The composition of fetal fluids of the marsupial Macropus eugenii

doi:10.1016/0012-1606(73)90165-6

Developmental Biology

Volume 33, Issue 1, July 1973, Pages 62-79

https://doi.org/10.1016/0012-1606(73)90165-6 Get rights and content

Abstract

The composition of the fetal fluids of the marsupial, Macropus eugenii, and their relationship to maternal serum and uterine secretion is described. The results show that growth of the embryo can be divided into two phases. In the first phase, when the vesicle is not attached to the uterus, the composition of the vesicle fluid resembles maternal serum only in its glucose and urea content, and is more concentrated in free amino acids and more dilute in proteins. The electrophoretic pattern resembles that of uterine flushings.

The second phase begins at attachment of the yolk sac to the uterine epithelium when the vascular region of the yolk sac has developed and embryogenesis begins. At this time, the composition of the yolk sac fluid is notably changed, particularly in its protein components, although maternal serum and endometrial secretion do not change. Most of the proteins found in the yolk sac fluid during this phase are probably of fetal origin. Each fluid compartment has its own unique composition; the allantois has high concentrations of urea, the amnion is dilute in all components, and the yolk sac has high concentrations of amino acids at all stages of gestation and of glucose during late gestation. The vascular area of the yolk sac is probably the important region for respiratory exchanges, while the nonvascular region persists as the route of transfer of nutrient material. It is suggested that the second phase is one of increasing fetal autonomy, made possible by the differentiation of organ systems (some of which appear to be functional early), as well as by possible conversion of material in the yolk sac itself.

