Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2013

Open Access 01-12-2013 | Research

Morphometric analysis of the placenta in the New World mouse Necromys lasiurus(Rodentia, Cricetidae): a comparison of placental development in cricetids and murids

Authors: Phelipe O Favaron, Andrea M Mess, Moacir F de Oliveira, Anne Gabory, Maria A Miglino, Pascale Chavatte-Palmer, Anne Tarrade

Published in: Reproductive Biology and Endocrinology | Issue 1/2013

Login to get access

Abstract

Background

Stereology is an established method to extrapolate three-dimensional quantities from two-dimensional images. It was applied to placentation in the mouse, but not yet for other rodents. Herein, we provide the first study on quantitative placental development in a sigmodontine rodent species with relatively similar gestational time. Placental structure was also compared to the mouse, in order to evaluate similarities and differences in developmental patterns at the end of gestation.

Methods

Fetal and placental tissues of Necromys lasiurus were collected and weighed at 3 different stages of gestation (early, mid and late gestation) for placental stereology. The total and relative volumes of placenta and of its main layers were investigated. Volume fractions of labyrinth components were quantified by the One Stop method in 31 placentae collected from different individuals, using the Mercator® software. Data generated at the end of gestation from N. lasiurus placentae were compared to those of Mus musculus domesticus obtained at the same stage.

Results

A significant increase in the total absolute volumes of the placenta and its main layers occurred from early to mid-gestation, followed by a reduction near term, with the labyrinth layer becoming the most prominent area. Moreover, at the end of gestation, the total volume of the mouse placenta was significantly increased compared to that of N. lasiurus although the proportions of the labyrinth layer and junctional zones were similar. Analysis of the volume fractions of the components in the labyrinth indicated a significant increase in fetal vessels and sinusoidal giant cells, a decrease in labyrinthine trophoblast whereas the proportion of maternal blood space remained stable in the course of gestation. On the other hand, in the mouse, volume fractions of fetal vessels and sinusoidal giant cells decreased whereas the volume fraction of labyrinthine trophoblast increased compared to N. lasiurus placenta.

