Placental Insufficiency Decreases Pancreatic Vascularity and Disrupts Hepatocyte Growth Factor Signaling in the Pancreatic Islet Endothelial Cell in Fetal Sheep

Rozance, Paul J.; Anderson, Miranda; Martinez, Marina; Fahy, Anna; Macko, Antoni R.; Kailey, Jenai; Seedorf, Gregory J.; Abman, Steven H.; Hay, William W.; Limesand, Sean W.

doi:10.2337/db14-0462

Cited by 45Pancreatic function and diabetesBirth, Development, and HealthPregnancy and preeclampsia studies

Placental Insufficiency Decreases Pancreatic Vascularity and Disrupts Hepatocyte Growth Factor Signaling in the Pancreatic Islet Endothelial Cell in Fetal Sheep

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Rozance, Paul J., Anderson, Miranda, Martinez, Marina, Fahy, Anna, Macko, Antoni R., Kailey, Jenai, Seedorf, Gregory J., Abman, Steven H. +2 more·2015·Diabetes

DOI 10.2337/db14-0462PMC PMC4303968

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Abstract

Hepatocyte growth factor (HGF) and vascular endothelial growth factor A (VEGFA) are paracrine hormones that mediate communication between pancreatic islet endothelial cells (ECs) and β-cells. Our objective was to determine the impact of intrauterine growth restriction (IUGR) on pancreatic vascularity and paracrine signaling between the EC and β-cell. Vessel density was less in IUGR pancreata than in controls. HGF concentrations were also lower in islet EC-conditioned media (ECCM) from IUGR, and islets incubated with control islet ECCM responded by increasing insulin content, which was absent with IUGR ECCM. The effect of ECCM on islet insulin content was blocked with an inhibitory anti-HGF antibody. The HGF receptor was not different between control and IUGR islets, but VEGFA was lower and the high-affinity VEGF receptor was higher in IUGR islets and ECs, respectively. These findings show that paracrine actions from ECs increase islet insulin content, and in IUGR ECs, secretion of HGF was diminished. Given the potential feed-forward regulation of β-cell VEGFA and islet EC HGF, these two growth factors are highly integrated in normal pancreatic islet development, and this regulation is decreased in IUGR fetuses, resulting in lower pancreatic islet insulin concentrations and insulin secretion.

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A growth-restricted fetus has fewer insulin-producing beta cells and reduced vascularization in the pancreas, and compromised structure and maturation of the brain, lungs, and liver.
“In addition, the pancreas has fewer insulin-producing beta cells and reduced vascularization (159, 340, 473), and the structure and maturation of the brain (142), lungs (358, 359, 424, 460) and liver (209, 474) are compromised.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [473]

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The impact of IUGR on pancreatic islet development and β-cell function
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Authors: Rozance, P. J., Anderson, M., Martinez, M., Fahy, A., Macko, A. R., Kailey, J., Seedorf, G. J., Abman, S. H., Hay, W. W., & Limesand, S. W.
Affiliations: University of Colorado Anschutz (US)
University of Arizona (US)
School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ
Corresponding author: Rozance, Paul J.
ORCID: Rozance, Paul J.
Seedorf, Gregory J.
Abman, Steven H.
Hay, William W.
Limesand, Sean W.
Venue: Diabetes
Publisher: American Diabetes Association
Published: 2014-09-22
Volume: 64
Issue: 2
Pages: 555-564
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/db14-0462
PMC: PMC4303968
OpenAlex: W2148719389
Cited by: 45
References: 43
Citations by year: 2025: 1 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 3 · 2018: 8 · 2017: 7 · 2016: 8 · 2015: 3
FWCI: 5.95
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.diabetesjournals.org/site/license (vor, 313 d)
Locations: Diabetes (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK088139)
National Institute of Child Health and Human Development (K08 HD060688)
Topics: Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: placental insufficiency, fetal growth restriction, hepatocyte growth factor, VEGF-A, fetal sheep, pancreatic islet development, VEGF receptors
MeSH terms: Animals, Female, Fetal Growth Retardation, Fetus, Islets of Langerhans, Pancreas, Placental Insufficiency, Pregnancy, Sheep, Signal Transduction, Hepatocyte Growth Factor, Endothelial Cells

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Placental Insufficiency Decreases Pancreatic Vascularity and Disrupts Hepatocyte Growth Factor Signaling in the Pancreatic Islet Endothelial Cell in Fetal Sheep

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