Opossum Development

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Introduction

Opossum and pups
Opossum and pups[1]

The opossums are a family of nocturnal semi-arboreal marsupials including the cuscuses, brushtail possums, and their close relatives.

Links: Category:Marsupial
Historic Embryology: 1918 big-eared opossum | 1928 breeding season

Some Recent Findings

  • Embryo implantation evolved from an ancestral inflammatory attachment reaction[2] "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. ...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." implantation
  • On the prenatal initiation of T cell development in the opossum Monodelphis domestica[3] "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." blood | thymus
  • A new mammalian model system for thalidomide teratogenesis: Monodelphis domestica [4] "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." thalidomide
More recent papers  
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Search term: Opossum Embryology

Reda Mohamed ##Title## Vet Sci: 2018, 5(2); PubMed 29690583

Reda Mohamed A Descriptive Morphometric Approach of the Skull and Mandible of the Common Opossum (Didelphis Marsupialis Linnaeus, 1758) in the Caribbean and its Clinical Application during Regional Anaesthesia. Vet Sci: 2018, 5(1); PubMed 29522485

Oliver W Griffith, Arun R Chavan, Stella Protopapas, Jamie Maziarz, Roberto Romero, Gunter P Wagner Embryo implantation evolved from an ancestral inflammatory attachment reaction. Proc. Natl. Acad. Sci. U.S.A.: 2017; PubMed 28747528

Daniel Sorensen, Amanda Sackett, Daniel J Urban, Jennifer Maier, Neil Vargesson, Karen E Sears A new mammalian model system for thalidomide teratogenesis: Monodelphis domestica. Reprod. Toxicol.: 2017; PubMed 28130151

Victoria L Hansen, Robert D Miller On the prenatal initiation of T cell development in the opossum Monodelphis domestica. J. Anat.: 2017; PubMed 28052333

Older papers  
  • Comparative gene expression analyses reveal heterochrony for Sox9 expression in the cranial neural crest during marsupial development[5] "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."
  • Developmental origins of precocial forelimbs in marsupial neonates[6] "Marsupial mammals are born in an embryonic state, as compared with their eutherian counterparts, yet certain features are accelerated. The most conspicuous of these features are the precocial forelimbs, which the newborns use to climb unaided from the opening of the birth canal to the teat. The developmental mechanisms that produce this acceleration are unknown. Here we show that heterochronic and heterotopic changes early in limb development contribute to forelimb acceleration. Using Tbx5 and Tbx4 as fore- and hindlimb field markers, respectively, we have found that, compared with mouse, both limb fields arise notably early during opossum development."

Taxon

Phylogenetic tree of marsupialsNilsson MA, Churakov G, Sommer M, Tran NV, Zemann A, Brosius J & Schmitz J. (2010). Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol. , 8, e1000436. PMID: 20668664 DOI.

Taxonomy ID:

Genbank common name: opossum

Rank: species

Genetic code: Translation table 1 (Standard)

Mitochondrial genetic code: Translation table 2 (Vertebrate Mitochondrial)

Lineage ( full )