Conclusions

Placental development differed between N. lasiurus and M. musculus domesticus. In particular, the low placental efficiency in N. lasiurus seemed to induce morphological optimization of fetomaternal exchanges. In conclusion, despite similar structural aspects of placentation in these species, the quantitative dynamics showed important differences.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gundersen HJ, Jensen EB: The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987, 147: 229-263. 10.1111/j.1365-2818.1987.tb02837.x.CrossRefPubMed Gundersen HJ, Jensen EB: The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987, 147: 229-263. 10.1111/j.1365-2818.1987.tb02837.x.CrossRefPubMed
2.
go back to reference Howard CV, Reed MG: Unbiased stereology: Three-dimensional measurement in microscopy. 2005, Garland Science/Bios Scientific, Abingdon, Oxon, 2 Howard CV, Reed MG: Unbiased stereology: Three-dimensional measurement in microscopy. 2005, Garland Science/Bios Scientific, Abingdon, Oxon, 2
3.
go back to reference Mayhew TM: Stereology and the placenta: where’s the point? – a review. Placenta. 2006, 27: S17-S25.CrossRefPubMed Mayhew TM: Stereology and the placenta: where’s the point? – a review. Placenta. 2006, 27: S17-S25.CrossRefPubMed
4.
go back to reference Mayhem TM, Burton GJ: Stereology and its impact on our understanding of human placental functional morphology. Microsc Res Tech. 1997, 38: 195-205. 10.1002/(SICI)1097-0029(19970701/15)38:1/2<195::AID-JEMT20>3.0.CO;2-J.CrossRef Mayhem TM, Burton GJ: Stereology and its impact on our understanding of human placental functional morphology. Microsc Res Tech. 1997, 38: 195-205. 10.1002/(SICI)1097-0029(19970701/15)38:1/2<195::AID-JEMT20>3.0.CO;2-J.CrossRef
5.
go back to reference Mayhew TM: Recent applications of the new stereology have thrown fresh light on how the placenta grows and develops its form. J Microsc. 1997, 186: 153-163. 10.1046/j.1365-2818.1997.1250683.x.CrossRefPubMed Mayhew TM: Recent applications of the new stereology have thrown fresh light on how the placenta grows and develops its form. J Microsc. 1997, 186: 153-163. 10.1046/j.1365-2818.1997.1250683.x.CrossRefPubMed
6.
go back to reference Mayhew TM, Jairam IC: Stereological comparison of 3D spatial relationships involving villi and intervillous pores in human placentas from control and diabetic pregnancies. J Anat. 2000, 197: 263-274. 10.1046/j.1469-7580.2000.19720263.x.PubMedCentralCrossRefPubMed Mayhew TM, Jairam IC: Stereological comparison of 3D spatial relationships involving villi and intervillous pores in human placentas from control and diabetic pregnancies. J Anat. 2000, 197: 263-274. 10.1046/j.1469-7580.2000.19720263.x.PubMedCentralCrossRefPubMed
7.
go back to reference Mayhew TM: A stereological perspective on placental morphology in normal and complicated pregnancies. J Anat. 2009, 215: 77-90. 10.1111/j.1469-7580.2008.00994.x.PubMedCentralCrossRefPubMed Mayhew TM: A stereological perspective on placental morphology in normal and complicated pregnancies. J Anat. 2009, 215: 77-90. 10.1111/j.1469-7580.2008.00994.x.PubMedCentralCrossRefPubMed
8.
go back to reference Higgins M, Felle P, Mooney EE, Bannigan J: McAuliffe Fm: stereology of the placenta in type 1 and type 2 diabetes. Placenta. 2011, 32: 564-569. 10.1016/j.placenta.2011.04.015.CrossRefPubMed Higgins M, Felle P, Mooney EE, Bannigan J: McAuliffe Fm: stereology of the placenta in type 1 and type 2 diabetes. Placenta. 2011, 32: 564-569. 10.1016/j.placenta.2011.04.015.CrossRefPubMed
9.
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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference Kannekens EM, Murray RD, Howard CV: Currie: a stereological method for estimating the feto-maternal exchange surface area in the bovine placentome at 135 days of gestation. Res Vet Sci. 2006, 81: 127-133. 10.1016/j.rvsc.2005.09.006.CrossRefPubMed Kannekens EM, Murray RD, Howard CV: Currie: a stereological method for estimating the feto-maternal exchange surface area in the bovine placentome at 135 days of gestation. Res Vet Sci. 2006, 81: 127-133. 10.1016/j.rvsc.2005.09.006.CrossRefPubMed
11.
