The DOI matches its Crossref record; 37 of the 38 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming
Mcmillen, I. C., & Robinson, J. S. (2005) · Physiological Reviews · doi:10.1152/physrev.00053.2003 · Cited by 1,910
Estimation of surface area from vertical sections
Baddeley, A. J., Gundersen, H. J. G., & Cruz-Orive, L. M. (1986) · Journal of Microscopy · doi:10.1111/j.1365-2818.1986.tb04282.x · Cited by 1,057
Placental-specific IGF-II is a major modulator of placental and fetal growth
Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., et al. (2002) · Nature · doi:10.1038/nature00819 · Cited by 1,054
Self-citationMothers, Babies, and Disease in Later Life
Gillman, M. W. (1995) · BMJ · doi:10.1136/bmj.310.6971.68a · Cited by 880
Mothers, Babies and Disease in Later Life
Barker, D. J. P., & Barker, D. J. P. (1994) · Medical Entomology and Zoology · Cited by 860
Development of Structures and Transport Functions in the Mouse Placenta
Watson, E. D., & Cross, J. C. (2005) · Physiology · doi:10.1152/physiol.00001.2005 · Cited by 580
Developmental Origins of Health and Disease: New Insights
Hanson, M. A., & Gluckman, P. D. (2008) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00186.x · Cited by 359
Programming placental nutrient transport capacity
Fowden, A. L., Ward, J. W., Wooding, F. P. B., Forhead, A. J., & Constancia, M. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.104141 · Cited by 334
Self-citationConstância, M., Angiolini, E., Sandovici, I., Smith, P., Smith, R., Kelsey, G., Dean, W., Ferguson-Smith, A., Sibley, C. P., Reik, W., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504468103 · Cited by 323 · cited 4×
“For example, in the small Igf2P0 mutant placenta, there is increased expression of amino acid transporters and enhanced amino acid transfer compared with the wild-type placenta (Constancia et al. 2005).”
BackgroundInfluentialSelf-citationSibley, C. P., Coan, P. M., Ferguson‐Smith, A. C., Dean, W., Hughes, J., Smith, P., Reik, W., Burton, G. J., Fowden, A. L., & Constância, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402508101 · Cited by 299
Self-citationDevelopmental Dynamics of the Definitive Mouse Placenta Assessed by Stereology1
Coan, P. M., Ferguson-Smith, A. C., & Burton, G. J. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024166 · Cited by 296
Self-citationCharalambous, M., Smith, F. M., Bennett, W. R., Crew, T. E., Mackenzie, F. E., & Ward, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1532175100 · Cited by 279
The Placenta and Intrauterine Programming
Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01663.x · Cited by 278
Self-citationImprinted Genes, Placental Development and Fetal Growth
Fowden, A. L., Sibley, C. P., Reik, W., & Constância, M. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091506 · Cited by 273
Self-citationJansson, N., Pettersson, J., Haafiz, A., Ericsson, A., Palmberg, I., Tranberg, M., Ganapathy, V., Powell, T. L., & Jansson, T. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.550004 · Cited by 265
Placental Phenotypes of Intrauterine Growth
Sibley, C. P., Turner, M. A., Cetin, I., Ayuk, P. T.-Y., Boyd, C. A. R., D'Souza, S. W., Glazier, J. D., Greenwood, S. L., Jansson, T., & Powell, T. L. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000181381.82856.23 · Cited by 250
Harding, J. E., & Johnston, B. (1995) · Reproduction Fertility and Development · doi:10.1071/rd9950539 · Cited by 226
Allen, W. R., Wilsher, S., Turnbull, C., Stewart, F., Ousey, J., Rossdale, P. D., & Fowden, A. L. (2002) · Reproduction · doi:10.1530/rep.0.1230445 · Cited by 223
Self-citationMash2 Acts Cell Autonomously in Mouse Spongiotrophoblast Development
Tanaka, M., Gertsenstein, M., Rossant, J., & Nagy, A. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8685 · Cited by 216
Molteni, R. A., Stys, S. J., & Battaglia, F. C. (1978) · PubMed · Cited by 200
Endocrine and metabolic programming during intrauterine development
Fowden, A. L., Giussani, D. A., & Forhead, A. J. (2005) · Early Human Development · doi:10.1016/j.earlhumdev.2005.06.007 · Cited by 196
Self-citationA mouse model for Glut-1 haploinsufficiency
Wang, D., Pascual, J. M., Yang, H., Engelstad, K., Mao, X., Cheng, J., Yoo, J. H., Noebels, J. L., & Vivo, D. C. D. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl032 · Cited by 185
