Department of Biological Sciences, School of Natural Sciences, Faculty of Science and Engineering, Macquarie University, NSW 2109, Australia.
School of BioSciences, University of Melbourne, Melbourne, VIC 3010, Australia.
Proc Natl Acad Sci U S A. 2024 Oct 15;121(42):e2310047121. doi: 10.1073/pnas.2310047121. Epub 2024 Oct 8.
In the first live-bearing mammals, pregnancy was likely short and ended with a brief period of inflammatory maternal-fetal interaction. This mode of reproduction has been retained in many marsupials. While inflammation is key to successful implantation in eutherians, a key innovation in eutherians is the ability to switch off this inflammation after it has been initiated. This extended period, in which inflammation is suppressed, likely allowed for an extended period of placentation. Extended placentation has evolved independently in one lineage of marsupials, the macropodids (wallabies and kangaroos), with placentation lasting beyond the 2 to 4 d seen in other marsupial taxa, which allows us to investigate the role of inflammation response after attachment in the extension of placentation in mammals. By comparing gene expression changes at attachment in three marsupial species, the tammar wallaby, opossum, and fat-tailed dunnart, we show that inflammatory attachment is an ancestral feature of marsupial implantation. In contrast to eutherians, where attachment-related (quasi-) inflammatory reaction is even involved in epitheliochorial placentation (e.g., pig), this study found no evidence of a distinct attachment-related reaction in wallabies. Instead, only a small number of inflammatory genes are expressed at distinct points of gestation, including before attachment, throughout placentation, and prostaglandins before birth. During parturition, a more distinct inflammatory reaction is detectable, likely involved in precipitating the parturition cascade similar to eutherians. We suggest that in wallaby, extended gestation became possible by avoiding an inflammatory attachment reaction, which is a different strategy than seen in eutherians.
在第一批有胎盘的哺乳动物中，妊娠时间可能很短，并且伴随着短暂的母体-胎儿炎症性相互作用期。这种生殖方式在许多有袋动物中得以保留。虽然炎症是真兽类成功着床的关键，但真兽类的一个关键创新是能够在启动炎症后将其关闭。这种炎症被抑制的延长时期可能允许胎盘形成延长。在有袋动物的一个分支——袋鼠科（沙袋鼠和袋鼠）中，胎盘形成独立地进化到延长的阶段，其胎盘形成持续时间超过其他有袋动物类群的 2 到 4 天，这使我们能够研究在附着后炎症反应在哺乳动物胎盘形成延长中的作用。通过比较三种有袋动物物种（塔马尔沙袋鼠、负鼠和胖尾袋貂）附着时的基因表达变化，我们表明炎症附着是有袋动物植入的一个古老特征。与真兽类不同，在真兽类中，附着相关（准）炎症反应甚至参与上皮绒毛膜胎盘形成（例如猪），这项研究在沙袋鼠中没有发现附着相关反应的明显证据。相反，只有少数炎症基因在妊娠的特定时间点表达，包括附着前、整个胎盘形成过程中和出生前的前列腺素。在分娩期间，可以检测到更明显的炎症反应，可能类似于真兽类参与引发分娩级联反应。我们认为，在沙袋鼠中，通过避免炎症附着反应，延长了妊娠时间，这与真兽类的策略不同。
