Skip to main content
Log in

Age-related Differences in the Sensitivity of the Fish Immune Response to a Coplanar PCB

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Polychlorinated biphenyls (PCBs) are widespread environmental pollutants. Because of their persistence and bioaccumulation in aquatic organisms (among other factors), the biological impact of PCB exposure on resident fish populations is of particular concern. To assess the effect(s) of an environmentally relevant coplanar PCB congener on the fish immune response, juvenile and aged Japanese medaka (Oryzias latipes) were injected i.p. with either vehicle or PCB 126 (at 0.01 or 1.0 µg/g BW) and examined after 3 and 14 days. CYP1A protein levels, examined as an indicator of PCB exposure, were significantly increased (compared to controls) in all fish treated with the highest PCB dose. Kidney phagocyte superoxide (O2 ·−) production was examined to indicate effects upon innate immune function. After 14 days, unstimulated O2 ·− production by kidney phagocytes from juvenile and aged medaka treated with the highest PCB dose was significantly increased compared to controls. Stimulated O2 ·− production by aged PCB-treated fish was unaffected (compared to controls) at both post-exposure timepoints. However, phagocytes from PCB-treated juvenile medaka demonstrated reduced O2 ·− production at 3 days post-exposure and increased levels after 14 days (compared to controls). These results demonstrate the sensitivity of medaka phagocyte function for examining PCB-induced immunotoxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arkoosh, M.R., Clemons, E., Myers, M. and Casillas, E. (1994). 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. 16, 293-314.

    Google Scholar 

  • Beatty, P.W., Vaughn, W.K. and Neal, R.A. (1978). Effect of alteration of rat hepatic mixed-function oxidase (MFO) activity on the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol. Appl. Pharma. 45, 513-19.

    Google Scholar 

  • Brown, A.P., Olivero-Verbel, J., Holdan, W.L. and Ganey, P.E. (1998). Neutrophil activation by polychlorinated biphenyls: structure-activity relationship. Toxicol. Sci. 46, 308-16.

    Google Scholar 

  • Carlson, E.A., Li, Y. and Zelikoff, J.T. (2002). Exposure of Japanese medaka (Oryzias latipes) to benzo[a]pyrene suppresses immune function and host resistance against bacterial challenge. Aquat. Toxicol. 56, 289-301.

    Google Scholar 

  • Cleland, G.B., McElroy, P.J. and Sonstegard, R.A. (1988). The effect of dietary exposure to aroclor 1254 and/or mirex on humoral immune expression of rainbow trout (Salmo gairdneri). Aquat. Toxicol. 2, 141-6.

    Google Scholar 

  • Davis, D. and Safe, S. (1990). Immunosuppressive activities of polychlorinated biphenyls in C57BL/6N mice: structure-activity relationships as Ah receptor agonists and partial antagonists. Toxicology. 63, 97-111.

    Google Scholar 

  • Duffy, J.E., Carlson, E., Li, Y., Prophete, C. and Zelikoff, J.T. Impact of polychlorinated biphenyls (PCBs) on the immune function of fish: age as a variable in determining adverse outcome. Mar. Environ. Res. 54, 559-63.

  • Ganey, P.E., Serois, J.E., Denison, M., Robinson, J.P. and Roth, R.A. (1993). Neutrophil function after exposure to polychlorinated biphenyls in vitro. Environ. Health Perspect. 101, 430-4.

    Google Scholar 

  • Harper, N., Connor, K., Steinberg, M. and Safe, S. (1995). Immunosuppressive activity of polychlorinated biphenyl mixtures and congeners: nonadditive (antagonistic) interactions. Fundam. Appl. Toxicol. 27, 131-9.

    Google Scholar 

  • Harper, N., Howie, L., Connor, K., Dickerson, R. and Safe, S. (1993). Immunosuppressive effects of highly chlorinated biphenyls and diphenyl ethers on T-cell dependent and independent antigens in mice. Toxicology 85, 123-35.