go back to reference Ribeiro AACM, Lacerda PMO, Melo MP, Balieiro JCC, Souza RR: Placental microstructure and efficiency in cloned bovines: a design-based stereological approach. Cell Tissue Res. 2008, 333: 105-114. 10.1007/s00441-008-0626-4.CrossRefPubMed Ribeiro AACM, Lacerda PMO, Melo MP, Balieiro JCC, Souza RR: Placental microstructure and efficiency in cloned bovines: a design-based stereological approach. Cell Tissue Res. 2008, 333: 105-114. 10.1007/s00441-008-0626-4.CrossRefPubMed
12.
go back to reference Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL: Influence of maternal size on placental, fetal and postnatal growth in horse. I. Development in utero. Reproduction. 2002, 123: 445-453. 10.1530/rep.0.1230445.CrossRefPubMed Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL: Influence of maternal size on placental, fetal and postnatal growth in horse. I. Development in utero. Reproduction. 2002, 123: 445-453. 10.1530/rep.0.1230445.CrossRefPubMed
13.
go back to reference Wilsher S, Allen WR: The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet J. 2003, 35: 476-483.CrossRefPubMed Wilsher S, Allen WR: The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet J. 2003, 35: 476-483.CrossRefPubMed
14.
go back to reference Sibbons P: The role of stereology in the study of placental transfer between fetal foal and mare. Equine Vet J. 2006, 38: 106-107. 10.1111/j.2042-3306.2006.tb05523.x.CrossRefPubMed Sibbons P: The role of stereology in the study of placental transfer between fetal foal and mare. Equine Vet J. 2006, 38: 106-107. 10.1111/j.2042-3306.2006.tb05523.x.CrossRefPubMed
15.
go back to reference Rutherford JN, Tardif SD: Developmental plasticity of the microscopic placental architecture in relation to litter size variation in the common marmoset monkey (Callithrix jacchus). Placenta. 2009, 30: 105-110. 10.1016/j.placenta.2008.10.010.PubMedCentralCrossRefPubMed Rutherford JN, Tardif SD: Developmental plasticity of the microscopic placental architecture in relation to litter size variation in the common marmoset monkey (Callithrix jacchus). Placenta. 2009, 30: 105-110. 10.1016/j.placenta.2008.10.010.PubMedCentralCrossRefPubMed
16.
go back to reference Samson JE, Mari G, Dick-Jr EJ, Hubbard GB, Ferry RJ, Schlabritz-Loutsevitch : The morphometry of maternal-fetal oxygen exchange barrier in the baboon model. Placenta. 2011, 32: 845-851. 10.1016/j.placenta.2011.07.083.PubMedCentralCrossRefPubMed Samson JE, Mari G, Dick-Jr EJ, Hubbard GB, Ferry RJ, Schlabritz-Loutsevitch : The morphometry of maternal-fetal oxygen exchange barrier in the baboon model. Placenta. 2011, 32: 845-851. 10.1016/j.placenta.2011.07.083.PubMedCentralCrossRefPubMed
17.
go back to reference Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JCP: Genes, development and evolution of the placenta. Placenta. 2003, 24: 123-130. 10.1053/plac.2002.0887.CrossRefPubMed Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JCP: Genes, development and evolution of the placenta. Placenta. 2003, 24: 123-130. 10.1053/plac.2002.0887.CrossRefPubMed
18.
go back to reference Malassiné A, Frendo JL, Evain-Brion D: A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003, 9: 531-539. 10.1093/humupd/dmg043.CrossRefPubMed Malassiné A, Frendo JL, Evain-Brion D: A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003, 9: 531-539. 10.1093/humupd/dmg043.CrossRefPubMed
19.
20.
go back to reference Salbaum JM, Kruger C, Zhang X, Arbour Delahaye N, Pavlinkova G, Burk DH, Kappen C: Altered gene expression and spongiotrophoblast differentiation in placenta from a mouse model of diabetes in pregnancy. Diabetologia. 2011, 54: 1909-1920. 10.1007/s00125-011-2132-6.CrossRefPubMed Salbaum JM, Kruger C, Zhang X, Arbour Delahaye N, Pavlinkova G, Burk DH, Kappen C: Altered gene expression and spongiotrophoblast differentiation in placenta from a mouse model of diabetes in pregnancy. Diabetologia. 2011, 54: 1909-1920. 10.1007/s00125-011-2132-6.CrossRefPubMed
21.
go back to reference Shrader RE, Hirsch KS, Levin J, Hurley LS: Attenuating effect of zinc on abnormal placental morphology in 6-mercaptopurine treated rats. Teratology. 1978, 17: 315-325. 10.1002/tera.1420170310.CrossRefPubMed Shrader RE, Hirsch KS, Levin J, Hurley LS: Attenuating effect of zinc on abnormal placental morphology in 6-mercaptopurine treated rats. Teratology. 1978, 17: 315-325. 10.1002/tera.1420170310.CrossRefPubMed
22.
go back to reference Malandro MS, Beveridge MJ, Kilberg MS, Novak DA: Effect of low-protein diet-induced intrauterine growth retardation on rat placenta lamino acid transport. Am J Physiol. 1996, 271: 295-303. Malandro MS, Beveridge MJ, Kilberg MS, Novak DA: Effect of low-protein diet-induced intrauterine growth retardation on rat placenta lamino acid transport. Am J Physiol. 1996, 271: 295-303.
