Biological Sciences Division
Published October 8, 2021 | Version v1
Journal article Open

Evolutionary transcriptomics implicates new genes and pathways in human pregnancy and adverse pregnancy outcomes

Creators

  • 1. University of Chicago
  • 2. Cornell University
  • 3. University Hospitals Coventry & Warwickshire
  • 4. University at Buffalo

Description

Evolutionary changes in the anatomy and physiology of the female reproductive system underlie the origins and diversification of pregnancy in Eutherian ("Placental") mammals. This developmental and evolutionary history constrains normal physiological functions and biases the ways in which dysfunction contributes to reproductive trait diseases and adverse pregnancy outcomes. Here, we show that gene expression changes in the human endometrium during pregnancy are associated with the evolution of human-specific traits and pathologies of pregnancy. We found that hundreds of genes gained or lost endometrial expression in the human lineage. Among these are genes that may contribute to human-specific maternal-fetal communication (HTR2B) and maternal-fetal immunotolerance (PDCD1LG2) systems, as well as vascular remodeling and deep placental invasion (CORIN). These data suggest that explicit evolutionary studies of anatomical systems complement traditional methods for characterizing the genetic architecture of disease. We also anticipate our results will advance the emerging synthesis of evolution and medicine ("evolutionary medicine") and be a starting point for more sophisticated studies of the maternal-fetal interface. Furthermore, the gene expression changes we identified may contribute to the development of diagnostics and interventions for adverse pregnancy outcomes.

Data availability

All gene expression data analysed during this study are publicly available, accession numbers of given in Figure 1 - source data 1.

The following previously published data sets were used:

Roost M Svan Iperen L Ariyurek Y Buermans HP Arindrarto W Devalla HD Passier R Mummery CL Carlotti Fde Koning E Pvan Zwet EW Goeman JJ Sousa Lopes SM (2015) NCBI Gene Expression Omnibus ID GSE19373. KeyGenes, a Tool to Probe Tissue Differentiation Using a Human Fetal Transcriptional Atlas. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE66302

Mika KM Lynch VJ (2021) NCBI Gene Expression Omnibus ID GSE155170. Evolutionary transcriptomics implicates HAND2 in the origins of implantation and regulation of gestation length. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE155170

Yang Z Liu J (2012) NCBI Gene Expression Omnibus ID GSE31041. oint analysis of microRNome and 3'-UTRome in the endometrium of rhesus monkey. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE31041

Liu J (2015) NCBI Gene Expression Omnibus ID GSE76115. Identification of gene expression changes in rabbit uterus during embryo implantation. https://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/geo/query/acc.cgi?acc=GSE76115

Woods LPerez-Garcia VKieckbusch JWang XDeMayo FColucci FHembrger M (2017) NCBI Gene Expression Omnibus ID GSE98901. Decidualisation and placentation defects are a major cause of age-related reproductive decline. https://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/geo/query/acc.cgi?acc=GSE98901

Lynch VJ Nnamani MC Kapusta A Brayer K (2015) NCBI Gene Expression Omnibus ID GSE57714. Decidualisation and placentation defects are a major cause of age-related reproductive decline. https://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/geo/query/acc.cgi?acc=GSE57714

Samborski A Graf AKrebs S Kessler B Bauersachs S (2013) NCBI Gene Expression Omnibus ID GSE43667. Deep sequencing of the porcine endometrial transcriptome on day 14 of pregnancy. https://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/geo/query/acc.cgi?acc=GSE43667

National Institute of Genetics (2014) NCBI Sequence Read Archive ID DRX012238. RNA sequencing of gravid endometrium (Endometrium/Uterus) of tammar wallaby, sample ID "4432", by paired-end library. https://www.ncbi.nlm.nih.gov/sra/?term=DRX012238

The University of Sydney (2017) NCBI Sequence Read Archive ID SRX3108600. Fat-tailed dunnart uterine transcriptome. https://www.ncbi.nlm.nih.gov/sra/?term=SRX3108600

University of Sydney (2015) NCBI Sequence Read Archive ID SRX498626. Lizard 3 - uterus of the omphalo-placenta. https://www.ncbi.nlm.nih.gov/sra/?term=SRX498626

University of Sydney (2016) NCBI Sequence Read Archive ID SRX2188820. RNAseq of Lerista bougainvillii non reproductive uterus. https://www.ncbi.nlm.nih.gov/sra/?term=SRX2188820

University of Sydney (2016) NCBI BioProject ID PRJNA533161. Investigating the evolution of long egg retention and viviparity in Saiphos equalis. https://www.ncbi.nlm.nih.gov/bioproject/PRJNA533161/

China Agricultural University (2015) NCBI Sequence Read Archive ID SRX180570. Gallus gallus Oviduct Transcriptome. https://www.ncbi.nlm.nih.gov/sra/SRX180570/

Institut National de la Recherche Agronomique (2015) NCBI Sequence Read Archive ID SRR5482408. RNA-seq of Numida meleagris: adult female uterus 12 hours post-ovulation. https://www.ncbi.nlm.nih.gov/sra/?term=SRR5482408

Shi L Wang C Fuscoe JC (2014) NCBI Gene Expression Omnibus ID GSE53960. A rat RNA-Seq transcriptomic BodyMap across 11 organs and 4 developmental stages. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE53960

Adams Waldorf KM Mohan AR Young RC Ngo L Das A Tsai J Bansal A Paolella L Soorana SR Gough M Astley C Vogel K Baldessari AE Bammler TK MacDonald JW Gravett MG Rajagopal L Johnson M (2015) NCBI Gene Expression Omnibus ID GSE63274. Uterine overdistention induces preterm labor mediated by inflammation: observations in pregnant women and nonhuman primates. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE63274

USP (2015) NCBI Sequence Read Archive ID SRR1685980. cDNA obtained from mRNA extracted from cows endometrium. https://www.ncbi.nlm.nih.gov/sra/?term=SRR1685980

Chinese Academy of Sciences (2018) NCBI Sequence Read Archive ID SRR7062131. European mouflon and Finnsheep Transcriptome. https://www.ncbi.nlm.nih.gov/sra/?term=SRR7062131

Chinese National GenBank (2018) Chinese National GenBank ID CNP0000203. Evolution of viviparity: Genomic and transcriptomic investigations of the transition from egg-laying to live birth. https://db.cngb.org/search/project/CNP0000203/

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Additional details

Identifiers

DOI
10.7554/eLife.69584
Other
oai:uchicago.tind.io:9896

Funding

March of Dimes Foundation
Prematurity Research Center
Burroughs Wellcome Fund
1013760
Wellcome Trust
212233/Z/18/Z

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Human Genetics, Organismal Biology and Anatomy