Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice
Open accessAbstract
Experimental reduction in placental growth often leads to increased placental efficiency measured as grams of fetus produced per gram of placenta, although little is known about the mechanisms involved. This study tested the hypothesis that the smallest placenta within a litter is the most efficient at supporting fetal growth by examining the natural intra‐litter variation in placental nutrient transfer capacity in normal pregnant mice. The morphology, nutrient transfer and expression of key growth and nutrient supply genes (Igf2 P0, Grb10, Slc2a1, Slc2a3, Slc38a1, Slc38a2 and Slc38a4) were compared in the lightest and heaviest placentas of a litter at days 16 and 19 of pregnancy, when mouse fetuses are growing most rapidly in absolute terms. The data show that there are morphological and functional adaptations in the lightest placenta within a litter, which increase active transport of amino acids per gram of placenta and maintain normal fetal growth close to term, despite the reduced placental mass. The specific placental adaptations differ with age. At E16, they are primarily morphological with an increase in the volume fraction of the labyrinthine zone responsible for nutrient exchange, whereas at E19 they are more functional with up‐regulated placental expression of the glucose transporter gene, Slc2a1/GLUT1 and one isoform the System A family of amino acid transporters, Slc38a2/SNAT2. Thus, this adaptability in placental phenotype provides a functional reserve capacity for maximizing fetal growth during late gestation when placental growth is compromised.
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As a result, the naturally small placenta also supports more fetal growth per gram and maintains a normal fetal growth rate in late gestation.
“As a result, the naturally small placenta also supports more fetal growth per gram and maintains a normal fetal growth rate in late gestation (114).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [114]
When fetal demand and supply are mismatched in the naturally small placenta, there are changes in expression of several imprinted genes, including Igf2 in association with sparing of the labyrinth zone, increased MeAIB and glucose transport and upregulated expression of the Slc38a2 amino acid transporters.
“When the fetal demand and supply are mismatched in the naturally small placenta, there are changes in expression of several imprinted genes, including Igf2 in association with sparing of the labyrinth zone, increased MeAIB and glucose transport and upregulated expression of the Slc38a2 amino acid transporters (114).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [114]
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McPherson, N. O., Bell, V. G., Zander‐Fox, D., Fullston, T., Wu, L., Robker, R. L., & Lane, M. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00230.2015 · Cited by 71 · see citing works
“In addition, increases in gene expression of the amino acid transporter Slc38a2 is associated with faster-growing fetuses (14).”
BackgroundYoung, R. E., Nelson, K. M., Hofbauer, S. I., Vijayakumar, T., Alameh, M., Weissman, D., Papachristou, C., Gleghorn, J. P., & Riley, R. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.11.014 · Cited by 73 · see citing works
“4) [68 – 70].”
Mother’s lifetime nutrition and the size, shape and efficiency of the placenta
Winder, N. R., Krishnaveni, G. V., Veena, S. R., Hill, J. C., Karat, C. L. S., Thornburg, K. L., Fall, C. H. D., & Barker, D. J. P. (2011) · Placenta · doi:10.1016/j.placenta.2011.09.001 · Cited by 67 · see citing works
“Higher maternal fat mass is associated with higher circulating concentrations of lipids and glucose [18], which may result in greater growth of the surface and greater transfer of these nutrients per unit of placental surface area [19].”
BackgroundDietary composition programmes placental phenotype in mice
Coan, P. M., Vaughan, O. R., McCarthy, J., Mactier, C., Burton, G. J., Constância, M., & Fowden, A. L. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.208629 · Cited by 67 · see citing works
“Upregulation of placental Slc2a1/GLUT1 expression and glucose clearance has also been observed in the naturally small placenta within a litter and when nutrient availability was reduced by undernutrition of pregnant mice (Coan et al. 2008, 2010).”