23.
go back to reference Roberts CT, Sohlstrom A, Kind KL, Karl RA, Khong TY, Robinson JS, Owens PC, Owens JA: Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta. 2001, 22: 177-185. 10.1053/plac.2000.0602.CrossRefPubMed Roberts CT, Sohlstrom A, Kind KL, Karl RA, Khong TY, Robinson JS, Owens PC, Owens JA: Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta. 2001, 22: 177-185. 10.1053/plac.2000.0602.CrossRefPubMed
24.
go back to reference Levario-Carrillo M, Olave ME, Corral DC, Alderete JG, Gagioti SM, Bevilacqua E: Placental morphology of rats prenatally exposed to methyl parathion. Exp Toxicol Pathol. 2004, 55: 489-496. 10.1078/0940-2993-00346.CrossRefPubMed Levario-Carrillo M, Olave ME, Corral DC, Alderete JG, Gagioti SM, Bevilacqua E: Placental morphology of rats prenatally exposed to methyl parathion. Exp Toxicol Pathol. 2004, 55: 489-496. 10.1078/0940-2993-00346.CrossRefPubMed
25.
go back to reference Mohallem SV, Lobo DJA, Pesquero CR, Assunção JV, Andre PA, Saldiva PHN, Dolhnikoff M: Decreased fertility in mice exposed to environmental air pollution in the city of Sao Paulo. Environ Res. 2005, 98: 196-202. 10.1016/j.envres.2004.08.007.CrossRefPubMed Mohallem SV, Lobo DJA, Pesquero CR, Assunção JV, Andre PA, Saldiva PHN, Dolhnikoff M: Decreased fertility in mice exposed to environmental air pollution in the city of Sao Paulo. Environ Res. 2005, 98: 196-202. 10.1016/j.envres.2004.08.007.CrossRefPubMed
26.
go back to reference Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC: Origin and characteristics of glycogen cells in the developing murine placenta. Dev Dyn. 2006, 235: 3280-3294. 10.1002/dvdy.20981.CrossRefPubMed Coan PM, Conroy N, Burton GJ, Ferguson-Smith AC: Origin and characteristics of glycogen cells in the developing murine placenta. Dev Dyn. 2006, 235: 3280-3294. 10.1002/dvdy.20981.CrossRefPubMed
27.
go back to reference Hoffmann DS, Weydert CJ, Lazartigues E, Kutschke WL, Kienzle MF, Leach JE, Sharma JA, Sharma RV, Davisson RL: Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension. 2008, 51: 1058-1065. 10.1161/HYPERTENSIONAHA.107.107219.CrossRefPubMed Hoffmann DS, Weydert CJ, Lazartigues E, Kutschke WL, Kienzle MF, Leach JE, Sharma JA, Sharma RV, Davisson RL: Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension. 2008, 51: 1058-1065. 10.1161/HYPERTENSIONAHA.107.107219.CrossRefPubMed
28.
go back to reference Veras MM, Damaceno-Rodrigues NR, Caldini EG, Ribeiro AACM, Mayhew TM, Saldiva PHN, Dolhnikoff M: Particulate urban Air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008, 79: 578-584. 10.1095/biolreprod.108.069591.CrossRefPubMed Veras MM, Damaceno-Rodrigues NR, Caldini EG, Ribeiro AACM, Mayhew TM, Saldiva PHN, Dolhnikoff M: Particulate urban Air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008, 79: 578-584. 10.1095/biolreprod.108.069591.CrossRefPubMed
29.
go back to reference Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, Fowden AL: Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol. 2010, 588: 527-538. 10.1113/jphysiol.2009.181214.PubMedCentralCrossRefPubMed Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, Fowden AL: Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol. 2010, 588: 527-538. 10.1113/jphysiol.2009.181214.PubMedCentralCrossRefPubMed
30.
go back to reference Li J, LaMarca B, Reckelhoff JF: A model of preeclampsia in rats: the reduced uterine perfusion pressure (RUPP) model. Am J Phys – Heart Circ Physiol. 2012, 303: H1-H8. 10.1152/ajpheart.00117.2012.CrossRef Li J, LaMarca B, Reckelhoff JF: A model of preeclampsia in rats: the reduced uterine perfusion pressure (RUPP) model. Am J Phys – Heart Circ Physiol. 2012, 303: H1-H8. 10.1152/ajpheart.00117.2012.CrossRef
31.
go back to reference Rennie MY, Dentmar J, Whiteley KJ, Jurisicova A, Adamson SL, Sled JG: Expansion of the fetomaternal vasculature in late gestation in strain dependent in mice. Am J Physiol – Heart Circ Physiol. 2012, 15: H1261-H1273.CrossRef Rennie MY, Dentmar J, Whiteley KJ, Jurisicova A, Adamson SL, Sled JG: Expansion of the fetomaternal vasculature in late gestation in strain dependent in mice. Am J Physiol – Heart Circ Physiol. 2012, 15: H1261-H1273.CrossRef
32.
