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Louis J Guillette - One of the best experts on this subject based on the ideXlab platform.
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Endocrine Activity of Extraembryonic Membranes Extends beyond Placental Amniotes
2016Co-Authors: Lori Cruze, Louis J Guillette, Heather J Hamlin, Lori C. Albergotti, Michael W. MccoyAbstract:Background: 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. Methodology/Principal Findings: We quantified mRNA expression of key steroidogenic enzymes involved in progesterone synthesis and found that 3b-hydroxysteroid dehydrogenase, which converts pregnenolone to progesterone exhibited a 464 fold increase in the CAM from day 8 to day 18 of embryonic development (F5, 68 = 89.282, p,0.0001). To further investigat
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Towards an Understanding of the Evolution of the Chorioallantoic Placenta: Steroid Biosynthesis and Steroid Hormone Signaling in the Chorioallantoic Membrane of an
2016Co-Authors: Oviparous Reptile, Michael W. Mccoy, Lori Cruze, Satomi Kohno, Louis J GuilletteAbstract:Amniotes, mammals, reptiles, and birds form common Extraembryonic Membranes during development to perform essential functions, such as protection, nutrient transfer, gas exchange, and waste removal. Together with the maternal uterus, Extraembryonic Membranes of viviparous (live-bearing) amniotes develop as an endocrine placenta that synthesizes and responds to steroid hormones critical for development. The ability of these Membranes to synthesize and respond to steroid hormone signaling has traditionally been considered an innova-tion of placental amniotes. However, our laboratory recently demonstrated that this ability extends to the chorioallantoic membrane (CAM) of an oviparous (egg-laying) amniote, the domestic chicken, and we hypothesized that steroidogenic Extraembryonic Membranes could be an evolutionarily con
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Short Title: Steroids and the Alligator CAM
2016Co-Authors: Oviparous Reptile, Michael W. Mccoy, Lori Cruze, Satomi Kohno, Louis J GuilletteAbstract:Summary sentence: The alligator chorioallantoic membrane has the capability to perform steroid biosynthesis and respond to steroid hormone signaling, providing further evidence that steroidogenic Extraembryonic Membranes are a shared characteristic of amniotes
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Endocrine Activity of Extraembryonic Membranes Extends beyond Placental Amniotes
2016Co-Authors: Lori C. Albergotti, Heather J Hamlin, Michael W. Mccoy, Louis J GuilletteAbstract:Background: 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. Methodology/Principal Findings: We quantified mRNA expression of key steroidogenic enzymes involved in progesterone synthesis and found that 3b-hydroxysteroid dehydrogenase, which converts pregnenolone to progesterone exhibited a 464 fold increase in the CAM from day 8 to day 18 of embryonic development (F5, 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 th
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Alterations in eicosanoid composition during embryonic development in the chorioallantoic membrane of the American alligator (Alligator mississippiensis) and domestic chicken (Gallus gallus).
General and comparative endocrinology, 2016Co-Authors: Theresa M. Cantu, John A. Bowden, Jacob Scott, Jimena B. Pérez-viscasillas, Kevin M. Huncik, Matthew P. Guillette, Louis J GuilletteAbstract:Eicosanoids are signaling lipids known to regulate several physiological processes in the mammalian placenta, including the initiation of parturition. Though all amniotes construct similar Extraembryonic Membranes during development, the composition and function of eicosanoids in Extraembryonic Membranes of oviparous reptiles is largely unknown. The majority of effort placed in eicosanoid investigations is typically targeted toward defining the role of specific compounds in disease etiology; however, comprehensive characterization of several pathways in eicosanoid synthesis during development is also needed to better understand the complex role of these lipids in comparative species. To this end, we have examined the chorioallantoic membrane (CAM) of the American alligator (Alligator mississippiensis) and domestic chicken (Gallus gallus) during development. Previously, our lab has demonstrated that the CAM of several oviparous species shared conserved steroidogenic activity, a feature originally attributed to mammalian amniotes. To further explore this, we have developed a liquid chromatography/tandem mass spectrometry method that is used here to quantify multiple eicosanoids in the CAM of two oviparous species at different stages of development. We identified 18 eicosanoids in the alligator CAM; the cyclooxygenase (COX) pathway showed the largest increase from early development to later development in the alligator CAM. Similarly, the chicken CAM had an increase in COX products and COX activity, which supports the LC-MS/MS analyses. Jointly, our findings indicate that the CAM tissue of an oviparous species is capable of eicosanoid synthesis, which expands our knowledge of placental evolution and introduces the possibility of future comparative models of placental function.
