Abstract
Hypertensive disorders of pregnancy complicate up to 10% of pregnancies worldwide, and they can be classified into (1) gestational hypertension, (2) preeclampsia, (3) chronic hypertension and (4) chronic hypertension with preeclampsia. Nitric oxide (NO) plays an essential role in the haemodynamic adaptations observed during pregnancy. It has been shown that the nitric oxide pathway’s dysfunction during pregnancy is associated with placental- and vascular-related diseases such as hypertensive disorders of pregnancy. This review aims to present a brief definition of hypertensive disorders of pregnancy and physiological maternal cardiovascular adaptations during pregnancy. We also detail how NO signalling is altered in the (a) systemic vasculature, (b) uterine artery/spiral arteries, (c) implantation and (d) placenta of hypertensive disorders during pregnancy. We conclude by summarizing the anti-hypertensive therapy of hypertensive disorders of pregnancy as a specific management strategy.
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References
Abbasi H, Dastgheib SA, Hadadan A, Karimi-Zarchi M, Javaheri A, Meibodi B, Zanbagh L, Tabatabaei RS, Neamatzadeh H (2021) Association of endothelial nitric oxide synthase 894G > T polymorphism with preeclampsia risk: a systematic review and meta-analysis based on 35 studies. Fetal Pediatr Pathol 40:455–470. https://doi.org/10.1080/15513815.2019.1710880
Abdel Razik M, El-Berry S, Abosereah M, Edris Y, Sharafeldeen A (2016) Prophylactic treatment for preeclampsia in high-risk teenage primigravidae with nitric oxide donors: a pilot study. J Matern-Fetal Neonatal Med 29:2617–2620. https://doi.org/10.3109/14767058.2015.1094793
ACOG practice bulletin no. 202: gestational hypertension and preeclampsia (2019) Obstet Gynecol 133:1. https://doi.org/10.1097/AOG.0000000000003018
Agatisa PK, Ness RB, Roberts JM, Costantino JP, Kuller LH, McLaughlin MK (2004) Impairment of endothelial function in women with a history of preeclampsia: an indicator of cardiovascular risk. Am J Physiol Heart Circ Physiol 286:H1389–H1393. https://doi.org/10.1152/ajpheart.00298.2003
Akbar F, Heinonen S, Pirskanen M, Uimari P, Tuomainen T-P, Salonen JT (2005) Haplotypic association of DDAH1 with susceptibility to pre-eclampsia. Mol Hum Reprod 11:73–77. https://doi.org/10.1093/molehr/gah116
Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, Granger JP (2001) Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension (Dallas TX) 1979(37):1191–1195. https://doi.org/10.1161/01.hyp.37.4.1191
Ali SMJ, Khalil RA (2015) Genetic, immune and vasoactive factors in the vascular dysfunction associated with hypertension in pregnancy. Expert Opin Ther Targets 19:1495–1515. https://doi.org/10.1517/14728222.2015.1067684
Amaral LM, Cornelius DC, Harmon A, Moseley J, Martin JN, LaMarca B (2015) 17-hydroxyprogesterone caproate significantly improves clinical characteristics of preeclampsia in the reduced uterine perfusion pressure rat model. Hypertension (Dallas TX) 1979(65):225–231. https://doi.org/10.1161/HYPERTENSIONAHA.114.04484
Amaral TAS, Ognibene DT, Carvalho LCRM, Rocha APM, Costa CA, Moura RS, Resende AC (2018) Differential responses of mesenteric arterial bed to vasoactive substances in L-NAME-induced preeclampsia: role of oxidative stress and endothelial dysfunction. Clin Exp Hypertens N Y N 1993(40):126–135. https://doi.org/10.1080/10641963.2017.1339073
American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins – Obstetrics (2019) ACOG practice bulletin no. 203: chronic hypertension in pregnancy. Obstet Gynecol 133:e26–e50. https://doi.org/10.1097/AOG.0000000000003020
Anderssohn M, Maass LM, Diemert A, Lüneburg N, Atzler D, Hecher K, Böger RH (2012) Severely decreased activity of placental dimethylarginine dimethylaminohydrolase in pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 161:152–156. https://doi.org/10.1016/j.ejogrb.2011.12.032
Ankumah N-AE, Sibai BM (2017) Chronic hypertension in pregnancy: diagnosis, management, and outcomes. Clin Obstet Gynecol 60:206–214. https://doi.org/10.1097/GRF.0000000000000255
Ariel I, Hochberg A, Shochina M (1998) Endothelial nitric oxide synthase immunoreactivity in early gestation and in trophoblastic disease. J Clin Pathol 51:427–431. https://doi.org/10.1136/jcp.51.6.427
