Peroxidatic Activation of Procarcinogens: A Role for Prostaglandin H Synthase in Initiation of Chemical Carcinogenesis

  • Terry V. Zenser
  • Bernard B. Davis
Chapter
Part of the Prostaglandins, Leukotrienes, and Cancer book series (PLAC, volume 1)

Abstract

Chemical carcinogenes is is thought to be initiated by the enzymatic generation of reactive electrophi1ic intermediates. Enzymatic activation of procarcinogens to carcinogens by the mixed-function oxidase system has been clearly documented to be involved in the initiation of cancer by certain chemicals (1, 2). However, due to the apparent lack of metabolism of certain procarcinogens by mixed-function oxidases and/or negligible enzyme activity in certain tissues, additional pathways for enzymatic activation of procarcinogens have been investigated.

Keywords

Chemical Carcinogenesis Eosinophil Peroxidase Epoxy Alcohol Sulindac Sulfide Medullary Slice 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Gelboin HV: Benzo [a]pyrene metabolism, activation, and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev (60): 1107–1166, 1980.PubMedGoogle Scholar
  2. 2.
    Conney AH: Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G.H.A. Clowes memorial lecture. Cancer Res (42): 4875–4917, 1982.PubMedGoogle Scholar
  3. 3.
    Saunders BC, Holmes-Siedle AG, Stark BP: Peroxidase. Butterworths, Washington, 1964.Google Scholar
  4. 4.
    Yamazaki I: Peroxidase. In: Hayaishi O (ed) Molecular mechanism of oxygen activation. Academic Press, New York, 1974, pp 535–555.Google Scholar
  5. 5.
    Morrison M, Schonbaum GR: Peroxidase-catalyzed halogenation. Annu Rev Biochem (45): 861–888, 1976.PubMedCrossRefGoogle Scholar
  6. 6.
    Wise RW, Zenser TV, Davis BB: Prostaglandin H synthase metabolism of the urinary bladder carcinogens benzidine and ANFT. Carcinogenesis (4): 285–289, 1983.PubMedCrossRefGoogle Scholar
  7. 7.
    Zenser TV, Mattammal MB, Armbrecht HJ, Davis BB: Benzidine binding to nucleic acids mediated by the peroxidative activity of prostaglandin endoperoxide synthetase. Cancer Res (40): 2839–2845, 1980.PubMedGoogle Scholar
  8. 8.
    Rapp NS, Zenser TV, Brown WW, Davis BB: Metabolism of benzidine by a prostaglandin-mediated process in renal inner medullary slices. J Pharmacol Exp Ther (215): 401–406, 1980.PubMedGoogle Scholar
  9. 9.
    Bolscher BGJM, Plat H, Wever R. Some properties of human eosinophil peroxidase, a comparison with other peroxidases. Biochim Biophys Acta (784): 177–186, 1984.PubMedCrossRefGoogle Scholar
  10. 10.
    Olsen RL, Little C: Purification and some properties of myeloperoxidase and eosinophil peroxidase from human blood. Biochem J (209): 781–787, 1983.PubMedGoogle Scholar
  11. 11.
    Saunders BC: Peroxidases and catalases. In: Eichhorn GL (ed) Inorganic biochemistry. Elsevier Science Publishers, New York, 1973, pp 988–1021.Google Scholar
  12. 12.
    Wagai N, Hosoya T: Partial purification of estrogen-dependent peroxidase of rat uterus and comparison of the properties with those of other animal peroxidases. J Biochem (91): 1931–1942, 1982.PubMedGoogle Scholar
  13. 13.
    Olsen RL, Little C: The peroxidase activity of rat uterus. Eur J Biochem (101): 333–339, 1979.PubMedCrossRefGoogle Scholar
  14. 14.
    Chance B: The spectra of the enzyme-substrate complexes of catalase and peroxidase. Arch Biochem Biophys (41): 404–415, 1952.PubMedCrossRefGoogle Scholar
  15. 15.
    Chance B: The kinetics and stoichiometry of the transition from the primary to the secondary peroxidase peroxide complexes. Arch Biochem Biophys (41): 416–424, 1952.PubMedCrossRefGoogle Scholar
  16. 16.
