Talk:Opossum Development

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Cite this page: Hill, M.A. (2024, April 26) Embryology Opossum Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Talk:Opossum_Development

2019

Sequence alteration in the enhancer contributes to the heterochronic Sox9 expression in marsupial cranial neural crest

Dev Biol. 2019 Dec 1;456(1):31-39. doi: 10.1016/j.ydbio.2019.08.010. Epub 2019 Aug 17.

Wakamatsu Y1, Suzuki K2. Author information 1 Department of Developmental Neuroscience, United Centers for Advanced Research and Translational Medicine (ART), Tohoku University Graduate School of Medicine, Sendai, Miyagi, 980-8575, Japan. Electronic address: wakasama@med.tohoku.ac.jp. 2 Department of Biology, Nihon University School of Dentistry at Matsudo, Chiba, 271-8587, Japan. Abstract Neonates of marsupial mammals are altricial at birth, because their gestation period is relatively short compared to placental mammals. Yet, as they need to travel to the teat from the birth canal, and suckle on the mother's milk, forelimbs and jaws develop significantly early. Previous studies in opossum (Monodelphis domestica), an experimental marsupial model, have revealed that cranial neural crest cells are generated significantly early compared to those in placental mammals, such as mouse, leading to an early development of jaw primordia. We have previously found that Sox9, an important neural crest-specifier gene, is expressed in the future cranial neural crest of the opossum embryonic ectoderm significantly earlier than that in mouse or quail embryos. As Sox9 is essential for neural crest formation in various vertebrates, it seems likely that the heterochronic expression of Sox9 is critical for the early cranial neural crest formation in the marsupial embryos. In this study, we show a marsupial-specific sequence in the Sox9 neural crest enhancer E3. We also reveal that the mouse E3 enhancer is activated in the cranial neural crest cells of quail embryos, that the E3 enhancer with marsupial-specific sequence is activated earlier in the Pax7-expressing neural border prior to the onset of endogenous Sox9 expression, and that a misexpression of cMyb, which is also a transcriptional activator of Pax7, in the neural border can ectopically activate the "marsupialized" enhancer. Thus, we suggest that the modification of the E3 enhancer sequence in the marsupial ancestor would have promoted the early expression of Sox9 in the neural border, facilitating the early formation of the cranial neural crest cells and the subsequent heterochronic development of the jaw primordia. Copyright © 2019 Elsevier Inc. All rights reserved. KEYWORDS: Cranial neural crest; Enhancer; Heterochrony; Marsupial; Neural border; Pax7; Sox9; cMyb PMID: 31430446 DOI: 10.1016/j.ydbio.2019.08.010

2018

Modepalli V, Kumar A, Sharp JA, Saunders NR, Nicholas KR & Lefèvre C. (2018). Gene expression profiling of postnatal lung development in the marsupial gray short-tailed opossum (Monodelphis domestica) highlights conserved developmental pathways and specific characteristics during lung organogenesis. BMC Genomics , 19, 732. PMID: 30290757 DOI.

Gene expression profiling of postnatal lung development in the marsupial gray short-tailed opossum (Monodelphis domestica) highlights conserved developmental pathways and specific characteristics during lung organogenesis.

After a short gestation, marsupials give birth to immature neonates with lungs that are not fully developed and in early life the neonate partially relies on gas exchange through the skin. Therefore, significant lung development occurs after birth in marsupials in contrast to eutherian mammals such as humans and mice where lung development occurs predominantly in the embryo. To explore the mechanisms of marsupial lung development in comparison to eutherians, morphological and gene expression analysis were conducted in the gray short-tailed opossum (Monodelphis domestica).

2017

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Griffith OW, Chavan AR, Protopapas S, Maziarz J, Romero R & Wagner GP. (2017). Embryo implantation evolved from an ancestral inflammatory attachment reaction. Proc. Natl. Acad. Sci. U.S.A. , 114, E6566-E6575. PMID: 28747528 DOI.