Arishe OO, Ebeigbe AB, Webb RC (2020) Mechanotransduction and uterine blood flow in preeclampsia: the role of mechanosensing piezo 1 ion channels. Am J Hypertens 33:1–9. https://doi.org/10.1093/ajh/hpz158
Ayala DE, Hermida RC, Mojón A, Fernández JR, Silva I, Ucieda R, Iglesias M (1997) Blood pressure variability during gestation in healthy and complicated pregnancies. Hypertension (Dallas TX) 1979(30):611–618. https://doi.org/10.1161/01.hyp.30.3.611
Bader RA, Bader ME, Rose DF, Braunwald E (1955) Hemodynamics at rest and during exercise in normal pregnancy as studies by cardiac catheterization. J Clin Invest 34:1524–1536. https://doi.org/10.1172/JCI103205
Banerjee P, Ghosh S, Dutta M, Subramani E, Khalpada J, Roychoudhury S, Chakravarty B, Chaudhury K (2013) Identification of key contributory factors responsible for vascular dysfunction in idiopathic recurrent spontaneous miscarriage. PLoS One 8:e80940. https://doi.org/10.1371/journal.pone.0080940
Barbagallo M, Dominguez LJ, Licata G, Shan J, Bing L, Karpinski E, Pang PKT, Resnick LM (2001) Vascular effects of progesterone: role of cellular calcium regulation. Hypertension (Dallas TX) 1979(37):142–147. https://doi.org/10.1161/01.hyp.37.1.142
Barron C, Mandala M, Osol G (2010) Effects of pregnancy, hypertension and nitric oxide inhibition on rat uterine artery myogenic reactivity. J Vasc Res 47:463–471. https://doi.org/10.1159/000313874
Baylis SA, Strijbos PJ, Sandra A, Russell RJ, Rijhsinghani A, Charles IG, Weiner CP (1999) Temporal expression of inducible nitric oxide synthase in mouse and human placenta. Mol Hum Reprod 5:277–286. https://doi.org/10.1093/molehr/5.3.277
Bernardi FC, Vuolo F, Petronilho F, Michels M, Ritter C, Dal-Pizzol F (2015) Plasma nitric oxide, endothelin-1, arginase and superoxide dismutase in the plasma and placentae from preeclamptic patients. An Acad Bras Cienc 87:713–719. https://doi.org/10.1590/0001-3765201520140069
Bernstein PS, Martin JN, Barton JR, Shields LE, Druzin ML, Scavone BM, Frost J, Morton CH, Ruhl C, Slager J, Tsigas EZ, Jaffer S, Menard MK (2017) National partnership for maternal safety: consensus bundle on severe hypertension during pregnancy and the postpartum period. Anesth Analg 125:540–547. https://doi.org/10.1213/ANE.0000000000002304
Bhavina K, Radhika J, Pandian SS (2014) VEGF and eNOS expression in umbilical cord from pregnancy complicated by hypertensive disorder with different severity. Biomed Res Int 2014:982159. https://doi.org/10.1155/2014/982159
Bigonnesse E, Sicotte B, Brochu M (2018) Activated NO pathway in uterine arteries during pregnancy in an IUGR rat model. Am J Physiol Heart Circ Physiol 315:H415–H422. https://doi.org/10.1152/ajpheart.00457.2017
Bisits A, Madsen G, Knox M, Gill A, Smith R, Yeo G, Kwek K, Daniel M, Leung TN, Cheung K, Chung T, Jones I, Toohill J, Tudehope D, Giles W (2004) The randomized nitric oxide tocolysis trial (RNOTT) for the treatment of preterm labor. Am J Obstet Gynecol 191:683–690. https://doi.org/10.1016/j.ajog.2004.02.019
Boeldt DS, Bird IM (2017) Vascular adaptation in pregnancy and endothelial dysfunction in preeclampsia. J Endocrinol 232:R27–R44. https://doi.org/10.1530/JOE-16-0340
Boeldt DS, Yi FX, Bird IM (2011) eNOS activation and NO function: pregnancy adaptive programming of capacitative entry responses alters nitric oxide (NO) output in vascular endothelium – new insights into eNOS regulation through adaptive cell signaling. J Endocrinol 210:243–258. https://doi.org/10.1530/JOE-11-0053
Bos M, Schoots MH, Fernandez BO, Mikus-Lelinska M, Lau LC, Eikmans M, van Goor H, Gordijn SJ, Pasch A, Feelisch M, van der Hoorn M-LP (2019) Reactive species interactome alterations in oocyte donation pregnancies in the absence and presence of pre-eclampsia. Int J Mol Sci 20:E1150. https://doi.org/10.3390/ijms20051150
Browne VA, Julian CG, Toledo-Jaldin L, Cioffi-Ragan D, Vargas E, Moore LG (2015) Uterine artery blood flow, fetal hypoxia and fetal growth. Philos Trans R Soc Lond Ser B Biol Sci 370:20140068. https://doi.org/10.1098/rstb.2014.0068
Buchbinder A, Sibai BM, Caritis S, Macpherson C, Hauth J, Lindheimer MD, Klebanoff M, Vandorsten P, Landon M, Paul R, Miodovnik M, Meis P, Thurnau G, National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units (2002) Adverse perinatal outcomes are significantly higher in severe gestational hypertension than in mild preeclampsia. Am J Obstet Gynecol 186:66–71. https://doi.org/10.1067/mob.2002.120080
