Venoarterial communication mediates arterial wall shear stress-induced maternal uterine vascular remodeling during pregnancy

Author:

Ko Nga Ling1,Mandalà Maurizio2,John Liam1,Gelinne Aaron1,Osol George1

Affiliation:

1. Department of Obstetrics, Gynecology, and Reproductive Sciences, Larner College of Medicine, University of Vermont, Burlington, Vermont

2. Department of Biology, Ecology, and Earth Science, University of Calabria, Cosenza, Italy

Abstract

Although expansive remodeling of the maternal uterine circulation during pregnancy is essential for maintaining uteroplacental perfusion and normal fetal growth, the underlying physiological mechanisms are not well understood. Using a rat model, surgical approaches were used to alter uterine hemodynamics and wall shear stress (WSS) to evaluate the effects of WSS and venoarterial communication (e.g., transfer of placentally derived growth signals from postplacental veins to preplacental arteries) on gestational uterine vascular remodeling. Changes in WSS secondary to ligation of the cervical but not the ovarian end of the main uterine artery and vein provoked significant expansive remodeling at the opposite end of both vessels, but only in pregnant animals. The ≈50% increase in lumen diameter (relative to the contralateral horn) was associated with an upregulation of total endothelial nitric oxide (NO) synthase expression and was abolished by in vivo NO synthase inhibition with N-nitro-l-arginine methyl ester. Complete removal of a venous segment adjacent to the uterine artery to eliminate local venous influences significantly attenuated the WSS-induced remodeling by about one-half ( P < 0.05). These findings indicate that, during pregnancy, 1) increased WSS stimulates uterine artery growth via NO signaling and 2) the presence of an adjacent vein is required for arterial remodeling to fully occur. NEW & NOTEWORTHY This study provides the first in vivo evidence for the importance of venous influences on arterial growth within the uteroplacental circulation.

Funder

HHS | National Institutes of Health (NIH)

Publisher

American Physiological Society

Subject

Physiology (medical),Cardiology and Cardiovascular Medicine,Physiology

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1. Guidelines for assessing maternal cardiovascular physiology during pregnancy and postpartum;American Journal of Physiology-Heart and Circulatory Physiology;2024-07-01

2. Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors;American Journal of Physiology-Heart and Circulatory Physiology;2023-10-01

3. Piezo1 channels mediate vasorelaxation of uterine arteries from pseudopregnant rats;Frontiers in Physiology;2023-06-01

4. Evidence of Nitric Oxide Impairment During Hypertensive Pregnancies;Advances in Maternal-Fetal Biomedicine;2023

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