S. A., and Anderson, K. E. (2002) Porphyria cutanea tarda: multiplicity of risk factors including HFE mutations, hepatitis C, and inherited uroporphyrinogen decarboxylase deficiency. Dig. Dis. Sci. 47, 419-426.
3. Elder, G. H. (2003) Porphyria Cutanea Tarda and Related Disorders. In The Porphyrin Handbook, Medical Aspects of Porphyrins (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) Vol. 14, pp 67-92, Academic Press, San Diego, CA.
4. Anderson, K. E., Sassa, S., Bishop, D. F., and Desnick R. J. (2001) Disorders of Heme Biosynthesis: X-Linked Sideroblastic Anemia and the Porphyrias. In The Metabolic and Molecular Basis of Inherited Disease, (Scriver, C. R., Sly, W. S., Valle, D., Vogelstein, B., and Childs, M. D., Eds.) 8th ed., pp 2991-3062, McGraw-Hill, New York.
5. Phillips, J. D., Jackson, L. K., Bunting, M., Franklin, M. R., Thomas, K. R., Levy, J. E., Andrews, N. C., and Kushner, J. P. (2001) A mouse model of familial porphyria cutanea tarda. Proc. Natl. Acad. Sci. U.S.A. 98, 259-264.
6. Nicholas, R. E., and Rimington, C. (1951) Isolation of unequivocal uroporphyrin III; a further study of turacin. Biochem. J. 50, 194-201.
7. Mauzerall, D., and Granick, S. (1958) Porphyrin biosynthesis in erythrocytes. III. Uroporphyrinogen and its decarboxylase. J. Biol. Chem. 232, 1141-1162.
8. Lin, W., and Timkovich, R. (1994) Oxygenated tetrapyrroles produced from porphyrinogens. Bioorg. Chem. 22, 72-94.
9. Guo, R., Lim, C. K., and De Matteis, F. (1996) Peroxylated and hydroxylated uroporphyrins: a study of their production in vitro in enzymic and chemical model systems. Biomed. Chromatogr. 10, 213-220.
10. Luo, J., and Lim, C. K. (1995) Isolation and characterization of new porphyrin metabolites in human porphyria cutanea tarda and in rats treated with hexachlorobenzene by HPTLC, HPLC and liquid secondary ion mass spectrometry. Biomed. Chromatogr. 9, 113-122.
11. Goldstein, J. A., Hickman, P., Bergman, H., and Vos, J. G. (1973) Hepatic porphyria induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in the mouse. Res. Commun. Chem. Pathol. Pharmacol. 6, 919-928.
12. Jones, K. G., and Sweeney, G. D. (1977) Association between induction of aryl hydrocarbon hydroxylase and depression of uroporphyrinogen decarboxylase activity. Res. Commun. Chem. Pathol. Pharmacol. 17, 631-637.
13. Smith, A. G., Francis, J. E., Kay, S. J., and Greig, J. B. (1981) Hepatic toxicity and uroporphyrinogen decarboxylase activity following a single dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mice. Biochem. Pharmacol. 30, 2825-2830.
14. Cantoni, L., dal Fiume, D., Ferraroli, A., Salmona, M., and Ruggieri, R. (1984) Different susceptibility of mouse tissues to porphyrogenic effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Lett. 20, 201-210.
15. Sweeney, G. D., Jones, K. G., Cole, F. M., Basford, D., and Krestynski, F. (1979) Iron deficiency prevents liver toxicity of 2,3,7,8-tetrachlorodibenzo- p-dioxin. Science 204, 332-335.
16. Jones, K. G., Cole, F. M., and Sweeney, G. D. (1981). The role of iron in the toxicity of 2,3,7,8-tetrachlorodibenzo-(p)-dioxin (TCDD). Toxicol. Appl. Pharmacol. 61, 74-88.
17. Greig, J. B., Francis, J. E., Kay, S. J., Lovell, D. P., and Smith, A. G. (1984) Incomplete correlation of 2,3,7,8-tetrachlorodibenzo-p-dioxin hepatotoxicity with Ah phenotype in mice. Toxicol. Appl. Pharmacol. 74, 17-25.
18. Smith, A. G., and Francis, J. E. (1983) Synergism of iron and hexachlorobenzene inhibits hepatic uroporphyrinogen decarboxylase in inbred mice. Biochem. J. 214, 909-913.