Buhimschi I, Yallampalli C, Chwalisz K, Garfield RE (1995) Pre-eclampsia-like conditions produced by nitric oxide inhibition: effects of L-arginine, D-arginine and steroid hormones. Hum Reprod Oxf Engl 10:2723–2730. https://doi.org/10.1093/oxfordjournals.humrep.a135775
Camarena Pulido EE, García Benavides L, Panduro Barón JG, Pascoe Gonzalez S, Madrigal Saray AJ, García Padilla FE, Totsuka Sutto SE (2016) Efficacy of L-arginine for preventing preeclampsia in high-risk pregnancies: a double-blind, randomized, clinical trial. Hypertens Pregnancy 35:217–225. https://doi.org/10.3109/10641955.2015.1137586
Carter AM, Enders AC, Pijnenborg R (2015) The role of invasive trophoblast in implantation and placentation of primates. Philos Trans R Soc Lond Ser B Biol Sci 370:20140070. https://doi.org/10.1098/rstb.2014.0070
Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS (2001) Association of maternal endothelial dysfunction with preeclampsia. JAMA 285:1607–1612. https://doi.org/10.1001/jama.285.12.1607
Chang J, Streitman D (2012) Physiologic adaptations to pregnancy. Neurol Clin 30:781–789. https://doi.org/10.1016/j.ncl.2012.05.001
Chappell LC, Enye S, Seed P, Briley AL, Poston L, Shennan AH (2008) Adverse perinatal outcomes and risk factors for preeclampsia in women with chronic hypertension: a prospective study. Hypertension (Dallas TX) 1979(51):1002–1009. https://doi.org/10.1161/HYPERTENSIONAHA.107.107565
Cheng M-H, Wang P-H (2009) Placentation abnormalities in the pathophysiology of preeclampsia. Expert Rev Mol Diagn 9:37–49. https://doi.org/10.1586/14737159.9.1.37
Chimini JS, Possomato-Vieira JS, da Silva MLS, Dias-Junior CA (2019) Placental nitric oxide formation and endothelium-dependent vasodilation underlie pravastatin effects against angiogenic imbalance, hypertension in pregnancy and intrauterine growth restriction. Basic Clin Pharmacol Toxicol 124:385–393. https://doi.org/10.1111/bcpt.13149
Chourdakis E, Fouzas S, Papadopoulou C, Oikonomou N, Hahalis G, Dimitriou G, Karatza AA (2020) Effect of early-onset preeclampsia on offspring’s blood pressure during the first month of life. J Pediatr 220:21–26.e1. https://doi.org/10.1016/j.jpeds.2020.01.033
Christianson RE (1976) Studies on blood pressure during pregnancy. I. Influence of parity and age. Am J Obstet Gynecol 125:509–513. https://doi.org/10.1016/0002-9378(76)90367-7
Chu ZM, Beilin LJ (1993) Mechanisms of vasodilatation in pregnancy: studies of the role of prostaglandins and nitric-oxide in changes of vascular reactivity in the in situ blood perfused mesentery of pregnant rats. Br J Pharmacol 109:322–329. https://doi.org/10.1111/j.1476-5381.1993.tb13573.x
Chwalisz K, Garfield RE (2000) Role of nitric oxide in implantation and menstruation. Hum Reprod Oxf Engl 15(Suppl 3):96–111. https://doi.org/10.1093/humrep/15.suppl_3.96
Chwalisz K, Winterhager E, Thienel T, Garfield RE (1999) Synergistic role of nitric oxide and progesterone during the establishment of pregnancy in the rat. Hum Reprod Oxf Engl 14:542–552. https://doi.org/10.1093/humrep/14.2.542
Clark SL, Cotton DB, Lee W, Bishop C, Hill T, Southwick J, Pivarnik J, Spillman T, DeVore GR, Phelan J (1989) Central hemodynamic assessment of normal term pregnancy. Am J Obstet Gynecol 161:1439–1442. https://doi.org/10.1016/0002-9378(89)90900-9
Conrad KP, Davis AK (1995) Nitric oxide synthase activity in placentae from women with pre-eclampsia. Placenta 16:691–699. https://doi.org/10.1016/0143-4004(95)90013-6
Conrad KP, Joffe GM, Kruszyna H, Kruszyna R, Rochelle LG, Smith RP, Chavez JE, Mosher MD (1993) Identification of increased nitric oxide biosynthesis during pregnancy in rats. FASEB 7:566–571
Cooke C-LM, Davidge ST (2003) Pregnancy-induced alterations of vascular function in mouse mesenteric and uterine arteries. Biol Reprod 68:1072–1077. https://doi.org/10.1095/biolreprod.102.009886
Corpa JM (2006) Ectopic pregnancy in animals and humans. Reprod Camb Engl 131:631–640. https://doi.org/10.1530/rep.1.00606
Costa RA, Hoshida MS, Alves EA, Zugaib M, Francisco RPV (2016) Preeclampsia and superimposed preeclampsia: the same disease? The role of angiogenic biomarkers. Hypertens Pregnancy 35:139–149. https://doi.org/10.3109/10641955.2015.1115063