GENETIC AND ENVIRONMENTAL EFFECTS ON FOETAL AND PLACENTAL GROWTH IN MICE
McLaren, A. L. D. (1965) · Reproduction · doi:10.1530/jrf.0.0090079 · Cited by 184
Regulation of Placental Efficiency for Nutrient Transport by Imprinted Genes
Angiolini, E., Fowden, A., Coan, P., Sandovici, I., Smith, P., Dean, W., Burton, G., Tycko, B., Reik, W., Sibley, C., et al. (2006) · Placenta · doi:10.1016/j.placenta.2005.12.008 · Cited by 179
Self-citationPlacental transport and fetal utilization of leucine in a model of fetal growth retardation
J. C. Ross, Fennessey, P. V., Wilkening, R. B., Battaglia, F. C., & Meschia, G. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.3.e491 · Cited by 146
Ain, R., Kent, L. N., & Soares, M. J. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.06039 · Cited by 124
Glucose transporter isoform-3 mutations cause early pregnancy loss and fetal growth restriction
Ganguly, A., McKnight, R. A., Raychaudhuri, S., Shin, B.-C., Ma, Z., Moley, K., & Devaskar, S. U. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00344.2006 · Cited by 114
Placental transporter activity and expression in relation to fetal growth
Sibley, C. P., Glazier, J. D., & D’Souza, S. W. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004034 · Cited by 86
Wallace, J. M., Bourke, D. A., Aitken, R. P., Milne, J. S., & Hay, W. W. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.023333 · Cited by 86
Godfrey, K. M., Matthews, N., Glazier, J. D., Jackson, A. A., Wilman, C., & Sibley, C. P. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.9.5132 · Cited by 85
Roberts, C. T., Owens, J. A., & Sferruzzi-Perri, A. N. (2008) · Placenta · doi:10.1016/j.placenta.2007.12.002 · Cited by 74
Godfrey, K. M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.9.3320 · Cited by 72
Sferruzzi-Perri, A. N., Owens, J. A., Standen, P., Taylor, R. L., Heinemann, G. K., Robinson, J. S., & Roberts, C. T. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00320.2006 · Cited by 66
Lack of correlation between placenta and offspring size in mouse interspecific crosses
Kurz, H., Zechner, U., Orth, A., & Fundele, R. H. (1999) · Anatomy and Embryology · doi:10.1007/s004290050284 · Cited by 46
Factors Affecting Fetal Pig Weight Late in Gestation
Waldorf, D. P., FOOTE, W. C., Self, H. L., Chapman, A. B., & Casida, L. E. (1957) · Journal of Animal Science · doi:10.2527/jas1957.164976x · Cited by 38
Owens, J. A., Falconer, J. S., & Robinson, J. S. (1987) · PubMed · Cited by 34
The relationship of umbilical glucose uptake to uterine blood flow.
Rb, W., Battaglia, F. C., & Meschia, G. (1985) · PubMed · Cited by 28
Flagged first, then by citations
1 of the 38 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Kelly RW, 1992, Nutrition and placental development, Proc Nutr Soc Aust, 17, 203
- 10.1111/j..2002.00085.x · DOI · Paper page
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717
Self-citationRegulation of Placental Development and Its Impact on Fetal Growth—New Insights From Mouse Models
Woods, L. M., Pérez-García, V., & Hemberger, M. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00570 · Cited by 464
“In fact, one study found that in normal pregnancies, the smallest placentas in a litter are more efficient in their nutrient transfer capacity to promote adequate fetal growth (105).”
BackgroundHow nutrition and the maternal microbiota shape the neonatal immune system
Macpherson, A. J., de Agüero, M. G., & Ganal-Vonarburg, S. C. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.58 · Cited by 378
Placental efficiency and adaptation: endocrine regulation
Fowden, A. L., Sferruzzi-Perri, A. N., Coan, P. M., Constância, M., & Burton, G. J. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.173013 · Cited by 359
“In small efficient mouse placentas at day 16 of pregnancy, the labyrinthine zone accounts for a greater proportion of the total volume so that there is 35% more surface area per gram of placenta compared to the large placenta in the litter (Coan et al. 2008a).”
BackgroundInfluentialSelf-citationPlacental Adaptation: What Can We Learn from Birthweight:Placental Weight Ratio?
Hayward, C. E., Lean, S. C., Sibley, C. P., Jones, R. L., Wareing, M., Greenwood, S. L., & Dilworth, M. R. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00028 · Cited by 286
Metadata
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
