Expansion of the fetoplacental vasculature in late gestation is strain dependent in mice
Open accessAbstract
How the fetoplacental arterial tree grows and expands during late gestational development is largely unknown. In this study, we quantified changes in arterial branching in the fetal exchange region of the mouse placenta during late gestation, when capillarization increases rapidly. We studied two commonly used mouse strains, CD1 and C57Bl/6 (B6), at embryonic days (E)13.5, 15.5, and 17.5. B6 mice differ from CD1 mice by exhibiting a blunted fetal weight gain in late gestation. We found that B6 capillarization and interhemal membrane thinning were reduced and placental hypoxia-inducible factor-1α and VEGF-A expression were higher than CD1 near term. Automated vascular segmentation of microcomputed tomography data sets revealed that the number of arterial vessels ≥50 μm remained constant during late gestation in both strains, despite large increases in downstream capillary volume quantified by stereology (+65% in B6 mice and +200% in CD1 mice). Arterial diameters expanded in both strains from E13.5 to E15.5; however, diameters continued to expand to E17.5 in B6 mice only. The diameter scaling coefficient at branch sites was near optimal (−3.0) and remained constant in CD1 mice, whereas it decreased, becoming abnormal, in B6 mice at term (−3.5 ± 0.2). Based on arterial tree geometry, resistance remained constant throughout late gestation (∼0.45 mmHg·s·μl−1) in CD1 mice, whereas it decreased by 50% in late gestation in B6 mice. Quantification of the fetoplacental vasculature revealed significant strain-dependent differences in arterial and capillary expansion in late gestation. In both strains, enlargement of the fetoplacental arterial tree occurred primarily by increased arterial diameters with no change in segment numbers in late gestation.
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
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?
Inter- and intra-species crosses between breeds of several species have shown that the mother can constrain the fetal genetic drive for growth while the fetal genome can influence the mother to provide more resources with consequences for fetal growth and pregnancy outcome.
“Inter-and intra-species crosses between breeds of several species have shown that the mother can constrain the fetal genetic drive for growth while, conversely, the fetal genome can influence the mother to provide more resources with consequences for fetal growth and pregnancy outcome (8,457,551).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [457]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Endothelial cells and VEGF in vascular development
Coultas, L., Chawengsaksophak, K., & Rossant, J. (2005) · Nature · doi:10.1038/nature04479 · Cited by 1,016 · see citing works
Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis
Hove, J. R., Köster, R. W., Forouhar, A. S., Acevedo‐Bolton, G., Fraser, S. E., & Gharib, M. (2003) · Nature · doi:10.1038/nature01282 · Cited by 1,000 · see citing works
Preparing for the First Breath: Genetic and Cellular Mechanisms in Lung Development
Morrisey, E. E., & Hogan, B. L. M. (2010) · Developmental Cell · doi:10.1016/j.devcel.2009.12.010 · Cited by 967 · see citing works
Hsia, C. C. W., Hyde, D. M., Ochs, M., & Weibel, E. R. (2010) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200809-1522st · Cited by 906 · see citing works
The branching programme of mouse lung development
Metzger, R. J., Klein, O. D., Martin, G. R., & Krasnow, M. A. (2008) · Nature · doi:10.1038/nature07005 · Cited by 787 · see citing works
Pathology of the Human Placenta
Benirschke, K., & Kaufmann, P. (1990) · Springer eBooks · doi:10.1007/978-1-4757-4193-3 · Cited by 689 · see citing works
On connecting large vessels to small. The meaning of Murray's law.
