Comparative hepatic activity of xenobiotic-metabolizing enzymes and concentrations of organohalogens and their hydroxylated analogues in captive greenland sledge dogs (Canis familiaris)

Environmental Toxicology and Chemistry

Volumn 28, Issue 1, 2009, Pages 162-172

  Verreault, Jonathan ^a   Maisonneuve, France ^a   Dietz, Rune ^b   Sonne, Christian ^b   Letcher, Robert J ^a  

^a CARLETON UNIVERSITY   (Canada)

^b NATIONAL ENVIRONMENTAL RESEARCH INSTITUTE   (Denmark)

Author keywords

Arctic; Biotransformation enzymes; Hydroxylated metabolites; Organohalogens; Sledge dog

Indexed keywords

BIOTRANSFORMATION ENZYMES; CATALYTIC ACTIVITY; CONTAMINATED DIET; CONTROL GROUPS; CYTOCHROME P450; EPOXIDE HYDROLASES; EROD ACTIVITY; ETHOXYRESORUFIN-O-DEETHYLASE; GREENLAND; HYDROXYLASES; HYDROXYLATED METABOLITES; MICROSOMAL ENZYMES; MINKE WHALES; ORGANOHALOGENS; PCB CONCENTRATION; PCB CONGENERS; PHASE I; PLASMA CONCENTRATION; POLYBROMINATED DIPHENYL ETHERS; PREDICTIVE POWER; SLEDGE DOG; TESTOSTERONE HYDROXYLATION; XENOBIOTIC-METABOLIZING ENZYMES;

BIOMOLECULES; CATALYSTS; CONCENTRATION (PROCESS); ECOLOGY; ELECTRIC CIRCUIT BREAKERS; ENZYME ACTIVITY; ENZYMES; ETHERS; HYDROXYLATION; METABOLISM; METABOLITES; NUTRITION; ORGANIC POLLUTANTS; PLASMAS; POLYCHLORINATED BIPHENYLS; PRINTED CIRCUITS;

CHEMICAL CONTAMINATION;

16BETA HYDROXYTESTOSTERONE; 6BETA HYDROXYTESTOSTERONE; ANDROSTENEDIONE; EPOXIDE HYDROLASE; ETHOXYRESORUFIN DEETHYLASE; MICROSOME ENZYME; ORGANOHALOGEN DERIVATIVE; POLYBROMINATED DIPHENYL ETHER; POLYCHLORINATED BIPHENYL; TESTOSTERONE; TESTOSTERONE DERIVATIVE; TESTOSTERONE HYDROXYLASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHOGLUCURONOSYL TRANSFERASE; CYTOCHROME P450 1A1; GLUCURONOSYLTRANSFERASE; HALOGEN; MIXED FUNCTION OXIDASE; ORGANIC COMPOUND; XENOBIOTIC AGENT;

BLOOD; CANID; CAPTIVE POPULATION; COMPARATIVE STUDY; CYTOCHROME; ENZYME ACTIVITY; METABOLISM; ORGANOHALOGEN; POLLUTION EXPOSURE; TESTOSTERONE; XENOBIOTICS;

ANIMAL EXPERIMENT; ARTICLE; BIOTRANSFORMATION; BLOOD LEVEL; CANIS FAMILIARIS; CONTROLLED STUDY; DOG; ENZYME ACTIVITY; HYDROXYLATION; LIVER MICROSOME METABOLISM; NONHUMAN; PREDICTION; PRIORITY JOURNAL; ANIMAL; COMPARATIVE STUDY; ENZYMOLOGY; FEMALE; GREENLAND; LIVER MICROSOME; METABOLISM;

BALAENOPTERA ACUTOROSTRATA; CANIS FAMILIARIS;

ANIMALS; CYTOCHROME P-450 CYP1A1; DOGS; EPOXIDE HYDROLASES; FEMALE; GLUCURONOSYLTRANSFERASE; GREENLAND; HALOGENS; HYDROXYLATION; MICROSOMES, LIVER; MIXED FUNCTION OXYGENASES; ORGANIC CHEMICALS; XENOBIOTICS;

EID: 65449171688     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1897/08-176.1     Document Type: Article

References (65)