    Google Scholar 

  • Imanishi, J., Oku, T., Oishi, K., Kishida, T., Nomura, H. and Mizutani, T. (1984). Reduced resistance to experimental viral and bacterial infections of mice treated with polychlorinated biphenyl. Biken J. 27, 195-8.

    Google Scholar 

  • Jin, X., Kennedy, S.W., DiMuccio, T. and Moon, T.W. (2001). Role of oxidative stress and antioxidant defense in 3,3′,4,4′,5-pentachlorobiphenyl-induced toxicity and species-differential sensitivity in chicken and duck embryos. Toxicol. Appl. Pharmacol. 172(3), 241-8.

    Google Scholar 

  • Kerkvliet, N.I., Baecher-Steppan, L., Smith, B.B., Youngberg, J.A., Henderson, M.C. and Buhler, D.R. (1990). Role of the Ah locus in suppression of cytotoxic T lymphocyte activity by halogenated hydrocarbons (PCBs and TCDD): structure-activity relationships and effects in C57B1/6 mice congenic at the Ah locus. Fundam. Appl. Pharmacol. 14, 532-41.

    Google Scholar 

  • Linder, R.E., Gaines, T.B. and Kimbrough, R.D. (1974). The effect of polychlorinated biphenyls on rat reproduction. Food Cosmet. Toxicol. 12, 63-77.

    Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-75.

    Google Scholar 

  • Lubet, R.A., Lamaire, B.N., Avery, D. and Kouri, R.E. (1986). Induction of immunotoxicity in mice by polyhalogenated biphenyls. Arch. Toxicol. 59, 71-7.

    Google Scholar 

  • McConnell, E.E. (1985). Comparative toxicity of PCBs and related compounds in various species of animals. Environ. Health Perspect. 60, 29-33.

    Google Scholar 

  • McFarland, V.A. and Clarke, J.U. (1989). Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: considerations for a congener-specific analysis. Environ. Health Perspect. 81, 225-39.

    Google Scholar 

  • Narayanan, P.K., Carter, W.O., Ganey, P.E., Roth, R.A., Voytik-Harbin, S.L. and Robinson, J.P. (1998). Impairment of human neutrophil oxidative burst by polychlorinated biphenyls: inhibition of superoxide dismutase activity. J. Leukocyte Biol. 63, 216-24.

    Google Scholar 

  • Nilsen, B.M., Berg, K. and Goksoyr, A. (1998). Induction of cytochrome P4501A (CYP1A) in fish. A biomarker for environmental pollution..In I.R. Phillips and E.A. Shepard (eds) Methods in Molecular Biology, Vol. 107: Cytochrome P450 Protocols, pp. 423-37. Totowa NJ: Humana Press, Inc.

    Google Scholar 

  • Pick, E. and Mizel, D. (1981). Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. J. Immunol. Meth. 46, 211-26.

    Google Scholar 

  • Regala, R.P., Rice, C.D., Schwedler, T.E. and Dorociak, I.R. (2001). The effects of tributyltin (TBT) and 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126) mixtures on antibody responses and phagocyte oxidative burst activity in channel catfish, Ictalurus punctatus. Arch. Environ. Contam. Toxicol. 40, 386-91.

    Google Scholar 

  • Rice, C.D. and Roszell, L.E. (1998). Tributyltin modulates 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126)-induced hepatic CYP1A activity in channel catfish, Ictalurus punctatus. J. Toxicol. Environ. Health Part A 55, 197-212.

    Google Scholar 

  • Rice, C.D. and Schlenk, D. (1995). Immune function and cytochrome P4501A activity after acute exposure to 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) in channel catfish. J. Aquat. Anim. Health 7, 195-204.

    Google Scholar 

  • Rice, C.D., Schlenk, D., Ainsworth, J. and Goksoyr, A. (1998). Cross-reactivity of monoclonal antibodies against peptide 277–294 of rainbow trout CYP1A1 with hepatic CYP1A among fish. Mar. Environ. Res. 46(1–5), 87-91.

