Book - Sex and internal secretions (1961) 14
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Section D Biology of Sperm and Ova, Fertilization, Implantation, the Placenta, and Pregnancy
P. Embryo-Endometrial Relationships
The interrelationship between the blastocyst and the endometrium at the time of attachment and implantation is not only exceedingly complex but also highly variable in different species. Irrespective of the complexity of the attachment, each type has as its purpose the apposition or intimate fusion of the fetal membranes to the maternal endometrial epithelium or stroma so that adequate physiologic exchange can take place.
Earlier studies on the experimental production of deciduomas by mechanical stimulation of the sensitized endometrium, and the dependence of implantation on the proper hormonal stimulation of the uterine mucosa, had the effect of swinging the pendulum of opinion toward the endometrium as being the most active agent in the process of nidation (Huber, 1915; Kirkham, 1916; Selye and McKeown, 1935; Krehbiel, 1937; Rossman, 1940). More recently, however, the observations ( 1 ) on the development of the attachment cone in some specific area of the trophoblastic wall just before attachment, (2) the changes in the viscosity and adhesiveness of the egg envelopes at the time of attachment, and on the developmental potentialities of ova transplanted to the anterior chamber of the eye and other sites have swung the pendulum back to the embryo and the role that it may l)lay in nidation (Asshcton, 1894; von Spec, 1901; Schoenfeld, 1903; Mossman, 1937; Fawcett, Wislocki and Waldo, 1947; Runner, 1947; Blandau, 1949a; and Boving, 1954, 1961 j.
The extensive i)rolil'eralion and differentiation in the endometrium of certain animals after ovulation undoubtedly arc iml)ortant in the nourishment and maintenance of the ovum in utero and in providing a suitable implantation site. The considerable growth and differentiation which the blastocysts of many animals undergo before they make contact with the uterine mucosa would indicate that more nutrients are required than are stored in the ooplasm of most mammalian eggs. The widespread occurrence of glucose, glycogen, lipids, phosphatases, iron, calcium, and many other substances, including vitamins and enzymes, in the endometrium may provide the necessary nourishment during the very early stages of implantation ( Wislocki and Dempsey, 1945) . Bloch (1939) described the secretion of an osmol)hilic substance by the uterine epithelium which is thought to be absorbed by the free mouse blastocyst. The work of Daron (1936), Markee (1940), Phelps (1946), Parry (1950), and Boving (1952a, 1961) has demonstrated that there is an increased blood supply immediately below the uterine epithelium at about the time of blastocyst attachment. The increased vascularity may not only provide nutrition to the uterine epithelium, but more importantly it provides blood vessels for specific physicochemical reactions between the trophoblast and endometrium (Boving, 1959a) . A similar increase in the blood supply in the antimesometrial area has been observed in the guinea pig (Bacsich and Wyburn, 1940). This is the area in which implantation invariably occurs in this species, and the localized hyperemia is considered to be a factor in tlie antimesometrial implantation.
It is well established that the presence of an actively secreting corpus luteum is essential if implantation is to be complete and successfully maintained. In rabbits progesterone is necessary, not only for the nutrition of the free blastocyst in utero, but also for implantation (Fraenkel, 1903; Corner, 1928b; Corner and Allen, 1929; Hafez and Pincus, 1956a, b) . Histochemical and quantitative tests have indicated that lipids are present in the endometrium in greater amounts during the luteal phase of the reproductive cycle than at any other time (Krehl)iel, 1937; van Dyke and Chen, 1940; Alden, 1947).
It is clear that the presence of an embryo in the cornu exerts a significant effect on the secretion of luteotrophic hormone and on the functional life of the corpus luteum. How these effects are producecl remains a challenging problem. We need to determine whether direct invasion of the endometrium is essential or whether mere expansion of the embryo can act as a trigger mechanism. Nalbandov and St. Clair (1958) have shown that if plastic beads of more than 2 mm. in diameter are inserted into the cornua on the 8th day of the estrous cycle in sheep, the cycle is significantly lengthened. Denervation of the cornu containing the beads prevented this change in length.