Links: Taxonomy Browser Phalangeridae
Marsupial - Opossum Taxon List  
Taxon Name Common Name
Chacodelphys formosa Chacoan pygmy opossum
Gracilinanus marica northern gracile opossum
Marmosops juninensis Junin slender opossum
Marmosops ojastii Ojasti's slender mouse opossum
Marmosops ocellatus spectacled slender opossum
Marmosops creightoni Voss' slender opossum
Marmosops bishopi Bishop's slender opossum
Marmosops fuscatus dusky slender opossum
Cryptonanus guahybae Guahiba gracile opossum
Monodelphis palliolata hooded red-sided opossum
Monodelphis gardneri Gardner's short-tailed opossum
Caenolestes convelatus northern shew opossum
Caenolestes sangay Sangay shrew opossum
Marmosops paulensis Brazilian slender opossum
Philander opossum fuscogriseus subspecies
Cryptosporidium sp. apicomplexans
Didelphis pernigra Andean white-eared opossum
Caluromys derbianus Derby's woolly opossum
Monodelphis umbristriata Red three-striped opossum
Monodelphis scalops Long-nosed short-tailed opossum
Monodelphis sorex Southern red-sided opossum
Monodelphis glirina Amazonian red-sided opossum
Thylamys tatei Tate's fat-tailed mouse opossum
Thylamys sponsorius Argentine fat-tailed mouse opossum
Cryptosporidium sp. oposapicomplexans
Micoureus constantiae White-bellied woolly mouse opossum
Marmosa tyleriana Tyleria mouse opossum
Marmosa xerophila Guajira mouse opossum
Monodelphis americana Northern three-striped opossum
Trichosurus cunninghami Mountain brushtail opossum
Monodelphis iheringi Ihering's three-striped opossum
Caenolestes caniventer grey-bellied shrew opossum
Marmosops invictus Panama slendeer opossum
Didelphis imperfecta Guianan white-eared opossum
Thylamys velutinus Dwarf fat-tailed mouse opossum
Marmosops handleyi Handley's slender mouse opossum
Monodelphis osgoodi Osgood's short-tailed opossum
Hyladelphys kalinowskii Kalinowski's opossum
Gracilinanus aceramarcae Aceramarca gracile mouse opossum
Gracilinanus emiliae Emilia's gracile mouse opossum
Thylamys cinderella Cinderella fat-tailed opossum
Micoureus paraguayanus Tate's wolly mouse opossum
Tlacuatzin canescens grayish mouse opossum
Philander frenatus Southeastern four-eyed oppossum
Marmosops incanus gray slender mouse opossum
Monodelphis theresa Theresa's short-tailed opossum
Marmosa mexicana Mexican mouse opossum
Marmosa andersoni Anderson's mouse opossum
Monodelphis kunsi Pygmy short-tailed Opossum
Monodelphis brevicaudata Red-legged short-tailed Opossum
Thylamys pusillus Common fat-tailed mouse opossum
Thylamys macrura long-tailed fat-tailed opossum
Thylamys elegans elegant fat-tailed opossum
Gracilinanus agilis Agile Gracile Mouse Opossum
Thylamys pallidior pallid fat-tailed opossum
Monodelphis emiliae Emilia's short-tailed opossum
Marmosops parvidens delicate slender mouse opossum
Marmosops noctivagus white-bellied slender mouse opossum
Marmosa murina murine mouse opossum
Marmosa lepida little rufous mouse opossum
Lestodelphys halli Patagonian opossum
Gracilinanus microtarsus Brazilian gracile mouse opossum
Caluromysiops irrupta black-shouldered opossum
Gnathostoma sp. from P.
Chironectes minimus water opossum
Marmosops dorothea Dorothy's slender mouse opossum
Marmosa robinsoni Robinson's mouse opossum
Didelphis aurita big-eared opossum
Caluromys philander bare-tailed woolly opossum
Lestoros inca Incan shrew opossum
Philander opossum Philander opossum
Monodelphis adusta sepia short-tailed opossum
Metachirus nudicaudatus brown four-eyed opossum
Marmosops impavidus Andean slender mouse opossum
Micoureus regina Short-furred woolly mouse opossum
Micoureus demerarae long-furred woolly mouse opossum
Marmosa rubra red mouse opossum
Didelphis albiventris white-eared opossum
Glironia venusta bushy-tailed opossum
Caluromys lanatus western woolly opossum
Lutreolina crassicaudata thick-tailed opossum
Caenolestes fuliginosus silky shrew opossum
Rhyncholestes raphanurus Chilean shrew opossum
Monodelphis domestica gray short-tailed opossum
Philander opossum gray four-eyed opossum
Didelphis marsupialis southern opossum
Didelphis virginiana North American opossum

Development Overview

Opossum and day 7 pups.jpg

Opossum and day 7 pups[7]

System Development

The marsupial neonate at birth has a variation between the degree of development of different systems.[8]

  • well-developed - digestive, respiratory and circulatory system.
  • not well-developed - retains fetal excretory system with a fully functional mesonephric kidney and undifferentiated gonads and genitalia.

Oocyte

Ovarian Follicle Development

Marsupial eggs are enclosed by a series of layers:[9]

  • zona pellucida, three zona proteins (ZPA, ZPB, ZPC)
      • an additional extracellular matrix coat that lines the zona pellucida also occurs in some species.
  • mucoid coat
  • outer shell coat.


Links: oocyte

Spermatozoa

Links: spermatozoa

References

  1. 22073202</pubmed>
  2. 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.
  3. 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.
  4. 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.
  5. Wakamatsu Y, Nomura T, Osumi N & Suzuki K. (2014). Comparative gene expression analyses reveal heterochrony for Sox9 expression in the cranial neural crest during marsupial development. Evol. Dev. , 16, 197-206. PMID: 24934187 DOI.
  6. Keyte AL & Smith KK. (2010). Developmental origins of precocial forelimbs in marsupial neonates. Development , 137, 4283-94. PMID: 21098569 DOI.
  7. Wheaton BJ, Callaway JK, Ek CJ, Dziegielewska KM & Saunders NR. (2011). Spontaneous development of full weight-supported stepping after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. PLoS ONE , 6, e26826. PMID: 22073202 DOI.
  8. Renfree MB, Pask AJ & Shaw G. (2001). Sex down under: the differentiation of sexual dimorphisms during marsupial development. Reprod. Fertil. Dev. , 13, 679-90. PMID: 11999321
  9. Selwood L. (2000). Marsupial egg and embryo coats. Cells Tissues Organs (Print) , 166, 208-19. PMID: 10729728 DOI.

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Cite this page: Hill, M.A. (2018, October 15) Embryology Opossum Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Opossum_Development

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© Dr Mark Hill 2018, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G