Elsevier

Placenta

Volume 26, Issues 2–3, February–March 2005, Pages 251-261
Placenta

Development of the haemophagous region and labyrinth of the placenta of the tenrec, Echinops telfairi

https://doi.org/10.1016/j.placenta.2004.06.001Get rights and content

Abstract

Our purpose was to determine how the central haemophagous region and cellular haemomonochorial labyrinth of the tenrec placenta are formed. The haemophagous region is preceded by a region of invasion of the endometrium by trophoblast comprising a cytotrophoblast layer covered by syncytial trophoblast and contiguous with numerous masses of multinucleate trophoblast. The trophoblast intrudes into the endometrium, eliminating the stroma, although small vessels and clumps of glandular epithelium persist. This extensive central region is connected to the forming disk by a ring of chorioallantois covered by a single layer of columnar trophoblast. Later the multinucleate masses and syncytial trophoblast degenerate. The unilaminar cytotrophoblast remains, is elaborated into folds, and phagocytoses glandular secretion, cell debris and erythrocytes. As the central area is transforming, fetal capillaries move into the cytotrophoblast pads surrounding the central zone. Prior to this, the cytotrophoblast has formed a multilayered structure and interrupted maternal vessels to create an anastomotic network of blood spaces lined by cytotrophoblast. The invasion of fetal capillaries transforms this preplacental pad into a cellular haemomonochorial labyrinth with the uninvaded portion forming an underlying spongy zone. Thus interaction of the trophoblast with the endometrium is substantially different in the central zone compared to the area of the preplacental pad.

Introduction

Tenrecs are regarded as among the most primitive of living mammals. They exhibit a number of conserved character states, including the presence of a cloaca, non-descending testes in males and variable body temperature [1]. Interest in them has been heightened since the molecular approach to phylogenetics resulted in separation of tenrecs from the insectivores and inclusion of this group in the superorder Afrotheria [2], [3], [4], [5]. Although considerable histological information is available on Tenrec, Hemicentetes and Setifer from the work of Goetz [6], [7], [8], Bluntschli [9], and Strauss [10], the genus Echinops had not been studied until a recent report on the placenta of the later stages of pregnancy [11]. This study of the definitive placenta of the Madagascan lesser hedgehog tenrec, Echinops telfairi, showed that it has a discoidal, labyrinthine, haemochorial type of placenta. The placental disks are oriented roughly antimesometrially with a central zone consisting of an elaborately folded haemophagous region. The central zone is surrounded by a circular labyrinth, with a peripheral paraplacental region extending over the mesometrial uterine lumen. Although the haemophagous region contains considerable pigment in the older placentas, there is only scant evidence of ongoing phagocytosis of erythrocytes. The major aspect of the placental disk consists of an extensive labyrinth with an underlying spongy zone. The manner in which the haemophagous region forms and the labyrinth is established has not been described for this genus and is the subject of the current report.

Section snippets

Materials and methods

The animals used in this study were housed as described previously [12] and tissues were collected and processed as reported in the previous study [11]. The gestation period of the females in our colony is 50–60 days and average litter size is 3–4 young [12]. Several conceptuses from each of five animals in early to mid gestation were collected. The crown-rump length (CRL) of the embryos averaged 3 mm in the youngest gestation (estimated gestational age 19 days). Three animals had gestation

Results

In these early stages of placental formation there is typically a central antimesometrial region that intrudes variably as a mound into the allantois (Figure 1). This central area is oriented roughly antimesometrially and is surrounded by a pad of trophoblast that is thick near the central area and narrows as it approaches a small region situated near the mesometrium, encompassing 1/3 to 1/4 of the circumference of the site, where the trophoblast neither penetrates nor adheres to the uterine

Discussion

The central zone which develops into the haemophagous region is an area of extensive invasion of the endometrium by multinucleate syncytial masses. These trophoblast masses not only penetrate the uterine epithelium, but appear to preferentially remove the stroma, initially leaving some remnants of glands and especially of small blood vessels. The multinucleate masses develop multiple lipid droplets and eventually degenerate. This eliminates most of the endometrium and most of the original

Acknowledgements

The authors would like to thank Ms Lis Teusch for technical assistance. The studies were supported in part by The Carlsberg Foundation, Denmark, and the Deutsche Forschungsgemeinschaft, grant Ku 624/3-1.

References (33)

  • R.H. Goetz

    Studien zur Placentation der Centetiden. I. Eine Neu-Untersuchung der Centetes Placenta

    Z Anat Entwicklungsgesch

    (1937)
  • R.H. Goetz

    Studien zur Placentation der Centetiden. II. Die Implantation und Frühentwicklung von Hemicentetes semispinosus (Cuvier)

    Z Anat Entwicklungsgesch

    (1937)
  • R.H. Goetz

    Studien zur Placentation der Centetiden. III. Die Entwicklung der Fruchthüllen und der Placenta bei Hemicentetes semispinosus (Cuvier)

    Z Anat Entwicklungsgesch

    (1938)
  • H. Bluntschli

    Die Frühentwicklung eines Centetinen (Hemicentetes semispinosus Cuv.)

    Rev Suisse Zool

    (1937)
  • F. Strauss

    Die Placentation von Ericulus setosus

    Rev Suisse Zool

    (1943)
  • H. Künzle

    Care and breeding of the Madagascan hedgehog tenrec, Echinops telfairi, under laboratory conditions

    Der Tierschutzbeauftragte

    (1998)
  • Cited by (23)

    • Placentation in the Hottentot Golden Mole, Amblysomus hottentotus (Afrosoricida: Chrysochloridae)

      2009, Placenta
      Citation Excerpt :

      Similarity to other members of the Afrosoricida, on the other hand, is much more tenuous. Both Amblysomus and Echinops [17,18], for example, have an allantois, yolk sac, labyrinth and spongy zone. The labyrinth, however, is haemodichorial in the golden mole with a syncytial outer layer, and cellular haemomonochorial in Echinops [17].

    • Reasons for Diversity of Placental Structure

      2009, Placenta
      Citation Excerpt :

      It also suggests that placental type is more fundamental than adaptations to seasonal and regional differences such as delayed implantation, delayed development, delayed fertilization, hibernation and estivation, which can vary within families. Finally, it is instructive to compare placentation in what is considered a relatively primitive mammal such as the hedgehog tenrec [24,25] and a primate such as the macaque. The hedgehog tenrec retains the allantois as a sac bringing the allantoic vessels to the forming chorioallantoic placenta.

    View all citing articles on Scopus
    View full text