    George P: The chemical nature of the second hydrogen peroxide compound formed by cytochrome c peroxidase and horseradish peroxidase. Biochem J (54): 267–276, 1953.PubMedGoogle Scholar
  17. 17.
    George P: Chemical nature of the secondary hydrogen peroxide compound formed by cytochrome c peroxidase and horseradish peroxidase. Nature (169): 612–613, 1952.PubMedCrossRefGoogle Scholar
  18. 18.
    Dolphin D: The electronic configurations of catalases and peroxidases in their high oxidation states: a definitive assessment. Israel J Chem (21): 67–71, 1981.Google Scholar
  19. 19.
    Rombauts WA, Schroeder WA, Morrison M: Bovine lactoperoxidase. Partial characterization of the further purified protein. Biochemistry (6): 2965–2977, 1967.PubMedCrossRefGoogle Scholar
  20. 20.
    Olsen RL, Little C: Comparative studies on oestrogen-induced rat uterus peroxidase and rat eosinophil peroxidase. Biochem J (207): 613–616, 1982.PubMedGoogle Scholar
  21. 21.
    Ohki S, Ogino N, Yamamoto S, Hayaishi O: Prostaglandin hydroperoxidase, an integral part of prostaglandin endoperoxide synthetase from bovine vesicular gland microsomes. J Biol Chem (254): 829–836, 1979.PubMedGoogle Scholar
  22. 22.
    Marnett LJ, Eling TE: Cooxidation during prostaglandin biosynthesis: a pathway for the metabolic activation of xenobiotics. In: Hodgson E, Bend JB, Philpot RM (eds) Reviews in biochemical toxicology. Elsevier Science Publishers, New York, 1983, pp 135–172.Google Scholar
  23. 23.
    Eling T, Boyd J, Reed G, Mason R, Sivarajah K: Xenobiotic metabolism by prostaglandin endoperoxide synthetase. Drug Metab Rev (14): 1023–1053, 1983.PubMedCrossRefGoogle Scholar
  24. 24.
    Gale PH, Egan RW: Prostaglandin endoperoxide synthase catalyzed oxidation reactions. In: Pryor WA (ed) Free radicals in biology, vol VI. Academic Press, Orlando, Florida, 1984, pp 1–38.Google Scholar
  25. 25.
    Roth GJ, Siok CJ, Ozols J: Structural characteristics of prostaglandin synthetase from sheep vesicular gland. J Biol Chem (255): 1301–1304, 1980.PubMedGoogle Scholar
  26. 26.
    Zenser TV, Mattammal MB, Davis BB: Mechanism of FANFT cooxidation by prostaglandin endoperoxide synthetase. J Pharmacol Exp Ther (214): 312–317, 1980.PubMedGoogle Scholar
  27. 27.
    Hemler M, Lands WEM, Smith WL: Purification of the cyclooxygenase that forms prostaglandins. Demonstration of two forms of iron in the holoenzyme. J Biol Chem (251): 5575–5579, 1976.PubMedGoogle Scholar
  28. 28.
    Ho PPK, Towner RD, Esterman MA: Purification and characterization of fatty acid cyclooxygenase from human platelets. Prep Biochem (10): 597–613, 1980.PubMedCrossRefGoogle Scholar
  29. 29.
    Ueno R, Shimizu T, Kondo K, Hayaishi O: Activation mechanism of prostaglandin endoperoxide synthetase by hemoproteins. J Biol Chem (257): 5584–5588, 1982.PubMedGoogle Scholar
  30. 30.
    Poulos TL, Kraut J: The stereochemistry of peroxidase catalysis. J Biol Chem (255): 8199–8205, 1980.PubMedGoogle Scholar
  31. 31.
    Chance B, Sies H, Boveris A: Hydroperoxide metabolism in mammalian organs. Physiol Rev (59): 527–605, 1979.PubMedGoogle Scholar
  32. 32.
    Klebs VE: Die pyrogene Substanz. Zentralblatt fur die Medicinischen Wissenschaften (6): 417–418, 1863.Google Scholar
  33. 33.
    Linossier MG: Contribution a Letude des ferments oxydants. Sur La Peroxydase dupus. Comptes Rendus Hebdomadaires des Seances et Memoires de la Societe de Biologie (50): 373–375, 1898.Google Scholar
  34. 34.
    Dougherty HW, Hen A, Kuehl FA Jr: The role of polymorphonuclear peroxidase-dependent oxidants in inflammation. Agents Actions (7): 167–173, 1980.Google Scholar
  35. 35.
    Egan RW, Gale PH, Baptista EM, Kennicott KL, VandenHeuvel WJA, Walker RW, Fagerness PE, Kuehl FA Jr: Oxidation reactions by prostaglandin cyclooxygenase-hydroperoxidase. J Biol Chem (256): 7352–7361, 1981.PubMedGoogle Scholar