Crews JK, Herrington JN, Granger JP, Khalil RA (2000) Decreased endothelium-dependent vascular relaxation during reduction of uterine perfusion pressure in pregnant rat. Hypertension (Dallas TX) 1979(35):367–372. https://doi.org/10.1161/01.hyp.35.1.367
Cross JC, Werb Z, Fisher SJ (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266:1508–1518. https://doi.org/10.1126/science.7985020
Cruz MO, Gao W, Hibbard JU (2011) Obstetrical and perinatal outcomes among women with gestational hypertension, mild preeclampsia, and mild chronic hypertension. Am J Obstet Gynecol 205:260.e1–260.e9. https://doi.org/10.1016/j.ajog.2011.06.033
Cureton N, Korotkova I, Baker B, Greenwood S, Wareing M, Kotamraju VR, Teesalu T, Cellesi F, Tirelli N, Ruoslahti E, Aplin JD, Harris LK (2017) Selective targeting of a novel vasodilator to the uterine vasculature to treat impaired uteroplacental perfusion in pregnancy. Theranostics 7:3715–3731. https://doi.org/10.7150/thno.19678
Cushen SC, Goulopoulou S (2017) New models of pregnancy-associated hypertension. Am J Hypertens 30:1053–1062. https://doi.org/10.1093/ajh/hpx063
D’Errico JN, Stapleton PA (2019) Developmental onset of cardiovascular disease-could the proof be in the placenta? Microcirc N Y N 1994(26):e12526. https://doi.org/10.1111/micc.12526
Davis JR, Giardina JB, Green GM, Alexander BT, Granger JP, Khalil RA (2002) Reduced endothelial NO-cGMP vascular relaxation pathway during TNF-alpha-induced hypertension in pregnant rats. Am J Physiol Regul Integr Comp Physiol 282:R390–R399. https://doi.org/10.1152/ajpregu.00270.2001
De Haas S, Ghossein-Doha C, Geerts L, van Kuijk SMJ, van Drongelen J, Spaanderman MEA (2017) Cardiac remodeling in normotensive pregnancy and in pregnancy complicated by hypertension: systematic review and meta-analysis. Ultrasound Obstet Gynecol 50:683–696. https://doi.org/10.1002/uog.17410
Desoye G, Hauguel-de Mouzon S (2007) The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care 30(Suppl 2):S120–S126. https://doi.org/10.2337/dc07-s203
Dötsch J, Hogen N, Nyúl Z, Hänze J, Knerr I, Kirschbaum M, Rascher W (2001) Increase of endothelial nitric oxide synthase and endothelin-1 mRNA expression in human placenta during gestation. Eur J Obstet Gynecol Reprod Biol 97:163–167. https://doi.org/10.1016/s0301-2115(00)00532-7
Duhig K, Vandermolen B, Shennan A (2018) Recent advances in the diagnosis and management of pre-eclampsia. F1000Research 7:242. https://doi.org/10.12688/f1000research.12249.1
Edey LF, Georgiou H, O’Dea KP, Mesiano S, Herbert BR, Lei K, Hua R, Markovic D, Waddington SN, MacIntyre D, Bennett P, Takata M, Johnson MR (2018) Progesterone, the maternal immune system and the onset of parturition in the mouse. Biol Reprod 98:376–395. https://doi.org/10.1093/biolre/iox146
Ehsanipoor RM, Fortson W, Fitzmaurice LE, Liao W-X, Wing DA, Chen D-B, Chan K (2013) Nitric oxide and carbon monoxide production and metabolism in preeclampsia. Reprod Sci Thousand Oaks Calif 20:542–548. https://doi.org/10.1177/1933719112459231
Eis AL, Brockman DE, Pollock JS, Myatt L (1995) Immunohistochemical localization of endothelial nitric oxide synthase in human villous and extravillous trophoblast populations and expression during syncytiotrophoblast formation in vitro. Placenta 16:113–126. https://doi.org/10.1016/0143-4004(95)90000-4
Eis AL, Brockman DE, Myatt L (1997) Immunolocalization of the inducible nitric oxide synthase isoform in human fetal membranes. Am J Reprod Immunol N Y N 1989 38:289–294. https://doi.org/10.1111/j.1600-0897.1997.tb00517.x
Ekerhovd E, Brännström M, Alexandersson M, Norström A (1997) Evidence for nitric oxide mediation of contractile activity in isolated strips of the human Fallopian tube. Hum Reprod Oxf Engl 12:301–305. https://doi.org/10.1093/humrep/12.2.301
Ekerhovd E, Brännström M, Weijdegård B, Norström A (1999) Localization of nitric oxide synthase and effects of nitric oxide donors on the human Fallopian tube. Mol Hum Reprod 5:1040–1047. https://doi.org/10.1093/molehr/5.11.1040
Erez O, Romero R, Maymon E, Chaemsaithong P, Done B, Pacora P, Panaitescu B, Chaiworapongsa T, Hassan SS, Tarca AL (2017) The prediction of late-onset preeclampsia: results from a longitudinal proteomics study. PLoS One 12:e0181468. https://doi.org/10.1371/journal.pone.0181468
Eskild A, Romundstad PR, Vatten LJ (2009) Placental weight and birthweight: does the association differ between pregnancies with and without preeclampsia? Am J Obstet Gynecol 201:595.e1–595.e5. https://doi.org/10.1016/j.ajog.2009.06.003
