TY - JOUR
T1 - Evolution of Embryo Implantation Was Enabled by the Origin of Decidual Stromal Cells in Eutherian Mammals
AU - Chavan, Arun R.
AU - Griffith, Oliver W.
AU - Stadtmauer, Daniel J.
AU - Maziarz, Jamie
AU - Pavlicev, Mihaela
AU - Fishman, Ruth
AU - Koren, Lee
AU - Romero, Roberto
AU - Wagner, Günter P.
AU - Chavan, Arun R.
AU - Wagner, Günter P.
N1 - Publisher Copyright: © 2020 Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution 2020.
PY - 2021/3/9
Y1 - 2021/3/9
N2 - Mammalian pregnancy evolved in the therian stem lineage, that is, before the common ancestor of marsupials and eutherian (placental) mammals. Ancestral therian pregnancy likely involved a brief phase of attachment between the fetal and maternal tissues followed by parturition - similar to the situation in most marsupials including the opossum. In all eutherians, however, embryo attachment is followed by implantation, allowing for a stable fetal-maternal interface and an extended gestation. Embryo attachment induces an attachment reaction in the uterus that is homologous to an inflammatory response. Here, we elucidate the evolutionary mechanism by which the ancestral inflammatory response was transformed into embryo implantation in the eutherian lineage. We performed a comparative uterine transcriptomic and immunohistochemical study of three eutherians, armadillo (Dasypus novemcinctus), hyrax (Procavia capensis), and rabbit (Oryctolagus cuniculus); and one marsupial, opossum (Monodelphis domestica). Our results suggest that in the eutherian lineage, the ancestral inflammatory response was domesticated by suppressing one of its modules detrimental to pregnancy, namely, neutrophil recruitment by cytokine IL17A. Further, we propose that this suppression was mediated by decidual stromal cells, a novel cell type in eutherian mammals. We tested a prediction of this model in vitro and showed that decidual stromal cells can suppress the production of IL17A from helper T cells. Together, these results provide a mechanistic understanding of early stages in the evolution of eutherian pregnancy.
AB - Mammalian pregnancy evolved in the therian stem lineage, that is, before the common ancestor of marsupials and eutherian (placental) mammals. Ancestral therian pregnancy likely involved a brief phase of attachment between the fetal and maternal tissues followed by parturition - similar to the situation in most marsupials including the opossum. In all eutherians, however, embryo attachment is followed by implantation, allowing for a stable fetal-maternal interface and an extended gestation. Embryo attachment induces an attachment reaction in the uterus that is homologous to an inflammatory response. Here, we elucidate the evolutionary mechanism by which the ancestral inflammatory response was transformed into embryo implantation in the eutherian lineage. We performed a comparative uterine transcriptomic and immunohistochemical study of three eutherians, armadillo (Dasypus novemcinctus), hyrax (Procavia capensis), and rabbit (Oryctolagus cuniculus); and one marsupial, opossum (Monodelphis domestica). Our results suggest that in the eutherian lineage, the ancestral inflammatory response was domesticated by suppressing one of its modules detrimental to pregnancy, namely, neutrophil recruitment by cytokine IL17A. Further, we propose that this suppression was mediated by decidual stromal cells, a novel cell type in eutherian mammals. We tested a prediction of this model in vitro and showed that decidual stromal cells can suppress the production of IL17A from helper T cells. Together, these results provide a mechanistic understanding of early stages in the evolution of eutherian pregnancy.
KW - homology
KW - interleukin-17
KW - marsupial
KW - mucosal inflammation
KW - placental
KW - pregnancy
UR - http://www.scopus.com/inward/record.url?scp=85099381029&partnerID=8YFLogxK
U2 - https://doi.org/10.1093/molbev/msaa274
DO - https://doi.org/10.1093/molbev/msaa274
M3 - مقالة
C2 - 33185661
SN - 0737-4038
VL - 38
SP - 1060
EP - 1074
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 3
ER -