期刊
MOLECULAR BIOLOGY AND EVOLUTION
卷 38, 期 3, 页码 1060-1074出版社
OXFORD UNIV PRESS
DOI: 10.1093/molbev/msaa274
关键词
pregnancy; mucosal inflammation; interleukin-17; placental; marsupial; homology
资金
- John Templeton Foundation [54860, 61329]
- National Cancer Institute of the National Institutes of Health [U54-CA209992]
- Perinatology Research Branch, Division of Obstetrics and Maternal-Fetal Medicine, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and
- Federal funds from NICHD/NIH/DHHS [HHSN275201300006C]
Evolutionary mechanism of ancestral inflammatory response transformed into embryo implantation in the eutherian lineage was elucidated by comparative study of several mammalian species. Decidual stromal cells were proposed to mediate the suppression of detrimental modules in the inflammatory response. The results provide a mechanistic understanding of early stages in the evolution of eutherian pregnancy.
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.
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