It has been found repeatedly that endometrial sensitivity to the formation of deciduomata is limited normally to the period of implantation and placentation (Loeb, 1908; Allen, 1931; Selye and McKeown, 1935; Krehbiel, 1937; Greenwald, 1958b). The traumatizing substances were physical, chemical, and electrical stimuli. From these studies, three facts were revealed: (1) The formation of the "maternal placenta" can be induced in the complete absence of the blastocyst (Krehbiel, 1937; Mossman, 1937; Dawson and Kosters, 1944). (2) Even though tissue destruction in the endometrium can be brought about by specific and nonspecific stimuli and even though the endresult may appear similar, the mechanisms producing the changes do not necessarily stem from the same basic stimulus. (3) All of the stimuli used are presumed to have as the basis of their action some kind of tissue injury.^ Notwithstanding, the histologic transformations of the deciduomas correspond exactly to those occurring normally in
^ The passage of an electric current of sufficient magnitude through the endometrium to induce the decidual response gives no evidence of tissue damage that can be detected microscopically. This of course does not eliminate the possibility^ that cellular injury has not occurred.
early pregnancy. Krehbiel (1937) found, for
example, in the experimentally induced deciduomas of the rat that glycogen and lipids
appeared intracellularly in cells which cytologically seemed identical with those of the
normal endometrium of pregnancy.
It would be interesting to know whether the same intensity of artificial stimulus would induce the decidual response in the uteri of a variety of animals. In the rat, for example, the slightest pressure against the superficial uterine epithelium, at the proper time after ovulation, is sufficient to initiate the decidual response. Thus a bit of lint, small clumps of cells, and glass or paraffin beads the approximate size of eggs effect an endometrial response identical with the response to the normally implanting embryo (Blandau, 1949a). In this species the very earliest changes in the subepithelial stroma begin when the blastocyst is attached only very tenuously to the uterine epithelium (Fig. 14.22). From this response of the endometrium, perhaps localized pressure is sufficient to induce the decidual reaction. Equally impressive is the fact that the decidual response begins before there is any alteration in the superficial uterine epithe
Fig. 11.22. I.MiigiiiKhii.il ^.riinn 1 hrough the antimesometiial wall of a pregnant rat killed on the 5th day. The loosely attached rat blastocyst has initiated the subepitheUal decidual response. There is no detectable alteration in the superficial epithelium. X 450.
limn detectable by microscopic means. Thus, any stimulus from living eggs or inert objects within the lumen is transmitted to the underlying stroma directly through the intact lining epithelium. Wimsatt (1944), in describing the earliest phases of implantation in the bat, came to the conclusion that the changes in the epithelium of the pocket into which the blastocyst comes to rest is "an expression of a localized physiologic reaction of the uterus to some chemical stimulus of unknown nature liberated by the ovum, which may produce this effect by acting locally on the epithelium or by inducing a local relaxation in the uterine muscle."
It is important to recall again that the destruction and removal of the uterine epithelium by the trophoblastic cells of the rat blastocyst do not begin until the embryo lies deeply within the decidual crypt and a sizable decidual response has been elicited (Alden, 1948). Therefore, the initiation of the decidual reaction and the active invasion of the endometrium by the trophoblast are two distinctly different phenomena separated by a considerable interval of time. In the guinea pig, rabbit, monkey, man, and possibly other mammals, the normal decidual response is not elicited until the embryo has effected the removal of the sujierficial uterine epithelium. Recently, it has been shown that there is a definite species difference in the response of the endometrium to glass or paraffin beads inserted into the uterus of properly timed females (Blandau, 1949a). In the rat, the beads initiated the decidual response and were implanted in a manner similar to blastocysts. In the guinea pig, the beads did not effect the removal of the uterine epithelium, and only occasionally was a minimal decidual response induced. Thus it would appear for the guinea pig, at least, not only that the .stimulus must be a direct one to the underlying stroma but that a certain amount of tissue injury or invasion is necessary before the decidual response can be initiated.
As we suggested earlier, the initiation of the decidual reaction may be the result of a localized pressure exerted by the blastocyst, or of the action of some chemical substance secreted by the egg, which is transmitted to a properly sensitized subepithelial stroma. Recently, Shelesnyak (1952, 1954, 1959a, 19591) I undertook to investigate the nature of the non-specific stimulus required to initiate the deciduomas by determining the effects of histamine and histamine antagonists on the endometrium. He theorized that some degree of injury was a common factor to all methods of uterine stimulation, that a histamine or histamine-like substance was present at the site of injury, and further, that at the time of blastocyst attachment there is an "estrogen surge" which acts to release histamine from the endometrium and which in turn initiates the decidual cell response. Evidence for the role of histamine in deciduoma production also includes the depletion of the mast cell population of the endometrium just before attachment. On this basis, after instilling diphenhydramine hydrochloride or other antihistamines into one horn, both cornua of pseudopregnant rats were stimulated to induce deciduoma development. Definite inhibition of deciduoma was noted in the cornu receiving the antihistamine, particularly if the drug was instilled before the transformation of endometrial cells to decidual cells. Consistent with this finding are the indications from extensive tests that drugs having a specific histamine antagonism are effective in suppressing the decidual cell reaction when introduced into the uterine lumen of rats and mice during pseudopregnancy. On the other hand, antihistamines injected subcutaneously in these animals ordinarily fail to prevent implantation. Species differences must also be considered. Boving (1959) was unable to find mast cells associated with rabbit trophoblast invasion.
