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Influences of sex, incubation temperature, and environmental quality on gonadal estrogen and androgen receptor messenger RNA expression in juvenile American alligators (Alligator mississippiensis) - PubMed

Influences of sex, incubation temperature, and environmental quality on gonadal estrogen and androgen receptor messenger RNA expression in juvenile American alligators (Alligator mississippiensis)

Brandon C Moore et al. Biol Reprod. 2010 Jan.

Abstract

Gonadal steroid hormone receptors play a vital role in transforming ligand signals into gene expression. We have shown previously that gonads from wild-caught juvenile alligators express greater levels of estrogen receptor 1 (ESR1) than estrogen receptor 2 (ESR2). Furthermore, sexually dimorphic ESR2 mRNA expression (female > male) observed in animals from the reference site (Lake Woodruff, FL, USA) was lost in alligators from the contaminated Lake Apopka (FL, USA). We postulated that environmental contaminant exposure could influence gonadal steroid hormone receptor expression. Here, we address questions regarding gonadal estrogen and androgen receptor (AR) mRNA expression in 1-yr-old, laboratory-raised alligators. What are relative expression levels within gonads? Do these levels vary between sexes or incubation temperatures? Can contaminant exposure change these levels? We observed a similar pattern of expression (ESR1 > AR > ESR2) in ovary and testis. However, both incubation temperature and environment modulated expression. Males incubated at 33.5 degrees C expressed greater AR levels than females incubated at 30 degrees C; dimorphic expression was not observed in animals incubated at 32 degrees C. Compared to Lake Woodruff alligators, Lake Apopka animals of both sexes showed lesser ESR2 mRNA expression levels. Employing cluster analyses, we integrated these receptor expression patterns with those of steroidogenic factors. Elevated ESR2 and CYP19A1 expressions were diagnostic of alligator ovary, whereas elevated HSD3B1, CYP11A1, and CYP17A1 expressions were indicative of testis. In contrast, AR, ESR1, and NR5A1 showed variable expressions that were not entirely associated with sex. These findings demonstrate that the mRNA expression of receptors required for steroid hormone signaling are modified by exposure to environmental factors, including temperature and contaminants.

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Figures

FIG. 1.
FIG. 1.

Body morphometrics measurements from 13-mo-old alligators. Incubation periods were 30 or 33.5°C (A, C, E, G, and I) and 32°C (B, D, F, H, and J). Crosshatched bars are Lake Apopka females (F), and black bars are Lake Woodruff females. Diagonal lined bars are Lake Apopka males (M), and white bars are Lake Woodruff males. Bars represent the mean ± SEM for body mass (A and B), snout-vent length (C and D), and total length (E and F). Condition indices (body mass/length measurement3) were calculated using either snout-vent length (SVL; G and H) or total length (TL; I and J). In J, an uppercase A and B over bars denotes a significant sex effect; in B, D, F, and J, a lowercase x and y over bars denotes a significant lake-of-origin effect.

FIG. 2.
FIG. 2.

Mean (± SEM) mRNA expression of ESR1 (A and D), ESR2 (B and E), and AR (C and F) in gonads of 13-mo-old alligators incubated at 30 or 33.5°C (A–C) or at 32°C (D–F). Crosshatched bars are Lake Apopka females (F), and black bars are Lake Woodruff females. Diagonal lined bars are Lake Apopka males (M), and white bars are Lake Woodruff males. In A–C, asterisks (*) denote a significant difference in expression between sexes. In D–F, an uppercase A or B over bars denotes a sex effect, and a lowercase x or y over brackets denotes a lake-of-origin effect. In A–C and D–F, respectively, expression measurements separated by dotted lines are proportional. L8, ribosomal protein L8 (Rpl8).

FIG. 3.
FIG. 3.

Mean (± SEM) mRNA expression of (A) NR5A1, (B) STAR, (C) CYP11A1, (D) HSD3B1, (E) CYP17A1, and (F) CYP19A1 in gonads of 13-mo-old, 30 or 33.5°C incubated alligators. Black bars represent females (F), and white bars represent males (M). Asterisks (*) denote a significant difference in expression between sexes. Expression measurements are not proportionally comparable. L8, ribosomal protein L8 (Rpl8).

FIG. 4.
FIG. 4.

Hierarchical cluster analysis of mRNA expression data from gonads of 13-mo-old Lake Woodruff alligators incubated at 30°C (vertical dotted line) or 33.5°C (vertical solid line) using Ward linkage clustering. The gray-scale, colorimetric gradient matrix displays lower expression in lighter colors and higher expressions in darker colors. Dendrograms show distance scales for individual animals in the horizontal and mRNA expressions in the vertical. Sex of individual animals is noted to the left of matrix. Horizontal lines separate numbered clusters. Vertical lines separate groups of similar gene expressions.

FIG. 5.
FIG. 5.

Hierarchical cluster analysis of mRNA expression data from gonads of 13-mo-old Lake Woodruff and Lake Apopka alligators incubated at 32°C using Ward linkage clustering. The gray-scale, colorimetric gradient matrix displays lower expressions in lighter colors and higher expressions in darker colors. Dendrograms show distance scales for individual animals in the horizontal and mRNA expressions in the vertical. Sex and lake of origin of individual animals are noted to the left of the matrix. Horizontal lines separate numbered clusters. Vertical lines separate groups of similar gene expressions.

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