Regulation of Implantation and Establishment of Pregnancy in Mammals: Tribute to 45 Year Anniversary of Roger V. Short's "Maternal Recognition of Pregnancy"

271 Pages·2015·5.13 MB·English

by  Rodney D. Geisert

Advances in Anatomy, Embryology and Cell Biology
Rodney D. Geisert
Fuller W. Bazer Editors
Regulation of
Implantation and
Establishment
of Pregnancy in
Mammals
Tribute to 45 Year Anniversary of Roger
V. Short's "Maternal Recognition of
Pregnancy"
Advances in Anatomy, Embryology and Cell Biology publishes critical reviews and
state-of-the-art surveys on all aspects of anatomy and of developmental, cellular and
molecular biology, with a special emphasis on biomedical and translational topics.
The series publishes volumes in two different formats:
(cid:129) C ontributed volumes, each collecting 5 to 15 focused reviews written by leading
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(cid:129) Single-authored or multi-authored monographs, providing a comprehensive
overview of their topic of research
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60595 Frankfurt/Main, Germany
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Editors
Prof. Dr. T.M. BÖCKERS, Institut für Anatomie und Zellbiologie, Universität Ulm, Ulm, Germany
e-mail: [email protected]
Prof. Dr. F. CLASCÁ, Department of Anatomy, Histology and Neurobiology
Universidad Autónoma de Madrid, Ave. Arzobispo Morcillo s/n, 28029 Madrid, Spain
e-mail: [email protected]
Dr. Z. KMIEC, Department of Histology and Immunology, Medical University of Gdansk,
Debinki 1, 80-211 Gdansk, Poland
e-mail: [email protected]
Prof. Dr. B. SINGH, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, Canada
e-mail: [email protected]
Prof. Dr. P. SUTOVSKY, S141 Animal Science Research Center, University of Missouri, Columbia, MO, USA
e-mail: [email protected]
Prof. Dr. J.-P. TIMMERMANS, Department of Veterinary Sciences, University of Antwerpen,
Groenenborgerlaan 171, 2020 Antwerpen, Belgium
e-mail: [email protected]
216
Advances in Anatomy,
Embryology
and Cell Biology
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Rodney D. Geisert (cid:129) Fuller W. Bazer
Editors
Regulation of
Implantation and
Establishment of
Pregnancy in
Mammals
Tribute to 45 Year Anniversary of
Roger V. Short’s “Maternal
Recognition of Pregnancy”
Editors
Rodney D. Geisert Fuller W. Bazer
S163 Animal Science Research Center Department of Animal Science
Division of Animal Sciences Texas A&M University
University of Missouri College Station , TX
Columbia , MO USA
USA
ISSN 0301-5556 ISSN 2192-7065 (electronic)
Advances in Anatomy, Embryology and Cell Biology
ISBN 978-3-319-15855-6 ISBN 978-3-319-15856-3 (eBook)
DOI 10.1007/978-3-319-15856-3
Library of Congress Control Number: 2015952829
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Contents
1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
Rodney D. Geisert
2 History of Maternal Recognition of Pregnancy . . . . . . . . . . . . . . . . . . . . 5
Fuller W. Bazer
3 The Role of Steroid Hormone Receptors
in the Establishment of Pregnancy in Rodents . . . . . . . . . . . . . . . . . . . . 27
Nyssa R. Adams and Francesco J. DeMayo
4 Transmembrane Mucin Expression and Function
in Embryo Implantation and Placentation . . . . . . . . . . . . . . . . . . . . . . . 51
Pamela E. Constantinou , Micaela Morgado , and Daniel D. Carson
5 Reflections on Rodent Implantation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Jeeyeon M. Cha and Sudhansu K. Dey
6 The Role of Progesterone in Maternal Recognition
of Pregnancy in Domestic Ruminants . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
Pat Lonergan and Niamh Forde
7 Implantation and Establishment of Pregnancy in Ruminants . . . . . . 105
Thomas E. Spencer and Thomas R. Hansen
8 Implantation and Establishment of Pregnancy in the Pig . . . . . . . . . 137
Rodney D. Geisert , Gregory A. Johnson , and Robert C. Burghardt
9 Pregnancy Recognition and Implantation of the Conceptus
in the Mare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
Claudia Klein
10 Implantation and Establishment of Pregnancy
