Immunomodulatory effects of dietary exposure to selected polycyclic aromatic hydrocarbons in the bluegill (Lepomis macrochirus)

International Journal of Toxicology

Volumn 29, Issue 5, 2010, Pages 532-545

  Connelly, Helen ^a   Means, Jay C ^a,b  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

dietary exposure; fish; immunosuppression; mitogen; PAH

Indexed keywords

2 AMINOANTHRACENE; 2 METHYLNAPHTHALENE; 9,10 DIMETHYLANTHRACENE; CALCIUM ION; CALCIUM IONOPHORE; CONCANAVALIN A; PHORBOL ESTER; POLYCYCLIC AROMATIC HYDROCARBON; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; FRESHWATER FISH; IMMUNOMODULATION; IMMUNOTOXICITY; INDICATOR ORGANISM; LEPOMIS MACROCHIRUS; LYMPHOCYTE PROLIFERATION; MITOGENESIS; NONHUMAN;

ANIMAL FEED; ANIMALS; ANTHRACENES; BIOLOGICAL MARKERS; CALCIUM; CARCINOGENS; CELL PROLIFERATION; CELLS, CULTURED; IMMUNOLOGIC FACTORS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MITOGENS; MODELS, ANIMAL; NAPHTHALENES; PERCIFORMES; POLYCYCLIC HYDROCARBONS, AROMATIC; RANDOM ALLOCATION; REPRODUCIBILITY OF RESULTS; TOXICITY TESTS;

LEPOMIS MACROCHIRUS;

EID: 78650063924     PISSN: 10915818     EISSN: 1092874X     Source Type: Journal    
DOI: 10.1177/1091581810377518     Document Type: Article

References (62)