1. Hakk H, Letcher RJ. 2003. Metabolism in the toxicokinetics and fate of brominated flame retardants - A review. Environ Int 29: 801-828.
2. Kawano M, Hasegawa J, Enomoto T, Onishi H, Nishio Y, Matsuda M, Wakimoto T. 2005. Hydroxylated polychlorinated biphenyls (OH-PCBs): Recent advances in wildlife contamination study. Environ Sci 12:315-324.
3. Letcher RJ, Klasson-Wehler E, Bergman Å. 2000. Methyl sulfone and hydroxylated metabolites of polychlorinated biphenyls. In Paasivita J, ed, The Handbook of Environmental Chemistry - New Types of Persistent Halogenated Compounds, Vol 3, Part K. Springer-Verlag, Heidelberg, Germany, pp 315-359.
4. Teuten EL, Xu L, Reddy CM. 2005. Two abundant bioaccumulated halogenated compounds are natural products. Science 307: 917-920.
5. Tampal N, Lehmler HJ, Espandiari P, Malmberg T, Robertson LW. 2002. Glucuronidation of hydroxylated polychlorinated biphenyls (PCBs). Chem Res Toxicol 15:1259-1266.
6. Houde M, Pacepavicius G, Wells RS, Fair PA, Letcher RJ, Alaee M, Bossart GD, Hohn AA, Sweeney J, Solomon KR, Muir DCG. 2006. Polychlorinated biphenyls and hydroxylated polychlorinated biphenyls in plasma of bottlenose dolphins (Tursiops truncatus) from the western Atlantic and the Gulf of Mexico. Environ Sci Technol 40:5860-5866.
7. McKinney MA, Martineau D, Dallaire AD, Béland P, De Guise S, LeBeuf M, Letcher RJ. 2006. Organohalogen contaminants and metabolites in the liver of beluga whales (Delphinapterus leucas) from two Canadian populations. Environ Toxicol Chem 25:1246-1257.
8. Verreault J, Gabrielsen GW, Chu S, Muir DCG, Andersen M, Hamaed A, Letcher RJ. 2005. Flame retardants and methoxylated and hydroxylated polybrominated diphenyl ethers in two Norwegian Arctic top predators: Glaucous gulls and polar bears. Environ Sci Technol 39:6021-6028.
9. Gebbink WA, Sonne C, Dietz R, Kirkegaard M, Born EW, Muir DCG, Letcher RJ. 2008. Target tissue selectivity and burdens of diverse classes of brominated and chlorinated contaminants in polar bears (Ursus maritimus) from East Greenland. Environ Sci Technol 152:621-629.
10. Sonne C, Dietz R, Larsen HJ, Loft KE, Kirkegaard M, Letcher RJ, Shahmiri S, Moller P. 2006. Impairment of cellular immunity in west Greenland sledge dogs (Canis familiaris) dietary exposed to polluted minke whale (Balaenoptera acutorostrata) blubber. Environ Sci Technol 40:2056-2062.
11. Sonne C, Leifsson PS, Dietz R, Kirkegaard M, Møller P, Jensen AJ, Letcher RJ, Shahmiri S. 2007. Renal lesions in Greenland sledge dogs (Canis familiaris) exposed to a natural dietary cocktail of persistent organic pollutants. Toxicol Environ Chem 89: 563-576.
12. Sonne C, Fonfara S, Dietz R, Kirkegaard M, Letcher RJ, Shahmiri S, Andersen S, Moller P. 2007. Multiple cytokine and acute-phase protein gene transcription in West Greenland sledge dogs (Canis familiaris) dietary exposed to organic environmental pollutants. Arch Environ Contam Toxicol 53:110-118.
13. Sonne C, Dietz R, Kirkegaard M, Letcher RJ, Shahmiri S, Andersen S, Moller P, Olsen AK, Jensen AL. 2008. Effects of organohalogen pollutants on hematological and urine clinical-chemical parameters in Greenland sledge dogs (Canis familiaris). Ecotoxicol Environ Saf 69:381-390.
14. Sonne C, Leifsson PS, Dietz R, Kirkegaard M, Møller P, Jensen AL, Letcher RJ. 2008. Greenland sledge dogs (Canis familiaris) develop liver lesions when exposed to a chronic and dietary low dose of an environmental organohalogen cocktail. Environ Res 106:72-80.
