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. 1994 Nov;60(11):3931–3938. doi: 10.1128/aem.60.11.3931-3938.1994

Metabolism of benz[a]anthracene by the filamentous fungus Cunninghamella elegans.

C E Cerniglia 1, D T Gibson 1, R H Dodge 1
PMCID: PMC201918  PMID: 7993083

Abstract

The metabolism of the carcinogen benz[a]anthracene (BA), a tetracyclic aromatic hydrocarbon, by Cunninghamella elegans was investigated. C. elegans grown on Sabouraud dextrose broth transformed [14C]BA to labeled BA trans-8,9-dihydrodiol (90%), BA trans-10,11-dihydrodiol (6%), and BA trans-3,4-dihydrodiol (4%), but not to BA trans-5,6-dihydrodiol. These metabolites were separated by thin-layer chromatography and reversed-phase high-performance liquid chromatography and were identified by UV and mass spectral techniques. A BA tetraol, 8 beta,9 alpha,10 alpha,11 beta-tetrahydroxy-8 alpha, 9 beta,10 beta,11 alpha-tetrahydro-BA, was also identified as a metabolite and may have arisen as an additional oxidation product of either BA 8,9- or 10,11-dihydrodiol. This is the first study in which a biologically produced BA tetraol has been identified. Our results suggest that the transformation of BA to trans-dihydrodiols by C. elegans is similar to the transformation of BA found in mammals, except that BA 5,6-dihydrodiol is not produced.