1. Davila DR, Davis DP, Campbell K., Cambier JC, Zigmond LA, Burchiel SW Role of alterations in Ca++-associated signaling pathways in the immunotoxicity of polycyclic aromatic hydrocarbons. J Toxicol Environ Health. 1995 ; 45 (2). 101-126.
2. Carlson EA, Li T., Zelikoff JT Suppressive effects of benzo[a]-pyrene upon fish immune function: evolutionary conserved cellular mechanisms of immunotoxicity. Mar Environ Res. 2004 ; 58 (2-5). 731-734.
3. Kennedy CJ, Farrell AP Immunological aleterations in juvenile n Pacific herring (Clupea pallasi), exposed to aqueous hydrocarbons derived from crude oil. Environ Poll. 2008 ; 153 (3). 638-648.
4. Burchiel SW, Thompson TA, Davis DP Alterations in mitogen induced calcium mobilization and intracellular free calcium produced by 7,12-dimethylbenz (a)anthracene in the Jurkat human T cell line. Int J Immunopharmacol. 1991 ; 13 (1). 109-115.
5. Stjernsward J. Effect of noncarcinogenic and carcinogenic hydrocarbons on antibody-forming cells measured at the cellular level. in vitro. J Natl Cancer Inst. 1996 ; 36 (6). 1189-1195.
6. Faisal M., Huggett RJ Effects of polycyclic aromatic hydrocarbons on the lymphocyte mitogenic responses in spot. Leiostomus xanthurus. Marine Environ Res. 1993 ; 35: 121-124.
7. Arkoosh MR, Clemons E., Huffman P., Sanborn HR, Casillas E., Stein JE Evaluation of the leukoproliferative response of English sole (Pleuronectes vetulus) as a biomarker for immune dysfunction. Marine Environ Res. 1996 ; 42 (1). 181-186.
8. Davila DR, Romero DL, Burchiel SW. Human T cells are highly sensitive to suppression of mitogenesis by polycyclic aromatic hydrocarbons and this effect is differentially reversed by alphanaphthoflavone. Toxicol Appl Pharmacol. 1996 ; 139 (2). 333-341.
9. Smith, DA, Schurig GG, Smith SA, Holiday SD Inhibited cytotoxic leukocyte activity in Tilapia (Oreochromis niloticus) following exposure to immunotoxic chemicals. Int J Toxicol. 2008 ; 18 (3). 167-172.
10. Archuleta MM, Schieven GL, Ledbetter JA, Deanin GG, Burchiel SW 7,12-dimethylbenz(a)anthracene activates protein-tyrosine kinases Fyn and Lck in the HPB-ALL human T-cell line and increases tyrosine phosphorylation of phospholipase Cgamma 1, formation of inositol 1,4,5-trisphosphate, and mobilization of intracellular calcium. Proc Natl Acad Sci. 1993 ; 90 (13). 6105-6109.
11. Mounho BJ, Davila DR, Burchiel SW Characterization of intracellular calcium responses produced by polycyclic aromatic hydrocarbons in surface marker-defined human peripheral blood mononuclear cells. Toxicol Appl Pharmacol. 1997 ; 145 (2). 323-330.
12. Benedetti S., Randelli E., Buonocore F., Zou J., Secombes CJ, Scapigliati G. Evolution of cytokine responses: IL-1b directly affects intracellular Ca2+ concentration of teleost fish leukocytes through a receptor-mediated mechanism. Cytokine. 2006 ; 34 (1-2). 9-16.
13. Davis DP, Burchiel SW Inhibition of calcium-dependent pathways of B cell activation by DMBA. Toxicol Appl Pharmacol. 1992 ; 116 (2). 202-208.
14. Burchiel SW, Davis DP, Ray SD, Barton SL DMBA induces programmed cell death (apoptosis) in the A20 1 murine B cell lymphoma. Fundam Appl Toxicol. 1993 ; 21 (1). 120-124.
15. Pallardy M., Mishal Z., Lebrec H., Bohuon C. Immune modification due to chemical interference with transmembrane signaling: application to polycyclic aromatic hydrocarbons. Int J Immunopharmacol. 1992 ; 14 (3). 377-382.
16. Dean JH, Luster MI, Boorman GA, Lauer LD, Leubke RW, Lawson L. Selective immunosuppression resulting from exposure to the carcinogenic congener of benzopyrene in B6C3F 1 mice. Clin Exp Immunol. 1983 ; 52 (1). 199-206.
17. Lubet RA, Brunda MJ, Taramelli D., Dansie D., Nebert DW, Kouri RE Induction of immunotoxicity by polycyclic hydrocarbons: Role of the Ah locus. Arch Toxicol. 1984 ; 56 (1). 18-24.
18. Dean JH, Ward EC, Murray MJ, et al. Immunosuppression following 7,12-dimethylbenz(a)anthracene exposure in B6C3F1 mice-II:Altered cell-mediated immunity and tumor resistance. Int J Immunopharmacol. 1986 ; 8 (2). 189-198.