BackgroundMethodSelf-citationJones, H. N., Crombleholme, T., & Habli, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074632 · Cited by 64 · see citing works
“GLUT1 expression is upregulated towards the end of gestation to meet the demand of the rapidly growing fetus [12].”
BackgroundGenomic imprinting as an adaptative model of developmental plasticity
Radford, E. J., Ferrón, S. R., & Ferguson-Smith, A. C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.063 · Cited by 64 · see citing works
“The placenta is also a highly plastic organ, responsive to foetal demand for resources [47].”
BackgroundAngiolini, E., Coan, P. M., Sandovici, I., Iwajomo, O. H., Peck, G., Burton, G. J., Sibley, C. P., Reik, W., Fowden, A. L., & Constância, M. (2011) · The FASEB Journal · doi:10.1096/fj.10-175273 · Cited by 64 · see citing works
“Although the signals regulating the nutrient supply capacity of the placenta remain unknown, the results of this and our previous studies (15, 18) show that the placenta is responsive to mismatches between nutrient availability and the fetal genetic drive for nutrient acquisition.”
BackgroundResultSelf-citationWinterhager, E., & Gellhaus, A. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00951 · Cited by 59 · see citing works
“In rodents, placental system A transporter activity is wellknown to be inversely correlated with placental weight; even reduced placental weight, which is not correlated with IUGR, required a higher level of transporter activity to compensate (Coan et al., 2008).”
BackgroundExpansion of the fetoplacental vasculature in late gestation is strain dependent in mice
Rennie, M. Y., Detmar, J., Whiteley, K. J., Jurisicova, A., Adamson, S. L., & Sled, J. G. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00776.2011 · Cited by 57 · see citing works
Bowman, C., Streck, R. D., & Chapin, R. E. (2010) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20249 · Cited by 57 · see citing works
“In the mouse model, this interesting placental adjustment to maintain fetal growth despite reduced placental size (Coan et al., 2008a) illustrates some of the inherent placental functional ability to adapt to variations or possibly insults to maternal-placental development.”
BackgroundEffect of the Anti-Oxidant Tempol on Fetal Growth in a Mouse Model of Fetal Growth Restriction1
Stanley, J. L., Andersson, I. J., Hirt, C. J., Moore, L. E., Dilworth, M. R., Chade, A., Sibley, C. P., Davidge, S. T., & Baker, P. N. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.111.096198 · Cited by 56 · see citing works
“are data from both normal mice [33] and those with a deletion of the placental Igf2 transcript [34] that suggest that when the fetal:placental weight ratios are increased (as they were here with our Tempol-treated Nos3 / mice), this is mediated through upregulation of System A transporter activity per gram-weight of p…”
BackgroundEnvironmental regulation of placental phenotype: implications for fetal growth
Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., & Fowden, A. L. (2011) · Reproduction Fertility and Development · doi:10.1071/rd11909 · Cited by 55 · see citing works
“Certainly, SNAT2/Slc38a2 expression is upregulated in naturally small placentae within mouse litters at Day 16 in association with normal growth of the pups during late gestation (Coan et al. 2008a).”
BackgroundResultInfluentialSelf-citationPhysiological and pathological functions of sphingolipids in pregnancy
Fakhr, Y., Brindley, D. N., & Hemmings, D. G. (2021) · Cellular Signalling · doi:10.1016/j.cellsig.2021.110041 · Cited by 54 · see citing works
Prenatal Endotoxemia and Placental Drug Transport in The Mouse: Placental Size-Specific Effects
Bloise, E., Bhuiyan, M., Audette, M. C., Sophie Petropoulos, A., Javam, M., Gibb, W., & Matthews, S. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065728 · Cited by 53 · see citing works
“Despite the fact that the smaller placentas within a litter transport nutrients more efficiently, smaller placentas display reduced numbers of fetal capillaries in the labyrinth zone [21].”