Everett TR, Lees CC (2012) Beyond the placental bed: placental and systemic determinants of the uterine artery Doppler waveform. Placenta 33:893–901. https://doi.org/10.1016/j.placenta.2012.07.011
Farzi F, Mehrafza M, Mirmansouri A, Oudi M, Hoseeini A (2005) Administration of NTG before embryo transfer does not increase pregnancy rate. IJRM 3:95–100
Feliers D, Chen X, Akis N, Choudhury GG, Madaio M, Kasinath BS (2005) VEGF regulation of endothelial nitric oxide synthase in glomerular endothelial cells. Kidney Int 68:1648–1659. https://doi.org/10.1111/j.1523-1755.2005.00575.x
Fickling SA, Williams D, Vallance P, Nussey SS, Whitley GS (1993) Plasma concentrations of endogenous inhibitor of nitric oxide synthesis in normal pregnancy and pre-eclampsia. Lancet Lond Engl 342:242–243. https://doi.org/10.1016/0140-6736(93)92335-q
Fisher SJ (2015) Why is placentation abnormal in preeclampsia? Am J Obstet Gynecol 213:S115–S122. https://doi.org/10.1016/j.ajog.2015.08.042
Flora Filho R, Zilberstein B (2000) [Nitric oxide: the simple messenger passing through complexity. Metabolism, synthesis and functions]. Rev Assoc Medica Bras 1992 46:265–271. https://doi.org/10.1590/s0104-42302000000300012
Fu Q (2018) Hemodynamic and electrocardiographic aspects of uncomplicated singleton pregnancy. Adv Exp Med Biol 1065:413–431. https://doi.org/10.1007/978-3-319-77932-4_26
Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376. https://doi.org/10.1038/288373a0
Garcia-Gonzalez C, Abdel-Azim S, Galeva S, Georgiopoulos G, Nicolaides KH, Charakida M (2020) Placental function and fetal weight are associated with maternal hemodynamic indices in uncomplicated pregnancies at 35-37 weeks of gestation. Am J Obstet Gynecol 222:604.e1–604.e10. https://doi.org/10.1016/j.ajog.2020.01.011
Garcia-Ruíz G, Flores-Espinosa P, Preciado-Martínez E, Bermejo-Martínez L, Espejel-Nuñez A, Estrada-Gutierrez G, Maida-Claros R, Flores-Pliego A, Zaga-Clavellina V (2015) In vitro progesterone modulation on bacterial endotoxin-induced production of IL-1β, TNFα, IL-6, IL-8, IL-10, MIP-1α, and MMP-9 in pre-labor human term placenta. Reprod Biol Endocrinol 13:115. https://doi.org/10.1186/s12958-015-0111-3
George EM, Palei AC, Dent EA, Granger JP (2013) Sildenafil attenuates placental ischemia-induced hypertension. Am J Physiol Regul Integr Comp Physiol 305:R397–R403. https://doi.org/10.1152/ajpregu.00216.2013
Ghabour MS, Eis ALW, Brockman DE, Pollock JS, Myatt L (1995) Immunohistochemical characterization of placental nitric oxide synthase expression in preeclampsia. Am J Obstet Gynecol 173:687–694. https://doi.org/10.1016/0002-9378(95)90324-0
Ghulmiyyah L, Sibai B (2012) Maternal mortality from preeclampsia/eclampsia. Semin Perinatol 36:56–59. https://doi.org/10.1053/j.semperi.2011.09.011
Gonçalves-Rizzi VH, Possomato-Vieira JS, Sales Graça TU, Nascimento RA, Dias-Junior CA (2016) Sodium nitrite attenuates hypertension-in-pregnancy and blunts increases in soluble fms-like tyrosine kinase-1 and in vascular endothelial growth factor. Nitric Oxide Biol Chem 57:71–78. https://doi.org/10.1016/j.niox.2016.05.004
Gonçalves-Rizzi VH, Possomato-Vieira JS, Nascimento RA, Caldeira-Dias M, Dias-Junior CA (2018) Maternal hypertension and feto-placental growth restriction is reversed by sildenafil: evidence of independent effects of circulating nitric oxide levels. Eur J Pharmacol 822:119–127. https://doi.org/10.1016/j.ejphar.2018.01.010
Goulopoulou S, Hannan JL, Matsumoto T, Webb RC (2012) Pregnancy reduces RhoA/Rho kinase and protein kinase C signaling pathways downstream of thromboxane receptor activation in the rat uterine artery. Am J Physiol Heart Circ Physiol 302:H2477–H2488. https://doi.org/10.1152/ajpheart.00900.2011
Grandvuillemin I, Buffat C, Boubred F, Lamy E, Fromonot J, Charpiot P, Simoncini S, Sabatier F, Dignat-George F, Peyter A-C, Simeoni U, Yzydorczyk C (2018) Arginase upregulation and eNOS uncoupling contribute to impaired endothelium-dependent vasodilation in a rat model of intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 315:R509–R520. https://doi.org/10.1152/ajpregu.00354.2017
Groten T, Lehmann T, Schleußner E, PETN Study Group (2019) Does Pentaerytrithyltetranitrate reduce fetal growth restriction in pregnancies complicated by uterine mal-perfusion? Study protocol of the PETN-study: a randomized controlled multicenter-trial. BMC Pregnancy Childbirth 19:336. https://doi.org/10.1186/s12884-019-2456-7