Tom W. Ecay - One of the best experts on this subject based on the ideXlab platform.
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Expression of calcium transport proteins in the Extraembryonic Membranes of a viviparous snake, Virginia striatula.
Journal of experimental zoology. Part B Molecular and developmental evolution, 2012Co-Authors: Santiago P. Fregoso, James R. Stewart, Tom W. EcayAbstract:Yolk is the primary source of calcium for embryonic growth and development for most squamates, irrespective of mode of parity. The calcified eggshell is a secondary source for embryonic calcium in all oviparous eggs, but this structure is lost in viviparous lineages. Virginia striatula is a viviparous snake in which embryos obtain calcium from both yolk and placental transport of uterine calcium secretions. The developmental pattern of embryonic calcium acquisition in V. striatula is similar to that for oviparous snakes. Calbindin-D(28K) is a marker for epithelial calcium transport activity and plasma membrane Ca(2+)-ATPase (PMCA) provides the energy to catalyze the final step in calcium transport. Expression of calbindin-D(28K) and PMCA was measured by immunoblotting in yolk sac splanchnopleure and chorioallantois of a developmental series of V. striatula to test the hypothesis that these proteins mediate calcium transport to embryos. In addition, we compared the expression of calbindin-D(28K) in Extraembryonic Membranes of V. striatula throughout development to a previously published expression pattern in an oviparous snake to test the hypothesis that the ontogeny of calcium transport function is independent of reproductive mode. Expression of calbindin-D(28K) increased in yolk sac splanchnopleure and chorioallantois coincident with calcium mobilization from yolk and uterine sources and with embryonic growth. The amount of PMCA in the chorioallantois did not change through development suggesting its expression is not rate limiting for calcium transport. The pattern of expression of calbindin-D(28K) and PMCA confirms our initial hypothesis that these proteins mediate embryonic calcium uptake. In addition, the developmental pattern of calbindin-D(28K) expression in V. striatula is similar to that of an oviparous snake, which suggests that calcium transport mechanisms and their regulation are independent of reproductive mode.
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Placental development and expression of calcium transporting proteins in the Extraembryonic Membranes of a placentotrophic lizard
Journal of morphology, 2011Co-Authors: Haley K. Stinnett, James R. Stewart, Tom W. Ecay, Rebecca A. Pyles, Jacquie F. Herbert, Michael B. ThompsonAbstract:Pseudemoia pagenstecheri is a viviparous Australian scincid lizard in which the maternal–embryonic placental interface is differentiated into structurally distinct regions. The chorioallantoic placenta contains an elliptical-shaped region, the placentome, characterized by hypertrophied uterine and embryonic epithelial cells supported by dense vascular networks. The remainder of the chorioallantoic placenta, the paraplacentome, is also highly vascularized but uterine and chorionic epithelia are thin. An omphaloplacenta with hypertrophied epithelia is located in the abembryonic hemisphere of the egg. There is extensive placental transport of organic and inorganic nutrients, e.g., 85–90% of neonatal calcium is received via placental transfer. Calcium uptake by Extraembryonic Membranes of squamates correlates with expression of the intracellular calcium binding protein, calbindin-D28K, and plasma membrane calcium ATPase (PMCA) is a marker for active calcium transport. We estimated expression of calbindin-D28K and PMCA in the chorioallantoic membrane in a developmental series of embryos using immunoblotting and used immunohistochemistry to define the cellular localization of calbindin-D28K to test the hypotheses that 1) expression of calcium transporting proteins is coincident with placental transport of calcium and 2) the placenta is functionally specialized for calcium transport in regions of structural differentiation. Calbindin-D28K and PMCA were detected at low levels in early stages of development and increased significantly prior to birth, when embryonic calcium uptake peaks. These data support the hypothesis that placental calcium secretion occurs over an extended interval of gestation, with increasing activity as embryonic demand escalates in late development. In addition, calbindin-D28K expression is localized in chorionic epithelial cells of the placentome and in the epithelium of the omphalopleure of the omphaloplacenta, which supports the hypothesis that regional structural differentiation in the placenta reflects functional specializations for calcium transport. J. Morphol. 2012. © 2011 Wiley Periodicals, Inc.