Griffith OW1,2, Chavan AR3,2, Protopapas S3,2, Maziarz J3,2, Romero R4,5,6,7, Wagner GP3,2,8,9. Author information Abstract The molecular changes that support implantation in eutherian mammals are necessary to establish pregnancy. In marsupials, pregnancy is relatively short, and although a placenta does form, it is present for only a few days before parturition. However, morphological changes in the uterus of marsupials at term mimic those that occur during implantation in humans and mice. We investigated the molecular similarity between term pregnancy in the marsupials and implantation in eutherian mammals using the gray short-tailed opossum (Monodelphis domestica) as a model. Transcriptomic analysis shows that term pregnancy in the opossum is characterized by an inflammatory response consistent with implantation in humans and mice. This immune response is temporally correlated with the loss of the eggshell, and we used immunohistochemistry to report that this reaction occurs at the materno-fetal interface. We demonstrate that key markers of implantation, including Heparin binding EGF-like growth factor and Mucin 1, exhibit expression and localization profiles consistent with the pattern observed during implantation in eutherian mammals. Finally, we show that there are transcriptome-wide similarities between the opossum attachment reaction and implantation in rabbits and humans. Our data suggest that the implantation reaction that occurs in eutherians is derived from an attachment reaction in the ancestral therian mammal which, in the opossum, leads directly to parturition. Finally, we argue that the ability to shift from an inflammatory attachment reaction to a noninflammatory period of pregnancy was a key innovation in eutherian mammals that allowed an extended period of intimate placentation. KEYWORDS: evolution; inflammation; marsupial; placenta; pregnancy Comment in Implantation in eutherians: Which came first, the inflammatory reaction or attachment? [Proc Natl Acad Sci U S A. 2018] Reply to Liu: Inflammation before implantation both in evolution and development. [Proc Natl Acad Sci U S A. 2018] PMCID: PMC5559003 DOI: 10.1073/pnas.1701129114

On the prenatal initiation of T cell development in the opossum Monodelphis domestica

Hansen VL & Miller RD. (2017). On the prenatal initiation of T cell development in the opossum Monodelphis domestica. J. Anat. , 230, 596-600. PMID: 28052333 DOI.

Hansen VL1, Miller RD1,2. Author information Abstract Thymus-dependent lymphocytes (T cells) are a critical cell lineage in the adaptive immune system of all jawed vertebrates. In eutherian mammals the initiation of T cell development takes place prenatally and the offspring of many species are born relatively immuno-competent. Marsupials, in contrast, are born in a comparatively altricial state and with a less well developed immune system. As such, marsupials are valuable models for studying the peri- and postnatal initiation of immune system development in mammals. Previous results supported a lack of prenatal T cell development in a variety of marsupial species. In the gray short-tailed opossum, Monodelphis domestica, however, there was evidence that αβT cells were present on postnatal day 1 and likely initiated development prenatally. Demonstrated here is the presence of CD3ε+ lymphocytes in late-stage embryos at a site in the upper thoracic cavity, the site of an early developing thymus. CD3ε+ cells were evident as early as 48 h prior to parturition. In day 14 embryos, where there is clear organogenesis, CD3ε+ cells were only found at the site of the early thymus, consistent with no extra-thymic sites of T cell development in the opossum. These observations are the first evidence of prenatal T cell lineage commitment in any marsupial. KEYWORDS: T cell; embryonic development; marsupial; thymus PMCID: PMC5345628 DOI: 10.1111/joa.12587

A new mammalian model system for thalidomide teratogenesis: Monodelphis domestica

Sorensen D, Sackett A, Urban DJ, Maier J, Vargesson N & Sears KE. (2017). A new mammalian model system for thalidomide teratogenesis: Monodelphis domestica. Reprod. Toxicol. , 70, 126-132. PMID: 28130151 DOI.

Sorensen D1, Sackett A1, Urban DJ1, Maier J1, Vargesson N2, Sears KE3. Author information Abstract From 1957 to 1962, thalidomide caused birth defects in >10,000 children. While the drug was pulled from the market, thalidomide is currently prescribed to treat conditions including leprosy. As a result, a new generation of babies with thalidomide defects is being born in the developing world. This represents a serious problem, as the mechanisms by which thalidomide disrupts development remain unresolved. This lack of resolution is due, in part, to the absence of an appropriate mammalian model for thalidomide teratogenesis. We test the hypothesis that opossum (Monodelphis domestica) is well suited to model human thalidomide defects. Results suggest that opossum embryos exposed to thalidomide display a range of phenotypes (e.g., heart, craniofacial, limb defects) and penetrance similar to humans. Furthermore, all opossums with thalidomide defects exhibit vascular disruptions. Results therefore support the hypotheses that opossums make a good mammalian model for thalidomide teratogenesis, and that thalidomide can severely disrupt angiogenesis in mammals. KEYWORDS: Angiogenesis; Congenital birth defects; Limb; Teratogen PMID: 28130151 DOI: 10.1016/j.reprotox.2017.01.010

