Placentation in Sigmodontinae: a rodent taxon native to South America
© Favaron et al; licensee BioMed Central Ltd. 2011
Received: 3 February 2011
Accepted: 25 April 2011
Published: 25 April 2011
Sigmodontinae, known as "New World rats and mice," is a large subfamily of Cricetidae for which we herein provide the first comprehensive investigation of the placenta.
Placentas of various gestational ages ranging from early pregnancy to near term were obtained for five genera, i.e. Necromys, Euryoryzomys, Cerradomys, Hylaeamys, and Oligoryzomys. They were investigated by means of histology, immunohistochemistry, a proliferation marker, DBA-lectin staining and transmission electron microscopy.
The chorioallantoic placenta was organized in a labyrinthine zone, spongy zone and decidua and an inverted yolk sac persisted until term. The chorioallantoic placenta was hemotrichorial. The interhemal barrier comprised fetal capillary endothelium and three layers of trophoblast, an outermost, cellular layer and two syncytial ones, with interspersed trophoblast giant cells (TGC). In addition, accumulations of TGC occurred below Reichert's membrane. The junctional zone contained syncytial trophoblast, proliferative cellular trophoblast, glycogen cells and TGC that were situated near to the maternal blood channels. In three of the genera, TGC were also accumulated in distinct areas at the placental periphery. PAS-positive glycogen cells derived from the junctional zone invaded the decidua. Abundant maternal uNK cells with positive response to PAS, vimentin and DBA-lectin were found in the decidua. The visceral yolk sac was completely inverted and villous.
The general aspect of the fetal membranes in Sigmodontinae resembled that found in other cricetid rodents. Compared to murid rodents there were larger numbers of giant cells and in some genera these were seen to congregate at the periphery of the placental disk. Glycogen cells were found to invade the decidua but we did not identify trophoblast in the walls of the deeper decidual arteries. In contrast these vessels were surrounded by large numbers of uNK cells. This survey of wild-trapped specimens from five genera is a useful starting point for the study of placentation in an important subfamily of South American rodents. We note, however, that some of these rodents can be captive bred and recommend that future studies focus on the study of time dated pregnancies.
Muridae and Cricetidae are the most species-rich families of rodents, with around 600 species in each family . For both taxa there are still important gaps in basic knowledge about reproductive biology. In particular, the development of the placenta is not well understood for the majority of species. Muridae includes several laboratory models, such as mouse and rat, for which placentation is very well documented [e.g., 2-9], yet 98% of the murid species have not been studied with regard to their placentation . Cricetidae is even less well covered although some basic data is available for the golden hamster Mesocricetus auratus from the subfamily Cricetinae [11–13]. In addition, some aspects of placentation have been documented for members of the subfamily Arvicolinae, namely voles and lemmings [14, 15], and the North American deer mouse Peromyscus maniculatus from the subfamily Neotominae [15, 16]. But for the largest subfamily, the Sigmodontinae, with 377 recognized species in 74 genera , data on placentation is very sparse. The only species studied so far is Calomys callosus, which has been used as an experimental model for parasitological and other diseases [17–22].
Sigmodontine rodents form a monophyletic clade [23–25]. These rodents are largely confined to the Neotropics , and are often referred to as "New World rats and mice". They are known to transmit diseases to humans and domestic animals. Antibody prevalence indicates that sigmodontine species are reservoirs of Hantavirus in the several regions of Brazil and other parts of Latin America . In addition, they are the most important reservoirs of zoonotic cutaneous leishmaniasis throughout their range . For this reason they are generally considered as pests. On the other hand, sigmodontine rodents usually possess restricted ranges, and are vulnerable to habitat loss. Thus, they may serve as indicators for biodiversity purposes . A better understanding of reproductive biology in these species is therefore desirable and needs to include a comprehensive analysis of placental development and structure.
We here provide a detailed study on placentation in five genera of sigmodontine rodents (Necromys, Euryoryzomys, Cerradomys, Hylaeamys and Oligoryzomys). Data on reproduction in this subfamily is sparse but where known gestation lasts 23 to 30 days, slightly longer than in mice, rats and other cricetids [9, 12, 26, 29]. Placentas from various gestational stages, ranging from early pregnancy to near term, have been studied by a variety of techniques including immunohistochemistry, DBA-lectin staining and transmission electron microscopy. The findings are compared and contrasted with what is known about placentation in other murid and cricetid rodents.