15. Verreault J, Dietz R, Sonne C, Gebbink WA, Shahmiri S, Letcher RJ. 2008. Comparative fate of organohalogen contaminants in two top carnivores in Greenland: Captive sledge dogs and wild polar bears. Comp Biochem Physiol C Toxicol Pharmacol 147: 306-315.
16. Verreault J, Sonne C, Dietz R, Letcher RJ. 2008. Dietary, age, and trans-generational effects on the fate of organohalogen contaminants in captive sledge dogs in Greenland. Environ Int (in press).
17. Bandiera SM, Torok SM, Lin S, Ramsay MA, Norstrom RJ. 1995. Catalytic and immunologic characterization of hepatic and lung cytochromes P450 in the polar bear. Biochem Pharmacol 49: 1135-1146.
18. Bandiera SM, Torok SM, Letcher RJ, Norstrom RJ. 1997. Immunoquantitation of cytochromes P4501A and P4502B and comparison with chlorinated hydrocarbon levels in archived polar bear liver samples. Chemosphere 34:1469-1479.
19. Letcher RJ, Norstrom RJ, Lin S, Ramsay MA, Bandiera SM. 1996. Immunoquantitation and microsomal monooxygenase activities of hepatic cytochromes P4501A and P4502B and chlorinated hydrocarbon contaminant levels in polar bear (Ursus maritimus). Toxicol Appl Pharmacol 137:127-140.
20. Hobbs KE, Muir DCG, Born EW, Dietz R, Haug T, Metcalfe T, Metcalfe C, ∅ien N. 2003. Levels and patterns of persistent organochlorines in minke whale (Balaenoptera acutorostrata) from the North Atlantic and European Arctic. Environ Pollut 121:239-252.
21. Kleivane L, Skaare JU. 1998. Organochlorine contaminants in northeast Atlantic minke whales (Balaenoptera acutorostrata). Environ Pollut 101:231-239.
22. Sonne C, Rigét FF, Jensen JEB, Hyldstrup L, Teilmann J, Dietz R, Kirkegaard M, Andersen S, Letcher RJ, Jakobsen J. 2008. Does the nutrition profile of vitamins, fatty acids, and microelements counteract the negative impact from organohalogen pollutants on bone mineral density in Greenland sledge dogs (Canis familiaris)? Environ Int 34:811-820.
23. Kennedy SW, Jones SP. 1994. Simultaneous measurement of cytochrome P4501A catalytic activity and total protein concentration with a fluorescence plate reader. Anal Biochem 222:217-223.
24. Li H, Letcher RJ. 2002. A high-performance-liquid-chromatography-based method for the determination of hydroxylated testosterone metabolites formed in vitro in liver microsomes from gray seal (Halichoerus grypus). J Chromatogr Sci 40:397-402.
25. Whalley PM, Bakes D, Grime K, Weaver RJ. 2001. Rapid highperformance liquid chromatographic method for the separation of hydroxylated testosterone metabolites. J Chromatogr B Biomed Sci Appl 760:281-288.
26. Eaton DL, Stapleton PL. 1989. Simultaneous determination of cytosolic glutathione-S-transferase and microsomal epoxide hydrolase activity toward benzo[a]pyrene-4,5-oxide by high-performance liquid chromatography. Anal Biochem 178:153-158.
27. Collier AC, Tingle MD, Keelan JA, Paxton JW, Mitchell MD. 2000. A highly sensitive fluorescent microplate method for the determination of UDP-glucuronosyl transferase activity in tissues and placental cell lines. Drug Metab Dispos 28:1184-1186.
28. Maervoet J, Covaci A, Schepens P, Sandau CD, Letcher RJ. 2004. A reassessment of the nomenclature of polychlorinated biphenyl (PCB) metabolites. Environ Health Perspect 112:291-294.
29. Hair JF, Anderson RE, Tatham RL, Black WC. 1998. Multivariate Data Analysis, 5th ed. Prentice Hall, Upper Saddle River, NJ, USA.
30. Jayyosi Z, Muc M, Erick J, Thomas PE, Kelley M. 1996. Catalytic and immunochemical characterization of cytochrome P450 isozyme induction in dog liver. Fundam Appl Toxicol 31:95-102.
31. Tanaka E, Narisawa C, Nakamura H, Sawa Y, Etoh H, Tadano K, Horie T, Ohkawa H, Misawa S. 1998. Changes in the enzymatic activities of beagle liver during maturation as assessed both in vitro and in vivo. Xenobiotica 28:795-802.