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Developmental expression of calcium transport proteins in Extraembryonic Membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae)
Journal of Experimental Biology, 2011Co-Authors: J. R. Stewart, Santiago P. Fregoso, Tom W. Ecay, B. Heulin, B. J. LinvilleAbstract:The eggshell of oviparous lizards is a significant source of calcium for embryos, whereas the eggshell of viviparous lizards, when present, contains little calcium. In view of the potential cost to embryonic nutrition occasioned by the loss of eggshell calcium, the large number of independent origins of viviparity among lizards is surprising. Concomitant evolution of viviparity and calcium placentotrophy would ameliorate the loss of eggshell calcium, but a mechanism linking these events has yet to be discovered. Zootoca vivipara, a lizard with geographic variation in its mode of parity, is an excellent model for studying mechanisms of calcium transport to oviparous and viviparous embryos because each is highly dependent on calcium secreted by the uterus (eggshell or placenta) and ontogenetic patterns of embryonic calcium mobilization are similar. We compared developmental expression of the calcium transport protein calbindin-D28K in yolk splanchnopleure and chorioallantoic Membranes of oviparous and viviparous embryos to test the hypothesis that the mechanism of calcium transport does not differ between modes of parity. We found that the ontogenetic pattern of protein expression is similar between reproductive modes and is correlated with calciumuptake from yolk and either eggshell or placenta. Calbindin-D28K is localized in the chorionic epithelium of embryos of both reproductive modes. These findings suggest that the embryonic calcium transport machinery is conserved in the transition between reproductive modes and that an adaptation of oviparous embryos for calcium uptake from eggshells functions similarly to transport calcium directly from uterine secretions.
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expression of calbindin d28k by yolk sac and chorioallantoic Membranes of the corn snake elaphe guttata
Journal of Experimental Zoology, 2004Co-Authors: Tom W. Ecay, James R. Stewart, Daniel G. BlackburnAbstract:The yolk splanchnopleure and chorioallantoic membrane of oviparous reptiles transport calcium from the yolk and eggshell to the developing embryo. Among oviparous amniotes, the mechanism of calcium mobilization to embryos has been studied only in domestic fowl, in which the mechanism of calcium transport of the yolk splanchnopleure differs from the chorioallantoic membrane. Transport of calcium is facilitated by calbindin-D28K in endodermal cells of the yolk splanchnopleure of chickens but the chorioallantoic membrane does not express calbindin-D28K. We used immunoblotting to assay for calbindin-D28K expression in yolk splanchnopleure and chorioallantoic membrane of the corn snake, Elaphe guttata, to test the hypothesis that the mechanism of calcium transport by Extraembryonic Membranes of snakes is similar to birds. High calbindin-D28K expression was detected in samples of yolk splanchnopleure and chorioallantoic membrane during late embryonic stages. We conclude that calbindin-D28K is expressed in these Extraembryonic Membranes to facilitate transport of calcium and that the mechanism of calcium transport of the chorioallantoic membrane of the corn snake differs from that of the chicken. Further, we conclude that calbindin-D28K expression is developmentally regulated and increases during later embryonic stages in the corn snake. J. Exp. Zool. (Mol. Dev. Evol.) 302B:000–000, 2004. © 2004 Wiley-Liss, Inc.
Thomas E Spencer - One of the best experts on this subject based on the ideXlab platform.
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Progesterone and placental hormone actions on the uterus: Insights from domestic animals
2016Co-Authors: Thomas E Spencer, Greg A. Johnson, Robert C. Burghardt, Fuller W. BazerAbstract:Progesterone is unequivocally required for maternal support of conceptus (embryo/fetus and associated Extraembryonic Membranes) survival and development. In cyclic sheep, proges-terone is paradoxically involved in suppressing and then initi-ating development of the endometrial luteolytic mechanism. In cyclic and pregnant sheep, progesterone negatively autoregu-lates progesterone receptor (PR) gene expression in the endo-metrial luminal (LE) and superficial glandular epithelium (GE). In cyclic sheep, PR loss is closely followed by increases in epi-thelial estrogen receptor (ERa) and then oxytocin receptor (OTR), allowing oxytocin to induce uterine release of luteolytic prostaglandin F2a pulses. In pregnant sheep, the conceptus pro-duces interferon tau (IFNt) that acts on the endometrium to inhibit transcription of the ERa gene and thus development o
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Endogenous retroviruses in trophoblast differentiation and placental development.
