REPRODUCTION
© 2017 Society for Reproduction and Fertility DOI: 10.1530/REP-17-0092
ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org
RESEARCH
High-throughput mRNA sequencing of stromal cells from
endometriomas and endometrium
Kadri Rekker
1,2
, Merli Saare
1,2
, Elo Eriste
2
, Tõnis Tasa
3,4
, Viktorija Kukuškina
4,5
, Anne Mari Roost
2
,
Kristi Anderson
2
, Külli Samuel
2
, Helle Karro
1,6
, Andres Salumets
1,2,7,8
and Maire Peters
1,2
1
Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tartu, Tartu, Estonia,
2
Competence Centre on Health Technologies, Tartu, Estonia,
3
Institute of Computer Science, University of Tartu,
Tartu, Estonia,
4
Estonian Genome Center, University of Tartu, Tartu, Estonia,
5
Institute of Molecular and Cell Biology,
University of Tartu, Tartu, Estonia,
6
Tartu University Hospital’s Women’s Clinic, Tartu, Estonia,
7
Department of
Biomedicine, Institute of Biomedicine and Translational Medicine, University of Tartu, Tartu, Estonia and
8
Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Hospital,
Helsinki, Finland
Correspondence should be addressed to K Rekker; Email: kadri.rekker@gmail.com
Abstract
The aetiology of endometriosis is still unclear and to fnd mechanisms behind the disease development, it is important to study each
cell type from endometrium and ectopic lesions independently. The objective of this study was to uncover complete mRNA profles in
uncultured stromal cells from paired samples of endometriomas and eutopic endometrium. High-throughput mRNA sequencing
revealed over 1300 dysregulated genes in stromal cells from ectopic lesions, including several novel genes in the context of
endometriosis. Functional annotation analysis of differentially expressed genes highlighted pathways related to cell adhesion,
extracellular matrix–receptor interaction and complement and coagulation cascade. Most importantly, we found a simultaneous
upregulation of complement system components and inhibitors, indicating major imbalances in complement regulation in ectopic
stromal cells. We also performed in vitro experiments to evaluate the effect of endometriosis patients’ peritoneal fuid (PF) on
complement system gene expression levels, but no signifcant impact of PF on C3, CD55 and CFH levels was observed. In conclusion,
the use of isolated stromal cells enables to determine gene expression levels without the background interference of other cell types.
In the future, a new standard design studying all cell types from endometriotic lesions separately should be applied to reveal novel
mechanisms behind endometriosis pathogenesis.
Reproduction (2017) 154 93–100
Introduction
Endometrial tissue outside the uterine cavity can
form lesions on ovaries and other peritoneal organs,
resulting in endometriosis. As the molecular aetiology
of endometriosis is still unclear, it is important to detect
gene expression alterations in endometriotic lesions
and eutopic endometrium of endometriosis patients.
Three major types of endometriotic lesions are known,
peritoneal lesions, ovarian endometriomas and deep
infltrating lesions (Nisolle & Donnez 1997), that are
distinct clinical entities with unique histopathogeneses
accompanied by specifc expression profles, depending
on the anatomical location of lesions (Meola et al. 2010,
Ballester et al. 2012, Filippi et al. 2016). Therefore, it
seems reasonable to study endometriomas and lesions
from other locations separately.
Several transcriptomic studies have been conducted
to fnd molecular alterations in endometrial cells
lining the inner surface of endometriomas (reviewed
in Sanchez et al. 2015). However, despite hundreds
to thousands of genes and specifc pathways that have
been revealed in these studies, the results remain
inconclusive and no common molecular markers or
pathways linked to endometriosis have been described.
The most probable reason for these discordances could
be the tissue heterogeneity of whole-lesion biopsies,
as in addition to endometrial cells the endometrioma
wall includes various proportions of ovarian stroma,
follicles and fbrous tissue that prevent the detection
of gene expression alterations characteristic to ectopic
endometrial cells (reviewed in Sanchez et al. 2014). There
are only a few studies utilizing pure cell populations for
exploring gene expression in endometriotic lesions. The
frst study applied laser capture microdissection to gather
epithelial cells from eu- and ectopic endometrial tissues
(Wu et al. 2006), while another study analysed cultured
immortalized stromal cells from ovarian endometriosis
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