BackgroundConnor, K. L., Kibschull, M., Matysiak‐Zablocki, E., Nguyen, T. T.-T. N., Matthews, S. G., Lye, S. J., & Bloise, E. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.108329 · Cited by 52 · see citing works
Natale, B. V., Mehta, P., Vu, P., Schweitzer, C. L., Gustin, K., Kotadia, R., & Natale, D. R. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-35606-x · Cited by 49 · see citing works
Goeden, N., & Bonnin, A. (2012) · Nature Protocols · doi:10.1038/nprot.2012.144 · Cited by 44 · see citing works
Leptin and the Placental Response to Maternal Food Restriction During Early Pregnancy in Mice1
Schulz, L. C., Schlitt, J. M., Caesar, G., & Pennington, K. A. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.112.103218 · Cited by 47 · see citing works
“[28], who showed an increase on Day 16 in the relative size of the labyrinth zone in the lightest placentas in a litter relative to that in the heaviest placentas.”
BackgroundTomi, M., Nishimura, T., & Nakashima, E. (2011) · Journal of Pharmaceutical Sciences · doi:10.1002/jps.22642 · Cited by 44 · see citing works
Strakovsky, R. S., & Schantz, S. L. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy224 · Cited by 44 · see citing works
“Species differences (specifically focusing on humans and rodents) in A, placental hormones, B, trophoblast invasion and decidualization, C, the fetal: placental weight ratio, and D, placental structure and classification (Adamson et al., 2002; Albrecht and Pepe, 2010; Benirschke and Kaufmann, 1995; Ben-Zimra et al., 2…”
BackgroundLópez‐Tello, J., Pérez-García, V., Khaira, J., Kusinski, L. C., Cooper, W. N., Andreani, A., Grant, I. D., de Liger, E. F., Lam, B., Hemberger, M., et al. (2019) · eLife · doi:10.7554/elife.45282 · Cited by 45 · see citing works
Self-citationEaton, M., Davies, A., Devine, J., Zhao, X., Simmons, D. G., Maríusdóttir, E., Natale, D. R. C., Matyas, J. R., Bering, E. A., Workentine, M. L., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0226735 · Cited by 44 · see citing works
“For example, male placentas are significantly heavier than female placentas [31] and it is known that differences in placenta size co-vary with morphological and functional adaptations [32].”
BackgroundJacobsen, H., Gnirß, K., Tekin-Bubenheim, N., Kouassi, N. M., Batalla, I. B., Berenbrok, N., Wolff, M., dos Reis, V. P., Zickler, M., Scholl, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25220-3 · Cited by 42 · see citing works
Corticosterone alters materno‐fetal glucose partitioning and insulin signalling in pregnant mice
Vaughan, O. R., Fisher, H. M., Dionelis, K. N., Jefferies, E. C., Higgins, J., Musiał, B., Sferruzzi-Perri, A. N., & Fowden, A. L. (2015) · The Journal of Physiology · doi:10.1113/jphysiol.2014.287177 · Cited by 42 · see citing works
“Indeed, previous observations show that natural variations in fetal weight are more closely related to placental transport of amino acids than glucose at D19 (Coan et al. 2008).”
BackgroundSelf-citationBilateral uterine vessel ligation as a model of intrauterine growth restriction in mice
Janot, M., Cortes-Dubly, M.-L., Rodriguez, S., & Huynh‐Do, U. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-62 · Cited by 41 · see citing works
Exposure of pregnant mice to triclosan impairs placental development and nutrient transport
Cao, X., Xu, H., Wang, X., & Chen, L. (2017) · Scientific Reports · doi:10.1038/srep44803 · Cited by 41 · see citing works
Feto‐ and utero‐placental vascular adaptations to chronic maternal hypoxia in the mouse
Cahill, L. S., Rennie, M. Y., Hoggarth, J., Yu, L. X., Rahman, A., Kingdom, J. C., Seed, M., Macgowan, C. K., & Sled, J. G. (2017) · The Journal of Physiology · doi:10.1113/jp274845 · Cited by 40 · see citing works
“Interhaemal membrane thickness was measured using ImageJ from a midline section stained for CD34 using stereological principles and corrected for shrinkage, as has previously been described in detail (Coan et al. 2004; Rennie et al. 2012).”
