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Published in: Reproductive Biology and Endocrinology 1/2012

Open Access 01-12-2012 | Research

The fetomaternal interface in the placenta of three species of armadillos (Eutheria, Xenarthra, Dasypodidae)

Authors: Lorenna C Rezende, Claudio G Barbeito, Phelipe O Favaron, Andrea Mess, Maria A Miglino

Published in: Reproductive Biology and Endocrinology | Issue 1/2012

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Abstract

Background

Placental characters vary among Xenarthra, one of four supraordinal clades of Eutheria. Armadillos are known for villous, haemochorial placentas similar to humans. Only the nine-banded armadillo has been well studied so far.

Methods

Placentas of three species of armadillos were investigated by means of histology, immunohistochemistry including proliferation marker, and transmission and scanning electron microscopy.

Results

The gross anatomy differed: Euphractus sexcinctus and Chaetophractus villosus had extended, zonary placentas, whereas Chaetophractus vellerosus had a disk. All taxa had complex villous areas within the maternal blood sinuses of the endometrium. Immunohistochemistry indicated the validity of former interpretations that the endothelium of the sinuses was largely intact. Tips of the villi and the columns entering the maternal tissue possessed trophoblast cell clusters with proliferation activity. Elsewhere, the feto-maternal barrier was syncytial haemochorial with fetal vessels near the surface.

