The transformative processes that prepare the endome-
trium for embryo implantation are unique to menstruating
species, and are thought to underlie the evolution of
menstruation. Although rodent species, which are easy
to manipulate, are common experimental models for
studies of endometrial receptivity and embryo implanta-
tion, findings obtained with these animals often cannot
be directly translated to humans.
Biological processes that have developed in the
human endometrium during the evolution of menstru-
ation are specialized versions of processes that are found
in other tissues, altered to regulate endometrial biology.
Understanding how the human endometrium under-
goes controlled and spatially limited tissue destruction,
resolution of inflammation, scar-free repair and re-
epithelialization followed by regeneration and transfor-
mation can inform our understanding of processes that
occur in other tissues.
In this Review, we describe the remodelling of the
endometrium before it becomes receptive for embryo
implantation, the dynamic fetal–maternal communi-
cation that contributes to successful implantation, the
endometrial defects that result in infertility and miscar-
riage and the detection and treatment of these disorders.
We also identify missing links, both experimental and
clinical, which should be investigated to enable progress
in the field, and areas where understanding of endo-
metrial biology might influence other fields and the
development of therapeutics.
Evolution of human menstruation
Unlike other organs, the human endometrium does not
have a single, constant function from birth to death.
The endometrium exists to provide a ‘fertile ground’
for implantation of an embryo and development of a
highly invasive placenta, which is achieved by an orderly
sequence of development and transformation within each
menstrual cycle, under the influence of the ovarian steroid
hormones
1
. The endometrial cells become terminally dif-
ferentiated during each menstrual cycle; in the absence of
conception, tissue shedding and regeneration for subse-
quent fertile cycles occurs. In menstruating species, decid-
ualization is spontaneous, rather than embryo-mediated.
Decidualization is the process of the transformation or
differentiation of human endometrial stromal fibroblasts
to secretory ‘epithelioid’ cells, which occurs under the
influence of the hormones oestrogen and progesterone,
along with cAMP and local paracrine factors.
The evolution of spontaneous decidualization is
thought to have occurred when genes that were ances-
trally expressed in other organs and tissue systems were
expressed in the endometrium. Transposable elements,
1
Centre for Reproductive
Health, Hudson Institute of
Medical Research, Clayton,
3168, Australia.
2
Department of Molecular
and Translational Medicine,
Monash University, Clayton,
3800, Australia.
3
Department of Physiology,
Monash University, Clayton,
3800, Australia.
4
Department of Obstetrics
and Gynaecology, Monash
University, Clayton, 3800,
Australia.
5
Department of Biochemistry
and Molecular Biology,
Monash University, Clayton,
3800, Australia.
6
The Ritchie Centre, Hudson
Institute of Medical Research,
Clayton, 3168, Australia.
7
Department of Anatomy and
Developmental Biology,
Monash University, Clayton,
3800, Australia.
Correspondence to E.D.
evdokia.dimitriadis@hudson.
org.au
doi:10.1038/nrendo.2016.116
Published online 22 Jul 2016
Fertile ground: human endometrial
programming and lessons in health
and disease
Jemma Evans
1–3
, Lois A. Salamonsen
1,2,4
, Amy Winship
1,2
, Ellen Menkhorst
1,2
,
Guiying Nie
1,2,5
, Caroline E. Gargett
4,6
and Eva Dimitriadis
1,2,7
Abstract | The human endometrium is a highly dynamic tissue that is cyclically shed, repaired,
regenerated and remodelled, primarily under the orchestration of oestrogen and progesterone,
in preparation for embryo implantation. Humans are among the very few species that menstruate
and that, consequently, are equipped with unique cellular and molecular mechanisms controlling
these cyclic processes. Many reproductive pathologies are specific to menstruating species, and
studies in animal models rarely translate to humans. Abnormal remodelling and regeneration of
the human endometrium leads to a range of reproductive complications. Furthermore, the
processes regulating endometrial remodelling and implantation, including those controlling
hormonal impact, breakdown and repair, stem/progenitor cell activation, inflammation and
cell invasion have broad applications to other fields. This Review presents current knowledge
regarding the normal and abnormal function of the human endometrium. The development of
biomarkers for prediction of uterine diseases and pregnancy disorders and future avenues
of investigation to improve fertility and enhance endometrial function are also discussed.
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