Seasonality of trout leukocytic sensitivity to toxicity: implications for immunotoxic biomonitoring

Abstract

Aflatoxin B 1 (AFB 1), a widespread food-borne mycotoxin and polycyclic aromatic hydrocarbon, is associated with hepatic carcinogenesis and immunomodulation in a wide variety of vertebrates. Although AFB 1 has been found to be a potent immunomodulator in endotherms, little in the way of immunological assessment has been published in ectothermic species. We found that rainbow trout leukocytes can demonstrate up to a 1000-fold greater sensitivity to the immunosuppression effects of AFB 1 in vitro than is observed with murine leukocytes. This suppression is manifested as a decrease in lymphocytic proliferation and immunoglobulin secretion in response to the polyclonal activator, Escherichia coli lipopolysaccharide. However, this sensitivity appears to be seasonal, exhibiting an acute phase during the July–December period of the year, with the sensitivity falling to lower, more murine-like levels from January to June. These levels of suppression were observed at AFB 1 concentrations which were not toxic to the leukocytes. This sensitivity appears to occur subsequent to a generalized winter-associated period of decreased immune reactivity that has been observed in a number of ectothermic species. It is not unusual to observe a variety of physiologically seasonal effects in ecotherms. Alterations in photoperiod have been noted to have a profound effect on levels of the hormones testosterone, estradiol, and cortisol, all of which been found to alter immune cell function as well as the biotransformation of xenobiotics. This has been specifically demonstrated in the rainbow trout with respect to the impacts of glucocorticoids, estradiol, as well as the process of sexual maturation on P450 activity. If these in vitro observations are indicative of whole animal effects, the dependence of immunotoxicological assessments on seasonality may have tremendous implications for the use of immunoassays for the purposes of biomonitoring in the field. Our results strongly suggest that xenobiotics may have immunosuppressive capabilities that vary over a 1000-fold in their impact depending upon the time of year. Thus, a lack of thorough screening could lead to erroneous conclusions as to the effects of xenobiotics on native fish populations. [Support: NIEHS ES05783.]