MethodStrakovsky, R. S., Zhou, D., & Pan, Y. (2010) · Journal of Nutrition · doi:10.3945/jn.110.127803 · Cited by 39 · see citing works
The problem with using the birthweight:placental weight ratio as a measure of placental efficiency
Christians, J. K., Grynspan, D., Greenwood, S. L., & Dilworth, M. R. (2018) · Placenta · doi:10.1016/j.placenta.2018.06.311 · Cited by 39 · see citing works
Irvin-Choy, N. S., Nelson, K. M., Dang, M. N., Gleghorn, J. P., & Day, E. S. (2021) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2021.102412 · Cited by 37 · see citing works
Meirelles, M. G., Veras, M. M., Alonso, M. A., Guimarães, C. D. F., Nichi, M., & Fernandes, C. B. (2017) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2017.03.226 · Cited by 37 · see citing works
Kelley, R. L., & Gardner, D. K. (2019) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2019.03.102 · Cited by 34 · see citing works
Dysregulation of placental ABC transporters in a murine model of malaria-induced preterm labor
Fontes, K. N., Reginatto, M. W., Silva, N. L., de Andrade, C. B. V., Bloise, F. F., Monteiro, V. R. D. S., Silva‐Filho, J. L., Império, G. E., Pimentel‐Coelho, P. M., Pinheiro, A. A. S., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-47865-3 · Cited by 35 · see citing works
Persistent DNA Damage and Senescence in the Placenta Impacts Developmental Outcomes of Embryos
Singh, V. P., McKinney, S., & Gerton, J. L. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.05.025 · Cited by 36 · see citing works
Zhou, Q., Fang, M.-D., Huang, T., Li, C., Yu, M., & Zhao, S. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-337 · Cited by 34 · see citing works
“In humans, smaller neonates are less likely to survive at birth and have a greater susceptibility to disease [5].”
BackgroundTan, K., Zhang, Z., Miao, K., Yu, Y., Sui, L., Tian, J., & An, L. (2016) · Molecular Human Reproduction · doi:10.1093/molehr/gaw028 · Cited by 35 · see citing works
Maternal muscle mass may influence system A activity in human placenta
Lewis, R. M., Greenwood, S. L., Cleal, J. K., Crozier, S. R., Verrall, L., Inskip, H. M., Cameron, I. T., Cooper, C., Sibley, C. P., Hanson, M. A., et al. (2010) · Placenta · doi:10.1016/j.placenta.2010.02.001 · Cited by 33 · see citing works
“Contrary to our birth weight/placental weight observations system A has also been shown to be up-regulated in small mouse placentas [35].”
BackgroundSaif, J., Ahmad, S., Rezai, H., Litvinova, K. S., Sparatore, A., Alzahrani, F. A., Wang, K., & Ahmed, A. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101814 · Cited by 33 · see citing works
“Increase in labyrinth zone area has been associated with a positive adaptation of placenta for better nourishment of fetus in mice [56].”
BackgroundSoliman, A. T., Eldabbagh, M., Saleem, W., Zahredin, K., Shatla, E., & Adel, A. (2013) · Journal of Tropical Pediatrics · doi:10.1093/tropej/fmt030 · Cited by 30 · see citing works
“This adaptability in placental phenotype provides a functional reserve capacity to better match the placental nutrient supply with the fetal nutrient demands but also a potential mechanism of signaling environmental conditions to the fetus, and possibly postnatal events including growth [10, 13].”