Guedes-Martins L (2017) Superimposed preeclampsia. Adv Exp Med Biol 956:409–417. https://doi.org/10.1007/5584_2016_82
Guerby P, Swiader A, Augé N, Parant O, Vayssière C, Uchida K, Salvayre R, Negre-Salvayre A (2019a) High glutathionylation of placental endothelial nitric oxide synthase in preeclampsia. Redox Biol 22:101126. https://doi.org/10.1016/j.redox.2019.101126
Guerby P, Swiader A, Tasta O, Pont F, Rodriguez F, Parant O, Vayssière C, Shibata T, Uchida K, Salvayre R, Negre-Salvayre A (2019b) Modification of endothelial nitric oxide synthase by 4-oxo-2(E)-nonenal(ONE) in preeclamptic placentas. Free Radic Biol Med 141:416–425. https://doi.org/10.1016/j.freeradbiomed.2019.07.015
Hall ME, George EM, Granger JP (2011) [The heart during pregnancy]. Rev Esp Cardiol 64:1045–1050. https://doi.org/10.1016/j.recesp.2011.07.009
Haukkamaa L, Moilanen L, Kattainen A, Luoto R, Kahonen M, Leinonen M, Jula A, Kesäniemi YA, Kaaja R (2009) Pre-eclampsia is a risk factor of carotid artery atherosclerosis. Cerebrovasc Dis Basel Switz 27:599–607. https://doi.org/10.1159/000216834
Heiss EH, Dirsch VM (2014) Regulation of eNOS enzyme activity by posttranslational modification. Curr Pharm Des 20:3503–3513. https://doi.org/10.2174/13816128113196660745
Homer CSE, Brown MA, Mangos G, Davis GK (2008) Non-proteinuric pre-eclampsia: a novel risk indicator in women with gestational hypertension. J Hypertens 26:295–302. https://doi.org/10.1097/HJH.0b013e3282f1a953
Huynh J, Dawson D, Roberts D, Bentley-Lewis R (2015) A systematic review of placental pathology in maternal diabetes mellitus. Placenta 36:101–114. https://doi.org/10.1016/j.placenta.2014.11.021
Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists’ Task Force on Hypertension in Pregnancy (2013) Obstet Gynecol 122:1122–1131. https://doi.org/10.1097/01.AOG.0000437382.03963.88
John L, Ko NL, Gokin A, Gokina N, Mandalà M, Osol G (2018) The Piezo1 cation channel mediates uterine artery shear stress mechanotransduction and vasodilation during rat pregnancy. Am J Physiol Heart Circ Physiol 315:H1019–H1026. https://doi.org/10.1152/ajpheart.00103.2018
Joyce JM, Phernetton TM, Magness RR (2002) Effect of uterine blood flow occlusion on shear stress-mediated nitric oxide production and endothelial nitric oxide synthase expression during ovine pregnancy. Biol Reprod 67:320–326. https://doi.org/10.1095/biolreprod67.1.320
Kalyanaraman B (2013) Teaching the basics of redox biology to medical and graduate students: oxidants, antioxidants and disease mechanisms. Redox Biol 1:244–257. https://doi.org/10.1016/j.redox.2013.01.014
Kao CK, Morton JS, Quon AL, Reyes LM, Lopez-Jaramillo P, Davidge ST (2016) Mechanism of vascular dysfunction due to circulating factors in women with pre-eclampsia. Clin Sci Lond Engl 1979(130):539–549. https://doi.org/10.1042/CS20150678
Kenneth L, Hall DR, Gebhardt S, Grové D (2010) Late onset preeclampsia is not an innocuous condition. Hypertens Pregnancy 29:262–270. https://doi.org/10.3109/10641950902777697
Khairy M, Dhillon RK, Chu J, Rajkhowa M, Coomarasamy A (2016) The effect of peri-implantation administration of uterine relaxing agents in assisted reproduction treatment cycles: a systematic review and meta-analysis. Reprod Biomed Online 32:362–376. https://doi.org/10.1016/j.rbmo.2016.01.004
Khan F, Belch JJF, MacLeod M, Mires G (2005) Changes in endothelial function precede the clinical disease in women in whom preeclampsia develops. Hypertension (Dallas TX) 1979(46):1123–1128. https://doi.org/10.1161/01.HYP.0000186328.90667.95
Kim YJ, Park HS, Lee HY, Ha EH, Suh SH, Oh SK, Yoo H-S (2006) Reduced L-arginine level and decreased placental eNOS activity in preeclampsia. Placenta 27:438–444. https://doi.org/10.1016/j.placenta.2005.04.011
Ko NL, Mandalà M, John L, Gelinne A, Osol G (2018) Venoarterial communication mediates arterial wall shear stress-induced maternal uterine vascular remodeling during pregnancy. Am J Physiol Heart Circ Physiol 315:H709–H717. https://doi.org/10.1152/ajpheart.00126.2018
Kossenjans W, Eis A, Sahay R, Brockman D, Myatt L (2000) Role of peroxynitrite in altered fetal-placental vascular reactivity in diabetes or preeclampsia. Am J Physiol Heart Circ Physiol 278:H1311–H1319. https://doi.org/10.1152/ajpheart.2000.278.4.H1311