in Human and Nonhuman Primates . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
Ren-Wei Su and Asgerally T. Fazleabas
v
vi Contents
11 The Dog: Nonconformist, Not Only
in Maternal Recognition Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
Mariusz P. Kowalewski , Aykut Gram , Ewa Kautz ,
and Felix R. Graubner
12 Embryonic Diapause and Maternal Recognition
of Pregnancy in Diapausing Mammals . . . . . . . . . . . . . . . . . . . . . . . . . 239
Marilyn B. Renfree
13 Predicting Embryo Presence and Viability . . . . . . . . . . . . . . . . . . . . . . 253
K. G. Pohler , J. A. Green , T. W. Geary , R. F. G. Peres ,
M. H. C. Pereira , J. L. M. Vasconcelos , and M. F. Smith
Chapter 1
Introduction
Rodney D. Geisert
Abstract Establishment and maintenance of pregnancy in a number of mammalian
species depends upon a tightly regulated interaction between the semiallogeneic
conceptus and the maternal uterine endometrium. The term “Maternal Recognition
of Pregnancy” is attributed to Roger V. Short’s paper titled “Implantation and the
Maternal Recognition of Pregnancy” which was published in proceedings from the
1969 Symposium on Foetal Autonomy. Professor Short’s landmark paper stimu-
lated increased interest in elucidating how the conceptus signals its presence to
assure maintenance of the corpus luteum beyond the normal length of the estrous or
menstrual cycle to allow pregnancy to be established and maintained. Ten years
following publication of Professor Short’s paper, a Ciba Foundation Symposium
entitled “Maternal Recognition of Pregnancy” brought together leading scientists to
discuss the multiple mechanisms and pathways by which different viviparous spe-
cies establish a successful pregnancy. The present volume on “Regulation of
Implantation and Establishment of Pregnancy in Mammals” brings together current
reviews from leading experts to address the diversity of mechanisms by which spe-
cies establish and maintain pregnancy. Implantation in mice, dogs, pigs, cattle,
sheep, horses, primates, humans and species in which embryonic diapause occurs
are discussed. Reviews will provide current knowledge on the role of endometrial
steroid receptors, adhesion factors, cytokines, interferons, steroids, prostaglandins,
growth factors and immune cells involved with regulation of conceptus
development.
R. D. Geisert
Division of Animal Sciences , University of Missouri ,
163 Animal Science Research Center , Columbia , MO 65211 , USA
e-mail: [email protected]
© Springer International Publishing Switzerland 2015 1
R.D. Geisert, F.W. Bazer (eds.), Regulation of Implantation and Establishment
of Pregnancy in Mammals: Tribute to 45 Year Anniversary of Roger V. Short’s
“Maternal Recognition of Pregnancy”, Advances in Anatomy, Embryology and
Cell Biology 216, DOI 10.1007/978-3-319-15856-3_1
2 R.D. Geisert
Establishment and maintenance of pregnancy in a number of mammalian species
depends upon a tightly regulated interaction between the semiallogeneic conceptus
and the maternal uterine endometrium. The term “Maternal Recognition of
Pregnancy” is attributed to Roger V. Short’s paper titled “Implantation and the
Maternal Recognition of Pregnancy” which was published in proceedings from the
1969 Symposium on Foetal Autonomy (Short, 1 969 ). Professor Short’s landmark
paper stimulated increased interest in elucidating how the conceptus signals its
presence to assure maintenance of the corpus luteum beyond the normal length of
the estrous or menstrual cycle to allow pregnancy to be established and maintained.
To gain an historical perspective on maternal recognition of pregnancy, I recom-
mend that every graduate student and young investigator involved with reproductive
biology read his review paper. The following quote, taken from the introduction of
Professor Short’s paper, indicates that the establishment of pregnancy involves more
than a simple biological pathway to “rescue” the corpus luteum from regressing
during pregnancy and outlines the fundamental questions regarding pregnancy rec-
ognition signaling mechanisms which researchers today continue to investigate
across a diverse variety of species.
