Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors
Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechan...
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Veröffentlicht in: | American journal of physiology. Heart and circulatory physiology 2023-10, Vol.325 (4), p.H790-H805 |
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description | Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.
Fetal growth throughout pregnancy relies on delivery of an increasing volume of maternal blood to the placenta. To facilitate this, the uterine vascular network adapts structurally and functionally, resulting in wider blood vessels with decreased flow-mediated reactivity. Impaired remodeling of the rate-limiting uterine radial arteries has been associated with fetal growth restriction. However, the mechanisms underlying normal or pathological radial artery remodeling are poorly understood. Here, we used pressure myography to determine the roles of hemodynamic (resistance, flow rate, shear stress) and paracrine [β-estradiol, progesterone, placental growth factor (PlGF), vascular endothelial growth factor] factors on rat radial artery reactivity. We show that β-estradiol, progesterone, and PlGF attenuate flow-mediated constriction of radial arteries from nonpregnant rats, allowing them to withstand higher flow rates in a similar manner to pregnant vessels. This effect was partly mediated by nitric oxide (NO) production. To better understand how the combination of paracrine factors and shear stress may impact human radial artery remodeling in the first half of gestation, computational models of uterine hemodynamics, incorporating physiological parameters for trophoblast plugging and spiral artery remodeling, were used to predict shear stress in the upstream radial arteries across the first half of pregnancy. Human microvascular endothelial cells subjected to these predicted shear stresses demonstrated higher NO production when paracrine factors were added. This suggests that synergistic effects of paracrine and hemodynamic factors induce uterine vascular remodeling and that alterations in this balance could impair radial artery adaptation, limiting blood flow to the placenta and negatively impacting fetal growth.
NEW & NOTEWORTHY Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction |
doi_str_mv | 10.1152/ajpheart.00205.2023 |
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Fetal growth throughout pregnancy relies on delivery of an increasing volume of maternal blood to the placenta. To facilitate this, the uterine vascular network adapts structurally and functionally, resulting in wider blood vessels with decreased flow-mediated reactivity. Impaired remodeling of the rate-limiting uterine radial arteries has been associated with fetal growth restriction. However, the mechanisms underlying normal or pathological radial artery remodeling are poorly understood. Here, we used pressure myography to determine the roles of hemodynamic (resistance, flow rate, shear stress) and paracrine [β-estradiol, progesterone, placental growth factor (PlGF), vascular endothelial growth factor] factors on rat radial artery reactivity. We show that β-estradiol, progesterone, and PlGF attenuate flow-mediated constriction of radial arteries from nonpregnant rats, allowing them to withstand higher flow rates in a similar manner to pregnant vessels. This effect was partly mediated by nitric oxide (NO) production. To better understand how the combination of paracrine factors and shear stress may impact human radial artery remodeling in the first half of gestation, computational models of uterine hemodynamics, incorporating physiological parameters for trophoblast plugging and spiral artery remodeling, were used to predict shear stress in the upstream radial arteries across the first half of pregnancy. Human microvascular endothelial cells subjected to these predicted shear stresses demonstrated higher NO production when paracrine factors were added. This suggests that synergistic effects of paracrine and hemodynamic factors induce uterine vascular remodeling and that alterations in this balance could impair radial artery adaptation, limiting blood flow to the placenta and negatively impacting fetal growth.
NEW & NOTEWORTHY Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.</description><identifier>ISSN: 0363-6135</identifier><identifier>EISSN: 1522-1539</identifier><identifier>DOI: 10.1152/ajpheart.00205.2023</identifier><identifier>PMID: 37539447</identifier><language>eng</language><publisher>Rockville, MD: American Physiological Society</publisher><ispartof>American journal of physiology. Heart and circulatory physiology, 2023-10, Vol.325 (4), p.H790-H805</ispartof><rights>Copyright © 2023 The Authors. 2023 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c383t-bf7ce4b225454ec78b381553781bfa257d751e7bdb02bd359150ed9df45ea2863</citedby><cites>FETCH-LOGICAL-c383t-bf7ce4b225454ec78b381553781bfa257d751e7bdb02bd359150ed9df45ea2863</cites><orcidid>0000-0001-5908-2862 ; 0000-0003-4789-9730 ; 0000-0002-3757-4177</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,3039,27924,27925</link.rule.ids></links><search><creatorcontrib>Allerkamp, H. H.</creatorcontrib><creatorcontrib>Leighton, S.</creatorcontrib><creatorcontrib>Pole, T.</creatorcontrib><creatorcontrib>Clark, A. R.</creatorcontrib><creatorcontrib>James, J. L.</creatorcontrib><title>Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors</title><title>American journal of physiology. Heart and circulatory physiology</title><description>Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.
Fetal growth throughout pregnancy relies on delivery of an increasing volume of maternal blood to the placenta. To facilitate this, the uterine vascular network adapts structurally and functionally, resulting in wider blood vessels with decreased flow-mediated reactivity. Impaired remodeling of the rate-limiting uterine radial arteries has been associated with fetal growth restriction. However, the mechanisms underlying normal or pathological radial artery remodeling are poorly understood. Here, we used pressure myography to determine the roles of hemodynamic (resistance, flow rate, shear stress) and paracrine [β-estradiol, progesterone, placental growth factor (PlGF), vascular endothelial growth factor] factors on rat radial artery reactivity. We show that β-estradiol, progesterone, and PlGF attenuate flow-mediated constriction of radial arteries from nonpregnant rats, allowing them to withstand higher flow rates in a similar manner to pregnant vessels. This effect was partly mediated by nitric oxide (NO) production. To better understand how the combination of paracrine factors and shear stress may impact human radial artery remodeling in the first half of gestation, computational models of uterine hemodynamics, incorporating physiological parameters for trophoblast plugging and spiral artery remodeling, were used to predict shear stress in the upstream radial arteries across the first half of pregnancy. Human microvascular endothelial cells subjected to these predicted shear stresses demonstrated higher NO production when paracrine factors were added. This suggests that synergistic effects of paracrine and hemodynamic factors induce uterine vascular remodeling and that alterations in this balance could impair radial artery adaptation, limiting blood flow to the placenta and negatively impacting fetal growth.