Thomas, K. N., Zimmel, K. N., Basel, A., Roach, A. N., Mehta, N. A., Thomas, K. R., Dotson, L. J., Bedi, Y. S., & Golding, M. C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.930375 · Cited by 30 · see citing works
“The progressive, dose-dependent histological changes to the placental labyrinth layer we observe are similar to previous studies examining placental responses during fetal growth restriction (Coan et al., 2008).”
ResultGanguly, A., Touma, M., Thamotharan, S., Vivo, D. C. D., & Devaskar, S. U. (2016) · Endocrinology · doi:10.1210/en.2016-1259 · Cited by 30 · see citing works
Vasilopoulou, E., Loubière, L. S., Heuer, H., Trajkovic‐Arsic, M., Darras, V., Visser, T. J., Lash, G. E., Whitley, G. S. J., McCabe, C. J., Franklyn, J. A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065402 · Cited by 29 · see citing works
“Against a uniform maternal genotype (heterozygous female carriers Mct8) in mice and amongst male conceptuses Mct8 knockout resulted in a 25% reduction in fetal to placental weight ratio compared to wild-type, which is indicative of reduced placental efficiency [50].”
BackgroundKwan, S. T., King, J. H., Grenier, J. K., Yan, J., Jiang, X., Roberson, M. S., & Caudill, M. A. (2018) · Nutrients · doi:10.3390/nu10040417 · Cited by 29 · see citing works
“5—a time when the placenta reaches its maximal size and the fetus is rapidly growing [21,22]—from dams receiving 1X or 4X choline supplementation.”
BackgroundStanelle‐Bertram, S., Gnirß, K., Speiseder, T., Thiele, S., Asante, I. A., Dreier, C., Kouassi, N. M., Preuß, A., Pilnitz-Stolze, G., Müller, U., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0236-1 · Cited by 29 · see citing works
Salazar‐Petres, E., Pereira‐Carvalho, D., López‐Tello, J., & Sferruzzi-Perri, A. N. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac056 · Cited by 32 · see citing works
“In addition, we evaluated the expression of imprinted genes Placental specific insulin growth factor 2 (Igf2P0) and Dlk1, which are involved in feto-placental growth and allocation of maternal resources [30, 31], and found no differences between the heaviest and the lightest of each sex (Figure 7F).”
BackgroundResultInfluentialTung, E., Roberts, C. T., Heinemann, G. K., Blasio, M. J. D., Kind, K. L., Wettere, W. H. E. J. V., Owens, J. A., & Gatford, K. L. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.112.100222 · Cited by 28 · see citing works
“Within mouse litters, placental expression of SLC38A2 is highest in the fastest-growing fetuses [33].”
BackgroundVaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., & Fowden, A. L. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.109678 · Cited by 28 · see citing works
“However, upregulation of system A amino acid transfer is observed in the mouse placenta when its growth is restricted either naturally or by genetic or nutritional manipulation [51–53].”
BackgroundSelf-citationTeoh, P. J., Menzies, F. M., Hansell, C. A. H., Clarke, M., Waddell, C., Burton, G. J., Nelson, S. M., & Nibbs, R. J. B. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401096 · Cited by 26 · see citing works
“Placentas can adapt morphologically and functionally in late gestation to meet the nutrient needs of the fetus (12), and it is possible that early defects in the formation or enlargement of the LZ in Ackr2-deficient placentas are corrected in late gestation to”
BackgroundSelf-citationCissé, Y. M., Chan, J. C., Nugent, B. M., Banducci, C., & Bale, T. L. (2020) · Placenta · doi:10.1016/j.placenta.2020.06.019 · Cited by 25 · see citing works
Zhang, J., Adams, M. A., & Croy, B. A. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2011.06.008 · Cited by 25 · see citing works
Lee, B., Shin, H., Oh, J., Park, J., Park, M., Yang, S. C., Jun, J. H., Hong, S., Song, H., & Lim, H. J. (2020) · Autophagy · doi:10.1080/15548627.2020.1778292 · Cited by 24 · see citing works
“This change, observed in L-NAMEinjected atg7 pregnant mice, is associated with optimal fetal growth, and therefore, is considered as a manifestation of placental adaptation [81].”