Material collected with values
Species and Collection Number
MAV (CEMAS 03)
MAV (CEMAS 04)
MAV (CEMAS 05)
MZUSP (APC 1140)
Santa Bárbara, SP
MZUSP (APC 1246-1)
Serra Geraldo Tocantins, TO
MZUSP (APC 1246-2)
Serra Geraldo Tocantins, TO
MZUSP (APC 1246-3)
Serra Geraldo Tocantins, TO
MAV (CEMAS 01)
MAV (CEMAS 02)
Cerradomys gr. subflavus
MZUSP (APC 1157)
Santa Barbara, SP
MZUSP (APC 1177)
Santa Barbara, SP
MZUSP (APC 1177-1)
Santa Barbara, SP
MZUSP (APC 1177-2)
Santa Barbara, SP
MAV (SJB 01)
São Joaquim da Barra, SP
MAV (SJB 02)
São Joaquim da Barra, SP
MZUSP (APC 1022-1)
Serra das Araras, MT
MZUSP (APC 1022-3)
Serra das Araras, MT
MZUSP (MRT 08415)
MZUSP (MRT 08408)
Cotia and Ibiuna, SP
Cotia and Ibiúna, SP
The museum specimens had been fixed in formaldehyde and stored in 70% alcohol. Tissue was processed by standard methods, embedded in paraffin (Paraplast; Oxford Labware, St Louis, MO, USA) and sectioned at 5 μm using an automatic microtome (Leica, RM2155, Germany).
Histology, immunohistochemistry and lectin staining
Sections were stained with hematoxylin and eosin (HE), Masson's trichrome, picrosirius, and periodic acid-Schiff (PAS). In addition, immunohistochemistry was performed following the approaches used in previous studies from our laboratory [see 30,31]. Cytokeratin was used to identify trophoblast cells and was detected by a rabbit polyclonal antibody (1:300; PU071-UP, Biogenex, San Ramon, California, U.S.A.). Mouse monoclonal anti-human primary antibodies were used to detect vimentin (1:300; V9, sc-6260, Santa Cruz Biotechnology, Santa Cruz, California, USA), α-smooth muscle actin (1:300; Clone 1A4, DakoCytomation, Carpinteria, California, USA), and PCNA (1:400; PC10, sc-56, Santa Cruz Biotechnology, Santa Cruz, California, USA). Negative controls were performed using anti-mouse IgG (1:500; AP308F, Chemicon International Temecula, California, USA) as the primary antibody solution.
In addition, samples from three species (Necromys lasiurus, Hylaeamys megacephalus, and Cerradomys gr. subflavus,) were stained using a Dolichos biflorus (DBA) lectin to identify mature uNK cells, following the protocol described by Zhang et al. .
Transmission electron microscopy
Samples for transmission electron microscopy, derived from freshly obtained material of Necromys and Euryoryzomys, were fixed in 2.5% glutaraldehyde. Tissues were maintained in this solution for 48 h and post-fixed for 2 h in 2% phosphate-buffered osmium tetroxide (pH 7.4, for 2 h), then washed in phosphate buffer (3 × 10 min) and immersed in 3% uranyl acetate solution overnight. After being re-washed in buffer (3 × 10 min), tissues were dehydrated in alcohol and immersed in propylene oxide for 10 min. Finally, the samples were embedded in Spurr's Resin (Polysciences, Warrington, PA, USA). Ultrathin sections were made on an automatic ultramicrotome (Ultracut R, Leica Microsystems, Germany), contrasted with 2% uranyl acetate and 0.5% lead citrate and studied in a transmission electron microscope (Morgagni 268D, FEI Company, The Netherlands; Mega View III camera, Soft Imaging System, Germany).
Junctional zone and giant cell region
Decidua and maternal blood supply
The visceral and parietal yolk sac
Sigmodontinae is a South American radiation of cricetid rodents. Placentation in this speciose subfamily has been little studied and information is limited to a single species Calomys callosus [17–22]. Our aim therefore was to study a broader sample. Whilst we were able to study different gestational stages from five genera these were collected mainly in the wild. In contrast to studies of laboratory rodents we did not have carefully spaced specimens of known gestational age.
As in other murid and cricetid rodents, the chorioallantoic placenta consisted of three readily identifiable zones: labyrinth, junctional zone and decidua. An inverted choriovitelline or yolk sac placenta persisted until term. Because this basic design resembles that of the mouse, for which placental development and cell lineages are best understood [2, 3, 5–8, 32–38], our findings are discussed in relation to this species as well as to other cricetid rodents such as the golden hamster, lemming and deer mouse [13–16].
