Endogenous Retroviruses and Placental Evolution, Development, and Diversity

Abstract

The main roles of placentas include physical protection, nutrient and oxygen import, export of gasses and fetal waste products, and endocrinological regulation. In addition to physical protection of the fetus, the placentas must provide immune protection throughout gestation. These basic functions are well-conserved; however, placentas are undoubtedly recent evolving organs with structural and cellular diversities. These differences have been explained for the last two decades through co-opting genes and gene control elements derived from transposable elements, including endogenous retroviruses (ERVs). However, the differences in placental structures have not been explained or characterized. This manuscript addresses the sorting of ERVs and their integration into the mammalian genomes and provides new ways to explain why placental structures have diverged.

Keywords: endogenous retrovirus (ERV); mammals; placenta; structural diversity.

Figure 1

Structural diversity of placentas as classified by the distribution of chorionic villi. Gross anatomy showing diffuse (pigs), cotyledonary (ruminants), zonary (cats and dogs), and discoid (rodents and primates). (A): Diffuse placentas have a uniform distribution of chorionic villi covering the chorion’s surface. (B): Cotyledonary placentas have numerous, discrete, button-like structures called cotyledons and they join with the maternal caruncle, forming a placentome. (C): Zonary placentas have a band-like zone of chorionic villi, of which both edges are primary exchange zones. (D): Discoid placentas form a regionalized disc-like structure. Red and blue lines are the artery and vein, respectively, which are joined to an umbilical cord.

Figure 2

Placental classification according to separation between fetal and maternal blood supplies. There are three layers of separate maternal and fetal blood in Hemochorial (primates and rodents); chorionic epithelium (syncytiotrophoblast), chorionic interstitium (basement membrane), and chorionic capillaries (fetal blood). In Endotheliochorial (dogs and cats), there are five layers between the maternal and fetal blood; endometrial capillaries (maternal blood), endometrial interstitium, chorionic epithelium, chorionic interstitium and chorionic capillaries. In Epitheliochorial (pigs and horses), six layers separate the maternal and fetal blood; endometrial capillaries, endometrial interstitium, endometrial epithelium, chorionic epithelium, chorionic interstitium, and chorionic capillaries.

Figure 3

Multiple acquisitions of ERV-derived genes expressed in placenta. The dendrogram indicates a taxonomic relationship of 45 species, including 42 mammals, two reptiles, and one bird. The phylogeny was obtained using the TimeTree website (http://www.timetree.org, accessed on 2 July 2022 [14]). ERV-derived genes expressed in the placenta are illustrated at the location of the presumed inserted lineage. The red or blue color indicated whether the ERV-derived genes were reported to have fusion activity or not, respectively. A gene in parentheses indicated the time of insertion where the gene without parenthesis is when it has acquired function. The details of each ERV-derived gene shown in the figure are summarized in Table 1.