    Google Scholar 

  • Schlezinger, J.J. and Stegeman, J.J. (2001). Induction and suppression of cytochrome P450 1A by 3,3′,4,4′,5-pentachlorobiphenyl and its relationship to oxidative stress in the marine fish scup (Stenotomus chrysops). Aquat. Toxicol. 52, 101-15.

    Google Scholar 

  • Schramm, H., Robertson, L.W. and Oesch, F. (1985). Differential regulation of hepatic glutathione transferase and glutathione peroxidase activities in the rat. Biochem. Pharmacol. 34, 3735-9.

    Google Scholar 

  • Silkworth, J.B., Antrim, L.A. and Kaminsky, L.S. (1984). Correlations between polychlorinated biphenyl immunotoxicity, the aromatic hydrocarbon locus, and liver microsomal enzyme induction in C57BL/6 and DBA/2 mice. Toxicol. Appl. Pharmacol. 75, 156-65.

    Google Scholar 

  • Silkworth, J.B. and Grabstein, E.M. (1982). Polychlorinated biphenyl immunotoxicity: dependence on isomer planarity and the Ah gene complex. Toxicol. Appl. Pharmacol. 65, 109-15.

    Google Scholar 

  • Smialowicz, R.J., Andrews, J.E., Riddle, M.M., Rogers, R.R., Luebke, R.W. and Copeland, C.B. (1989). Evaluation of the immunotoxicity of low level PCB exposure in the rat. Toxicology 56, 197-211.

    Google Scholar 

  • Stack, A.S., Altman-Hamamdzic, S., Morris, P.J., London, S.D. and London, L. (1999). Polychlorinated biphenyl mixtures (aroclors) inhibit LPS-induced murine splenocyte proliferation in vitro. Toxicology 139, 137-54.

    Google Scholar 

  • Tryphonas, H., Luster, M.I., Schiffman, G., Dawson, L.-L., Dodgen, M., Germolec, D., Hayward, S., Bryce, F., Loo, J.C.K., Mandy, F. and Arnold, D.L. (1991). Effect of chronic exposure of PCB (Aroclor 1254) on specific and non-specific immune parameters in the rhesus. (Macaca mulatta) monkey. Fundam. Appl. Toxicol. 16, 773-86.

    Google Scholar 

  • Twaroski, T.P., O'Brien, M.L. and Robertson, L.W. (2001). Effects of selected polychlorinated biphenyl (PCB) congeners on hepatic glutathione, glutathione-related enzymes, and selenium status: implications for oxidative stress. Biochem. Pharmacol. 62, 273-81.

    Google Scholar 

  • Voie, O.A., Tysklind, M., Andersson, P.L. and Fonnum, F. (2000). Activation of respiratory burst in human granulocytes by polychlorinated biphenyls: a structure-activity study. Toxicol. Appl. Toxicol. 167, 188-24.

    Google Scholar 

  • Voie, O.A., Wiik, P., Fonnum, F. (1998). Ortho-substituted polychlorinated biphenyls activate respiratory burst measured as lumino-amplified chemoluminescence in human granulocytes. Toxicol. Appl. Pharmacol. 150, 369-75.

    Google Scholar 

  • Zelikoff, J.T., Wang, W., Islam, N., Twerdok, L.E. Curry, M., Beaman, J. and Flescher, E. (1996). Assays of reactive oxygen intermediates and antioxidant enzymes: potential biomarkers for predicting the effects of environmental pollution..In G.K. Ostrander (ed.) Techniques in Aquatic Toxicology. pp. 287-306. New York NY: Lewis Publishers.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. T. Zelikoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duffy, J., Carlson, E., Li, Y. et al. Age-related Differences in the Sensitivity of the Fish Immune Response to a Coplanar PCB. Ecotoxicology 12, 251–259 (2003). https://doi.org/10.1023/A:1022511028617

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022511028617

Navigation