期刊论文详细信息
Reproductive Biology and Endocrinology
Morphometric analysis of the placenta in the New World mouse Necromys lasiurus (Rodentia, Cricetidae): a comparison of placental development in cricetids and murids
Anne Tarrade1  Pascale Chavatte-Palmer1  Maria A Miglino2  Anne Gabory3  Moacir F de Oliveira4  Andrea M Mess2  Phelipe O Favaron2 
[1] Foundation PremUp, Paris, France;Department of Surgery, School of Veterinary Medicine, University of Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, Cidade Universitária, São Paulo, SP, CEP 05508-270, Brazil;ENVA, Maisons-Alfort, F-94704, France;Department of Animal Science, Universidade Federal Rural do Semi-Árido, Mossoró, Rio Grande do Norte, 59625-900, Brazil
关键词: Evolution;    Trophoblast;    Fetal vessels;    Haemochorial placenta;    Labyrinth;    Junctional zone;    Decidua;    Sigmodontinae;    Stereology;    Placenta;   
Others  :  812661
DOI  :  10.1186/1477-7827-11-10
 received in 2012-11-19, accepted in 2013-02-18,  发布年份 2013
PDF
【 摘 要 】

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.

【 授权许可】

   
2013 Favaron et al; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140709091917139.pdf 1619KB PDF download
Figure 1. 201KB Image download
【 图 表 】

Figure 1.

【 参考文献 】
  • [1]Gundersen HJ, Jensen EB: The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987, 147:229-263.
  • [2]Howard CV, Reed MG: Unbiased stereology: Three-dimensional measurement in microscopy. 2nd edition. Garland Science/Bios Scientific, Abingdon, Oxon; 2005.
  • [3]Mayhew TM: Stereology and the placenta: where’s the point? – a review. Placenta 2006, 27:S17-S25.
  • [4]Mayhem TM, Burton GJ: Stereology and its impact on our understanding of human placental functional morphology. Microsc Res Tech 1997, 38:195-205.
  • [5]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.
  • [6]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.
  • [7]Mayhew TM: A stereological perspective on placental morphology in normal and complicated pregnancies. J Anat 2009, 215:77-90.
  • [8]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.
  • [9]Coan PM, Ferguson-Smith AC, Burton GJ: Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod 2004, 70:1806-1813.
  • [10]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.
  • [11]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.
  • [12]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.
  • [13]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.
  • [14]Sibbons P: The role of stereology in the study of placental transfer between fetal foal and mare. Equine Vet J 2006, 38:106-107.
  • [15]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.
  • [16]Samson JE, Mari G, Dick-Jr EJ, Hubbard GB, Ferry RJ Jr, Schlabritz-Loutsevitch : The morphometry of maternal-fetal oxygen exchange barrier in the baboon model. Placenta 2011, 32:845-851.
  • [17]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.
  • [18]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.
  • [19]Carter AM: Animal models of human placentation - a review. Placenta 2007, 28:S41-S47.
  • [20]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.
  • [21]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.
  • [22]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]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.
  • [24]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.
  • [25]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.
  • [26]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.
  • [27]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.
  • [28]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.
  • [29]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.
  • [30]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.
  • [31]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.
  • [32]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.
  • [33]Zhang JH, Yamada AT, Croy BA: DBA-lectin reactivity defines natural killer cells that have homed to mouse decidua. Placenta 2009, 30:968-973.
  • [34]Hu D, Cross JC: Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol 2010, 54:341-354.
  • [35]Senner CE, Hemberger M: Regulation of early trophoblast differentiation – Lessons from the mouse. Placenta 2010, 31:944-950.
  • [36]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.
  • [37]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.
  • [38]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.
  • [39]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.
  • [40]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.
  • [41]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.
  • [42]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.
  • [43]Ferro EAV, Bevilacqua E: Trophoblastic invasion of the uterine epithelium in Calomys callosus (Rodentia, Cricetidae). J Morphol 1994, 221:139-152.
  • [44]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. BioMed Central Full Text
  • [45]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.
  • [46]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.
  • [47]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.
  • [48]Reed MG, Howard CV, DE Yanés GS: One-stop stereology: the estimation of 3D parameters using isotropic rulers. J Microsc 2010, 239:54-65.
  • [49]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.
  • [50]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.
  • [51]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.
  • [52]Belkacemi L, Nelson DM, Desai M, Ross MG: Maternal undernutrition influences placental-fetal development. Biol Reprod 2010, 83:325-331.
  • [53]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.
  • [54]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.
  • [55]Soloveva V, Linzer DIH: Differentiation of placental trophoblast giant cells requires dowregulation of p53 and Rb. Placenta 2004, 25:29-36.
  文献评价指标  
  下载次数:50次 浏览次数:130次