Labyrinth and interhemal barrier
The labyrinth consisted of maternal blood channels enclosed by trophoblast and running roughly parallel to fetal capillaries. As in other murid  and cricetid [11, 12, 15, 16, 21] rodents, there were three layers of trophoblast, the inner two syncytial and the outer one cellular. Details of the structure of the interhemal barrier, such as the variation in thickness and the complex infolding of layer TII, were similar to what has been described in other subfamilies of cricetid rodents [12, 17]. In the mouse all three trophoblast layers are derived from the same lineage . They have distinct patterns of gene expression, however, and form discrete populations early in development . Whilst we did find giant cells in the labyrinth, it remains to be shown if they are equivalent to the sinusoidal giant cells identified in the mouse on the basis of gene expression and polyploidy [34, 37]. Although a hemotrichorial placenta is present in all murid and cricetid rodents so far examined, there are seven known variants of the interhemal barrier in rodents  and our previous analysis suggested that the hemotrichorial type of barrier is a derived character state .
As in other murid and cricetid placentae [6, 13, 33], there was a prominent junctional zone devoid of fetal vessels but with large trophoblast-lined maternal blood spaces. Two distinct types of trophoblast are found here: spongiotrophoblasts and glycogen cells. They were long thought to have a common origin but glycogen cells may be derived from precursors in the ectoplacental cone that, like them, express protocadherin 12 . In the mouse placenta at E16.5 about 40% of the spongy zone is made up of glycogen cells but the proportion diminishes towards term . We found relatively few glycogen cells in our specimens but this was difficult to interpret since gestational ages were not known.
Trophoblast giant cells
The classical giant cells of the rodent placenta, first recognized by their large size and high degree of polyploidy , are now referred to as parietal TGCs . A few of them, sometimes known as primary giant cells, are derived from the mural trophectoderm, but the majority comes from the Tpbpa-negative lineage of the polar trophectoderm . In the mouse they form a nearly continuous layer that marks the boundary between fetal and maternal tissues, although this boundary is breeched once the glycogen cells begin to invade the decidua. As expected, parietal TGCs were found at this location in the sigmodont placenta. In addition, in three genera, the giant cells formed a layer many cells thick at the margin of the disk. A similar accumulation of giant cells is not known from mouse placenta where the total population of parietal TGCs is estimated to be only twenty thousand .
Decidua and maternal blood vessels
The extent to which trophoblast invades maternal blood vessels differs among murid rodents . In the mouse it has been thought for many years that trophoblast invasion is confined to vessels in the fetal part of the placenta . In contrast, in the rat, trophoblast invasion by the endovascular route plays an important part in remodeling of the uterine spiral arteries [9, 43]. More recently it has been recognized that in mouse some trophoblasts migrate by a perivascular route and end up in the lumen of the maternal arteries [2, 34]. Trophoblast invasion of maternal arteries certainly occurs in the golden hamster, a cricetid rodent [13, 44]. In contrast, in sigmodonts, we did not find cytokeratin-positive cells in the walls of the spiral arteries and the vessel endothelium was largely intact. Cytokeratin-positive cells were not found in the mesometrial triangle. Whilst this is suggestive of shallow trophoblast invasion in sigmodonts, it clearly is an aspect that needs to be systematically explored in specimens of known gestational age.
Uterine NK cells
The uNK cells are the dominant leukocyte population in the gravid uterus of rodents and primates. In human pregnancy they are responsible for the earliest events in spiral artery transformation, which occur prior to trophoblast invasion . In the mouse they play an even greater role in adaptation of the maternal arteries, which fail to widen in the absence of uNK cells . Although murine uNK cells produce a number of cytokines, the key molecule appears to be interferon-gamma . For cricetid rodents, the presence of uNK cells in the walls of transformed spiral arteries was first shown in the golden hamster . We have shown that they are present in large numbers in sigmodont rodents and are similarly associated with the spiral arteries. It is likely that they play an important role in vessel widening and remodeling similar to what has been shown experimentally in the mouse.
