Assessing impacts of precocious steroid exposure on thyroid physiology and gene expression patterns in the American alligator (Alligator mississippiensis)

Thomas M Galligan; Matthew D Hale; Jessica A McCoy; Dieldrich S Bermudez; Louis J Guillette Jr; Benjamin B Parrott

doi:10.1016/j.ygcen.2018.11.002

Assessing impacts of precocious steroid exposure on thyroid physiology and gene expression patterns in the American alligator (Alligator mississippiensis)

Gen Comp Endocrinol. 2019 Jan 15:271:61-72. doi: 10.1016/j.ygcen.2018.11.002. Epub 2018 Nov 5.

Authors

Thomas M Galligan¹, Matthew D Hale², Jessica A McCoy³, Dieldrich S Bermudez⁴, Louis J Guillette Jr⁵, Benjamin B Parrott⁶

Affiliations

¹ Medical University of South Carolina, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA; Virginia Polytechnic Institute and State University, College of Natural Resources and the Environment, Department of Fish and Wildlife Conservation, 101 Cheatham Hall, 310 West Campus Drive, Blacksburg, VA 24060, USA. Electronic address: thomg09@vt.edu.
² Medical University of South Carolina, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA; University of Georgia, Savannah River Ecology Laboratory, PO Drawer E, Aiken, SC 29802, USA; University of Georgia, Eugene P. Odum School of Ecology, 140 E. Green Street, Athens, GA 30602. Electronic address: matthew.hale@uga.edu.
³ Medical University of South Carolina, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA; College of Charleston, 66 George Street, Charleston, SC 29424, USA.
⁴ Mars Inc., Global Innovation Center, 1132 W. Blackhawk Street, Chicago, IL 60642, USA.
⁵ Medical University of South Carolina, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA.
⁶ Medical University of South Carolina, Hollings Marine Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA; University of Georgia, Savannah River Ecology Laboratory, PO Drawer E, Aiken, SC 29802, USA; University of Georgia, Eugene P. Odum School of Ecology, 140 E. Green Street, Athens, GA 30602. Electronic address: benparrott@srel.uga.edu.

PMID: 30408484
DOI: 10.1016/j.ygcen.2018.11.002

Abstract

The thyroid gland is sensitive to steroid hormone signaling, and many thyroid disrupting contaminants also disrupt steroid hormone homeostasis, presenting the possibility that thyroid disruption may occur through altered steroid hormone signaling. To examine this possibility, we studied short-term and persistent impacts of embryonic sex steroid exposure on thyroid physiology in the American alligator. Alligators from a lake contaminated with endocrine disrupting contaminants (Lake Apopka, FL, USA) have been shown to display characteristics of thyroid and steroid hormone disruption. Previous studies suggest these alterations arise during development and raise the possibility that exposure to maternally deposited contaminants might underlie persistent organizational changes in both thyroidal and reproductive function. Thus, this population provides a system to investigate contaminant-mediated organizational thyroid disruption in an environmentally-relevant context. We assess the developmental expression of genetic pathways involved in thyroid hormone biosynthesis and find that expression of these genes increases prior to hatching. Further, we show that nuclear steroid hormone receptors are also expressed during this period, indicating the developing thyroid is potentially responsive to steroid hormone signaling. We then explore functional roles of steroid signaling during development on subsequent thyroid function in juvenile alligators. We exposed alligator eggs collected from both Lake Apopka and a reference site to 17β-estradiol and a non-aromatizable androgen during embryonic development, and investigated effects of exposure on hatchling morphometrics and thyroidal gene expression profiles at 5 months of age. Steroid hormone treatment did not impact the timing of hatching or hatchling size. Furthermore, treatment with steroid hormones did not result in detectable impacts on thyroid transcriptional programs, suggesting that precocious or excess estrogen and androgen exposure does not influence immediate or long-term thyroidal physiology.

Keywords: Alligator; Endocrine disruption; Organochlorine pesticide; Steroid hormone; Thyroid.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Alligators and Crocodiles / embryology
Alligators and Crocodiles / genetics*
Alligators and Crocodiles / physiology*
Animals
Biosynthetic Pathways / genetics
Female
Gene Expression Regulation, Developmental* / drug effects
Gonadal Steroid Hormones / genetics
Gonadal Steroid Hormones / metabolism
Linear Models
Male
Receptors, Cytoplasmic and Nuclear / genetics
Receptors, Cytoplasmic and Nuclear / metabolism
Steroids / adverse effects*
Thyroid Gland / embryology
Thyroid Gland / physiology*
Thyroid Hormones / biosynthesis

Substances

Gonadal Steroid Hormones
Receptors, Cytoplasmic and Nuclear
Steroids
Thyroid Hormones