19. Smith, A. G., and Francis, J. E. (1993) Genetic variation of iron-induced uroporphyria in mice. Biochem. J. 291, 29-35.
20. Smith, A. G., Clothier, B., Robinson, S., Scullion, M. J., Carthew, P., Edwards, R., Luo, J., Lim, C. K., and Toledano, M. (1998) Interaction between iron metabolism and 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice with variants of the Ahr gene: a hepatic oxidative mechanism. Mol. Pharmacol. 53, 52-61.
21. Shertzer, H. G., Nebert, D. W., Puga, A., Ary, M., Sonntag, D., Dixon, K., Robinson, L. J., Cianciolo, E., and Dalton, T. P. (1998) Dioxin causes a sustained oxidative stress response in the mouse. Biochem. Biophys. Res. Commun. 253, 44-48.
22. Senft, A. P., Dalton, T. P., Nebert, D. W., Genter, M. B., Hutchinson, R. J., and Shertzer, H. G. (2002) Dioxin increases reactive oxygen production in mouse liver mitochondria. Toxicol. Appl. Pharmacol. 178, 15-21.
23. Senft, A. P., Dalton, T. P., Nebert, D. W., Genter, M. B., Puga, A., Hutchinson, R. J., Kerzee, J. K., Uno, S., and Shertzer, H. G. (2002) Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radical Biol. Med. 33, 1268-1278.
24. Lim, C. K., Rideout, J. M., and Wright, D. J. (1983) High-performance liquid chromatography of naturally occurring 8-, 7-, 6-, 5- and 4-carboxylic porphyrin isomers. J. Chromatogr. 282, 629-641.
25. Guo, R., Chai, W., Rideout, J. M., Lawson, A. M., and Lim, C. K. (1990) Isolation and characterization of beta-hydroxypropionic acid- and hydroxyacetic acid-uroporphyrin I in the urine of a patient with congenital erythropoietic porphyria by high performance liquid chromatography and liquid secondary ion mass spectrometry. Biomed. Chromatogr. 4, 141-143.
26. Danton, M., and Lim, C. K. (2006) Porphyrin profiles in blood, urine and faeces by HPLC/electrospray ionization tandem mass spectrometry. Biomed. Chromatogr. 20, 612-621.
27. Jackson, A. H., Sancovich, H. A., Ferramola, A. M., Evans, N., Games, D. E., Matlin, S. A., Elder, G. H., and Smith, S. G. (1976) Macrocyclic intermediates in the biosynthesis of porphyrins. Philos. Trans. R. Soc. London, Ser. B 273, 191-206.
28. Smith, A. G., and Francis, J. E. (1987) Chemically-induced formation of an inhibitor of hepatic uroporphyrinogen decarboxylase in inbred mice with iron overload. Biochem. J. 246, 221-226.
29. Sinclair, P. R., Gorman, N., Trask, H. W., Bement, W. J., Szakacs, J. G., Elder, G. H., Balestra, D., Sinclair, J. F., and Gerhard, G. S. (2003) Uroporphyria caused by ethanol in Hfe(-/-) mice as a model for porphyria cutanea tarda. Hepatology 37, 351-358.
30. Jackson, A. H., Sancovich, H. A., and Ferramola de Sancovich, A. M. (1980) Synthetic and biosynthetic studies of porphyrins III. Structure of the intermediates between uroporphyrinogen III and heptacarboxylic III. Synthesis of fourteen hetacarboxylic, hexacarboxylic and pentacarboxylic porphyrins related to uroporphyrin III. Bioorg. Chem. 9, 71-120.
31. Smith, A. G., and Francis, J. E. (1981) Investigations of rat liver uroporphyrinogen decarboxylase. Comparisons of porphyrinogens I and III as substrates and the inhibition by porphyrins. Biochem. J. 195, 241-250.
32. Luo, J., and Lim, C. K. (1993) Order of uroporphyrinogen III decarboxylation on incubation of porphobilinogen and uroporphyrinogen III with erythrocyte uroporphyrinogen decarboxylase. Biochem. J. 289, 529-532.
33. Francis, J. E., and Smith, A. G. (1988) Oxidation of uroporphyrinogens by hydroxyl radicals. Evidence-for nonporphyrin products as potential inhibitors of uroporphyrinogen decarboxylase. FEBS Lett. 233, 311-314.
34. Morehouse, K. M., Sipe, H. J., Jr., and Mason, R. P. (1989) The one-electron oxidation of porphyrins to porphyrin pi-cation radicals by peroxidases: an electron spin resonance investigation. Arch. Biochem. Biophys. 273, 158-164.