BackgroundArias, A., Schander, J. A., Bariani, M. V., Correa, F., Rubio, A. P. D., Cella, M., Cymeryng, C. B., Wolfson, M. L., Franchi, A. M., & Aisemberg, J. (2021) · Molecular Human Reproduction · doi:10.1093/molehr/gaab006 · Cited by 21 · see citing works
Charnock, J. C., Dilworth, M. R., Aplin, J., Sibley, C. P., Westwood, M., & Crocker, I. P. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00379.2015 · Cited by 22 · see citing works
Steane, S. E., Fielding, A. M., Kent, N. L., Andersen, I., Browne, D. J., Tejo, E. N., Gårdebjer, E. M., Kalisch-Smith, J. I., Sullivan, M. A., Moritz, K. M., et al. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14685 · Cited by 22 · see citing works
Favaron, P. O., Mess, A., de Oliveira, M. F., Gabory, A., Miglino, M. A., Chavatte‐Palmer, P., & Couturier‐Tarrade, A. (2013) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-11-10 · Cited by 22 · see citing works
“It is important to note, however, that the absolute volume of the mouse placenta at the end of gestation ([9,28,50,53], our results) was 3-fold higher than that of N.”
ResultReginatto, M., Fontes, K. N., Monteiro, V., Silva, N., Andrade, C., Gomes, H. R., Império, G., Bloise, F., Kluck, G., Atella, G., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.706499 · Cited by 16 · see citing works
de Andrade, C. B. V., Lopes, L. V. A., Ortiga-Carvalho, T. M., Matthews, S. G., & Bloise, E. (2022) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2022.116344 · Cited by 21 · see citing works
Nishimura, T., Chishu, T., Tomi, M., Nakamura, R., Sato, K. C., Kose, N., Sai, Y., & Nakashima, E. (2012) · Drug Metabolism and Pharmacokinetics · doi:10.2133/dmpk.dmpk-11-rg-103 · Cited by 21 · see citing works
Fischer, F., Kretschmer, T., Seifert, P., Howanski, J., Krieger, E., Rödiger, J., Fink, B., Yin, Z., Bauer, M., Zenclussen, M. L., et al. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.171386 · Cited by 20 · see citing works
- Authors
- Coan, P. M., Angiolini, E., Sandovici, I., Burton, G. J., Constância, M., & Fowden, A. L.
- Affiliations
- University of Cambridge (GB)
- Babraham Institute (GB)
- Corresponding author
- Coan, P. M.
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2008-09-15
- Volume
- 586
- Issue
- 18
- Pages
- 4567-4576
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC2614013
- OpenAlex
- W2123416686
- Cited by
- 194
- References
- 38
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 8 · 2023: 8 · 2022: 11 · 2021: 14 · 2020: 12 · 2019: 11 · 2018: 11 · 2017: 9 · 2016: 9 · 2015: 7 · 2014: 8 · 2013: 14 · 2012: 23
- FWCI
- 14.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/B50118X/1, BB/C513626/1, BB/B50118X/2)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- placental nutrient transfer, placental size, fetal growth, placental efficiency, amino acid transport, glucose transport, GLUT1, SNAT2, SLC38A2, SLC2A1, SLC38A4, SLC38A1, Grb10, placental morphology, placental development, mouse pregnancy
- MeSH terms
- Adaptation, Physiological, Animals, Female, Gestational Age, Insulin-Like Growth Factor II, Maternal-Fetal Exchange, Mice, Inbred C57BL, Organ Size, Placenta, Pregnancy, Pregnancy, Animal, Fetal Weight, Amino Acid Transport System A, Fetal Development, Glucose Transporter Type 1, Glucose Transporter Type 3, Mice, GRB10 Adaptor Protein
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