Krause BJ, Hanson MA, Casanello P (2011) Role of nitric oxide in placental vascular development and function. Placenta 32:797–805. https://doi.org/10.1016/j.placenta.2011.06.025
Kukor Z, Valent S, Tóth M (2000) Regulation of nitric oxide synthase activity by tetrahydrobiopterin in human placentae from normal and pre-eclamptic pregnancies. Placenta 21:763–772. https://doi.org/10.1053/plac.2000.0584
Kulandavelu S, Whiteley KJ, Qu D, Mu J, Bainbridge SA, Adamson SL (2012) Endothelial nitric oxide synthase deficiency reduces uterine blood flow, spiral artery elongation, and placental oxygenation in pregnant mice. Hypertension (Dallas TX) 1979(60):231–238. https://doi.org/10.1161/HYPERTENSIONAHA.111.187559
Kumar S, Gordon GH, Abbott DH, Mishra JS (2018) Androgens in maternal vascular and placental function: implications for preeclampsia pathogenesis. Reproduction Camb Engl 156:R155–R167. https://doi.org/10.1530/REP-18-0278
Kusinski LC, Stanley JL, Dilworth MR, Hirt CJ, Andersson IJ, Renshall LJ, Baker BC, Baker PN, Sibley CP, Wareing M, Glazier JD (2012) eNOS knockout mouse as a model of fetal growth restriction with an impaired uterine artery function and placental transport phenotype. Am J Physiol Regul Integr Comp Physiol 303:R86–R93. https://doi.org/10.1152/ajpregu.00600.2011
Lain KY, Catalano PM (2007) Metabolic changes in pregnancy. Clin Obstet Gynecol 50:938–948. https://doi.org/10.1097/GRF.0b013e31815a5494
Landeros RV, Pastore MB, Magness RR (2019) Effects of the catechol and methoxy metabolites of 17β-Estradiol on nitric oxide production by ovine uterine artery endothelial cells. Reprod Sci Thousand Oaks Calif 26:459–468. https://doi.org/10.1177/1933719118783265
Lappas M, Mitton A, Mittion A, Permezel M (2010) In response to oxidative stress, the expression of inflammatory cytokines and antioxidant enzymes are impaired in placenta, but not adipose tissue, of women with gestational diabetes. J Endocrinol 204:75–84. https://doi.org/10.1677/JOE-09-0321
Lazdam M, de la Horra A, Diesch J, Kenworthy Y, Davis E, Lewandowski AJ, Szmigielski C, Shore A, Mackillop L, Kharbanda R, Alp N, Redman C, Kelly B, Leeson P (2012) Unique blood pressure characteristics in mother and offspring after early onset preeclampsia. Hypertension (Dallas TX) 1979(60):1338–1345. https://doi.org/10.1161/HYPERTENSIONAHA.112.198366
Leeman L, Dresang LT, Fontaine P (2016) Hypertensive disorders of pregnancy. Am Fam Physician 93:121–127
Li J, Umar S, Amjedi M, Iorga A, Sharma S, Nadadur RD, Regitz-Zagrosek V, Eghbali M (2012) New frontiers in heart hypertrophy during pregnancy. Am J Cardiovasc Dis 2:192–207
Lindheimer MD, Taler SJ, Cunningham FG (2010) Hypertension in pregnancy. J Am Soc Hypertens 4:68–78. https://doi.org/10.1016/j.jash.2010.03.002
LoMauro A, Aliverti A (2015) Respiratory physiology of pregnancy: physiology masterclass. Breathe Sheff Engl 11:297–301. https://doi.org/10.1183/20734735.008615
Lorca RA, Lane SL, Bales ES, Nsier H, Yi H, Donnelly MA, Euser AG, Julian CG, Moore LG (2019) High altitude reduces NO-dependent myometrial artery vasodilator response during pregnancy. Hypertension (Dallas TX) 1979(73):1319–1326. https://doi.org/10.1161/HYPERTENSIONAHA.119.12641
Lu J, Wang Z, Cao J, Chen Y, Dong Y (2018) A novel and compact review on the role of oxidative stress in female reproduction. Reprod Biol Endocrinol 16:80. https://doi.org/10.1186/s12958-018-0391-5
Luo J-Y, Fu D, Wu Y-Q, Gao Y (2016) Inhibition of the JAK2/STAT3/SOSC1 signaling pathway improves secretion function of vascular endothelial cells in a rat model of pregnancy-induced hypertension. Cell Phy-siol Biochem Int J Exp Cell Physiol Biochem Pharmacol 40:527–537. https://doi.org/10.1159/000452566
Maltepe E, Fisher SJ (2015) Placenta: the forgotten organ. Annu Rev Cell Dev Biol 31:523–552. https://doi.org/10.1146/annurev-cellbio-100814-125620
Mannaerts D, Faes E, Cornette J, Gyselaers W, Spaanderman M, Goovaerts I, Stoop T, Roelant E, Jacquemyn Y, Van Craenenbroeck EM (2019) Low-flow mediated constriction as a marker of endothelial function in healthy pregnancy and preeclampsia: a pilot study. Pregnancy Hypertens 17:75–81. https://doi.org/10.1016/j.preghy.2019.02.001
Mara Suburo A, Chaud M, Franchi A, Polak JM, Gimeno MA (1995) Distribution of neuronal and non-neuronal NADPH diaphorases and nitric oxide synthases in rat uterine horns under different hormonal conditions. Biol Reprod 52:631–637. https://doi.org/10.1095/biolreprod52.3.631