Parietal and visceral yolk sac
The yolk sac was no different in structure from what has been described for other murid and cricetid rodents [10, 14, 48–50]. Recently it was reported  that there are no caveolae-like structures in the yolk sac endoderm of the mouse. Likewise, this appears to be the case in Necromys and Euryoryzomys, the two sigmodonts we examined by TEM. This is an interesting contrast to what consistently is found in the guinea pig  and other hystricognath rodents [e.g. 31,52,53].
Implications for the biology of sigmodont rodents
The sigmodont rodents reached South America at the time of the Great American Interchange in the Pliocene Epoch or perhaps even earlier . They underwent a rapid radiation that led them to occupy a variety of habitats, including the xeric biomes Cerrado and Caatinga of Brazil [54, 55]. Despite their potential importance as bioindicators  and their undoubted significance as reservoirs of disease , they are much less well studied than, for example, the hystricomorph rodents of Latin America (e.g. [30, 31, 51–53, 56–58]).
In most respects placentation in this subfamily closely resembles what has been described for other cricetid rodents [13, 15]; the close similarity in the fine structure of the interhemal barrier has already been remarked upon. As we have shown elsewhere, the hemotrichorial type of placenta first appeared in the common ancestor or murid and cricetid rodents . Likewise the prominent role of maternal uNK cells in placentation is a feature that sigmodonts share with other cricetid and murid rodents [13, 46]. The most striking finding in the present material was the relative abundance of trophoblast giant cells first described in Calomys  and here extended to a further five genera. In murid rodents giant cells produce a wide range of hormones and cytokines such as proliferin  and the significance of the expanded giant cell population in sigmodonts cries for closer attention.
It is, however, unlikely that our understanding of placentation in this subfamily can be further advanced by field studies. It would be better to establish a breeding program and obtain a series of time dated pregnancies from a single species such as Calomys callosus or Necromys lasiurus, both of which have been bred in captivity. The feasibility of such an approach is apparent from an earlier study of trophoblast invasion at the start of pregnancy .
In summary the general aspect of the fetal membranes in Sigmodontinae resembled that found in other cricetid rodents. The chorioallantoic placenta was organized in a labyrinthine zone, junctional zone and decidua and an inverted yolk sac persisted until term. The interhemal barrier was of the hemotrichorial type. The junctional zone was comprised of spongiotrophoblast, glycogen cells and trophoblast giant cells. Compared to murid rodents there were much larger numbers of giant cells and in some genera these were seen to congregate at the periphery of the placental disk. Glycogen cells were found to invade the decidua but we did not identify trophoblast in the walls of the deeper decidual arteries. In contrast these vessels were surrounded by large numbers of uNK cells. This survey of wild-trapped specimens from five genera is a useful starting point for the study of placentation in an important subfamily of South American rodents. We note, however, that some of these rodents can be captive bred and recommend that future studies focus on the study of time dated pregnancies.
We thank Prof. Dr. Mario de Vivo, Curator of Mammals at the Zoology Museum of the University of Sao Paulo, Brazil, for the loan of sigmodontine specimens and Dr. Rodrigo Del Vale and his working group at Sao Joaquim da Barra for providing additional material. We are grateful for technical support to several members of the University Sao Paulo and the Universidade Federal Rural do Semi-Árido, Mossoró, Rio Grande do Norte. This research was supported by grants from FAPESP (Proc. 07/51491-3 and 09/53392-8).