American Journal of Reproductive Immunology, 2010Co-Authors: Sarah G. Black, Fredrick Arnaud, Massimo Palmarini, Thomas E SpencerAbstract:Endogenous retroviruses (ERVs) are present in the genome of all vertebrates and originated from infections of the germline of the host by exogenous retroviruses. ERVs have coevolved with their hosts for millions of years and are recognized to contribute to genome plasticity, protect the host against infection of related pathogenic and exogenous retroviruses, and play a vital role in development of the placenta. Consequently, some ERVs have been positively selected and maintained in the host genome throughout evolution. This review will focus on the critical role of ERVs in development of the mammalian placenta and specifically highlight the biological role of sheep JSRV-related endogenous betaretroviruses in conceptus (embryo and associated Extraembryonic Membranes) development.
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Endogenous retroviruses in trophoblast differentiation and placental development.
American Journal of Reproductive Immunology, 2010Co-Authors: Sarah G. Black, Fredrick Arnaud, Massimo Palmarini, Thomas E SpencerAbstract:Endogenous retroviruses (ERVs) are present in the genome of all vertebrates and originated from infections of the germline of the host by exogenous retroviruses. ERVs have coevolved with their hosts for millions of years and are recognized to contribute to genome plasticity, protect the host against infection of related pathogenic and exogenous retroviruses, and play a vital role in development of the placenta. Consequently, some ERVs have been positively selected and maintained in the host genome throughout evolution. This review will focus on the critical role of ERVs in development of the mammalian placenta and specifically highlight the biological role of sheep JSRV-related endogenous betaretroviruses in conceptus (embryo and associated Extraembryonic Membranes) development.
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Progesterone and Placental Hormone Actions on the Uterus: Insights from Domestic Animals
Biology of Reproduction, 2004Co-Authors: Thomas E Spencer, Greg A. Johnson, Robert C. Burghardt, Fuller W. BazerAbstract:Abstract Progesterone is unequivocally required for maternal support of conceptus (embryo/fetus and associated Extraembryonic Membranes) survival and development. In cyclic sheep, progesterone is paradoxically involved in suppressing and then initiating development of the endometrial luteolytic mechanism. In cyclic and pregnant sheep, progesterone negatively autoregulates progesterone receptor (PR) gene expression in the endometrial luminal (LE) and superficial glandular epithelium (GE). In cyclic sheep, PR loss is closely followed by increases in epithelial estrogen receptor (ERα) and then oxytocin receptor (OTR), allowing oxytocin to induce uterine release of luteolytic prostaglandin F2α pulses. In pregnant sheep, the conceptus produces interferon tau (IFNτ) that acts on the endometrium to inhibit transcription of the ERα gene and thus development of the endometrial luteolytic mechanism. After Day 13 of pregnancy, the endometrial epithelia do not express the PR, whereas the stroma and myometrium remain ...
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Trophoblast biology: Forum introduction
Reproductive Biology and Endocrinology, 2004Co-Authors: Thomas E Spencer, Fuller W. BazerAbstract:In mammals, a carefully orchestrated dialogue between the mother and conceptus (embryo/fetus and associate Extraembryonic Membranes) is initiated during the peri-implantation period of pregnancy as the trophoblast develops, functions to signal pregnancy recognition, and initiates implantation. The purpose of this Forum is to highlight comparative aspects of trophoblast morphogenesis and function in mammals.
Santiago P. Fregoso - One of the best experts on this subject based on the ideXlab platform.
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Expression of calcium transport proteins in the Extraembryonic Membranes of a viviparous snake, Virginia striatula.