  36. 36.
    Hsu IC, Harris CC, Yamaguchi M: Induction of ouabain-resistant mutation and sister chromatid exchanges in Chinese hamster cells with chemical carcinogens mediated by human pulmonary macrophages. J Clin Invest (64): 1245–1252, 1979.PubMedCrossRefGoogle Scholar
  37. 37.
    Marnett LJ, Johnson JT, Bienkowski MJ: Arachidonic acid-dependent metabolism of 7, 8-dihydroxy-7,8-dihydrobenzo [a]pyrene by ram seminal vesicles. FEBS Lett (106): 13–16, 1979.PubMedCrossRefGoogle Scholar
  38. 38.
    Reed GA, Marnett LJ: Metabolism and activation of 7, 8-dihydrobenzo [a]pyrene during prostaglandin biosynthesis. J Biol Chem (257): 11368–11376, 1982.PubMedGoogle Scholar
  39. 39.
    Sivarajah K, Lasker JM, Eling TE: Prostaglandin synthetase-dependent cooxidation of (+)-benzo [a]-pyrene-7, 8-dihydrodiol by human lung and other mammalian tissues. Cancer Res (41): 1834–1839, 1981.PubMedGoogle Scholar
  40. 40.
    Metzler M, McLachlan JA: Peroxidase-medi ated oxidation, a possible pathway for metabolic activation of diethylstilbestrol. Biochem Biophys Res Comnun (85): 874–884, 1978.CrossRefGoogle Scholar
  41. 41.
    Degen GH, Eling TE, McLachlan JA: Oxidative metabolism of diethylstilbestrol by prostaglandin synthetase. Cancer Res (42): 919–923, 1982.PubMedGoogle Scholar
  42. 42.
    Ham EA, Cirillo VJ, Zanetti ME, Kuehl FA Jr: Estrogen-directed synthesis of specific prostaglandins in uterus. Proc Natl Acad Sci USA (72): 1420–1424, 1975.PubMedCrossRefGoogle Scholar
  43. 43.
    Harper HA, Rodwell VW, Mayes PA: Review of physiological chemistry. Lange Medical Publications, Los Altos, California, 1969, p 201–203.Google Scholar
  44. 44.
    Eyer P: The red cell as a sensitive target for activated toxic arylamines. Arch Toxicol Suppl (6): 3–12, 1983.PubMedGoogle Scholar
  45. 45.
    Golly I, Hlavica P: The role of hemoglobin in the N-oxidation of 4-chloroani 1 ine. Biochim Biophys Acta (760): 69–76, 1983.PubMedGoogle Scholar
  46. 46.
    Pace-Asciak CR, Mizuno K, Yamamoto S: Resolution by DEAE-cel1ulose chromatography of the enzymatic steps in the transformation of arachidonic acid into 8,11,12- and 10, 11, 12-trihydroxy-eicosatrienoic acid by the rat lung. Prostaglandins (25): 79–84, 1983.PubMedCrossRefGoogle Scholar
  47. 47.
    Dix TA, Marnett LJ: Hematin-catalyzed rearrangement of hydroperoxyl inoleic acid to epoxy alcohols via an oxygen rebound. J Am Chem Soc (105): 7001–7002, 1983.CrossRefGoogle Scholar
  48. 48.
    Dix TA, Marnett LJ: Free radical epoxidation of 7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene by hematin and polyunsaturated fatty acid hydroperoxides. J Am Chem Soc (103): 6744–6746, 1981.CrossRefGoogle Scholar
  49. 49.
    Zenser TV, Mattammal MB, Brown WW, Davis BB: Cooxygenation by prostaglandin cyclooxygenase from rabbit inner medulla. Kidney Int (16): 688–694, 1979.PubMedCrossRefGoogle Scholar
  50. 50.
    Degen GH, Wong A, Eling TE, Barrett JC, McLachlan JA: Involvement of prostaglandin synthetase in the peroxidative metabolism of diethylstil best rol in Syrian hamster embryo fibroblast cell cultures. Cancer Res (43): 992–996, 1983.PubMedGoogle Scholar
  51. 51.
    Sivarajah K, Jones KG, Fouts JR, Devereux T, Shirley JE, Eling TE: Prostaglandin synthetase and cytochrome P-450-dependent metabolism of (±)benzo(a)pyrene 7,8-dihydrodiol by enriched populations of rat clara cells and alveolar type II cells. Cancer Res (43): 2632–2636, 1983.PubMedGoogle Scholar
  52. 52.
    Wise RW, Zenser TV, Davis BB: Peroxidase metabolism of the urinary bladder carcinogen 2-amino-4-(5-nitro-2-furyl)thiazole. Cancer Res (43): 1518–1522, 1983.PubMedGoogle Scholar