- Musser GG, Carleton MD: Superfamily Muroidea. Mammal Species of the World: A Taxonomic and Geographic Reference. Edited by: Wilson DE, Reeder DM. 2005, Baltimore: Johns Hopkins University Press, 894-1531.Google Scholar
- Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC: Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol. 2002, 250: 358-373. 10.1006/dbio.2002.0773.View ArticleGoogle Scholar
- Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC: Origin and characteristics of glycogen cells in the developing murine placenta. Develop Dynamics. 2006, 235: 3280-3294. 10.1002/dvdy.20981.View ArticleGoogle Scholar
- Zhang JH, Yamada AT, Croy BA: DBA-lectin reactivity defines natural killer cells that have homed to mouse decidua. Placenta. 2009, 30: 968-973. 10.1016/j.placenta.2009.08.011.View ArticleGoogle Scholar
- Zhang JH, Chen Z, Smith GN, Croy BA: Natural killer cell-triggered vascular transformation: maternal care before birth?. Cell Molec Immunol. 2011, 8: 1-11.View ArticleGoogle Scholar
- Hu D, Cross JC: Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010, 54: 341-54. 10.1387/ijdb.082768dh.View ArticleGoogle Scholar
- Senner CE, Hemberger M: Regulation of early trophoblast differentiation - Lessons from the mouse. Placenta. 2010, 31: 944-950. 10.1016/j.placenta.2010.07.013.View ArticleGoogle Scholar
- Tesser RB, Scherholz PLA, Nascimento L, Katz SG: Trophoblast glycogen cells differentiate early in the mouse ectoplacental cone: putative role during placentation. Histochem Cell Biol. 2010, 134: 83-92. 10.1007/s00418-010-0714-x.View ArticleGoogle Scholar
- Vercruysse L, Caluwaerts S, Luyten C, Pijnenborg R: Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta. 2006, 27: 22-33. 10.1016/j.placenta.2004.11.004.View ArticleGoogle Scholar
- Mess A: Evolutionary transformations of chorioallantoic placental characters in Rodentia with special reference to hystricognath species. J Exp Zool (Comp Exp Biol) A. 2003, 299: 78-98.View ArticleGoogle Scholar
- Carpenter SJ: Light and electron microscopic observations on the morphogenesis of the chorioallantoic placenta of the golden hamster (Cricetus auratus). Days seven through nine of gestation. Am J Anat. 1972, 135: 445-476. 10.1002/aja.1001350403.View ArticleGoogle Scholar
- Carpenter SJ: Ultrastructural observations on the maturation of the placental labyrinth of the golden hamster (days 10 to 16 of gestation). Am J Anat. 1975, 143: 315-47. 10.1002/aja.1001430305.View ArticleGoogle Scholar
- Pijnenborg R, Robertson WB, Brosens I: The arterial migration of trophoblast in the uterus of golden hamster, Mesocricetus auratus. J Reprod Fertil. 1974, 40: 269-80. 10.1530/jrf.0.0400269.View ArticleGoogle Scholar
- Sansom GS: Early development and placentation in Arvicola (Microtus) amphibius, with special reference to the origin of the placental giant cells. J Anat Lond. 1922, 56: 333-365.Google Scholar
- King BF, Hastings RA: The comparative fine structure of the interhemal membrane of chorioallantoic placentas from six genera of myomorph rodents. Am J Anat. 1977, 149: 165-180. 10.1002/aja.1001490204.View ArticleGoogle Scholar
- Enders AC: A comparative study of the fine structure of the trophoblast in several hemochorial placentas. Am J Anat. 1965, 116: 29-67. 10.1002/aja.1001160103.View ArticleGoogle Scholar
- Ferro EAV, Bevilacqua E: Trophoblastic invasion of the uterine epithelium in Calomys callosus (Rodentia, Cricetidae). J Morphol. 1994, 221: 139-152. 10.1002/jmor.1052210204.View ArticleGoogle Scholar
- Ferro EAV, Bevilacqua E, Favoreto-Junior S, Silva DAO, Mortara RA, Mineo JR: Calomys callosus (Rodentia:Cricetidae) trophoblast cells as host cells to toxoplasma gondii in early pregnancy. Parasitol Res. 1999, 85: 647-654. 10.1007/s004360050609.View ArticleGoogle Scholar
- Moraes N, Zago D, Gagioti S, Hoshida MS, Bevilacqua E: NADPH-diaphorase activity and nitric oxide synthase isoforms in the trophoblast of Calomys callosus. J Anat. 2001, 198: 443-453. 10.1017/S002187820100749X.PubMed CentralView ArticleGoogle Scholar