The theory that some mechanism of histamine release is responsible for initiating the decidual cell reaction would logically imply that the blastocyst is an active histamine secretor or that it indirectly effects a rise of "free" histamine in the cornua, or interferes with its destruction. In all of the work that has been reported in the attempt to establish histamine as the primary evocator in the decidual cell response and implantation, the blastocyst has been ignored. There has been no attempt to examine the living blastocyst itself and to determine the effects of the various drugs used on it. Con
sequently, the conclusions drawn as to the
failure of implantation are equivocal because
the condition of the implanting agent in the
experiment has not been evaluated. Also relevant is the fact mentioned earlier that the
decidual response in the rat and mouse is
evoked, not only by living embryos, but also
by many inert objects inducing the response
without evidence of epithelial destruction.
The mechanism of histamine release under
these conditions must be based on some unknown factor.
The appearance of implantation cones, just before and durine attachment of the blastocyst to the endometrium in guinea pigs, rabbits, squirrels, chipmunks, and probably primates, raises the question as to whether the embryo may not initially send protoplasmic extensions between the epithelial cells lining the lumen and thus secrete some substance which not only initiates the decidual response, but also effects the removal of underlying endometrial tissue (compare Figs. 14.23, 14.24 and 14.25) (Mossman, 1937; Wislocki and Streeter, 1938; Boving, 1954, 1959a j. It is interesting that during this initial invasion in the guinea pig, rabbit, and man, there is a negligible amount of endometrial necrosis. In the description of the implantation stages of the macaque, Wislocki and Streeter also emphasized that during the earliest
INNER CELL MASS
Fig. 14 23. Section of a ciuili.'a pig lila.-lo.-yst
showing the \eiy earliest stage in the attachment
of the abembiyonal pole cells to the maternal
endometrium. X 500.
864
Fig. 14.24. The (•.-Illy M.-itic of attacliiucnt of the O-day maca.iuc M im.hxm The .Miihryonic
pole is directed towards the uterine epithelium (Wislocki and Streeter, 1938).
Fig. 14.25. A section through an implanting rabbit blastocyst showing an unusually narrow
trophoblast invasion of the uterine epithelium. There is no evidence of epithelial debris
within the trophoblast cells. A group of clumped uterine epithelial nuclei surrounded by pale
cytoplasm lies to the left of the invading foot (Boving, 1959a). Fixation: Sousa, Azan stain.
X600.
phases of embryonic attachment to the uterine epithelium, the subepithelial mucosa shows no reaction whatever. When joined, these observations remind us that as yet there is no conclusive evidence that the implanting embryo secretes cytolytic enzymes but may secrete other substances.
The most imaginative experimental approach to the problems of embryo spacing, attachment, and implantation is the work of Boving (1959a, b and c, 1961) on the rabbit. He has clearly shown that, in this animal, invasion is promoted by a chemical substance elaborated witliin the blastocyst and transferred to the maternal circulation. The invasion-promoting substance has been characterized as being in the form of bicarbonate which induces a localized high 1)H. Circulating progesterone increases the level of endometrial carbonic anhydrase and accelerates the removal of bicarbonate from the embryo by catalyzing the formation of carbonic acid. The carbonic acid is converted to carbon dioxide which is removed by the maternal circulation. The local pH rises and the various blastocysts' membranes become very sticky, particularly at the site of attachment. The physicochemical interrelationship of the trophoblast and endometrial epithelium effects a dissociation of the epithelium, thus opening a path for the trophoblast.
At this writing, the precise roles of the egg and endometrium during implantaton are unknown and remain a challenging problem. The numerous modifications of the implantation processes in the different mammalian families create difficulties of interpretation in what is already an unusually complex problem. As more detailed descriptions of the embryo-endometrial relationships appear, it seems clear that neither the ovum nor the endometrium is primarily responsible for implantation, but that both play mutual and overlapping roles. One of the greatest gaps in our knowledge of implantation for any animal is a detailed description of the process itself and the precise timing of the events in this phenomenon. The various experimental approaches to the physiologic and biochemical mechanisms of implantation have quickened our interest and broadened our view of the complex metabolic processes required if implantation is to be successful, but our efforts to interpret correctly the data from biochemical, physiologic, and pharmacologic investigations will be limited until more accurate information has been obtained bearing on the morphologic features of the process itself.
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Reference: Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.
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