Evidence map›Paper›PMID 33185661›Full record

ArticleMolecular biology and evolution2021

Evolution of Embryo Implantation Was Enabled by the Origin of Decidual Stromal Cells in Eutherian Mammals.

Arun R Chavan, Oliver W Griffith, Daniel J Stadtmauer, Jamie Maziarz, Mihaela Pavlicev, Ruth Fishman, Lee Koren, Roberto Romero, Günter P Wagner

Open access · hybridAbstract readComparative Study
In one paragraph

Article in Molecular biology and evolution, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 26 papers.

0numbers the graph read from it
0cells of the map it votes in
26citing papers in PubMed
2.0field-weighted citation impact, top 12% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

26 citing papers in PubMed, 51 citations in OpenAlex.

  1. Review
  2. Article
  3. Stepwise evolution of placental cell types.Nature ecology & evolution · 2025
    Article
  4. Article
  5. Article
  6. Article
  7. Hallmarks of uterine receptivity predate placental mammals.bioRxiv : the preprint server for biology · 2024
    Article
  8. Article
  9. Article
  10. The Role of the Endometrium in Implantation: A Modern View.International journal of molecular sciences · 2024
    Review
  11. Article
  12. Paradoxical expression of NRP1 in decidual stromal and immune cells reveals a novel inflammation balancing mechanism during early pregnancy.Inflammation research : official journal of the European Histamine Research Society ... [et al.] · 2023
    Article
  13. Human embryo implantation.Development (Cambridge, England) · 2023
    Review
  14. Review
  15. Review
  16. Article
  17. Embryonic specializations for vertebrate placentation.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2022
    Review
  18. Evolutionary divergence of embryo implantation in primates.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2022
    Review
  19. Article
  20. Co-option of stress mechanisms in the origin of evolutionary novelties.Evolution; international journal of organic evolution · 2022
    Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

9 authors at 5 institutions in 4 countries.

Arun R ChavanDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT.
Oliver W GriffithDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT.
Daniel J StadtmauerDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT.
Jamie MaziarzDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT.
Mihaela PavlicevDepartment of Evolutionary Biology, University of Vienna, Vienna, Austria.
Ruth FishmanThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.
Lee KorenThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.
Roberto RomeroPerinatology 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 Human Services, Bethesda, MD, and Detroit, MI.
Günter P WagnerDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT.
Yale University · USBar-Ilan University · ILNational Institutes of Health · USUniversity of Vienna · ATWayne State University · US

Funding

Yale Clinical and Translational Science Award (U Component)UL1TR001863 · NCATS · YALE UNIVERSITY · PI John H. Krystal, LUCILA OHNO-MACHADO · 2016 to 2026
$102.9M
Systems analysis of phenotypic switch in control of cancer invasionU54CA209992 · NCI · YALE UNIVERSITY · PI LEVCHENKO, ANDRE · 2016 to 2021
$10.1M
NCATS NIH HHS UL1 TR001863NCI NIH HHS U54 CA209992NICHD NIH HHS HHSN275201300006C
6 · The paper itself

Abstract

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.

Indexed as

Biological EvolutionEmbryo ImplantationAnimalsDeciduaEutheriaFemaleGene ExpressionInterleukin-17Models, BiologicalNeutrophil InfiltrationOpossumsRabbitsStromal CellsUterusInterleukin-17homologyinterleukin-17marsupialmucosal inflammationplacentalpregnancy

Identifiers

PMID33185661
PMCPMC7947829
OpenAlexW3100055473

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.