Effects of phytoestrogens on growth-related and lipogenic genes in rainbow trout (Oncorhynchus mykiss)

Authors: Cleveland, Beth; MANOR, MEGHAN - Cornell University

Submitted to: Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2015
Publication Date: 4/1/2015
Citation: Cleveland, B.M., Manor, M.L. 2015. Effects of phytoestrogens on growth-related and lipogenic genes in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 170:28-37. DOI: 10.1016/j.cbpc.2015.02.001.

Interpretive Summary: Soy proteins are being incorporated into aquafeeds as a more sustainable alternative to fishmeal. However, soybeans contain compounds called phytoestrogens that can mimic estrogen. In rainbow trout, estrogen has negative effects on growth performance, therefore determining if phytoestrogens can produce similar effects will indicate if these chemicals might inhibit growth when fish consume soy-based aquafeeds. Fish were injected with estrogen and two phytoestrogens, genistein and daidzein, and the expression of genes related to growth and lipid metabolism was determined. In liver phytoestrogens regulated gene expression in a similar pattern as estrogen, and the response to genistein was dose-dependent. In muscle phytoestrogens produce gene expression patterns that differed from estrogen, suggesting these compounds regulate genes through different physiological mechanisms. In summary, these findings indicate that consumption of phytoestrogens as part of soy-based diets may affect growth performance and nutrient retention in rainbow trout.

Technical Abstract: The objective of the current study was to determine whether estradiol (E2) or the primary soy phytoestrogens genistein and daidzein regulate expression of growth-related and lipogenic genes in rainbow trout. Juvenile rainbow trout (5 mon, 65.8 ± 1.8 g) received intraperitoneal injections of E2, genistein, or daidzein (5 µg/g body weight) or a higher dose of genistein (50 µg/g body weight). Liver and white muscle were harvested 24 hr post-injection and analyzed for gene expression. In liver, expression of vitellogenin (vtg) and estrogen receptor alpha (era1) increased in all treatments compared to a vehicle treated control in a manner that reflected treatment estrogenicity (E2 > genistein (50 µg/g) > genistein (5 µg/g) = daidzein (5 µg/g)). Estradiol and genistein (50 g/g) reduced components of the growth hormone (GH)/insulin-like growth factor (IGF) axis in liver, including increased expression of IGF binding protein-2b1 (igfbp2b1) and reduced igfbp5b1. Also in liver E2 and genistein (50 g/g) affected expression of components of the transforming growth factor beta signaling mechanism, reduced expression of ppar and rxr transcription factors, and increased expression of fatty acid synthesis genes srebp1, acly, fas, scd1, and gpat and lipid binding proteins fabp3 and lpl. In muscle E2 and genistein (50 g/g) increased era1 and erb1 expression and decreased erb2 expression. Other genes responded to phytoestrogens in a manner that suggested regulation by estrogen receptor-independent mechanisms, including increased ghr2, igfbp2a, igfbp4, and igfbp5b1. Expression of muscle regulatory factors pax7 and myod were increased by E2 and genistein. Genistein also reduced myog expression. Collectively, these data indicate genistein and daidzein, at exposure levels comparable to dietary intake, affect expression of genes in rainbow trout that regulate physiological mechanisms central to growth and nutrient retention. Effects of phytoestrogens and E2 were similar in liver and support phytoestrogen activation of estrogen receptors and the redirection of nutrients away from muscle growth. Expression patterns in muscle tissue suggest that phytoestrogens affect growth-related mechanisms partially through estrogen-independent mechanisms.