19. Ward EC, Murray MJ, Lauer LD, House RV, Dean JH Persistent suppression of humoral and cell-mediated immunity in mice following exposure to the polycyclic aromatic hydrocarbon 7,12-dimethylbenz[a]anthracene. Int J Immunopharmacol. 1986 ; 8 (1). 13-22.
20. Thurmond LM, House RV, Lauer LD, Dean JH Suppression of splenic lymphocyte function by 7,12-dimethylbenz(a)anthracene (DMBA) in vitro. Toxicol Appl Pharmacol. 1988 ; 93 (3). 369-377.
21. Wojdani A., Alfred LJ Alterations in cell-mediated immune functions induced in mouse splenic lymphocytes by polycyclic aromatic hydrocarbons. Cancer Res. 1984 ; 44 (3). 942-945.
22. Thurmond LM, Lauer LD, House RV, Cook JC, Dean JH Immunosuppression following exposure to 7,12-dimethylbenz(a)anthracene (DMBA) in Ah-responsive and Ah-nonresponsive mice. Toxicol Appl Pharmacol. 1987 ; 91 (3). 450-460.
23. Tomar RS, Lim S., Gill SS The effects of epoxidized xenobiotics on mitogen responsiveness and antibody-producing ability of murine spleen cells in vitro. Int J Immunopharmacol. 1991 ; 13 (1). 57-65.
24. Downward J., Graves JD, Warne PH, Rayter S., Cantrell DA Stimulation of p21ras upon T-cell activation. Nature. 1990 ; 346 (6286). 719-723.
25. Kraft AS, Anderson WB Phorbol esters increase the amount of Ca2+, phospholipid-dependent protein kinase associated with plasma membrane. Nature. 1983 ; 301 (5901). 621-623.
26. Whitehurst CE, Owaki H., Bruder JT, Rapp UR, Geppert TD The MEK kinase activity of the catalytic domain of RAF-1 is regulated independently of Ras binding in T cells. J Biol Chem. 1995 ; 270 (10). 5594-5599.
27. Reed PW, Lardy HA A23187: a divalent cation ionophore. J Biol Chem. 1972 ; 247 (21). 6970-6977.
28. Truneh A., Albert F., Golstein P., et al. Early steps of lymphocyte activation by-passed by calcium ionophores and phorbol esters acting in synergy. Nature. 1985 ; 313 (6000). 318-320.
29. Miller NW, Clem LW A culture system for mitogen-induced proliferation of channel catfish (Ictalurus punctatus) peripheral blood lymphocytes. Meth Cell Sci. 1988 ; 11 (2). 69-73.
30. Lin GL, Ellsaesser CF, Clem LW, Miller NW Phorbol ester/calcium ionophore activate fish leukocytes and induce long-term cultures. Dev Comp Immmunol. 1992 ; 16 (2-3). 153-163.
31. Means JC Compound-specific GC /MS analysis of parent and alkylated polynuclear aromatic hydrocarbons in water, sediments and tissues. J Assoc Off Analyt Chem. 1998 ; 81 (3). 657-672.
32. Novak EJ, Rabinovitch PS Improved sensitivity in flow cytometric intracellular ionized calcium measurement using fluo-3/fura red fluorescence ratios. Cytometry. 1994 ; 17 (2). 135-141.
33. Hashimoto S., Takahashi Y., Tomita Y., et al. Mechanism of calcium ionophore and phorbol ester-induced T-cell activation. Scand. J Immunol. 1991 ; 33 (4). 393-403.
34. Clevers HC, Versteegen JMT, Logtenberg T., et al. Synergestic action of A23187 and phorbol ester on human B cell activation. J Immunol. 1985 ; 135 (6). 3827-3830.
35. Smith AM, Potter M., Merchant EB Antibody forming cells in the pronephros of the teleost. Lepomis macrochirus. J Immunol. 1967 ; 99 (5). 876-882.
36. Kusher DI, Crim JW Immunosuppression in bluegill (Lepomis macrochirus) induced by environmental exposure to cadmium. Fish Shellfish Immunol. 1991 ; 1 (3). 157-161.
37. Secombes CJ, Zou J., Liang K., et al. Cytokine genes in fish. Aqua-cult. 1999 ; 172: 93-102.
38. Secombes CJ, Wang T., Hong S., et al. Cytokines and innate immunity in fish. Dev Comp Immunol. 2001 ; 25 (8-9). 713-723.
39. Magnadóttir B. Innate immunity in fish (overview). Fish Shellfish Immunol. 2006 ; 20 (2). 137-151.
40. Borst J., Brouns GS, de Vries E., Verschuren MC, Mason DY, van Dongen JJ Antigen receptors on T & B lymphocytes: parallels in organization and function. Immun Rev. 1993 ; 132: 49-84.
41. Mustelin T., Coggeshall KM, Isakov N., Altman A. T cell antigen receptor-mediated activation of phospholipase C requires tyrosine phosphorylation. Science. 1990 ; 247 (4950). 1584-1587.
42. Burnett KG, Schwarz LK Leukocyte proliferation mediated by protein kinase C in the marine teleost fish. Sciaenops ocellatus. Dev Comp Immunol. 1994 ; 18 (1). 33-43.