go back to reference Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC: Interations between trophoblast cells and the maternal and fetal circulations in the mouse placenta. Dev Biol. 2002, 250: 358-373. 10.1006/dbio.2002.0773.CrossRefPubMed Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC: Interations between trophoblast cells and the maternal and fetal circulations in the mouse placenta. Dev Biol. 2002, 250: 358-373. 10.1006/dbio.2002.0773.CrossRefPubMed
33.
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.CrossRefPubMed 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.CrossRefPubMed
34.
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: 341-354. 10.1387/ijdb.082768dh.CrossRefPubMed Hu D, Cross JC: Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010, 54: 341-354. 10.1387/ijdb.082768dh.CrossRefPubMed
35.
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.CrossRefPubMed 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.CrossRefPubMed
36.
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.CrossRefPubMed 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.CrossRefPubMed
37.
go back to reference Zhang JH, Chen Z, Smith GN, Croy BA: Natural Killer cell-triggered vascular transformation: maternal care before birth?. Cell Mol Immunol. 2011, 8: 1-11.PubMedCentralCrossRefPubMed Zhang JH, Chen Z, Smith GN, Croy BA: Natural Killer cell-triggered vascular transformation: maternal care before birth?. Cell Mol Immunol. 2011, 8: 1-11.PubMedCentralCrossRefPubMed
38.
go back to reference Vercruysse L, Caluwaerts S, Luyten C, Pijnenborg R: Interstitial trophoblast invasion in the decidua and mesometrial triangle during last third pregnancy in the rat. Placenta. 2006, 27: 22-33. 10.1016/j.placenta.2004.11.004.CrossRefPubMed Vercruysse L, Caluwaerts S, Luyten C, Pijnenborg R: Interstitial trophoblast invasion in the decidua and mesometrial triangle during last third pregnancy in the rat. Placenta. 2006, 27: 22-33. 10.1016/j.placenta.2004.11.004.CrossRefPubMed
39.
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.CrossRefPubMed 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.CrossRefPubMed
40.
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: 269-280. 10.1530/jrf.0.0400269.CrossRefPubMed Pijnenborg R, Robertson WB, Brosens I: The arterial migration of trophoblast in the uterus of golden hamster, Mesocricetus auratus. J Reprod Fertil. 1974, 40: 269-280. 10.1530/jrf.0.0400269.CrossRefPubMed
41.
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: 315-347. 10.1002/aja.1001430305.CrossRefPubMed 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: 315-347. 10.1002/aja.1001430305.CrossRefPubMed
42.
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.CrossRefPubMed 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.CrossRefPubMed
43.
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.CrossRefPubMed 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.CrossRefPubMed
44.
go back to reference Favaron PO, Carter AM, Ambrosio CE, Morini AC, Mess AM, Oliveira MF, Miglino MA: Placentation in Sigmodontinae: a rodent taxon native to South America. Reprod Biol Endocrinol. 2011, 9: 55A-10.1186/1477-7827-9-55.CrossRef Favaron PO, Carter AM, Ambrosio CE, Morini AC, Mess AM, Oliveira MF, Miglino MA: Placentation in Sigmodontinae: a rodent taxon native to South America. Reprod Biol Endocrinol. 2011, 9: 55A-10.1186/1477-7827-9-55.CrossRef
45.
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
46.
go back to reference Evans HE, Sack WO: Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat Histol Embryol. 1973, 2: 11-45. 10.1111/j.1439-0264.1973.tb00253.x.CrossRef Evans HE, Sack WO: Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat Histol Embryol. 1973, 2: 11-45. 10.1111/j.1439-0264.1973.tb00253.x.CrossRef
47.
go back to reference Lecarpentier E, Morel O, Tarrade A, Dahirel M, Bonneau M, Gayat E, Evain-Brion D, Chavatte-Palmer P, Tsatsaris V: Quantification of utero-placental vascularization in a rabbit model of IUGR with three-dimensional power Dopper angiography. Placenta. 2012, 33: 769-775. 10.1016/j.placenta.2012.06.013.CrossRefPubMed Lecarpentier E, Morel O, Tarrade A, Dahirel M, Bonneau M, Gayat E, Evain-Brion D, Chavatte-Palmer P, Tsatsaris V: Quantification of utero-placental vascularization in a rabbit model of IUGR with three-dimensional power Dopper angiography. Placenta. 2012, 33: 769-775. 10.1016/j.placenta.2012.06.013.CrossRefPubMed