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Marsupials and eutherians are mammals that differ in their physiological traits, predominately their reproductive and developmental strategies; eutherians give birth to well-developed young, while marsupials are born highly altricial after a much shorter gestation. These developmental traits also result in differences in the development of the immune system of eutherian and marsupial species. In eutherians, B-cells are the key to humoral immunity as they are found in multiple lymphoid organs and have the unique ability to mediate the production of antigen-specific antibodies in the presence of extracellular pathogens. The development of B-cells in marsupials has been reported and hypothesised to be similar to that of eutherians, except that haematopoiesis occurs in the liver, postpartum, until the bone marrow fully matures. In eutherians, specific genes are linked to specific stages in B-cell development, maturation, and differentiation processes, and have been identified including immunoglobulins (heavy and light chains), cluster of differentiation markers (CD10, 19, 34 and CD79α/β), signal transduction molecules (BTK, Lyn and Syk) and transcriptional regulators (EBF1, E2A, and Pax5). This review aims to discuss the known similarities and differences between marsupial and eutherian B-cells, in regards to their genetic presence, homology, and developmental stages, as well as to highlight the areas requiring further investigation. By enhancing our understanding of the genes that are involved with B-cells in the marsupial lineage, it will, in turn, aid our understanding of the marsupial immune system and support the development of specific immunological reagents for research and wildlife conservation purposes.
Conceptus Coats of Marsupials and Monotremes
2018, Current Topics in Developmental Biology
Mammals evolved from oviparous reptiles that laid eggs in a dry, terrestrial environment, thus requiring large amounts of yolk to support development and tough, outer coats to protect them. Eutherian mammals such as humans and mice exhibit an “extreme” form of viviparity in which yolk and conceptus coats have become largely redundant. However, the “other” mammals—monotremes and marsupials—have retained and modified some features of reptilian development that provide valuable insights into the evolution of viviparity in mammals. Most striking of these are the conceptus coats, which include the zona pellucida, the mucoid coat, and the shell coat. We discuss current knowledge of these coats in monotremes and marsupials, their possible roles, and recently identified components such as the zona pellucida protein ZPAX, conceptus coat mucin (CCM), and nephronectin (NPNT).
Antimicrobial activity of red-tailed phascogale (Phascogale calura) serum
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Antimicrobial substances in serum include circulating complement proteins and acute phase proteins (APPs). We identified gene sequences for APPs, haptoglobin (Hp), C-reactive protein (CRP) and serum amyloid A (SAA) in marsupial genomes. Hp and SAA levels were measured in red-tailed phascogale (Phascogale calura) sera using commercially available assays. Hp levels were higher in males than females, while SAA levels suggest the phascogales used in this study were healthy. Serum was co-cultured with four bacterial species. Bacterial growth was inhibited after incubation at 37 °C, however effectiveness differed with bacteria and incubation time. The least amount of bacterial growth was noticed after introduction to K. pneumoniae, and most when introduced to P. aeruginosa. Despite marsupials not having mature immune tissues at birth, and unable to mount specific immune responses, this study suggests other immune strategies, such as APPs in serum likely aid marsupials in their defence against pathogens.
The Immune System of Monotremes and Marsupials
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Marsupials and monotremes are two lineages of mammals that have characteristically short gestation periods and give birth to immunologically naive young. These and other unique reproductive characteristics separate them from eutherian mammals. While originally thought to be ‘primitive,’ marsupials and monotremes have all cells and receptors required for a functioning immune system, including immune tissues, T and B cells, immunoglobulins, cytokines, and antigen receptors. Research in this field has progressed slowly due to the lack of species-specific reagents. However the increased availability of genome sequencing technology in the past decade has enabled in-depth analysis of marsupial and monotreme immunology. In addition, comparison across mammals has revealed insights into the evolution of the mammalian immune system.
Trophoblast specialisations during pregnancy in the tammar wallaby, Macropus eugenii: A morphological and lectin histochemical study
2014, Placenta
Citation Excerpt :
The thin, membranous yolk-sac placenta forms an intimate association with the endometrium and comprises non-vascular bilaminar and vascular trilaminar areas of trophoblast, both covered by endoderm cells that line the yolk sac. It has been proposed that the bilaminar area is concerned primarily with histiotrophe uptake while the trilaminar area is mainly involved in gas exchange [2–4]. The microvillous surface of the trophoblast lies over – and may interdigitate with – the microvilli of the underlying uterine epithelium which covers an endometrium supplied with blood vessels and furnished with uterine glands.
The tammar wallaby has a short gestation (26.5 days) and vascular modifications to expedite transport during that brief pregnancy. Here we examine trophoblast structural attributes that would facilitate materno-fetal exchange.
Four specimens of Macropus eugenii between days 23 and 26 gestation were examined using electron microscopy and 24 lectins to characterise glycosylated secretions and their internalisation.
Two trophoblast phenotypes were found, flattened cells generally in contact with the underlying uterine epithelium and giant cells associated with histiotrophe. The latter appeared to penetrate uterine clefts, occasionally detach and become necrotic. Lectin histochemistry and ultrastructure indicated the presence of many lysosomes and residual bodies especially in trophoblast giant cells; these contained glycans, mainly apically, which were also detected in secretions and cell debris. Trophoblast basal membranes bore extensive filopodia. Giant cells were less common in vascular trilaminar areas and here the trophoblast barrier became thinner near term.
Loss of Maackia amurensis agglutinin binding suggested cleavage of terminal sialic acid residues as an early post-internalisation event in the trophoblast. Lectin staining indicated degradation occurred in an apical–basal direction, and the heavily glycosylated basal membrane appeared specialised for transport out of the cell.
Granules seen ultrastructurally and histochemically, particularly in giant trophoblast cells of the bilaminar area, suggest that internalised histiotrophe is broken down here and nutrients transferred to the embryo via the specialised basal plasma membrane. The trilaminar vascular area contained mostly flattened trophoblast cells, supporting the suggestion that gaseous exchange is its primary function.
The fetomaternal interface shows vascular hypoglycosylation in the tammar wallaby Macropus eugenii: Comparison with a range of non-mammalian and eutherian placentae
2013, Placenta
Citation Excerpt :
The tammar wallaby, Macropus eugenii, has a choriovitelline (yolk sac) placenta apposed to the uterine epithelium for a period of 26–27 days, consisting of non-vascular (bilaminar) and vascular (trilaminar) regions of the omphalopleure [1]. The bilaminar region appears to be the primary route for transfer of nutrients, while the trilaminar omphalopleure is likely the site of most gaseous exchange [1–3]. Uterine gland secretions (histiotrophe) nourish the embryo via a close interdigitation of the trophoblast with the uterine endometrium until birth after which development of the young is completed within the mother's pouch.
Blood vessel glycosylation at the fetomaternal interface of four near-term specimens of tammar wallaby, Macropus eugenii, has been examined at days 23–26 of the 26.5 day pregnancy and compared with that of other species.
A panel of 23 lectins was used to compare vasculature in tammar with non-mammalian (shark, skink) and eutherian species at early and late gestation (camel, horse and alpaca), and term/near-term (cat, lion, dog, mink and elephant).
Strikingly low levels of all the glycans tested, apart from sialic acids, were found in capillary endothelium of both the trilaminar omphalopleure and underlying surface endometrium of the tammar, though deeper endometrial vessels showed normally high levels of glycosylation. Only maternal vasculature of the mink placenta showed a comparable lack of expression.
One reason for a reduced endothelial glycocalyx may be to facilitate diffusion of gases and nutrients as the tammar trophoblast lacks the indentation by overlying vessels that is seen in the other near-term placentae. Early epitheliochorial placentae of other species with equal diffusion distances to the tammar, showed normal vascular glycosylation. However, their pregnancies are much longer.
The hypoglycosylation of tammar vessels at the fetomaternal interface may allow continued transfer of nutrients and gaseous exchange during the extremely rapid period of organogenesis which occurs during the short 26.5 day pregnancy of this marsupial. Given the short gestation period of the tammar, we suggest that a thinner endothelial glycocalyx has evolved to facilitate diffusion of gases and nutrients between the maternal and fetal compartments.