The maternal organism fi rst becomes aware of the presence of an embryo in the uterus in
diverse ways. In most mammals, this critical piece of information must be relayed to the
mother at an early stage of gestation, and we will begin by considering in general terms
both the nature of the message and the mode of its transmission. We shall then be in a posi-
tion to investigate variations on the basic pattern, species by species.
O ne of the fi rst outward and visible signs that an embryo has made its presence felt in
the uterus is when the corpus luteum of the cycle becomes transformed into a corpus luteum
of pregnancy, and estrous or menstrual cycles cease to recur. Let us therefore examine this
luteotropic action of the conceptus in a little more detail. Can the stimulus be initiated by the
embryo before it has achieved an anatomical union with the endometrium? Is the stimulus
itself mechanical in nature, giving rise to afferent neural stimuli to the hypothalamus, which
in turn bring about the release of luteotropic hormone(s) from the anterior pituitary, or does
the conceptus have a hormonal action, elaborating its own luteotropic substances? In those
species in which the endometrium of the nonpregnant uterus seems to produce a luteolytic
factor, how does the embryo act to neutralize this effect? These are some of the questions to
which we must attempt to the fi nd the answers. Furthermore, it may be a mistake to concen-
trate all our attention on luteal maintenance as the fi rst premonition of a pregnancy; funda-
mental differences between the pregnant and nonpregnant animal may begin to become
apparent soon after fertilization, and in a number of species, the lifespan and secretory
activity of the corpus luteum is unaffected by pregnancy. Undoubtedly much still lies out-
side our comprehension in this most fascinating area of investigation (Short 1 969 ).
T en years following the publication of Professor Short’s paper, a Ciba Foundation
Symposium entitled “Maternal Recognition of Pregnancy” (Ciba Foundation
Symposium, 1 979) brought together leading scientists to discuss the multiple mech-
anisms and pathways by which different viviparous species establish a successful
pregnancy. The diversity of mechanisms to establish and maintain luteal function
alone are clearly evident from the following species variation: (1) in the bitch, the
corpora lutea (CL) are maintained for the length of pregnancy whether or not mat-
ing occurs; (2) in mice and rats, a sterile mating extends the lifespan of the CL from
4 to 12 days through vaginal stimulation by the erect penal spines (Fig. 1 .1 ) that
1 Introduction 3

Fig. 1.1 Penile spines of the glans penis of rats stimulate the vagina of the female during mating
to extend CL lifespan beyond a normal 4-day estrous cycle. If maternal recognition of pregnancy
is considered extending CL function beyond the estrous cycle, the penile spines could be consid-
ered one of the earliest signaling mechanisms evoked even before fertilization. However, establish-
ment of a pregnancy by viable blastocysts/conceptuses involves a more elaborate interaction
between the maternal endometrium and implanting conceptus. Note that the short estrous cycle,
mating-induced CL extension, and the ability to induce embryonic diapause place mice and rats
among the more effi cient and prolifi c species of mammals for reproduction
induce the diurnal release of prolactin; (3) in humans and subprimates, release of a
conceptus-derived factor (chorionic gonadotrophin, CG) acts directly on CL to
maintain function; and (4) the release of conceptus-derived factors indirectly inhib-
its the release or production of luteolytic pulses of prostaglandin F2α (luteolysin)
from the endometrium. Of course, PGF2α had not been identifi ed as a luteolytic
hormone at the time of Short’s paper. However, maternal recognition of pregnancy
involves considerably more than extending luteal function. The attaching or implant-
ing conceptus must stimulate adequate maternal blood fl ow to the placenta for trans-
fer of oxygen and nutrients and induce the maternal endometrium to provide the
spatiotemporal pattern of secretions and nutrient transport mechanisms necessary
for continued development and survival of the conceptus throughout pregnancy
while altering the maternal immune system to prevent rejection of the semialloge-
neic conceptus.
O ver the past few decades, technological advances in transcriptomics, pro-
teomics, metabolomics, and glycomics along with the ability to selectively knock-
out genes of interest has greatly advanced our understanding of maternal-conceptus
interactions that are essential for the establishment and maintenance of a successful