32. Nishibe Y, Wakabayashi M, Harauchi T, Ohno K. 1998. Characterization of cytochrome P450 (CYP3A12) induction by rifampicin in dog liver. Xenobiotica 28:549-557.
33. Uchida T, Komori M, Kitada M, Kamataki T. 1990. Isolation of cDNAs coding for three different forms of liver microsomal cytochrome P450 from polychlorinated biphenyl-treated beagle dogs. Mol Pharmacol 38:644-651.
34. Graves PE, Elhag GA, Ciaccio PJ, Bourque DP, Halpert JR. 1990. cDNA and deduced amino acid sequences of a dog hepatic cytochrome P450IIB responsible for the metabolism of 2,2′,4,4′, 5,5′-hexachlorobiphenyl. Arch Biochem Biophys 281:106-115.
35. Blaisdell J, Goldstein JA, Bai SA. 1998. Isolation of a new canine cytochrome P450 CDNA from the cytochrome P450 2C subfamily (CYP2C41) and evidence for polymorphic differences in its expression. Drug Metab Dispos 26:278-283.
36. Sakamoto K, Kirita S, Baba T, Nakamura Y, Yamazoe Y, Kato R, Takanaka A, Matsubara T. 1995. A new cytochrome P450 form belonging to the CYP2D in dog liver microsomes: Purification, cDNA cloning, and enzyme characterization. Arch Biochem Biophys 319:372-382.
37. Lankford SM, Bai SA, Goldstein JA. 2000. Cloning of canine cytochrome P450 2E1 cDNA: Identification and characterization of two variant alleles. Drug Metab Dispos 28:981-986.
38. Ciaccio PJ, Graves PE, Bourque DP, Glinsmann-Gibson B, Halpert JR. 1991. cDNA and deduced amino acid sequences of a dog liver cytochrome P450 of the IIIA gene subfamily. Biochim Biophys Acta 1088:319-322.
39. Fraser DJ, Feyereisen R, Harlow GR, Halpert JR. 1997. Isolation, heterologous expression, and functional characterization of a novel cytochrome P4503A enzyme from a canine liver cDNA library. J Pharmacol Exp Ther 283:1425-1432.
40. Korytko PJ, Casey AC, Bush B, Quimby FW. 1999. Induction of hepatic cytochromes P450 in dogs exposed to a chronic low dose of polychlorinated biphenyls. Toxicol Sci 47:52-61.
41. Ariyoshi N, Koga N, Oguri K, Yoshimura H. 1992. Metabolism of 2,4,5,2′,4′,5′-hexachlorobiphenyl with liver microsomes of phenobarbital-treated dog: The possible formation of PCB 2,3-arene oxide intermediate. Xenobiotica 22:1275-1290.
42. Duignan DB, Sipes IG, Leonard TB, Halpert JR. 1987. Purifi-cation and characterization of the dog hepatic cytochrome P450 isozyme responsible for the metabolism of 2,2′,4,4′,5,5′-hexachlorobiphenyl. Arch Biochem Biophys 255:290-303.
43. Duignan DB, Sipes IG, Ciaccio PJ, Halpert JR. 1988. The metabolism of xenobiotics and endogenous compounds by the constitutive dog liver cytochrome P450 PBD-2. Arch Biochem Biophys 267:294-304.
44. Sipes IG, Slocumb ML, Perry DF, Carter DE. 1982. 2,4,5,2′,4′, 5′-Hexachlorobiphenyl: Distribution, metabolism, and excretion in the dog and the monkey. Toxicol Appl Pharmacol 65:264-272.
45. Hay-Kraus BL, Greenblatt DJ, Venkatakrishnan K, Court MH. 2000. Evidence for propofol hydroxylation by cytochrome P4502B11 in canine liver microsomes: Breed and gender differences. Xenobiotica 30:575-588.
46. Court MH, Hay-Kraus BL, Hill DW, Kind AJ, Greenblatt DJ. 1999. Propofol hydroxylation by dog liver microsomes: Assay development and dog breed differences. Drug Metab Dispos 27: 1293-1299.
47. Kamimura H. 2006. Genetic polymorphism of cytochrome P450s in beagles: Possible influence of CYP1A2 deficiency on toxicological evaluations. Arch Toxicol 80:732-738.
48. Ohmori S, Taniguchi T, Rikihisa T, Kanakubo Y, Kitada M. 1993. Species differences of testosterone 16-hydroxylases in liver microsomes of guinea pig, rat and dog. Xenobiotica 23:419-426.