- Ferro EA, Silva DA, Bevilacqua E, Mineo JR: Effect of Toxoplasma gondii infection kinetics on trophoblast cell population in Calomys callosus, a model of congenital toxoplasmosis. Infect Immun. 2002, 70: 7089-7094. 10.1128/IAI.70.12.7089-7094.2002.PubMed CentralView ArticleGoogle Scholar
- Limongi JE, Ferro EAV: Barreira placentária de Calomys callosus (Rodentia, Cricetidae). Biosc J. 2003, 19: 89-94.Google Scholar
- Franco PS, Silva DAO, Costa IN, Gomes AO, Silva ALN, Pena JDO, Mineo JR, Ferro EAV: Evaluation of vertical transmission of Toxoplasma gondii in Calomys callosusmodel after reinfection with heterologous and virulent strain. Placenta. 2011, Google Scholar
- Weksler M: Phylogeny of Neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Mol Phylogenet Evol. 2003, 29: 331-49. 10.1016/S1055-7903(03)00132-5.View ArticleGoogle Scholar
- Jansa SA, Weksler M: Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phylogenet Evol. 2004, 31: 256-276. 10.1016/j.ympev.2003.07.002.View ArticleGoogle Scholar
- Weksler M, Percequillo AR, Voss RS: Ten new genera of Oryzomyine rodents (Cricetidae: Sigmodontinae). Am Mus Nov. 2006, 3537: 1-29. 10.1206/0003-0082(2006)3537[1:TNGOOR]2.0.CO;2.View ArticleGoogle Scholar
- Eisenberg JF, Redford KH: Mammals of the Neotropics. 2000, Ecuador, Bolivia, Brazil. Chicago: Chicago University Press, 3: 1-624.Google Scholar
- Figueiredo LT, Moreli ML, de-Sousa RL, Borges AA, de-Figueiredo GG, Machado AM, Bisordi I, Nagasse-Sugahara TK, Suzuki A, Pereira LE, de-Souza RP, de-Souza LT, Braconi CT, Harsi CM, de-Andrade-Zanotto PM, Viral diversity Genetic Network Consortium: Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg Infect Dis. 2009, 15: 561-7. 10.3201/eid1504.080289.PubMed CentralView ArticleGoogle Scholar
- Püttker T, Pardini R, Meyer-Lucht Y, Sommer S: Response of five small mammal species to micro-scale variations in vegetation structure in secondary Atlantic Forest remnants, Brazil. MBC Ecol. 2008, 8: 9-Google Scholar
- Francisco AL, Magnusson WE, Sanaiotti TM: Variation in growth and reproduction of Bolomys lasiurus (Rodentia: Muridae) in an Amazonian savanna. J Trop Ecol. 1995, 11: 419-428. 10.1017/S0266467400008889.View ArticleGoogle Scholar
- Oliveira MF, Mess A, Ambrósio CE, Dantas CAG, Favaron PO, Miglino MA: Chorioallantoic placentation in Galea spixii (Rodentia, Caviomorpha, Caviidae). Reprod Biol Endocrinol. 2008, 6: 39-10.1186/1477-7827-6-39.PubMed CentralView ArticleGoogle Scholar
- Kanashiro C, Santos TC, Miglino MA, Mess AM, Carter AM: Growth and development of the placenta in capybara (Hydrochaeris hydrochaeris). Reprod Biol Endocrinol. 2009, 7: 57-10.1186/1477-7827-7-57.PubMed CentralView ArticleGoogle Scholar
- Bevilacqua EM, Abrahamsohn PA: Trophoblast invasion during implantation of the mouse embryo. Arch Biol Med Exp. 1989, 22: 107-118.Google Scholar
- Georgiades P, Ferguson-Smith AC, Burton GJ: Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002, 23: 3-19. 10.1053/plac.2001.0738.View ArticleGoogle Scholar
- Simmons DG, Fortier AL, Cross JC: Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol. 2007, 304: 567-578. 10.1016/j.ydbio.2007.01.009.View ArticleGoogle Scholar
- Coan PM, Ferguson-Smith AC, Burton GJ: Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod. 2004, 70: 1806-1813. 10.1095/biolreprod.103.024166.View ArticleGoogle Scholar
- Simmons DG, Cross JC: Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol. 2005, 284: 12-24. 10.1016/j.ydbio.2005.05.010.View ArticleGoogle Scholar
- Hemberger M: Characteristics and significance of trophoblast giant cells. Placenta. 2008, 28 (Suppl 1): 4-9.View ArticleGoogle Scholar
- Hemberger M: Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics. 2010, 5: 24-29. 10.4161/epi.5.1.10589.View ArticleGoogle Scholar
- Mess AM, Carter AM: Evolution of the interhaemal barrier in the placenta of rodents. Placenta. 2009, 30: 914-918. 10.1016/j.placenta.2009.07.008.View ArticleGoogle Scholar
- Bouillot S, Rampon C, Tillet E, Huber P: Tracing the glycogen cells with protocadherin 12 during mouse placenta development. Placenta. 2006, 27: 882-888. 10.1016/j.placenta.2005.09.009.View ArticleGoogle Scholar