Journal of experimental zoology. Part B Molecular and developmental evolution, 2012Co-Authors: Santiago P. Fregoso, James R. Stewart, Tom W. EcayAbstract:Yolk is the primary source of calcium for embryonic growth and development for most squamates, irrespective of mode of parity. The calcified eggshell is a secondary source for embryonic calcium in all oviparous eggs, but this structure is lost in viviparous lineages. Virginia striatula is a viviparous snake in which embryos obtain calcium from both yolk and placental transport of uterine calcium secretions. The developmental pattern of embryonic calcium acquisition in V. striatula is similar to that for oviparous snakes. Calbindin-D(28K) is a marker for epithelial calcium transport activity and plasma membrane Ca(2+)-ATPase (PMCA) provides the energy to catalyze the final step in calcium transport. Expression of calbindin-D(28K) and PMCA was measured by immunoblotting in yolk sac splanchnopleure and chorioallantois of a developmental series of V. striatula to test the hypothesis that these proteins mediate calcium transport to embryos. In addition, we compared the expression of calbindin-D(28K) in Extraembryonic Membranes of V. striatula throughout development to a previously published expression pattern in an oviparous snake to test the hypothesis that the ontogeny of calcium transport function is independent of reproductive mode. Expression of calbindin-D(28K) increased in yolk sac splanchnopleure and chorioallantois coincident with calcium mobilization from yolk and uterine sources and with embryonic growth. The amount of PMCA in the chorioallantois did not change through development suggesting its expression is not rate limiting for calcium transport. The pattern of expression of calbindin-D(28K) and PMCA confirms our initial hypothesis that these proteins mediate embryonic calcium uptake. In addition, the developmental pattern of calbindin-D(28K) expression in V. striatula is similar to that of an oviparous snake, which suggests that calcium transport mechanisms and their regulation are independent of reproductive mode.
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Developmental expression of calcium transport proteins in Extraembryonic Membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae)
Journal of Experimental Biology, 2011Co-Authors: J. R. Stewart, Santiago P. Fregoso, Tom W. Ecay, B. Heulin, B. J. LinvilleAbstract:The eggshell of oviparous lizards is a significant source of calcium for embryos, whereas the eggshell of viviparous lizards, when present, contains little calcium. In view of the potential cost to embryonic nutrition occasioned by the loss of eggshell calcium, the large number of independent origins of viviparity among lizards is surprising. Concomitant evolution of viviparity and calcium placentotrophy would ameliorate the loss of eggshell calcium, but a mechanism linking these events has yet to be discovered. Zootoca vivipara, a lizard with geographic variation in its mode of parity, is an excellent model for studying mechanisms of calcium transport to oviparous and viviparous embryos because each is highly dependent on calcium secreted by the uterus (eggshell or placenta) and ontogenetic patterns of embryonic calcium mobilization are similar. We compared developmental expression of the calcium transport protein calbindin-D28K in yolk splanchnopleure and chorioallantoic Membranes of oviparous and viviparous embryos to test the hypothesis that the mechanism of calcium transport does not differ between modes of parity. We found that the ontogenetic pattern of protein expression is similar between reproductive modes and is correlated with calciumuptake from yolk and either eggshell or placenta. Calbindin-D28K is localized in the chorionic epithelium of embryos of both reproductive modes. These findings suggest that the embryonic calcium transport machinery is conserved in the transition between reproductive modes and that an adaptation of oviparous embryos for calcium uptake from eggshells functions similarly to transport calcium directly from uterine secretions.
Lori Cruze - One of the best experts on this subject based on the ideXlab platform.
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Endocrine Activity of Extraembryonic Membranes Extends beyond Placental Amniotes
2016Co-Authors: Lori Cruze, Louis J Guillette, Heather J Hamlin, Lori C. Albergotti, Michael W. MccoyAbstract:Background: 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. Methodology/Principal Findings: We quantified mRNA expression of key steroidogenic enzymes involved in progesterone synthesis and found that 3b-hydroxysteroid dehydrogenase, which converts pregnenolone to progesterone exhibited a 464 fold increase in the CAM from day 8 to day 18 of embryonic development (F5, 68 = 89.282, p,0.0001). To further investigat
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Towards an Understanding of the Evolution of the Chorioallantoic Placenta: Steroid Biosynthesis and Steroid Hormone Signaling in the Chorioallantoic Membrane of an
2016Co-Authors: Oviparous Reptile, Michael W. Mccoy, Lori Cruze, Satomi Kohno, Louis J GuilletteAbstract:Amniotes, mammals, reptiles, and birds form common Extraembryonic Membranes during development to perform essential functions, such as protection, nutrient transfer, gas exchange, and waste removal. Together with the maternal uterus, Extraembryonic Membranes of viviparous (live-bearing) amniotes develop as an endocrine placenta that synthesizes and responds to steroid hormones critical for development. The ability of these Membranes to synthesize and respond to steroid hormone signaling has traditionally been considered an innova-tion of placental amniotes. However, our laboratory recently demonstrated that this ability extends to the chorioallantoic membrane (CAM) of an oviparous (egg-laying) amniote, the domestic chicken, and we hypothesized that steroidogenic Extraembryonic Membranes could be an evolutionarily con
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Short Title: Steroids and the Alligator CAM
2016Co-Authors: Oviparous Reptile, Michael W. Mccoy, Lori Cruze, Satomi Kohno, Louis J GuilletteAbstract:Summary sentence: The alligator chorioallantoic membrane has the capability to perform steroid biosynthesis and respond to steroid hormone signaling, providing further evidence that steroidogenic Extraembryonic Membranes are a shared characteristic of amniotes
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Evidence of steroid hormone activity in the chorioallantoic membrane of a Turtle (Pseudemys nelsoni).