35. Jacobs, J. M., Jacobs, N. J., Kuhn, C. B., Gorman, N., Dayan, F. E., Duke, S. O., Sinclair, J. F., and Sinclair, P. R. (1996) Oxidation of porphyrinogens by horseradish peroxidase and formation of a green pyrrole pigment. Biochem. Biophys. Res. Commun. 227, 195-199.
36. Jacobs, N. J., Kruszyna, H. G., Hier, J. S., Dayan, F. E., Duke, S. O., Pont, F., and Montforts, F. P. (1999) Glutathione-dependent oxidative modification of protoporphyrin and other dicarboxylic porphyrins by mammalian and plant peroxidases. Biochem. Biophys. Res. Commun. 259, 195-200.
37. Shen, D., Dalton, T. P., Nebert, D. W., and Shertzer, H. G. (2005) Glutathione redox state regulates mitochondrial reactive oxygen production. J. Biol. Chem. 280, 25305-25312.
38. De Matteis, F., Harvey, C., Reed, C., and Hempenius, R. (1988) Increased oxidation of uroporphyrinogen by an inducible liver microsomal system. Possible relevance to drug-induced uroporphyria. Biochem. J. 250, 161-169.
39. Jacobs, J. M., Sinclair, P. R., Bement, W. J., Lambrecht, R. W., Sinclair, J. F., and Goldstein, J. A. (1989) Oxidation of uroporphyrinogen by methylcholanthrene-induced cytochrome P-450. Essential role of cytochrome P-450d. Biochem. J. 258, 247-253.
40. Lambrecht, R. W., Sinclair, P. R., Gorman, N., and Sinclair, J. F. (1992) Uroporphyrinogen oxidation catalyzed by reconstituted cytochrome P450IA2. Arch. Biochem. Biophys. 294, 504-510.
41. Sinclair, P. R., Gorman, N., Dalton, T., Walton, H. S., Bement, W. J., Sinclair, J. F., Smith, A. G., and Nebert, D. W. (1998) Uroporphyria produced in mice by iron and 5-aminolaevulinic acid does not occur in Cyp1a2(-/-) null mutant mice. Biochem. J. 330, 149-153.
42. Smith, A. G., Clothier, B., Carthew, P., Childs, N. L., Sinclair, P. R., Nebert, D. W., and Dalton, T. P. (2001) Protection of the Cyp1a2(-/-) null mouse against uroporphyria and hepatic injury following exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 173, 89-98.
43. Gorman, N., Walton, H. S., Bement, W. J., Honsinger, C. P., Szakacs, J. G., Sinclair, J. F., and Sinclair, P. R. (1999) Role of small differences in CYP1A2 in the development of uroporphyria produced by iron and 5-aminolevulinate in C57BL/6 and SWR slrains of mice. Biochem. Pharmacol. 58, 375-382.
44. Robinson, S. W., Clolhier, B., Akhlar, R. A., Yang, A. L., Lalour, I., Van Ijperen, C., Festing, M. F., and Smith, A. G. (2002) Non-Ahr gene susceptibility loci for porphyria and liver injury induced by the interaction of 'dioxin' with iron overload in mice. Mol. Pharmacol. 61, 674-681.
45. Cantoni, L., dal Fiume, D., Rizzardini, M., and Ruggieri, R. (1984) In vitro inhibitory effect on porphyrinogen carboxylyase of liver extracts from TCDD treated mice. Toxicol. Lett. 20, 211-217.
46. Lambrecht, R. W., Jacobs, J. M., Sinclair, P. R., and Sinclair, J. F. (1990) Inhibition of uroporphyrinogen decarboxylase activity. The role of cytochrome P-450-mediated uroporphyrinogen oxidation. Biochem. J. 269, 437-441.
47. Franklin, M. R., Phillips, J. D., and Kushner, J. P. (2005) Attenuation of polychlorinated biphenyl induced uroporphyria by iron deprivation. Environ. Toxicol. Pharmacol. 20, 417-423.
48. Smith, A. G., Francis, J. E., and Greig, J. B. (1985) Continued depression of hepatic uroporphyrinogen decarboxylase activity caused by hexachlorobenzene or 2,3,7,8-tetrachlorodibenzo-p-dioxin despite regeneration after partial hepatectomy. Biochem. Pharmacol. 34, 1817-1820.