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following larval exposure to 2.5 μg L -1 atrazine, including nuptial pad and breeding gland
development, measured as cross-sectional areas in histological sections, and a reduced
propensity to enter amplexus and breed.
9.3.5 Biomarkers of a Mechanism for Emasculation/Feminization
Gender in amphibians is genetically predetermined, although as we have observed above,
sexual phenotype, or at least several subphenotypic characteristics, can be influenced by
environmental factors. However, the manifestation of phenotype is determined by physi-
ological processes that can be followed through the expression of various biomarkers.
Gonadal development is controlled by the sex hormones, estrogen and testosterone.
Disruption of sexual differentiation by environmental contaminants is commonly asso-
ciated with mimicry of estrogen. One of the most common biomarkers for estrogenic
effects, particularly in fish, is an increase in circulating VTG (Tarrant et al. 2008). However,
increased titers of VTG have not been observed among amphibians exposed to atrazine
(Mosconi et al. 2005; McDaniel et al. 2008; Oka et al. 2008). Therefore, the mechanism by
which atrazine exerts an endocrine effect appears not be via increased induction of estro-
genic pathways leading to the production of VTG (Sanderson 2006).
Both estrogen and testosterone are steroids with a common metabolic genesis. Estrogen
is metabolized from testosterone by a single metabolic step catalyzed by the enzyme
aromatase (Figure 9.13). Both Tavera-Mendoza (2002a) and Hayes (2005) speculated that
the alleged endocrine disruptive effects of atrazine were mediated via an induction of
aromatase. In high doses, atrazine has been demonstrated to increase aromatase activity
in mammalian cell lines (e.g., Holloway et al. 2008), and conversely, inhibition of aroma-
tase, thereby preventing the conversion of testosterone to estrogen, effectively resulting
in male phenotype in otherwise genetically female newts ( Pleurodeles waltl ) (Chardard
and Dournon 1999). Therefore, it was reasonable to hypothesize that atrazine-induced
increases in aromatase expression or activity could reduce the concentrations of circulat-
ing testosterone and promote the development (or perhaps the retention) of female char-
acteristics. In support of this hypothesis, exposure of adult male X. laevis to 2.5-250 μg
L -1 of atrazine for a period of 36-46 days resulted in significantly lower titers of testoster-
one in the plasma of X. laevis (Hayes et al. 2002a; Hecker et al. 2005b; Hayes et al. 2010).
OH
OH
Testosterone
Aromatase
H
H
H
H
H
H
O
HO
Estradiol
5 β -reductase
5 α -reductase
OH
OH
H
H
H
H
H
H
H
O
5β-dihydrotestosterone
H
5α-dihydrotestosterone
FIGURE 9.13
Pathways for testosterone catabolism.
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