Sherman, T. F. (1981) · The Journal of General Physiology · doi:10.1085/jgp.78.4.431 · Cited by 661 · see citing works
Comparative Developmental Anatomy of the Murine and Human Definitive Placentae
Georgiades, P., Ferguson-Smith, A. C., & Burton, G. J. (2002) · Placenta · doi:10.1053/plac.2001.0738 · Cited by 641 · see citing works
Interactions between Trophoblast Cells and the Maternal and Fetal Circulation in the Mouse Placenta
Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C., & Cross, J. C. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0773 · Cited by 617 · see citing works
Self-citationDevelopment 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 583 · see citing works
(2002) · PubMed · Cited by 550 · see citing works
Genetic Control of Branching Morphogenesis
Metzger, R. J., & Krasnow, M. A. (1999) · Science · doi:10.1126/science.284.5420.1635 · Cited by 502 · see citing works
Reneman, R. S., Arts, T. G. J., & Hoeks, A. P. G. (2006) · Journal of Vascular Research · doi:10.1159/000091648 · Cited by 428 · see citing works
Krebs, C., Macara, L., Leiser, R., BOWMAN, A. W., Greer, I. A., & Kingdom, J. C. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70103-5 · Cited by 427 · see citing works
Anson‐Cartwright, L., Dawson, K. M., Holmyard, D., Fisher, S. J., Lazzarini, R. A., & Cross, J. C. (2000) · Nature Genetics · doi:10.1038/77076 · Cited by 418 · see citing works
Determination of membrane thickness distribution from orthogonal intercepts
Jensen, E. B. V., Gundersen, H. J. G., & Østerby, R. (1979) · Journal of Microscopy · doi:10.1111/j.1365-2818.1979.tb00149.x · Cited by 360 · see citing works
Macara, L., Kingdom, J. C., Kaufmann, P., Kohnen, G., Hair, J., More, I. A. R., Lyall, F., & Greer, I. A. (1996) · Placenta · doi:10.1016/s0143-4004(05)80642-3 · Cited by 352 · see citing works
Genes, Development and Evolution of the Placenta
Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H., & Kingdom, J. C. (2003) · Placenta · doi:10.1053/plac.2002.0887 · Cited by 348 · see citing works
Developmental 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 · see citing works
Yolk sac–derived primitive erythroblasts enucleate during mammalian embryogenesis
Kingsley, P. D., Malik, J. T., Fantauzzo, K. A., & Palis, J. (2004) · Blood · doi:10.1182/blood-2003-12-4162 · Cited by 253 · see citing works
Origin and characteristics of glycogen cells in the developing murine placenta
Coan, P. M., Conroy, N., Burton, G. J., & Ferguson‐Smith, A. C. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20981 · Cited by 243 · see citing works
Particulate Urban Air Pollution Affects the Functional Morphology of Mouse Placenta1
Veras, M. M., Damaceno-Rodrigues, N. R., Caldini, E. G., Ribeiro, A. A. C. M., Mayhew, T. M., Saldiva, P. H. N., & Dolhnikoff, M. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.108.069591 · Cited by 243 · see citing works
Scaling laws of vascular trees: of form and function
Kassab, G. S. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00579.2005 · Cited by 223 · see citing works
Large variations in absolute wall shear stress levels within one species and between species
Cheng, C., Helderman, F., Tempel, D., Segers, D., Hierck, B. P., Poelmann, R. E., van Tol, A., Duncker, D. J., Robbers‐Visser, D., Ursem, N. T. C., et al. (2006) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2006.11.019 · Cited by 211 · see citing works
Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., & Fowden, A. L. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2009.181214 · Cited by 199 · see citing works
Tools for targeted manipulation of the mouse genome.
van der Weyden, L., Adams, D., & Bradley, A. (2002) · Physiological Genomics · doi:10.1152/physiolgenomics.00074.2002 · Cited by 197 · see citing works
Interactions between Trophoblast Cells and the Maternal and Fetal Circulation in the Mouse Placenta
Adamson, S. L. (2002) · Developmental Biology · doi:10.1016/s0012-1606(02)90773-6 · Cited by 197 · see citing works
Self-citationCoan, P. M., Angiolini, E., Sandovici, I., Burton, G. J., Constância, M., & Fowden, A. L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.156133 · Cited by 194 · see citing works
Cox, B., Kotlyar, M., Evangelou, A. I., Ignatchenko, V., Ignatchenko, A., Whiteley, K. J., Jurišica, I., Adamson, S. L., Rossant, J., & Kislinger, T. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.37 · Cited by 165 · see citing works
Self-citationStructural morphology of renal vasculature
Nordsletten, D., Blackett, S. A., Bentley, M. D., Ritman, E. L., & Smith, N. P. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00814.2005 · Cited by 160 · see citing works
Jackson, M., Mayhew, T. M., & Boyd, P. A. (1992) · Placenta · doi:10.1016/0143-4004(92)90060-7 · Cited by 158 · see citing works
Regulation of Hypoxia Inducible Factors (HIF) in Hypoxia and Normoxia During Placental Development
Patel, J., Landers, K., Mortimer, R. H., & Richard, K. (2010) · Placenta · doi:10.1016/j.placenta.2010.08.008 · Cited by 157 · see citing works
Rheology of the microcirculation.
