Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2011

Open Access 01-12-2011 | Research

Placentation in Sigmodontinae: a rodent taxon native to South America

Authors: Phelipe O Favaron, Anthony M Carter, Carlos E Ambrósio, Adriana C Morini, Andrea M Mess, Moacir F de Oliveira, Maria A Miglino

Published in: Reproductive Biology and Endocrinology | Issue 1/2011

Login to get access

Abstract

Background

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.

Methods

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.

Results

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.

Conclusion

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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. 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.
2.
go back to reference 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.CrossRef 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.CrossRef
3.
go back to reference 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.CrossRef 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.CrossRef
4.
go back to reference 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.CrossRef 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.CrossRef
5.
go back to reference 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.CrossRef 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.CrossRef
6.
go back to reference 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.CrossRef 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.CrossRef
7.
go back to reference 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.CrossRef 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.CrossRef
8.
go back to reference 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.CrossRef 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.CrossRef
9.
go back to reference 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.CrossRef 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.CrossRef
10.
go back to reference 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.CrossRef 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.CrossRef
11.
go back to reference 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.CrossRef 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.CrossRef
12.
go back to reference 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.CrossRef 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.CrossRef
13.
go back to reference 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.CrossRef 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.CrossRef
14.
go back to reference 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. 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.
15.
go back to reference 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.CrossRef 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.CrossRef
16.
go back to reference 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.CrossRef 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.CrossRef
17.
go back to reference 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.CrossRef 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.CrossRef
18.
go back to reference 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.CrossRef 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.CrossRef
19.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
20.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
21.
go back to reference Limongi JE, Ferro EAV: Barreira placentária de Calomys callosus (Rodentia, Cricetidae). Biosc J. 2003, 19: 89-94. Limongi JE, Ferro EAV: Barreira placentária de Calomys callosus (Rodentia, Cricetidae). Biosc J. 2003, 19: 89-94.
22.
go back to reference 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, 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,
23.
go back to reference 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.CrossRef 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.CrossRef
24.
go back to reference 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.CrossRef 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.CrossRef
25.
go back to reference 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.CrossRef 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.CrossRef
26.
go back to reference Eisenberg JF, Redford KH: Mammals of the Neotropics. 2000, Ecuador, Bolivia, Brazil. Chicago: Chicago University Press, 3: 1-624. Eisenberg JF, Redford KH: Mammals of the Neotropics. 2000, Ecuador, Bolivia, Brazil. Chicago: Chicago University Press, 3: 1-624.
27.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
28.
go back to reference 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- 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-
29.
go back to reference 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.CrossRef 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.CrossRef
30.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
31.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
32.
go back to reference Bevilacqua EM, Abrahamsohn PA: Trophoblast invasion during implantation of the mouse embryo. Arch Biol Med Exp. 1989, 22: 107-118. Bevilacqua EM, Abrahamsohn PA: Trophoblast invasion during implantation of the mouse embryo. Arch Biol Med Exp. 1989, 22: 107-118.
33.
go back to reference 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.CrossRef 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.CrossRef
34.
go back to reference 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.CrossRef 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.CrossRef
35.
go back to reference 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.CrossRef 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.CrossRef
36.
go back to reference 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.CrossRef 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.CrossRef
37.
go back to reference Hemberger M: Characteristics and significance of trophoblast giant cells. Placenta. 2008, 28 (Suppl 1): 4-9.CrossRef Hemberger M: Characteristics and significance of trophoblast giant cells. Placenta. 2008, 28 (Suppl 1): 4-9.CrossRef
38.
go back to reference Hemberger M: Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics. 2010, 5: 24-29. 10.4161/epi.5.1.10589.CrossRef Hemberger M: Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics. 2010, 5: 24-29. 10.4161/epi.5.1.10589.CrossRef
39.
go back to reference 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.CrossRef 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.CrossRef
40.
go back to reference 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.CrossRef 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.CrossRef
41.
go back to reference 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.CrossRef 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.CrossRef
42.
go back to reference 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. 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.
43.
go back to reference 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.CrossRef 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.CrossRef
44.
go back to reference Pijnenborg R: Placentation in the golden hamster (Mesocricetus auratus Waterhouse). Thesis, Katholieke Universiteit Leuven. 1975, Leuven: acco, 1-144. Pijnenborg R: Placentation in the golden hamster (Mesocricetus auratus Waterhouse). Thesis, Katholieke Universiteit Leuven. 1975, Leuven: acco, 1-144.
45.
go back to reference Harris LK: Review: Trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta. 2010, 31 (Suppl 1): S93-S98.CrossRef Harris LK: Review: Trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta. 2010, 31 (Suppl 1): S93-S98.CrossRef
46.
go back to reference 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.CrossRef 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.CrossRef
47.
go back to reference 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.CrossRef 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.CrossRef
48.
go back to reference Jollie WP: Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 1990, 41: 361-81. 10.1002/tera.1420410403.CrossRef Jollie WP: Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 1990, 41: 361-81. 10.1002/tera.1420410403.CrossRef
49.
go back to reference 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.CrossRef 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.CrossRef
50.
go back to reference 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.CrossRef 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.CrossRef
51.
go back to reference 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.CrossRef 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.CrossRef
52.
go back to reference 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.CrossRef 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.CrossRef
53.
go back to reference 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.CrossRef 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.CrossRef
54.
go back to reference 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.CrossRef 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.CrossRef
55.
go back to reference 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.CrossRef 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.CrossRef
56.
go back to reference 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.CrossRef 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.CrossRef
57.
go back to reference 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.CrossRef 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.CrossRef
58.
go back to reference Mess A: The guinea pig placenta: model of placental growth dynamics. Placenta. 2007, 28: 812-815. 10.1016/j.placenta.2007.02.005.CrossRef Mess A: The guinea pig placenta: model of placental growth dynamics. Placenta. 2007, 28: 812-815. 10.1016/j.placenta.2007.02.005.CrossRef
59.
go back to reference 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.CrossRef 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.CrossRef
Metadata
Title
Placentation in Sigmodontinae: a rodent taxon native to South America
Authors
Phelipe O Favaron
Anthony M Carter
Carlos E Ambrósio
Adriana C Morini
Andrea M Mess
Moacir F de Oliveira
Maria A Miglino
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2011
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-9-55

Other articles of this Issue 1/2011

Reproductive Biology and Endocrinology 1/2011 Go to the issue