Conclusions

Differences among armadillos occurred in regard to the extension of the placenta, whereas the fine structure was similar. Parallels to the human suggest that armadillos are likely to be useful animal models for human placentation.
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Literature
1.
go back to reference Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ: Molecular phylogenetics and the origins of placental mammals. Nature. 2001, 409: 614-618. 10.1038/35054550.CrossRefPubMed Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ: Molecular phylogenetics and the origins of placental mammals. Nature. 2001, 409: 614-618. 10.1038/35054550.CrossRefPubMed
2.
go back to reference Springer MS, Stanhope MJ, Madsen O, Jong WW: Molecules consolidate the placental mammal tree. Trends Ecol Evol. 2004, 19: 430-438. 10.1016/j.tree.2004.05.006.CrossRefPubMed Springer MS, Stanhope MJ, Madsen O, Jong WW: Molecules consolidate the placental mammal tree. Trends Ecol Evol. 2004, 19: 430-438. 10.1016/j.tree.2004.05.006.CrossRefPubMed
3.
go back to reference Springer MS, Murphy WJ: Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev. 2007, 82: 375-392.CrossRefPubMed Springer MS, Murphy WJ: Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev. 2007, 82: 375-392.CrossRefPubMed
4.
go back to reference Delsuc F, Scally M, Madsen O, Stanhope MJ, Jong WW, Catzeflis FM, Springer MS, Douzery EJP: Molecular phylogeny of living Xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Mol Biol Evol. 2002, 19: 1656-1671. 10.1093/oxfordjournals.molbev.a003989.CrossRefPubMed Delsuc F, Scally M, Madsen O, Stanhope MJ, Jong WW, Catzeflis FM, Springer MS, Douzery EJP: Molecular phylogeny of living Xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Mol Biol Evol. 2002, 19: 1656-1671. 10.1093/oxfordjournals.molbev.a003989.CrossRefPubMed
5.
go back to reference Mess A, Carter AM: Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J Exp Zool Part B: Mol Dev Evol. 2006, 306B: 140-163. 10.1002/jez.b.21079.CrossRef Mess A, Carter AM: Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J Exp Zool Part B: Mol Dev Evol. 2006, 306B: 140-163. 10.1002/jez.b.21079.CrossRef
6.
go back to reference Mess A, Carter AM: Evolution of the placenta during the early radiation of placental mammals. Comp Biochem Physiol. 2007, 148: 769-779. 10.1016/j.cbpa.2007.01.029. Part ACrossRef Mess A, Carter AM: Evolution of the placenta during the early radiation of placental mammals. Comp Biochem Physiol. 2007, 148: 769-779. 10.1016/j.cbpa.2007.01.029. Part ACrossRef
7.
go back to reference Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R: Evolution of the mammalian placenta revealed by phylogenetic analysis. PNAS. 2006, 103: 3203-3208. 10.1073/pnas.0511344103.PubMedCentralCrossRefPubMed Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R: Evolution of the mammalian placenta revealed by phylogenetic analysis. PNAS. 2006, 103: 3203-3208. 10.1073/pnas.0511344103.PubMedCentralCrossRefPubMed
8.
go back to reference Elliot MG, Crespi BJ: Phylogenetic evidence for early hemochorial placentation in Eutheria. Placenta. 2009, 30: 49-67.CrossRef Elliot MG, Crespi BJ: Phylogenetic evidence for early hemochorial placentation in Eutheria. Placenta. 2009, 30: 49-67.CrossRef
9.
go back to reference Martin RD: Evolution of placentation in primates: implications of mammalian phylogeny. Evol Biol. 2008, 35: 125-145. 10.1007/s11692-008-9016-9.CrossRef Martin RD: Evolution of placentation in primates: implications of mammalian phylogeny. Evol Biol. 2008, 35: 125-145. 10.1007/s11692-008-9016-9.CrossRef
10.
go back to reference Thornburg LL, Hunt JS: Contemparary comparative placenta research - an interview with Allen Enders. Int J Dev Biol. 2010, 54: 231-236. 10.1387/ijdb.082837kt.CrossRef Thornburg LL, Hunt JS: Contemparary comparative placenta research - an interview with Allen Enders. Int J Dev Biol. 2010, 54: 231-236. 10.1387/ijdb.082837kt.CrossRef
11.
go back to reference Enders AC: Development and structure of the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat. 1960, 94: 34-45.PubMedCentralPubMed Enders AC: Development and structure of the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat. 1960, 94: 34-45.PubMedCentralPubMed
12.
go back to reference Enders AC: Electron microscopic observations on the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat. 1960, 94: 205-215.PubMedCentralPubMed Enders AC: Electron microscopic observations on the villous haemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J Anat. 1960, 94: 205-215.PubMedCentralPubMed
13.
go back to reference Enders AC: Placentation in armadillos, with emphasis on development of the placenta in polyembryonic species. The biology of the Xenarthra. Edited by: Vizcaíno SFL, Loughry WJ. 2008, University Press of Florida, Gainesville, 172-180. Enders AC: Placentation in armadillos, with emphasis on development of the placenta in polyembryonic species. The biology of the Xenarthra. Edited by: Vizcaíno SFL, Loughry WJ. 2008, University Press of Florida, Gainesville, 172-180.
14.
go back to reference Carter AM, Enders AC: The evolving placenta: Different developmental paths to a hemochorial relationship. Placenta. 2012, 33: S92-S98.CrossRefPubMed Carter AM, Enders AC: The evolving placenta: Different developmental paths to a hemochorial relationship. Placenta. 2012, 33: S92-S98.CrossRefPubMed
15.
go back to reference Benirschke K, Kaufmann P, Baergen R: Pathology of the human placenta. 2006, Springer, New York, 1050- Benirschke K, Kaufmann P, Baergen R: Pathology of the human placenta. 2006, Springer, New York, 1050-
16.
17.
go back to reference Strahl VH: Über den Bau der Placenta von Dasypus novemcinctus. Anat Anz. 1913, 44: 440-447. Strahl VH: Über den Bau der Placenta von Dasypus novemcinctus. Anat Anz. 1913, 44: 440-447.
18.
go back to reference Fernández M: Zur Anordnung der Embryonen und Form der Placenta bei Tatusia novemcincta. Anat Anz. 1914, 46: 253-258. Fernández M: Zur Anordnung der Embryonen und Form der Placenta bei Tatusia novemcincta. Anat Anz. 1914, 46: 253-258.
19.