48.
go back to reference Reed MG, Howard CV, DE Yanés GS: One-stop stereology: the estimation of 3D parameters using isotropic rulers. J Microsc. 2010, 239: 54-65. 10.1111/j.1365-2818.2009.03356.x.CrossRefPubMed Reed MG, Howard CV, DE Yanés GS: One-stop stereology: the estimation of 3D parameters using isotropic rulers. J Microsc. 2010, 239: 54-65. 10.1111/j.1365-2818.2009.03356.x.CrossRefPubMed
49.
go back to reference Favaron PO, Carter AM, Mess AM, Oliveira MF, Miglino MA: An unusual feature of yolk sac placentation in Necromys lasiurus (Rodentia, Cricetidae, Sigmodontinae). Placenta. 2012, 33: 578-580. 10.1016/j.placenta.2012.02.011.CrossRefPubMed Favaron PO, Carter AM, Mess AM, Oliveira MF, Miglino MA: An unusual feature of yolk sac placentation in Necromys lasiurus (Rodentia, Cricetidae, Sigmodontinae). Placenta. 2012, 33: 578-580. 10.1016/j.placenta.2012.02.011.CrossRefPubMed
50.
go back to reference Coan PM, Angiolini E, Sandovici I, Burton GJ, Constância M, Fowden AL: Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in the mice. J Physiol. 2008, 586: 4567-4576. 10.1113/jphysiol.2008.156133.PubMedCentralCrossRefPubMed Coan PM, Angiolini E, Sandovici I, Burton GJ, Constância M, Fowden AL: Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in the mice. J Physiol. 2008, 586: 4567-4576. 10.1113/jphysiol.2008.156133.PubMedCentralCrossRefPubMed
51.
go back to reference van Patot MC T, Murray AJ, Beckey V, Cindrova-Davies T, Johns J, Zwerdlinger L, Jauniaux E, Burton GJ, Serkova NJ: Human placental metabolic adaptation to chronic hypoxia, high altitude: hypoxic preconditioning. Am J Physiol. Regulator, integrative and comparative physiology. 2010, 298: 166-172. 10.1152/ajpregu.00383.2009.CrossRef van Patot MC T, Murray AJ, Beckey V, Cindrova-Davies T, Johns J, Zwerdlinger L, Jauniaux E, Burton GJ, Serkova NJ: Human placental metabolic adaptation to chronic hypoxia, high altitude: hypoxic preconditioning. Am J Physiol. Regulator, integrative and comparative physiology. 2010, 298: 166-172. 10.1152/ajpregu.00383.2009.CrossRef
52.
go back to reference Belkacemi L, Nelson DM, Desai M, Ross MG: Maternal undernutrition influences placental-fetal development. Biol Reprod. 2010, 83: 325-331. 10.1095/biolreprod.110.084517.CrossRefPubMed Belkacemi L, Nelson DM, Desai M, Ross MG: Maternal undernutrition influences placental-fetal development. Biol Reprod. 2010, 83: 325-331. 10.1095/biolreprod.110.084517.CrossRefPubMed
53.
go back to reference Coan PM, Fowden AL, Constância M, Ferguson-Smith AC, Burton GJ, Sibley CP: Disproportional effects of Igf2 knockout on placental morphology and diddusional exchange characteristics in the mouse. J Physiol. 2008, 586: 5023-5032. 10.1113/jphysiol.2008.157313.PubMedCentralCrossRefPubMed Coan PM, Fowden AL, Constância M, Ferguson-Smith AC, Burton GJ, Sibley CP: Disproportional effects of Igf2 knockout on placental morphology and diddusional exchange characteristics in the mouse. J Physiol. 2008, 586: 5023-5032. 10.1113/jphysiol.2008.157313.PubMedCentralCrossRefPubMed
54.
go back to reference Kurtz H, Zechner U, Orth A, Fundele R: Lake correlation between placenta and offspring size in mouse interspecific crosses. Anat Embryol. 1999, 200: 335-343. 10.1007/s004290050284.CrossRef Kurtz H, Zechner U, Orth A, Fundele R: Lake correlation between placenta and offspring size in mouse interspecific crosses. Anat Embryol. 1999, 200: 335-343. 10.1007/s004290050284.CrossRef
55.
go back to reference Soloveva V, Linzer DIH: Differentiation of placental trophoblast giant cells requires dowregulation of p53 and Rb. Placenta. 2004, 25: 29-36. 10.1016/S0143-4004(03)00215-7.CrossRefPubMed Soloveva V, Linzer DIH: Differentiation of placental trophoblast giant cells requires dowregulation of p53 and Rb. Placenta. 2004, 25: 29-36. 10.1016/S0143-4004(03)00215-7.CrossRefPubMed
Metadata
Title
Morphometric analysis of the placenta in the New World mouse Necromys lasiurus(Rodentia, Cricetidae): a comparison of placental development in cricetids and murids
Authors
Phelipe O Favaron
Andrea M Mess
Moacir F de Oliveira
Anne Gabory
Maria A Miglino
Pascale Chavatte-Palmer
Anne Tarrade
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2013
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-11-10

Other articles of this Issue 1/2013

Reproductive Biology and Endocrinology 1/2013 Go to the issue