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Selected References

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  1. Cerniglia C. E., Campbell W. L., Freeman J. P., Evans F. E. Identification of a novel metabolite in phenanthrene metabolism by the fungus Cunninghamella elegans. Appl Environ Microbiol. 1989 Sep;55(9):2275–2279. doi: 10.1128/aem.55.9.2275-2279.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cerniglia C. E., Gibson D. T. Oxidation of benzo[a]pyrene by the filamentous fungus Cunninghamella elegans. J Biol Chem. 1979 Dec 10;254(23):12174–12180. [PubMed] [Google Scholar]
  3. Cerniglia C. E., White G. L., Heflich R. H. Fungal metabolism and detoxification of polycyclic aromatic hydrocarbons. Arch Microbiol. 1985 Nov;143(2):105–110. doi: 10.1007/BF00411031. [DOI] [PubMed] [Google Scholar]
  4. Cooper C. S., Macnicoll A. D., Ribeiro O., Gervasi P. G., Hewer A., Walsh C., Pal K., Grover P. L., Sims P. The involvement of a non-'bay-region' diol-epoxide in the metabolic activation of benza[a]anthracene in hamster embryo cells. Cancer Lett. 1980 Mar;9(1):53–59. doi: 10.1016/0304-3835(80)90140-8. [DOI] [PubMed] [Google Scholar]
  5. Gibson D. T., Mahadevan V., Jerina D. M., Yogi H., Yeh H. J. Oxidation of the carcinogens benzo [a] pyrene and benzo [a] anthracene to dihydrodiols by a bacterium. Science. 1975 Jul 25;189(4199):295–297. doi: 10.1126/science.1145203. [DOI] [PubMed] [Google Scholar]
  6. Herbes S. E., Schwall L. R. Microbial transformation of polycyclic aromatic hydrocarbons in pristine and petroleum-contaminated sediments. Appl Environ Microbiol. 1978 Feb;35(2):306–316. doi: 10.1128/aem.35.2.306-316.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Levin W., Thakker D. R., Wood A. W., Chang R. L., Lehr R. E., Jerina D. M., Conney A. H. Evidence that benzo(a)anthracene 3,4-diol-1,2-epoxide is an ultimate carcinogen on mouse skin. Cancer Res. 1978 Jun;38(6):1705–1710. [PubMed] [Google Scholar]
  8. MacNicoll A. D., Cooper C. S., Ribeiro O., Gervasi P. G., Hewer A., Walsh C., Grover P. L., Sims P. The involvement of a non-'bay-region' diol-epoxide in the formation of benz(a)anthracene-DNA adducts in a rat-liver microsomal system. Biochem Biophys Res Commun. 1979 Nov 28;91(2):490–497. doi: 10.1016/0006-291x(79)91548-1. [DOI] [PubMed] [Google Scholar]
  9. Mahaffey W. R., Gibson D. T., Cerniglia C. E. Bacterial oxidation of chemical carcinogens: formation of polycyclic aromatic acids from benz[a]anthracene. Appl Environ Microbiol. 1988 Oct;54(10):2415–2423. doi: 10.1128/aem.54.10.2415-2423.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Pothuluri J. V., Freeman J. P., Evans F. E., Cerniglia C. E. Fungal transformation of fluoranthene. Appl Environ Microbiol. 1990 Oct;56(10):2974–2983. doi: 10.1128/aem.56.10.2974-2983.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Sisler F. D., Zobell C. E. Microbial Utilization of Carcinogenic Hydrocarbons. Science. 1947 Nov 28;106(2761):521–522. doi: 10.1126/science.106.2761.521. [DOI] [PubMed] [Google Scholar]
  12. Slaga T. J., Huberman E., Selkirk J. K., Harvey R. G., Bracken W. M. Carcinogenicity and mutagenicity of benz(a)anthracene diols and diol-epoxides. Cancer Res. 1978 Jun;38(6):1699–1704. [PubMed] [Google Scholar]
  13. Sutherland J. B. Detoxification of polycyclic aromatic hydrocarbons by fungi. J Ind Microbiol. 1992 Jan;9(1):53–61. doi: 10.1007/BF01576368. [DOI] [PubMed] [Google Scholar]
  14. Swaisland A. J., Hewer A., Pal K., Keysell G. R., Booth J., Grover P. L., Sims P. Polycyclic hydrocarbon epoxides: the involvement of 8,9-dihydro-8,9-dihydroxybenz (a) anthracene 10,11-oxide in reactions with the DNA of benz (a) anthracene-treated hamster embryo cells. FEBS Lett. 1974 Oct 1;47(1):34–38. doi: 10.1016/0014-5793(74)80420-5. [DOI] [PubMed] [Google Scholar]
  15. Thakker D. R., Levin W., Yagi H., Ryan D., Thomas P. E., Karle J. M., Lehr R. E., Jerina D. M., Conney A. H. Metabolism of benzo[a]anthracene to its tumorigenic 3,4-dihydrodiol. Mol Pharmacol. 1979 Jan;15(1):138–153. [PubMed] [Google Scholar]
  16. Tierney B., Hewer A., MacNicoll A. D., Giovanni Gervasi P., Rattle H., Walsh C., Grover P. L., Sims P. The formation of dihydrodiols by the chemical or enzymic oxidation of benz[a] anthracene and 7,12-dimethylbenz[a] anthracene. Chem Biol Interact. 1978 Nov;23(2):243–257. doi: 10.1016/0009-2797(78)90010-8. [DOI] [PubMed] [Google Scholar]
  17. Wood A. W., Levin W., Chang R. L., Lehr R. E., Schaefer-Ridder M., Karle J. M., Jerina D. M., Conney A. H. Tumorigenicity of five dihydrodiols of benz(a)anthracene on mouse skin: exceptional activity of benz(a)anthracene 3,4-dihydrodiol. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3176–3179. doi: 10.1073/pnas.74.8.3176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Wood A. W., Levin W., Lu A. Y., Ryan D., West S. B., Lehr R. E., Schaefer-Ridder M., Jerina D. M., Conney A. H. Mutagenicity of metabolically activated benzo[a]anthracene 3,4-dihydrodiol: evidence for bay region activation of carcinogenic polycyclic hydrocarbons. Biochem Biophys Res Commun. 1976 Sep 20;72(2):680–686. doi: 10.1016/s0006-291x(76)80093-9. [DOI] [PubMed] [Google Scholar]
  19. Yang S. K., McCourt D. W., Gelboin H. V., Miller J. R., Roller P. P. Stereochemistry of the hydrolysis products and their acetonides of two stereoisomeric benzo[a]pyrene 7,8-diol 9,10-epoxides. J Am Chem Soc. 1977 Jul 20;99(15):5124–5130. doi: 10.1021/ja00457a036. [DOI] [PubMed] [Google Scholar]

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