43. MacDougal KC, Johnson MD, Burnett KG Exposure to mercury alters early activation events in fish leukocytes. Environ Health Perspect. 1996 ; 104 (10). 1102-1106.
44. van Ginkel FW, Pascual DW, Clem LW Proteolytic fragmentation of channel catfish antibodies. Dev Comp Immunol. 1991 ; 15 (1-2). 41-51.
45. Verburg-Van Kemenade BM, Saeij JP, Flik G., Willems PH Ca2+ signals during early lymphocyte activation in carp. Cyprinus carpio. L. J Exp Biol. 1998 ; 201 (pt 4). 591-598.
46. Faisal M., Marzouk MSM, Smith CL, Huggett RJ Mitogen induced proliferative responses of lymphocytes from spot (Leiostomus xanthurus) exposed to polycyclic aromatic hydrocarbon contaminated environments. Immunopharmacol Immunotoxicol. 1991 ; 13 (3). 311-327.
47. Tahir A., Secombes CJ The effects of diesel oil-based drilling mud extracts on immune responses of rainbow trout. Arch Environ Contam Toxicol. 1995 ; 29 (1). 27-32.
48. Tahir A., Fletcher TC, Houlihan DF, Secombes CJ Effect of short-term exposure to oil-contaminated sediments on the immune response of dab. Limanda limanda. Aquat Toxicol. 1993 ; 27: 71-82.
49. Arkoosh MR, Clemens E., Myers M., Casillas E. Suppression of B-cell mediated immunity in juvenile Chinook salmon (Oncorhynchus tshawytscha) after exposure to either a polycyclic aromatic hydrocarbon or to polychlorinated biphenyls. Immunopharmacol Immunotoxicol 1994 ; 16 (2). 293-314.
50. Farber E. Clonal adaptation during carcinogenesis. Biochem Pharmacol. 1990 ; 39 (12). 1837-1846.
51. Yamashita U., Hamaoka T. Selective suppression of host T cell and macrophage activities during 7,12-dimethylbenz[a]anthracene-induced carcinogenesis. Gann. 1982 ; 73 (5). 773-782.
52. Griffin KA, Johnson CB, Breger RK, Franlclin RB Effects of inducers and inhibitors of cytochrome P-450-linked monooxygenases on the toxicity, in vitro metabolism and in vivo irreversible binding of 2methyluaphthalene in mice. J Pharmacol Exp Ther. 1982 ; 221 (3). 5-17.
53. Lander HM, Hajjar DP, Hempstead BL, et al. A molecular redox switch on p21ras. Structural basis for the nitric oxide-p21ras interaction. J Biol Chem. 1997 ; 272 (7). 4323-4326.
54. Sweet LI, Zelikoff JT Toxicology and immunotoxicology of mercury: a comparative review of fish and humans. J Toxicol Environ Health B Crit Rev. 2001 ; 4 (2). 161-205.
55. June CH, Fletcher MC, Ledbetter JA, et al. Inhibition of tyrosine phosphorylation prevents T cell receptor-mediated signal transduction. Proc Natl Acad Sci. 1990 ; 87 (19). 7722-7726.
56. Lee M., Kirlin W., Sturrup M., Rodriguez J., Urso P. Variation in the response of T cells to concanavilin A after in vitro exposure to benzo(a)pyrene and 2-aminofluorene. Immunopharmacol Immunotoxicol. 1996 ; 18 (2). 309-321.
57. Burchiel SW, Davis DP, Ray SD, Archuleta MM, Thilsted JP, Corcoran GB DMBA-induced cytotoxicity in lymphoid and non-lymphoid organs of B6C3F1 mice: relation of cell death to target cell intracellular calcium and DNA damage. Toxicol Appl Pharm. 1992 ; 113 (1). 126-132.
58. Krieger JA, Davila DR, Lytton J., Born JL, Burchiel SW Inhibition of sarcoplasmic/endoplasmic reticulum calcium ATPases (SERCA) by polycyclic aromatic hydrocarbons in HPB-ALL human T cells and other tissues. Toxicol Appl Pharmacol. 1995 ; 133 (1). 102-108.
59. Whitehurst CE, Boulton TG, Cobb MH, Gepper TD Extracellular signal-regulated kinases in T cells. Anti-CD3 and 4 beta-phorbol 12-myristate 13-acetate-induced phosphorylation and activation. J Immunol. 1992 ; 148 (10). 3230-3237.
60. Weiss A.T. Lymphocyte activation. In: Paul WE, ed. Fundamental Immunology. 3 rd ed. New York,NY: Raven Press ; 1993: 467-504.
61. Tsien RY, Pozzan T., Rink TJ T-cell mitogens cause early changes in cytoplasmic free Ca2+ and membrane potential in lymphocytes. Nature. 1982 ; 295 (5844). 68-71.
62. Vandenberghe PA, Ceuppens JL Flow cytometric measurement of cytoplasmic free calcium in human peripheral blood T lymphocytes with fluo-3, a new fluorescent calcium indicator. J Immunol Methods. 1990 ; 127 (2). 197-205.