NEW & NOTEWORTHY Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.</description><issn>0363-6135</issn><issn>1522-1539</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNpVkU1v1DAURS0EokPhF7Dxkk0Gf8RxskKoooBUiQWwtp7tlxlXiR1sByn_nrRTkFi9xT33vMUl5C1nR86VeA_3yxkh1yNjgqmjYEI-I4c9EQ1XcnhODkx2sum4VFfkVSn3jDGlO_mSXEm9A22rD2T6vkXMp1BqcDTjaZ2ghhRpGulaMYeINIMPMNH9E-aNgoelXpia6LJXIkS3UbvRBTK4xwpET884J79FmHfxCK6mXF6TFyNMBd883Wvy8_bTj5svzd23z19vPt41TvayNnbUDlsrhGpVi073VvZcKal7bkcQSnutOGrrLRPWSzVwxdAPfmwVgug7eU0-XLzLamf0DmPNMJklhxnyZhIE838Sw9mc0m_DWddKxuRuePdkyOnXiqWaORSH0wQR01qM6NtukKxTw47KC-pyKiXj-O8PZ-ZhKPN3KPM4lHkYSv4BsJCK1A</recordid><startdate>20231001</startdate><enddate>20231001</enddate><creator>Allerkamp, H. H.</creator><creator>Leighton, S.</creator><creator>Pole, T.</creator><creator>Clark, A. R.</creator><creator>James, J. L.</creator><general>American Physiological Society</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5908-2862</orcidid><orcidid>https://orcid.org/0000-0003-4789-9730</orcidid><orcidid>https://orcid.org/0000-0002-3757-4177</orcidid></search><sort><creationdate>20231001</creationdate><title>Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors</title><author>Allerkamp, H. H. ; Leighton, S. ; Pole, T. ; Clark, A. R. ; James, J. L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c383t-bf7ce4b225454ec78b381553781bfa257d751e7bdb02bd359150ed9df45ea2863</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Allerkamp, H. H.</creatorcontrib><creatorcontrib>Leighton, S.</creatorcontrib><creatorcontrib>Pole, T.</creatorcontrib><creatorcontrib>Clark, A. R.</creatorcontrib><creatorcontrib>James, J. L.</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>American journal of physiology. Heart and circulatory physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Allerkamp, H. H.</au><au>Leighton, S.</au><au>Pole, T.</au><au>Clark, A. R.</au><au>James, J. L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors</atitle><jtitle>American journal of physiology. Heart and circulatory physiology</jtitle><date>2023-10-01</date><risdate>2023</risdate><volume>325</volume><issue>4</issue><spage>H790</spage><epage>H805</epage><pages>H790-H805</pages><issn>0363-6135</issn><eissn>1522-1539</eissn><abstract>Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.
Fetal growth throughout pregnancy relies on delivery of an increasing volume of maternal blood to the placenta. To facilitate this, the uterine vascular network adapts structurally and functionally, resulting in wider blood vessels with decreased flow-mediated reactivity. Impaired remodeling of the rate-limiting uterine radial arteries has been associated with fetal growth restriction. However, the mechanisms underlying normal or pathological radial artery remodeling are poorly understood. Here, we used pressure myography to determine the roles of hemodynamic (resistance, flow rate, shear stress) and paracrine [β-estradiol, progesterone, placental growth factor (PlGF), vascular endothelial growth factor] factors on rat radial artery reactivity. We show that β-estradiol, progesterone, and PlGF attenuate flow-mediated constriction of radial arteries from nonpregnant rats, allowing them to withstand higher flow rates in a similar manner to pregnant vessels. This effect was partly mediated by nitric oxide (NO) production. To better understand how the combination of paracrine factors and shear stress may impact human radial artery remodeling in the first half of gestation, computational models of uterine hemodynamics, incorporating physiological parameters for trophoblast plugging and spiral artery remodeling, were used to predict shear stress in the upstream radial arteries across the first half of pregnancy. Human microvascular endothelial cells subjected to these predicted shear stresses demonstrated higher NO production when paracrine factors were added. This suggests that synergistic effects of paracrine and hemodynamic factors induce uterine vascular remodeling and that alterations in this balance could impair radial artery adaptation, limiting blood flow to the placenta and negatively impacting fetal growth.
NEW & NOTEWORTHY Placenta-specific paracrine factors β-estradiol, progesterone, and placental growth factor attenuate flow-mediated constriction of the rate-limiting uterine radial arteries, enabling higher flow rates in pregnancy. These paracrine factors induce their actions in part via nitric oxide mediated mechanisms. A synergistic combination of paracrine factors and shear stress is likely necessary to produce sufficient levels of nitric oxide during early human pregnancy to trigger adequate uterine vascular adaptation.</abstract><cop>Rockville, MD</cop><pub>American Physiological Society</pub><pmid>37539447</pmid><doi>10.1152/ajpheart.00205.2023</doi><orcidid>https://orcid.org/0000-0001-5908-2862</orcidid><orcidid>https://orcid.org/0000-0003-4789-9730</orcidid><orcidid>https://orcid.org/0000-0002-3757-4177</orcidid><oa>free_for_read</oa></addata></record> |
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title | Synergistic regulation of uterine radial artery adaptation to pregnancy by paracrine and hemodynamic factors |
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