Pulmonary modulation of benzo[a]pyrene-induced hemato-and hepatotoxicity in broilers

Poultry Science

Volumn 89, Issue 7, 2010, Pages 1379-1388

  Latif, I K ^a   Karim, A J ^a   Zuki, A B Z ^a   Zamri Saad, M ^a   Niu, J P ^b   Noordin, M M ^b  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b LANZHOU UNIVERSITY   (China)

Author keywords

Benzo a pyrene; Broiler; Hematotoxicity; Hepatoxicity; Oxidative stress

Indexed keywords

AVES; GALLUS GALLUS;

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BENZO[A]PYRENE; CREATINE KINASE; CYTOCHROME P450; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HEMOGLOBIN; LACTIC ACID; MALONALDEHYDE;

AIR POLLUTANT; ANIMAL; ANIMAL DISEASE; ARTICLE; BLOOD; BLOOD CELL COUNT; CHEMICALLY INDUCED DISORDER; CHICKEN; DRUG EFFECT; ENZYMOLOGY; HEMATOCRIT; LIVER; LUNG; LUNG DISEASE; MALE; METABOLISM; MICROSOME; OXIDATIVE STRESS; PHYSIOLOGY; RANDOMIZATION; TOXIC HEPATITIS;

AIR POLLUTANTS; ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BENZO(A)PYRENE; BLOOD CELL COUNT; CHICKENS; CREATINE KINASE; CYTOCHROME P-450 ENZYME SYSTEM; DRUG-INDUCED LIVER INJURY; GAMMA-GLUTAMYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HEMATOCRIT; HEMOGLOBINS; LACTIC ACID; LIVER; LUNG; LUNG DISEASES; MALE; MALONDIALDEHYDE; MICROSOMES; OXIDATIVE STRESS; RANDOM ALLOCATION;

EID: 77955879654     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2009-00622     Document Type: Article

References (54)