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^☆: This study was supported in part by a grant from the Commonwealth Scientific and Industrial Research Organization to Dr. C. H. Tyndale-Biscoe.

¹: Present address: Department of Zoology, The University of Tennessee, Knoxville, Tennessee 37916.

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Full paperThe composition of fetal fluids of the marsupial Macropus eugenii☆

Abstract

Amer. J. Obstet. Gynecol

Amer. J. Obstet. Gynecol

J. Biol. Chem

Methods in Enzymol

Develop. Biol

Develop. Biol

Amer. J. Obstet. Gynecol

Amer. J. Obstet. Gynecol

The colorimetric determination of urea

J. Biol. Chem

The origin and nature of proteins of the liquor amnii in the rhesus monkey: a new protein with some unusual properties

J. Physiol. (London)

The metabolism of carbohydrate and volatile fatty acids in the marsupial, Setonix brachyurus

Quart. J. Exp. Physiol

Biochemisch-entwicklungsphysiologische Untersuchungen am Proteinmilieu für die Blastozystenentwicklung des Kaninchens (Oryctolagus cuniculus)

Zool. Jahrb. (Anat.) Bd

Composition of amniotic fluid

Clin. Obstet. Gynecol

The transmission of passive immunity from mother to young

Electrophoretic studies of serum proteins of foetal rabbits

Modified reagents for the determination of urea and ammonia

Clin. Chim. Acta

Simplified “disc” (polyacrylamide gel) electrophoresis

Ann. N. Y. Acad. Sci

Composition of the foetal fluids of the rabbit

J. Embryol. Exp. Morphol

Disc electrophoresis. II. Method and application to human serum proteins

Ann. N. Y. Acad. Sci

The composition and origin of the allantoic fluid in the rabbit

J. Embryol. Exp. Morphol

Full paper
The composition of fetal fluids of the marsupial Macropus eugenii☆