Pries, A. R., & Secomb, T. W. (2003) · PubMed · Cited by 156 · see citing works
Lyall, F., Young, A., Boswell, F., et al. (1997) · Placenta · doi:10.1016/s0143-4004(97)80061-6 · Cited by 152 · see citing works
Acharya, G., Wilsgaard, T., Berntsen, G., et al. (2005) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.1902 · Cited by 144 · see citing works
Intrauterine growth restriction and placental angiogenesis
Barut, F., Barut, A., Gün, B. D., Kandemir, N. O., Harma, M. I., Harma, M., Aktunç, E., & Özdamar, Ş. O. (2010) · Diagnostic Pathology · doi:10.1186/1746-1596-5-24 · Cited by 139 · see citing works
Mu, J., & Adamson, S. L. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00031.2006 · Cited by 130 · see citing works
Self-citationGenomic evolution of the placenta using co-option and duplication and divergencePreprint
Knox, K., & Baker, J. C. (2008) · Genome Research · doi:10.1101/gr.071407.107 · Cited by 126 · see citing works
Chorioallantoic Morphogenesis and Formation of the Placental Villous Tree
Cross, J. C., Simmons, D. G., & Watson, E. D. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb03212.x · Cited by 119 · see citing works
40 MHz Doppler characterization of umbilical and dorsal aortic blood flow in the early mouse embryo
Phoon, C. K. L., Aristizábal, O., & Turnbull, D. H. (2000) · Ultrasound in Medicine & Biology · doi:10.1016/s0301-5629(00)00278-7 · Cited by 107 · see citing works
Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity
Burton, G. J., & Jauniaux, E. R. M. (1995) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1995.tb10849.x · Cited by 91 · see citing works
Ishiwata, T., Nakazawa, M., Pu, W. T., Tevosian, S. G., & Izumo, S. (2003) · Circulation Research · doi:10.1161/01.res.0000100389.57520.1a · Cited by 89 · see citing works
Detmar, J., Rennie, M. Y., Whiteley, K. J., Qu, D., Taniuchi, Y., Shang, X., Casper, R. F., Adamson, S. L., Sled, J. G., & Jurisicova, A. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90436.2008 · Cited by 89 · see citing works
Self-citationRennie, M. Y., Detmar, J., Whiteley, K. J., Yang, J., Jurisicova, A., Adamson, S. L., & Sled, J. G. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00510.2010 · Cited by 82 · see citing works
Self-citationRennie, M. Y., Whiteley, K. J., Kulandavelu, S., Adamson, S. L., & Sled, J. G. (2007) · Placenta · doi:10.1016/j.placenta.2006.12.005 · Cited by 74 · see citing works
Self-citationKulandavelu, S., Qu, D., & Adamson, S. L. (2006) · Hypertension · doi:10.1161/01.hyp.0000218440.71846.db · Cited by 66 · see citing works
Self-citationWard, N. L., Moore, E., Noon, K., Spassil, N., Keenan, E., Ivanco, T. L., & LaManna, J. C. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00909.2006 · Cited by 59 · see citing works
Vasomotor responses of the umbilical circulation in fetal sheep
Adamson, S. L., Morrow, R. J., Bull, S. B., & Langille, B. L. (1989) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1989.256.5.r1056 · Cited by 57 · see citing works
Self-citationPhoon, C. K. L., Aristizábal, O., & Turnbull, D. H. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00869.2001 · Cited by 55 · see citing works
Branching Morphology of the Rat Hepatic Portal Vein Tree: A Micro-CT Study
den Buijs, J. O., Bajzer, Ž., & Ritman, E. L. (2006) · Annals of Biomedical Engineering · doi:10.1007/s10439-006-9150-4 · Cited by 54 · see citing works
Huang, Y., Guo, X., & Kassab, G. S. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00803.2005 · Cited by 54 · see citing works
Comparative structural and hemodynamic analysis of vascular trees