1. Alonso-Alvarez, C., I. Munilla, M. López-Alonso, and A. Ve-lando. 2007. Sublethal toxicity of the Prestige oil spill on yellow-legged gulls. Environ. Int. 33:773-781. doi:10.1016/j.en-vint.2007.02.012
2. Andrieux, L., S. Langouët, A. Fautrel, F. Ezan, J. A. Krauser, J. F. Savouret, P. Guengerich, G. Baffet, and A. Guillouzo. 2004. Aryl hydrocarbon receptor activation and cytochrome P450 1a induction by the mitogen-activated protein kinase inhibitor U0126 in hepatocytes. Mol. Pharmacol. 65:934-943. doi:10.1124/ mol.65.4.934
3. Briedé, J. J., R. W. L. Godschalk, M. T. G. Emans, T. M. C. M. De Kok, E. Van Agen, J. Van Maanen, F. J. Van Schooten, and J. C. S. Kleinjans. 2004. In vitro and in vivo studies on oxygen free radical and DNA adduct formation in rat lung and liver during benzo(a)pyrene metabolism. Free Radic. Res. 38:995-1002. doi:10.1080/10715760400000976
4. Briggs, K. T., M. E. Gershwin, and D. W. Anderson. 1997. Consequences of petrochemical ingestion and stress on the immune system of seabirds. J. Mar. Sci. 54:718-725. doi:10.1006/ jmsc.1997.0254
5. Brown, R. E., J. D. Brain, and N. Wang. 1997. The avian respiratory system: A unique model for studies of respiratory toxicosis and for monitoring air quality. Environ. Health Perspect. 105:188-200.
6. Corbanie, E. A., M. G. R. Matthijs, J. H. H. van Eck, J. P. Remon, W. J. M. Landman, and C. Vervaet. 2006. Deposition of differently sized airborne microspheres in the respiratory tract of chickens. Avian Pathol. 35:475-485. doi:10.1080/03079450601028845
7. Crespo, R., S. Yamashiro, and D. B. Hunter. 1998. Development of the thoracic air sacs of turkeys with age and rearing conditions. Avian Dis. 42:35-44.
8. Dabbert, C. B., and K. C. Powell. 1993. Serum enzymes as indicators of capture myopathy in mallards (Anas platyrhynchos). J. Wildl. Dis. 29:304-309.
9. Dalton, T. P., A. Puga, and H. G. Shertzer. 2002. Induction of cellular oxidative stress by aryl hydrocarbon receptor activation. Chem. Biol. Interact. 141:77-95. doi:10.1016/S0009-2797(02)00067-4
10. De Jong, W. H., D. E. Kroese, G. J. Vos, and H. Van Loveren. 1999. Detection of immunotoxicity of benzo(a)pyrene in a sub-acute toxicity study after oral exposure in rats. Toxicol. Sci. 50:214-220.
11. de Oliveira, S. K., M. Hoffmeister, S. Gambaryan, W. Muller-Esterl, J. A. Guimaraes, and A. P. Smolenski. 2007. Phosphodiesterase 2A forms a complex with the cochaperone XAP2 and regulates nuclear translocation of the aryl hydrocarbon receptor. J. Biol. Chem. 282:13656-13663. doi:10.1074/jbc.M610942200
12. Frappell, P. B., D. S. Hinds, and D. F. Boggs. 2001. Scaling of respiratory variables and the breathing pattern in birds: An allometric and phylogenetic approach. Physiol. Biochem. Zool. 74:75-89.
13. Garçon, G., P. Gosset, S. Garry, T. Marez, M. H. Hannothiaux, and P. Shirali. 2001. Pulmonary induction of proinflammatory mediators following the rat exposure to benzo(a)pyrene-coated onto Fe2O3 particles. Toxicol. Lett. 121:107-117. doi:10.1016/ S0378-4274(01)00326-5
14. Garg, U. K., A. K. Pal, G. J. Jha, and S. B. Jadhao. 2004. Haema-to-biochemical and immunopathophysiological effects of chronic toxicity with synthetic pyrethroid, organophosphate and chlorinated pesticides in broiler chicks. Int. J. Immunopharmacol. 4:1709-1722. doi:10.1016/j.intimp.2004.08.002
15. Goksøyr, A., and L. Förlin. 1992. The cytochrome P-450 system in fish, aquatic toxicology and environmental monitoring. Aquat. Toxicol. 22:287-312. doi:10.1016/0166-445X(92)90046-P
16. Golet, G. H., P. E. Seiser, A. D. Mc Guire, D. D. Roby, J. B. Fischer, and K. J. Kuletz. 2002. Long term direct and indirect effects of the ExxonValdez oil spill on pigeon guillemots in Prince William Sound, Alaska. Mar. Ecol. Prog. Ser. 241:287-304.
17. Grasman, K. A. 2002. Assessing immunological function in toxico-logical studies of avian wildlife. Integr. Comp. Biol. 42:34-42. doi:10.1093/icb/42.1.34