49. Williams TM, Kind AJ, Hill DW. 2000. Drug metabolism: In vitro biotransformation of anabolic steroids in canines. J Vet Pharmacol Ther 23:57-66.
50. Shou M, Norcross R, Sandig G, Lu P, Li Y, Lin Y, Mei Q, Rodrigues AD, Rushmore TH. 2003. Substrate specificity and kinetic properties of seven heterologously expressed dog cytochromes P450. Drug Metab Dispos 31:1161-1169.
51. Ryan DE, Levin W. 1990. Purification and characterization of hepatic microsomal cytochrome P450. Pharmacol Ther 45:153-239.
52. Ciaccio PJ, Halpert JR. 1989. Characterization of a phenobarbitalinducible dog liver cytochrome P450 structurally related to rat and human enzymes of the P450IIIA (steroid-inducible) gene subfamily. Arch Biochem Biophys 271:284-299.
53. Liu YT, Hao HP, Liu CX, Wang GJ, Xie HG. 2007. Drugs as CYP3A probes, inducers, and inhibitors. Drug Metab Rev 39: 699-721.
54. Fretland AJ, Omiecinski CJ. 2000. Epoxide hydrolases: Biochemistry and molecular biology. Chem Biol Interact 129:41-59.
55. Ariyoshi N, Tanaka M, Ishii Y, Oguri K. 1994. Purification and characterization of dog liver microsomal epoxide hydrolase. J Biochem (Tokyo) 115:985-990.
56. Dragnev KH, Beebe LE, Jones CR, Fox SD, Thomas PE, Nims RW, Lubet RA. 1994. Subchronic dietary exposure to Aroclor 1254 in rats: Accumulation of PCBs in liver, blood, and adipose tissue and its relationship to induction of various hepatic drugmetabolizing enzymes. Toxicol Appl Pharmacol 125:111-122.
57. Meijer J, DePierre JW. 1987. Hepatic levels of cytosolic, microsomal, and "mitochondrial" epoxide hydrolases and other drugmetabolizing enzymes after treatment of mice with various xenobiotics and endogenous compounds. Chem Biol Interact 62: 249-269.
58. Ariyoshi N, Yoshimura H, Oguri K. 1993. Identification of in vitro metabolites of 2,4,6,2′,4′,6′-hexachlorobiphenyl from phenobarbital-treated dog liver microsomes. Biol Pharm Bull 16: 852-857.
59. Soars MG, Smith DJ, Riley RJ, Burchell B. 2001. Cloning and characterization of a canine UDP-glucuronosyltransferase. Arch Biochem Biophys 391:218-224.
60. Soars MG, Fettes M, O'Sullivan AC, Riley RJ, Ethell BT, Burchell B. 2003. Cloning and characterization of the first drugmetabolizing canine UDP-glucuronosyltransferase of the 2B subfamily. Biochem Pharmacol 65:1251-1259.
61. Fisher JW, Campbell J, Muralidhara S, Bruckner JV, Ferguson D, Mumtaz M, Harmon B, Hedge JM, Crofton KM, Kim H, Almekinder TL. 2006. Effect of PCB 126 on hepatic metabolism of thyroxine and perturbations in the hypothalamic- pituitary-thyroid axis in the rat. Toxicol Sci 90:87-95.
62. Hallgren S, Sinjari T, Håkansson H, Darnerud PO. 2001. Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch Toxicol 75:200-208.
63. Tseng LH, Li MH, Tsai SS, Lee CW, Pan MH, Yao WJ, Hsu PC. 2008. Developmental exposure to decabromodiphenyl ether (PBDE 209): Effects on thyroid hormone and hepatic enzyme activity in male mouse offspring. Chemosphere 70:640-647.
64. Taura KI, Yamada H, Hagino Y, Ishii Y, Mori MA, Oguri K. 2000. Interaction between cytochrome P450 and other drug-metabolizing enzymes: Evidence for an association of CYP1A1 with microsomal epoxide hydrolase and UDP-glucuronosyltransferase. Biochem Biophys Res Commun 273:1048-1052.
65. Kuiper RV, Bergman A, Vos JG, van den Berg M. 2004. Some polybrominated diphenyl ether (PBDE) flame retardants with wide environmental distribution inhibit TCDD-induced EROD activity in primary cultured carp (Cyprinus carpio) hepatocytes. Aquat Toxicol 68:129-139.