Altered sex hormone concentrations and gonadal mRNA expression levels of activin signaling factors in hatchling alligators from a contaminated Florida lake

Abstract

Activins and estrogens participate in regulating the breakdown of ovarian germ cell nests and follicle assembly in mammals. In 1994, our group reported elevated frequencies of abnormal, multioocytic ovarian follicles in 6 month old, environmental contaminant-exposed female alligators after gonadotropin challenge. Here, we investigated if maternal contribution of endocrine disrupting contaminants to the egg subsequently alters estrogen/inhibin/activin signaling in hatchling female offspring, putatively predisposing an increased frequency of multioocytic follicle formation. We quantified basal and exogenous gonadotropin-stimulated concentrations of circulating plasma steroid hormones and ovarian activin signaling factor mRNA abundance in hatchling alligators from the same contaminated (Lake Apopka) and reference (Lake Woodruff) Florida lakes, as examined in 1994. Basal circulating plasma estradiol and testosterone concentrations were greater in alligators from the contaminated environment, whereas activin/inhibin βA subunit and follistatin mRNA abundances were lower than values measured in ovaries from reference lake animals. Challenged, contaminant-exposed animals showed a more robust increase in plasma estradiol concentration following an acute follicle stimulating hormone (FSH) challenge compared with reference site alligators. Aromatase and follistatin mRNA levels increased in response to an extended FSH challenge in the reference site animals, but not in the contaminant-exposed animals. In hatchling alligators, ovarian follicles have not yet formed; therefore, these endocrine differences are likely to affect subsequent ovarian development, including ovarian follicle assembly.

Differential Incubation Temperatures Result in Dimorphic DNA Methylation Patterning of the SOX9 and Aromatase Promoters in Gonads of Alligator (Alligator mississippiensis) Embryos1

“…Alligators from environments contaminated with endocrine-disrupting compounds display disorders of the reproductive system that resemble well-documented human reproductive disorders including alterations in circulating sex hormone levels, morphological abnormalities of ovarian follicles, and a decreased robustness of sexually dimorphic gene expression [57][58][59]. Interestingly, ovarian expression of CYP19A1 is decreased in hatchlings originating from a contaminated site compared to those from a relatively pristine site [60]. These alterations in gene expression likely have epigenetic underpinnings as eggs removed from contaminated environments and placed in the laboratory yield juvenile alligators in which the aforementioned abnormalities persist [61].…”

Epigenetic programming alterations in alligators from environmentally contaminated lakes

“…A number of previous studies have demonstrated that alligators from lakes containing a variety of environmental toxicants have significant developmental and reproductive impairments when compared to those animals living in relatively pristine environments (Hamlin and Guillette, 2010; Orlando and Guillette, 2007). A well established example results from comparisons between two central Florida, USA lakes: Lake Apopka (AP) is characterized by moderate levels of agricultural and industrial contaminants, many of which are known endocrine disrupting chemicals (EDCs), and Lake Woodruff (WO) serves as reference site as it is geographically proximate but has remained relatively pristine and undeveloped (Guillette et al, 1994; Gunderson et al, 2001; Milnes et al, 2005, 2008; Moore et al, 2010; Rooney et al, 2003), Fig. 1.…”

Influence of tissue, age, and environmental quality on DNA methylation in Alligator mississippiensis

“…Yet, understanding of the molecular mechanisms mediating the effects of poor environmental quality on reproductive health remain incomplete. Interestingly, our group has shown that many of these perturbations, including altered gonadal gene expression, persist in laboratoryreared juvenile alligators originating from field-collected eggs (Moore et al 2010a(Moore et al , 2010b(Moore et al , 2011. Thus, the origins of these long-lasting impacts on reproductive health are likely to have roots in early development and may be mediated by epigenetic mechanisms.…”