18. Habig, W. H., M. J. Pabst, and W. B. Jakoby. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249:7130-7139.
19. Harr, K. E. 2002. Clinical chemistry of companion avian species: A review. Vet. Clin. Pathol. 31:140-151. doi:10.1111/j.1939-165X.2002.tb00295.x
20. Hartman, P. E., and D. W. Shankel. 1990. Antimutagens and anti-carcinogens; a survey of putative interceptor molecules. Environ. Mol. Mutagen. 15:145-182.
21. Hirabayashi, Y., and T. Inoue. 2009. Aryl hydrocarbon receptor biology and xenobiotic responses in hematopoietic progenitor cells. Biochem. Pharmacol. 77:521-535. doi:10.1016/j.bcp.2008.09.030
22. Karchner, S. I., D. G. Franks, S. W. Kennedy, and M. E. Hahn. 2006. The molecular basis for differential dioxin sensitivity in birds: Role of the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. USA 103:6252-6257. doi:10.1073/pnas.0509950103
23. Kendall, M., A. Duarte, T. Rocha-Santos, R. Hamilton, and I. Williams. 2002. Airborne particulate-associated polyaromatic hydrocarbons, n-alkanes, elemental and organic carbon in three European cities. J. Environ. Monit. 4:890-896. doi:10.1039/ b203888a
24. Kennedy, S. W., A. Lorenzen, S. P. Jones, M. E. Hahn, and J. J. Stegeman. 1996. Cytochrome P4501A induction in avian hepato-cyte cultures: A promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 141:214-230. doi:10.1006/ taap.1996.0278
25. Kepley, C. L., F. T. Lauer, J. M. Oliver, and S. W. Burchiel. 2003. Environmental polycyclic aromatic hydrocarbons, benzo(a) pyrene (BaP) and BaP-quinones, enhance IgE mediated hista-mine release and IL-4 production in human basophils. Clin. Immunol. 107:10-19. doi:10.1016/S1521-6616(03)00004-4
26. Kiama, S. G., J. S. Adekunle, and J. N. Maina. 2008. Comparative in vitro study of interactions between particles and respiratory surface macrophages, erythrocytes, and epithelial cells of the chicken and the rat. J. Anat. 213:452-463. doi:10.1111/j.1469-7580.2008.00951.x
27. King, S., J. S. Meyer, and A. R. J. Andrews. 2002. Screening method for polycyclic aromatic hydrocarbons in soil using hollow fibre membrane solvent microextraction. J. Chromatogr. A 982:201-208.
28. Knuckles, M. E., F. Inyang, and A. Ramesh. 2001. Acute and sub-chronic oral toxicities of benzo[a]pyrene in F-344 rats. Toxicol. Sci. 61:382-388.
29. Latif, I. K., A. J. Karim, A. B. Z. Zuki, M. Zamri-Saad, J. P. Niu, and M. M. Noordin. 2009. Respiratory macrophage activity and pulmonary morphology following exposure to benzo(a)pyrene in broilers. Online J. Vet. Res. 13:128-135.
30. Lim, J. T., and S. H. Ooi. 1998. Effects of biomass burning in Southeast Asia on metereological conditions in Malaysia. Pages 55-70 in Towards a Cleaner Atmospheric Environment. A. R. Sheikh-Omar, A. Awang, M. N. Hassan, F. M. Yusoff, M. S. Othman, and N. M. Mustapha, ed. UPM Press, Serdang, Malaysia.
31. Lorenzoni, A. G., G. F. Erf, N. C. Rath, and R. F. Wideman. 2009. Cellular component of lavage fluid from broilers with normal versus aerosol-primed airways. Poult. Sci. 88:303-308. doi:10.3382/ ps.2008-00379
32. Lorenzoni, A. G., and R. F. Wideman. 2008. Intratracheal administration of bacterial lipopolysaccharide elicits pulmonary hypertension in broilers with primed airways. Poult. Sci. 87:645-654. doi:10.3382/ps.2007-00483
33. Lumeij, J. T. 1997. Avian clinical biochemistry. Pages 845-854 in Clinical Biochemistry of Domestic Animals. J. Kaneko, J. Harvey, and M. Bruss, ed. Academic Press, New York, NY.
34. Mitchell, E., and J. Johns. 2008. Avian hematology and related disorders. Vet. Clin. North Am. Exot. Anim. Pract. 11:501-522. doi:10.1016/j.cvex.2008.03.004
35. Noordin, M. M., A. R. Sheikh-Omar, M. S. Rosley, C. C. Tan, and M. Zamri-Saad. 1998. Animal health and productivity during episodes of haze. Pages 130-135 in Towards a Cleaner Atmospheric Environment. A. R. Sheikh-Omar, A. Awang, M. N. Hassan, F. M. Yusoff, M. S. Othman, and N. M. Mustapha, ed. UPM Press, Serdang, Malaysia.
36. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
37. Ohkawa, H., N. Ohishi, and K. Yagi. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351-358.
38. Okey, A. B. 2007. An aryl hydrocarbon receptor odyssey to the shores of toxicology: The Deichmann lecture, International Congress of Toxicology-XI. Toxicol. Sci. 98:5-38. doi:10.1093/tox-sci/kfm096
39. Omura, T., and R. Sato. 1964. The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239:2370-2378.
40. Pang, P. H., Y. H. Lin, Y. H. Lee, H. H. Hou, S. P. Hsu, and S. H. Juan. 2008. Molecular mechanisms of p21 and p27 induction by 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, involved in antiproliferation of human umbilical vascular endothe-lial cells. J. Cell. Physiol. 215:161-171. doi:10.1002/jcp.21299
41. Reed, D. J. 1990. Glutathione: Toxicological implications. Annu. Rev. Pharmacol. Toxicol. 30:603-631.
42. Rivière, J. L., J. Bach, and G. Grolleau. 1985. Effects of prochloraz on drug metabolism in the Japanese quail, grey partridge, chicken, and pheasant. Arch. Environ. Contam. Toxicol. 14:299-306. doi:10.1007/BF01055406
43. Saegerman, C., L. Pussemier, A. Huyghebaert, M. L. Scippo, and D. Berkvens. 2006. On-farm contamination of animals with chemical contaminants. Rev. Sci. Tech. 25:655-673.
44. Sallie, K., J. M. Tredger, and R. William. 1991. Drugs and the liver. Biopharm. Drug Dispos. 12:251-259.
45. Seiser, P. E., L. K. Duffy, A. D. Mc Guire, D. D. Roby, G. H. Golet, and M. A. Litzow. 2000. Comparison of pigeon guillemot, Cep-phus columba, blood parameters from oiled and unoiled areas of Alaska eight years after the Exxon Valdez oil spill. Mar. Pollut. Bull. 40:152-164. doi:10.1016/S0025-326X
46. Sellers, R. S., D. Morton, B. Michael, N. Roome, J. K Johnson, B. L. Yano, R. Perry, and K. Schafer. 2007. Society of Toxi-cologic Pathology Position Paper: Organ weight recommendations for toxicology studies. Toxicol. Pathol. 35:751-755. doi:10.1080/01926230701595300
47. Singh, K. P., F. L. Casado, L. A. Opanashuk, and T. A. Gasiewicz. 2009. The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77:577-587. doi:10.1016/j. bcp.2008.10.001
48. Stewart, R. K., C. J. Serabjit-Singh, and T. E. Massey. 1996. Glu-tathione-S-transferase-catalyzed conjugation of bioactivated afla-toxin B1 in rabbit lung and liver. Toxicol. Appl. Pharmacol. 140:499-507.
49. Sun, J. D., R. K. Wolff, and G. M. Kanapilly. 1982. Deposition, retention, and biological fate of inhaled benzo[a]pyrene adsorbed onto ultrafine particles and as a pure aerosol. Toxicol. Appl. Pharmacol. 65:231-244. doi:10.1016/0041-008X
50. Szczesna-Skorupa, E., C. D. Chen, H. Liu, and B. Kemper. 2004. Gene expression changes associated with the endoplasmic reticulum stress response induced by microsomal cytochrome P450 overproduction. J. Biol. Chem. 279:13953-13961. doi:10.1074/ jbc.M312170200
51. Trust KA., D. Esler, B. R. Woodin, and J. J. Stegeman. 2000. Cytochrome P4501A induction in sea ducks inhabiting near-shore areas of Prince William Sound, Alaska. Mar. Pollut. Bull. 40:397-403. doi:10.1016/S0025-326X
52. Wang, G., R. Reisdorph, R. E. Clark Jr., R. Miskimins, R. Lindahl, and W. K. Miskimins. 2003. Cyclin dependent kinase inhibitor p27 (Kip1) is upregulated by hypoxia via an ARNT dependent pathway. J. Cell. Biochem. 90:548-560.
53. Yasui, T., E.-Y. Kim, H. Iwata, D. G. Franks, S. I. Karchner, M. E. Hahn, and S. Tanabe. 2007. Functional characterization and evolutionary history of two aryl hydrocarbon receptor isoforms (AhR1 and AhR2) from avian species. Toxicol. Sci. 99:101-117. doi:10.1093/toxsci/kfm139
54. Zimniak, L., S. Awasthi, S. Srivastava, and P. Zimniak. 1997. Increased resistance to oxidative stress in transfected cultured cells overexpressing glutathione-S-transferase mGSTA4-4. Toxicol. Appl. Pharmacol. 143:221-229. doi:10.1006/taap.1996.8070