2015

Exogenous retinoic acid induces digit reduction in opossums (Monodelphis domestica) by disrupting cell death and proliferation, and apical ectodermal ridge and zone of polarizing activity function

Birth Defects Res A Clin Mol Teratol. 2015 Mar;103(3):225-34. doi: 10.1002/bdra.23347. Epub 2015 Feb 6.

Molineaux AC1, Maier JA, Schecker T, Sears KE.

Abstract

BACKGROUND: Retinoic acid (RA) is a vitamin A derivative. Exposure to exogenous RA generates congenital limb malformations (CLMs) in species from frogs to humans. These CLMs include but are not limited to oligodactyly and long-bone hypoplasia. The processes by which exogenous RA induces CLMs in mammals have been best studied in mouse, but as of yet remain unresolved. METHODS: We investigated the impact of exogenous RA on the cellular and molecular development of the limbs of a nonrodent model mammal, the opossum Monodelphis domestica. Opossums exposed to exogenous retinoic acid display CLMs including oligodactly, and results are consistent with opossum development being more susceptible to RA-induced disruptions than mouse development. RESULTS: Exposure of developing opossums to exogenous RA leads to an increase in cell death in the limb mesenchyme that is most pronounced in the zone of polarizing activity, and a reduction in cell proliferation throughout the limb mesenchyme. Exogenous RA also disrupts the expression of Shh in the zone of polarizing activity, and Fgf8 in the apical ectodermal ridge, and other genes with roles in the regulation of limb development and cell death. CONCLUSION: Results are consistent with RA inducing CLMs in opossum limbs by disrupting the functions of the apical ectodermal ridge and zone of polarizing activity, and driving an increase in cell death and reduction of cell proliferation in the mesenchyme of the developing limb. © 2015 Wiley Periodicals, Inc. KEYWORDS: Fgf8; RA; Shh; limb development; teratogen

PMID 25656823

2014

Comparative gene expression analyses reveal heterochrony for Sox9 expression in the cranial neural crest during marsupial development

Evol Dev. 2014 Jul-Aug;16(4):197-206. doi: 10.1111/ede.12083. Epub 2014 Jun 17.

Wakamatsu Y1, Nomura T, Osumi N, Suzuki K.

Abstract

Compared to placental mammals, marsupials have short gestation period, and their neonates are relatively immature. Despite these features, marsupial neonates must travel from the birth canal to the teat, suckle and digest milk to complete development. Thus, certain organs and tissues of marsupial neonates, such as forelimbs to crawl and jaw elements to suckle, must develop early. Previous reports showed that cranial neural crest (CNC) cells, as the source of ectomesenchyme of jaw elements, are generated significantly early in gray short-tailed opossum (Monodelphis domestica) compared to other amniote models, such as mouse. In this study, we examined the expression of genes known to be important for neural crest formation, such as BMP2/BMP4 (neural crest inducer), Pax7 (neural border specifier), Snail1 and Sox9/Sox10 (neural crest specifier) in Monodelphis domestica, and compared the expression patterns with those in mouse, chicken, and gecko embryos. Among those genes, the expression of Sox9 was turned on early and broadly in the premigratory CNC cells, and persisted in the ectomesenchyme of the cranial anlagen in opossum embryos. In contrast, Sox9 expression diminished in the CNC cells of other animals at the early phase of migration. Comparison of the onset of Pax7 and Sox9 expression revealed that Sox9 expression in the prospective CNC was earlier and broader than Pax7 expression in opossum, suggesting that the sequence of border specification and neural crest specification is altered. This study provides the first clue for understanding the molecular basis for the heterochronic development of the CNC cells and jaw elements in marsupials. © 2014 Wiley Periodicals, Inc.

PMID 24934187