Endocrine activity of extraembryonic membranes extends beyond placental amniotes

• Published in: PloS one Vol. 4; no. 5; p. e5452
• Main Authors: Albergotti, Lori C, Hamlin, Heather J, McCoy, Michael W, Guillette, Jr, Louis J
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 08-05-2009; Public Library of Science (PLoS)
• Subjects: Animals; Biochemistry; Biological evolution; Biology; Biosynthesis; Birds; Chickens - metabolism; Cholesterol; Chorioallantoic membrane; Chorioallantoic Membrane - metabolism; Cytochrome; Dehydrogenases; Developmental Biology; Diabetes and Endocrinology/Reproductive Endocrinology; Egg laying; Embryogenesis; Embryonic development; Embryonic growth stage; Endocrine System - metabolism; Enzymes; Estrogen Receptor alpha - genetics; Estrogen Receptor alpha - metabolism; Evolutionary Biology/Developmental Evolution; Female; Gene expression; Gene Expression Regulation, Developmental; Genomes; Historical account; Hormones; Innovations; Mammals; Membranes; Metabolic wastes; Nutrients; Physiology; Physiology/Endocrinology; Physiology/Reproductive Physiology; Placenta; Placenta - metabolism; Polymerase chain reaction; Pregnancy; Pregnenolone; Progesterone; Progesterone - biosynthesis; Protein Isoforms - genetics; Protein Isoforms - metabolism; Protein Transport; Proteins; Receptors, Progesterone - genetics; Receptors, Progesterone - metabolism; Reptiles; RNA; RNA, Messenger - genetics; RNA, Messenger - metabolism; Signal Transduction; Steroidogenesis; Structure-function relationships; Synthesis; Tissues; Toads; Uterus; Water exchange; Florida
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0005452

During development, all amniotes (mammals, reptiles, and birds) form extraembryonic membranes, which regulate gas and water exchange, remove metabolic wastes, provide shock absorption, and transfer maternally derived nutrients. In viviparous (live-bearing) amniotes, both extraembryonic membranes and maternal uterine tissues contribute to the placenta, an endocrine organ that synthesizes, transports, and metabolizes hormones essential for development. Historically, endocrine properties of the placenta have been viewed as an innovation of placental amniotes. However, an endocrine role of extraembryonic membranes has not been investigated in oviparous (egg-laying) amniotes despite similarities in their basic structure, function, and shared evolutionary ancestry. In this study, we ask whether the oviparous chorioallantoic membrane (CAM) of chicken (Gallus gallus) has the capability to synthesize and receive signaling of progesterone, a major placental steroid hormone.
We quantified mRNA expression of key steroidogenic enzymes involved in progesterone synthesis and found that 3beta-hydroxysteroid dehydrogenase, which converts pregnenolone to progesterone exhibited a 464 fold increase in the CAM from day 8 to day 18 of embryonic development (F(5, 68) = 89.282, p<0.0001). To further investigate progesterone synthesis, we performed explant culture and found that the CAM synthesizes progesterone in vitro in the presence of a steroid precursor. Finally, we quantified mRNA expression and performed protein immunolocalization of the progesterone receptor in the CAM.
Collectively, our data indicate that the chick CAM is steroidogenic and has the capability to both synthesize progesterone and receive progesterone signaling. These findings represent a paradigm shift in evolutionary reproductive biology by suggesting that endocrine activity of extraembryonic membranes is not a novel characteristic of placental amniotes. Rather, we hypothesize that these membranes may share an additional unifying characteristic, steroidogenesis, across amniotes at large.