General and comparative endocrinology, 2013Co-Authors: Lori Cruze, Heather J Hamlin, Michael W. Mccoy, Satomi Kohno, Louis J GuilletteAbstract:Endocrine properties of Extraembryonic Membranes have traditionally been viewed as a characteristic of placental amniotes. However, our laboratory recently demonstrated that this ability extends to the Extraembryonic Membranes of two oviparous amniotes (chicken and alligator) indicating that endocrine Extraembryonic Membranes are not an innovation of placental amniotes and suggesting that this could be a shared amniote characteristic. In this study, we test our hypothesis that the chorioallantoic membrane (CAM) obtained from non-archosaurian obligate oviparous amniotes such as turtles, have the potential for steroid hormone activity. To investigate synthesis of a major placental hormone, we performed explant culture and found that the turtle CAM synthesizes progesterone in vitro in the presence of a steroid precursor. In addition, to examine whether the CAM has the ability to respond to steroid signaling, we quantified mRNA expression of the progesterone, androgen, and two estrogen receptors. Finally, to determine if steroid receptor mRNA is translated to protein, we performed immunolocalization of the progesterone receptor. Our data demonstrate that the turtle CAM exhibits steroid synthesis and has steroid hormone signaling capabilities. To that end, steroid hormone activity has now been demonstrated in the CAMs of three oviparous species that represent three independent lineages within oviparous Reptilia that have never exhibited viviparity; thus these data support our hypothesis that endocrine activity of Extraembryonic Membranes is a conserved trait of Amniota.
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towards an understanding of the evolution of the chorioallantoic placenta steroid biosynthesis and steroid hormone signaling in the chorioallantoic membrane of an oviparous reptile
Biology of Reproduction, 2012Co-Authors: Louis J Guillette, Lori Cruze, Michael W. Mccoy, Satomi KohnoAbstract:Amniotes, mammals, reptiles, and birds form common Extraembryonic Membranes during development to perform essential functions, such as protection, nutrient transfer, gas exchange, and waste removal. Together with the maternal uterus, Extraembryonic Membranes of viviparous (live-bearing) amniotes develop as an endocrine placenta that synthesizes and responds to steroid hormones critical for development. The ability of these Membranes to synthesize and respond to steroid hormone signaling has traditionally been considered an innovation of placental amniotes. However, our laboratory recently demonstrated that this ability extends to the chorioallantoic membrane (CAM) of an oviparous (egg-laying) amniote, the domestic chicken, and we hypothesized that steroidogenic Extraembryonic Membranes could be an evolutionarily conserved characteristic of all amniotes because of similarities in basic structure, function, and shared evolutionary ancestry. In this study, we examined steroid hormone synthesis and signaling in the CAM of another oviparous amniote, the American alligator (Alligator mississippiensis). We quantified mRNA expression of a steroidogenic factor involved in the regulation of steroidogenesis (NR5A1), the key steroidogenic enzymes involved in the synthesis of progestins (HSD3B1), androgens (CYP17A1), and estrogens (CYP19A1), and the receptors involved in the signaling of progestins (PR), androgens (AR), estrogens (ESR1 and ESR2), and glucocorticoids (GR). Furthermore, we performed protein immunolocalization for PR and ESR1. Collectively, our findings indicate that the alligator CAM has the capability to regulate, synthesize, and respond to steroid hormone signaling, thus, supporting our hypothesis that the Extraembryonic Membranes of Amniota share a unifying characteristic, that is, the ability to synthesize and respond to steroid hormones.