go back to reference Enders AC, Welsh AO: Structural interactions of trophoblast and uterus during hemochorial placenta formation. J Exp Zool. 1993, 266: 578-587. 10.1002/jez.1402660608.CrossRefPubMed Enders AC, Welsh AO: Structural interactions of trophoblast and uterus during hemochorial placenta formation. J Exp Zool. 1993, 266: 578-587. 10.1002/jez.1402660608.CrossRefPubMed
21.
go back to reference Fernández M: Über einige Entwickelungsstadien des Peludo (Dasypus villosus) und ihre Beziehung zum Problem der spezifischen Polyembryonie des Genus Tatusia. Anat Anz. 1915, 48: 305-327. Fernández M: Über einige Entwickelungsstadien des Peludo (Dasypus villosus) und ihre Beziehung zum Problem der spezifischen Polyembryonie des Genus Tatusia. Anat Anz. 1915, 48: 305-327.
22.
go back to reference Adamoli VC, Cetica PD, Merani MS, Solari AJ: Comparative morphologic placental types in Dasypodidae (Chaetophractus villosus, Cabassous chacoensis, Tolypeutes matacus and Dasypus hybridus). Biocell. 2001, 25: 17-22.PubMed Adamoli VC, Cetica PD, Merani MS, Solari AJ: Comparative morphologic placental types in Dasypodidae (Chaetophractus villosus, Cabassous chacoensis, Tolypeutes matacus and Dasypus hybridus). Biocell. 2001, 25: 17-22.PubMed
24.
go back to reference Redford KH, Eisenberg JF: Mammals of the Neotropics. The Southern Cone. Chile, Argentinia, Uruguay, Paraguay. 1992, University of Chicago Press, Illinois, 440- Redford KH, Eisenberg JF: Mammals of the Neotropics. The Southern Cone. Chile, Argentinia, Uruguay, Paraguay. 1992, University of Chicago Press, Illinois, 440-
25.
go back to reference Redford KH: The Edentates of the cerrado. Edentata. 1994, 1: 4-10. Redford KH: The Edentates of the cerrado. Edentata. 1994, 1: 4-10.
26.
go back to reference Cuellar E: Biology and ecology of armadillos in the Bolivian chaco. The biology of the Xenarthra. Edited by: Vizcaíno SF, Loughry WJ. 2008, University Press of Florida, Gainesville Cuellar E: Biology and ecology of armadillos in the Bolivian chaco. The biology of the Xenarthra. Edited by: Vizcaíno SF, Loughry WJ. 2008, University Press of Florida, Gainesville
27.
go back to reference García SV: Especies locales, mercado y transporte en las investigaciones embriológicas: el estudio de la poliembrionía en armadillos a principios del siglo XX. Hist Ciênc Saúde-Manguinhos. 2008, 15: 697-717.CrossRefPubMed García SV: Especies locales, mercado y transporte en las investigaciones embriológicas: el estudio de la poliembrionía en armadillos a principios del siglo XX. Hist Ciênc Saúde-Manguinhos. 2008, 15: 697-717.CrossRefPubMed
28.
go back to reference Bonato Vc, Martins EG, Machado G, da-Silva CQ, dos Reis SrF: Ecology of the Armadillos Cabassous unicinctus and Euphractus sexcinctus (Cingulata: Dasypodidae) in a Brazilian Cerrado. J Mammal. 2009, 89: 168-174.CrossRef Bonato Vc, Martins EG, Machado G, da-Silva CQ, dos Reis SrF: Ecology of the Armadillos Cabassous unicinctus and Euphractus sexcinctus (Cingulata: Dasypodidae) in a Brazilian Cerrado. J Mammal. 2009, 89: 168-174.CrossRef
29.
go back to reference Miglino MA, Carter AM, Ambrosio CE, Bonatelli M, De Oliveira MF, Dos Santos, Ferraz RH, Rodrigues RF, Santos TC: Vascular organization of the hystricomorph placenta: a comparative study in the agouti, capybara, Guinea pig, paca and Rock cavy. Placenta. 2004, 25: 438-448. 10.1016/j.placenta.2003.11.002.CrossRefPubMed Miglino MA, Carter AM, Ambrosio CE, Bonatelli M, De Oliveira MF, Dos Santos, Ferraz RH, Rodrigues RF, Santos TC: Vascular organization of the hystricomorph placenta: a comparative study in the agouti, capybara, Guinea pig, paca and Rock cavy. Placenta. 2004, 25: 438-448. 10.1016/j.placenta.2003.11.002.CrossRefPubMed
30.
go back to reference Kanashiro C, Santos TC, Miglino MA, Mess AM, Carter AM: Growth and development of the placenta in the capybara (Hydrochaeris hydrochaeris). Reprod Biol Endocrinol. 2009, 7: 57-10.1186/1477-7827-7-57.PubMedCentralCrossRefPubMed Kanashiro C, Santos TC, Miglino MA, Mess AM, Carter AM: Growth and development of the placenta in the capybara (Hydrochaeris hydrochaeris). Reprod Biol Endocrinol. 2009, 7: 57-10.1186/1477-7827-7-57.PubMedCentralCrossRefPubMed
31.
go back to reference Oliveira MF, Favaron PO, Ambrosio CE, Miglino MA, Mess A: Chorioallantoic and yolk sac placentation in Thrichomys laurentinus (Echimyidae) and the evolution of hystricognath rodents. J Exp Zool B (Mol Dev Evol). 2012, 318: 13-25.CrossRef Oliveira MF, Favaron PO, Ambrosio CE, Miglino MA, Mess A: Chorioallantoic and yolk sac placentation in Thrichomys laurentinus (Echimyidae) and the evolution of hystricognath rodents. J Exp Zool B (Mol Dev Evol). 2012, 318: 13-25.CrossRef
32.
go back to reference Vicovac LJ, Jones CJP, Aplin JD: Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta. 1995, 16: 41-56. 10.1016/0143-4004(95)90080-2.CrossRefPubMed Vicovac LJ, Jones CJP, Aplin JD: Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta. 1995, 16: 41-56. 10.1016/0143-4004(95)90080-2.CrossRefPubMed
33.
go back to reference Huppertz B, Frank HG, Kingdom JCP, Reister F, Kaufmann P: Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem Cell Biol. 1998, 110: 495-508. 10.1007/s004180050311.CrossRefPubMed Huppertz B, Frank HG, Kingdom JCP, Reister F, Kaufmann P: Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem Cell Biol. 1998, 110: 495-508. 10.1007/s004180050311.CrossRefPubMed
34.
go back to reference Pijnenborg R, Robertson WB, Brosens I, Dixon G: Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta. 1981, 2: 71-92. 10.1016/S0143-4004(81)80042-2.CrossRefPubMed Pijnenborg R, Robertson WB, Brosens I, Dixon G: Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta. 1981, 2: 71-92. 10.1016/S0143-4004(81)80042-2.CrossRefPubMed
35.
go back to reference Kaufmann P, Castellucci M: Extravillous trophoblast in the human placenta. Placenta. 1997, 18: 21-65.CrossRef Kaufmann P, Castellucci M: Extravillous trophoblast in the human placenta. Placenta. 1997, 18: 21-65.CrossRef
Metadata
Title
The fetomaternal interface in the placenta of three species of armadillos (Eutheria, Xenarthra, Dasypodidae)
Authors
Lorenna C Rezende
Claudio G Barbeito
Phelipe O Favaron
Andrea Mess
Maria A Miglino
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2012
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-10-38

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