Yang, J., Yu, L. X., Rennie, M. Y., Sled, J. G., & Henkelman, R. M. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00363.2009 · Cited by 53 · see citing works
Self-citationEndo, H., Okamoto, A., Yamada, K., Nikaido, T., & Tanaka, T. (2005) · International Journal of Molecular Medicine · doi:10.3892/ijmm.16.1.79 · Cited by 50 · see citing works
Rajakumar, A., Jeyabalan, A., Markovic, N., Ness, R. B., Gilmour, C., & Conrad, K. P. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00097.2007 · Cited by 49 · see citing works
Vascular Corrosion Casting of the Uteroplacental and Fetoplacental Vasculature in Mice
Whiteley, K. J., Pfarrer, C. D., & Adamson, S. L. (2005) · Humana Press eBooks · doi:10.1385/1-59259-983-4:369 · Cited by 42 · see citing works
Self-citationStimulatory and inhibitory signaling molecules that regulate renal branching morphogenesis
Bridgewater, D. J., & Rosenblum, N. D. (2008) · Pediatric Nephrology · doi:10.1007/s00467-008-1048-y · Cited by 36 · see citing works
Kline, T. L., Zamir, M., & Ritman, E. L. (2011) · Cells Tissues Organs · doi:10.1159/000323482 · Cited by 34 · see citing works
Changes in Blood Flow to the Ovine Chorin and Amnion Across Gestation
Hedriana, H. L., Brace, R. A., & Gilbert, W. M. (1995) · Journal of the Society for Gynecologic Investigation · doi:10.1177/107155769500200602 · Cited by 24 · see citing works
Burton, G. J., & Feneley, M. R. (1992) · PubMed · Cited by 23 · see citing works
The “self-similarity logic” applied to the development of the vascular system
Guidolin, D., Enrico Crivellato, B., & Ribatti, D. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2010.12.045 · Cited by 17 · see citing works
Analysis of microvasculature in whole kidney specimens using micro-CT
Sled, J. G., Marxen, M., & Henkelman, R. M. (2004) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.559731 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [20]Detmar J Regulation of Cell Death During Murine Placental Development and Its Dysregulation Due to Xenobiotic Exposure (PhD dissertation) Toronto, ON, Canada: University of Toronto, 2007
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 · see citing works
- Authors
- Rennie, M. Y., Detmar, J., Whiteley, K. J., Jurisicova, A., Adamson, S. L., & Sled, J. G.
- Affiliations
- Hospital for Sick Children (CA)
- Mount Sinai Hospital (CA)
- Corresponding author
- Adamson, S. Lee
- Venue
- American Journal of Physiology-Heart and Circulatory Physiology
- Publisher
- American Physiological Society
- Published
- 2012-03-15
- Volume
- 302
- Issue
- 6
- Pages
- H1261-H1273
- ISSN
- 0363-6135 (ISSN-L)
- 1522-1539
- PMC
- PMC3311476
- OpenAlex
- W1988621470
- Cited by
- 57
- References
- 62
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 8 · 2020: 4 · 2019: 5 · 2018: 1 · 2017: 8 · 2016: 5 · 2015: 6 · 2014: 4 · 2013: 7
- FWCI
- 6.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Heart and Circulatory Physiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP93618, MOP86734)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- late pregnancy, arterial branching, capillarization, vascular resistance, strain differences, C57BL/6 mice, ICR mice, VEGF-A, fetal weight gain, placental development
- MeSH terms
- Animals, Arteries, Capillaries, Female, Fetus, Genotype, Gestational Age, Hemodynamics, Immunohistochemistry, Litter Size, Mice, Inbred C57BL, Microscopy, Electron, Scanning, Phenotype, Placenta, Pregnancy, Species Specificity, Blotting, Western, Neovascularization, Physiologic, Fetal Weight, Placental Circulation, Vascular Endothelial Growth Factor A, Mice, Hypoxia-Inducible Factor 1, alpha Subunit, X-Ray Microtomography
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