  53. 53.
    Zenser TV, Mattamnal MB, Davis BB: Cooxidation of benzidine by renal medullary prostaglandin cyclooxygenase. J Pharmacol Exp Ther (211): 460–464, 1979.PubMedGoogle Scholar
  54. 54.
    Ziegler DM, Poulsen LL: Hepatic microsomal mixed-function amine oxidase. In: Fleischer S, Packer L (eds) Methods in enzymology, vol LII Biomembranes, Part C: Biological oxidations microsomal, cytochrome P-450, and other hemoprotein systems. Academic Press, New York, 1978, pp 142–151.Google Scholar
  55. 55.
    Wise RW, Zenser TV, Davis BB: Oxidation of the carcinogen benzidine to free radical cations may initiate the carcinogenic process. Fed Proc (43): 589 (abstract), 1984.Google Scholar
  56. 56.
    Pagels WR, Sachs RJ, Marnett LJ, Dewitt DL, Day JS, Smith WL: Inmunochemical evidence for the involvement of prostaglandin H synthase in hydroperoxide-dependent oxidations by ram seminal vesicle microsomes. J Biol Chem (258): 6517–6523, 1983.PubMedGoogle Scholar
  57. 57.
    Klemencic JM, Wang CY: Mutagenicity of nitrofurans. In: Bryan GT (ed) Carcinogenesis, a comprehensive survey. Raven Press, New York, 1978, pp 99–130.Google Scholar
  58. 58.
    Mattammal MB, Zenser TV, Davis BB: Prostaglandin hydroperoxidase-mediated 2-amino-4-(5-nitro-2-furyl)-14C-thiazole metabolism and nucleic acid binding. Cancer Res (41): 4961–4966, 1981.PubMedGoogle Scholar
  59. 59.
    Rice JR, Zenser TV, Davis BB: Structural characterization of thioether conjugates of 2-amino-4-(5-nitro-2-furyl)thiazole catalyzed by prostaglandin H synthase. Fed Proc (43): 346 (abstract), 1984.Google Scholar
  60. 60.
    Cohen SM, Zenser TV, Murasaki G, Fukushima S, Mattammal MB, Rapp NS, Davis BB: Aspirin inhibition of N-[4-(5-ni tro-2-furyl)-2-thiazolyl]formamide-induced lesions of the urinary bladder correlated with inhibition of metabolism by bladder prostaglandin endoperoxide synthetase. Cancer Res (41): 3355–3359, 1981.PubMedGoogle Scholar
  61. 61.
    Murasaki G, Zenser TV, Davis BB, Cohen SM: Inhibition by aspirin of N-[4-(5-nitro-2-furyl)-2-thiazolyl]-formamide induced bladder carcinogenesis and enhancement of forestomach carcinogenesis. Carcinogenesis (5): 53–55, 1984.PubMedCrossRefGoogle Scholar
  62. 62.
    Fischer SM, Slaga TJ: Modulation of prostaglandin synthesis and tumor promotion. In: Powles TJ, Bockman RS, Honn KV, Ramwell P (eds) Prostaglandins and cancer: first international conference. Alan R Liss Inc, New York, 1982, pp 255–264.Google Scholar
  63. 63.
    Zenser TV, Mattammal MB, Wise RW, Rice JR, Davis BB: Prostaglandin H synthase-catalyzed activation of benzidine: a model to assess pharmacologic intervention of the initiation of chemical carcinogenesis. J Pharmacol Exp Ther (227): 545–550, 1983.PubMedGoogle Scholar
  64. 64.
    Miller JA: Carcinogenesis by chemicals: an overview-G.H.A. Clowes memorial lecture. Cancer Res (30): 559–576, 1970.PubMedGoogle Scholar
  65. 65.
    Marnett LJ, Siedlik PH, Fung LWM: Oxidation of phenidone and BW755C by prostaglandin endoperoxide synthetase. J Biol Chem (257): 6957–6964, 1982.PubMedGoogle Scholar
  66. 66.
    Gilman AG, Murad F: Thyroid and antithyroid drugs. In: Goodman LS, Gilman A (eds) The pharmacological basis of therapeutics. MacMillan Publishing Co, New York, 1975, pp 1398–1422.Google Scholar
  67. 67.
    Zelman SJ, Rapp NS, Zenser TV, Mattammal MB, Davis BB: Antithyroid drugs interact with renal medullary prostaglandin H synthase. J Lab Clin Med (104): 185–192, 1984.PubMedGoogle Scholar

Copyright information

© Martinus Nijhoff Publishing, Boston 1985

Authors and Affiliations

  • Terry V. Zenser
  • Bernard B. Davis

There are no affiliations available

Personalised recommendations