- Zybina TG, Zybina EV: Cell reproduction and genome multiplication in the proliferative and invasive trophoblast cell populations of mammalian placenta. Cell Biol Int. 2005, 29: 1071-1083. 10.1016/j.cellbi.2005.10.015.View ArticleGoogle Scholar
- Redline RW, Lu CY: Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship. Lab Invest. 1989, 61: 27-36.Google Scholar
- Caluwaerts S, Vercruysse L, Luyten C, Pijnenborg R: Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta. 2005, 26: 574-584. 10.1016/j.placenta.2004.09.007.View ArticleGoogle Scholar
- Pijnenborg R: Placentation in the golden hamster (Mesocricetus auratus Waterhouse). Thesis, Katholieke Universiteit Leuven. 1975, Leuven: acco, 1-144.Google Scholar
- Harris LK: Review: Trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta. 2010, 31 (Suppl 1): S93-S98.View ArticleGoogle Scholar
- Croy BA, Di Santo JP, Greenwood JD, Chantakru S, Ashkar AA: Transplantation into genetically alymphoid mice as an approach to dissect the roles of uterine natural killer cells during pregnancy-a review. Placenta. 2000, 21 (Suppl A): S77-S80.View ArticleGoogle Scholar
- Monk JM, Leonard S, McBey BA, Croy BA: Induction of murine spiral artery modification by recombinant human interferon-gamma. Placenta. 2005, 26: 835-838. 10.1016/j.placenta.2004.10.016.View ArticleGoogle Scholar
- Jollie WP: Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 1990, 41: 361-81. 10.1002/tera.1420410403.View ArticleGoogle Scholar
- King BF, Enders AC: Comparative development of the mammalian yolk sac. The human yolk sac and yolk sac tumors. Edited by: Nogales FF. 1993, Berlin: Springer-Verlag, 1-32.View ArticleGoogle Scholar
- Mohanty S, Anderson CL, Robinson JM: The expression of caveolin-1 and the distribution of caveolae in the murine placenta and yolk sac: Parallels to the human placenta. Placenta. 2010, 31: 144-150. 10.1016/j.placenta.2009.11.007.View ArticleGoogle Scholar
- King BF, Enders AC: The fine structure of the guinea pig visceral yolk sac placenta. Am J Anat. 1970, 127: 397-414. 10.1002/aja.1001270405.View ArticleGoogle Scholar
- Mess A: Chorioallantoic and yolk sac placentation in the dassie rat Petromus typicus and its significance for the evolution of Hystricognath Rodentia. Placenta. 2007, 28: 1229-1233. 10.1016/j.placenta.2007.05.005.View ArticleGoogle Scholar
- Miglino MA, Franciolli ALR, Oliveira MF, Ambrosio CE, Bonatelli M, Machado MRF, Mess A: Development of the inverted visceral yolk sac in three species of caviids (Rodentia, Caviomorpha, Caviidae). Placenta. 2008, 29: 748-752. 10.1016/j.placenta.2008.05.007.View ArticleGoogle Scholar
- Almeida FC, Bonvicino CR, Cordeiro-Estrela P: Phylogeny and temporal diversification of Calomys (Rodentia, Sigmodontinae): Implications for the biogeography of an endemic genus of the open/dry biomes of South America. Mol Phylogenet Evol. 2006, 42: 449-466.View ArticleGoogle Scholar
- Bonvicino CR, Lemos B, Weksler M: Small mammals of Chapada dos Veadeiros National Park (Cerrado of Central Brazil): ecologic, karyologic, and taxonomic considerations. Braz J Biol. 2005, 65: 395-406. 10.1590/S1519-69842005000300004.View ArticleGoogle Scholar
- Luckett WP: Superordinal and intraordinal affinities of rodents: developmental evidence from the dentition and placentation. Evolutionary Relationships among Rodents Volume 92. Edited by: Luckett WP, Hartenberger J-L. 1985, New York: Plenum Press, NATO ASI-Series, 227-276.View ArticleGoogle Scholar
- Mess A: Development of the chorioallantoic placenta in Octodon degus - a model for growth processes in caviomorph rodents?. J Exp Zool (Mol Dev Evol) B. 2007, 308: 371-383.View ArticleGoogle Scholar
- Mess A: The guinea pig placenta: model of placental growth dynamics. Placenta. 2007, 28: 812-815. 10.1016/j.placenta.2007.02.005.View ArticleGoogle Scholar
- Hemberger M, Nozaki T, Masutani M, Cross JC: Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion. Dev Dyn. 2003, 227: 185-191. 10.1002/dvdy.10291.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.