Marinoni E, Di Iorio R, Lucchini C, Di Netta T, Letizia C, Cosmi EV (2004) Adrenomedullin and nitric oxide synthase at the maternal-decidual interface in early spontaneous abortion. J Reprod Med 49:153–161
Marshall SA, Hannan NJ, Jelinic M, Nguyen TPH, Girling JE, Parry LJ (2018) Animal models of preeclampsia: translational failings and why. Am J Physiol Regul Integr Comp Physiol 314:R499–R508. https://doi.org/10.1152/ajpregu.00355.2017
Mashini IS, Albazzaz SJ, Fadel HE, Abdulla AM, Hadi HA, Harp R, Devoe LD (1987) Serial noninvasive evaluation of cardiovascular hemodynamics during pregnancy. Am J Obstet Gynecol 156:1208–1213. https://doi.org/10.1016/0002-9378(87)90146-3
Matsubara K, Matsubara Y, Hyodo S, Katayama T, Ito M (2010) Role of nitric oxide and reactive oxygen species in the pathogenesis of preeclampsia. J Obstet Gynaecol Res 36:239–247. https://doi.org/10.1111/j.1447-0756.2009.01128.x
Maul H, Longo M, Saade GR, Garfield RE (2003) Nitric oxide and its role during pregnancy: from ovulation to delivery. Curr Pharm Des 9:359–380. https://doi.org/10.2174/1381612033391784
Maynard SE, Min J-Y, Merchan J, Lim K-H, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111:649–658. https://doi.org/10.1172/JCI17189
Mazzanti L, Cecati M, Vignini A, D’Eusanio S, Emanuelli M, Giannubilo SR, Saccucci F, Tranquilli AL (2011) Placental expression of endothelial and inducible nitric oxide synthase and nitric oxide levels in patients with HELLP syndrome. Am J Obstet Gynecol 205:236.e1–236.e7. https://doi.org/10.1016/j.ajog.2011.04.022
Mazzuca MQ, Li W, Reslan OM, Yu P, Mata KM, Khalil RA (2014) Downregulation of microvascular endothelial type B endothelin receptor is a central vascular mechanism in hypertensive pregnancy. Hypertension (Dallas TX) 1979(64):632–643. https://doi.org/10.1161/HYPERTENSIONAHA.114.03315
McLaughlin K, Audette MC, Parker JD, Kingdom JC (2018) Mechanisms and clinical significance of endothelial dysfunction in high-risk pregnancies. Can J Cardiol 34:371–380. https://doi.org/10.1016/j.cjca.2018.01.006
McMaster MT, Zhou Y, Fisher SJ (2004) Abnormal placentation and the syndrome of preeclampsia. Semin Nephrol 24:540–547. https://doi.org/10.1016/s0270-9295(04)00124-x
Milstien S, Katusic Z (1999) Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function. Biochem Biophys Res Commun 263:681–684. https://doi.org/10.1006/bbrc.1999.1422
Mitchell BM, Cook LG, Danchuk S, Puschett JB (2007) Uncoupled endothelial nitric oxide synthase and oxidative stress in a rat model of pregnancy-induced hypertension. Am J Hypertens 20:1297–1304. https://doi.org/10.1016/j.amjhyper.2007.08.007
Mohaupt M (2007) Molecular aspects of preeclampsia. Mol Asp Med 28:169–191. https://doi.org/10.1016/j.mam.2007.02.005
Mol BWJ, Roberts CT, Thangaratinam S, Magee LA, de Groot CJM, Hofmeyr GJ (2016) Pre-eclampsia. Lancet Lond Engl 387:999–1011. https://doi.org/10.1016/S0140-6736(15)00070-7
Morton JS, Care AS, Davidge ST (2017) Mechanisms of uterine artery dysfunction in pregnancy complications. J Cardiovasc Pharmacol 69:343–359. https://doi.org/10.1097/FJC.0000000000000468
Motamer M, Haghjooy Javanmard S, Mortazavi ZS, Bahrani S (2019) Evaluation the effect of testosterone on the number of endothelial progenitor cells and amount of SDF-1α, PDGF, bFGF, and NO. Int J Prev Med 10:214. https://doi.org/10.4103/ijpvm.IJPVM_79_18
Motta C, Grosso C, Zanuzzi C, Molinero D, Picco N, Bellingeri R, Alustiza F, Barbeito C, Vivas A, Romanini MC (2015) Effect of sildenafil on pre-eclampsia-like mouse model induced by L-name. Reprod Domest Anim Zuchthyg 50:611–616. https://doi.org/10.1111/rda.12536
Motta-Mejia C, Kandzija N, Zhang W, Mhlomi V, Cerdeira AS, Burdujan A, Tannetta D, Dragovic R, Sargent IL, Redman CW, Kishore U, Vatish M (2017) Placental vesicles carry active endothelial nitric oxide synthase and their activity is reduced in preeclampsia. Hypertension (Dallas TX) 1979(70):372–381. https://doi.org/10.1161/HYPERTENSIONAHA.117.09321
Murad F (1994) Regulation of cytosolic guanylyl cyclase by nitric oxide: the NO-cyclic GMP signal transduction system. Adv Pharmacol San Diego Calif 26:19–33. https://doi.org/10.1016/s1054-3589(08)60049-6
Mutinati M, Piccinno M, Roncetti M, Campanile D, Rizzo A, Sciorsci R (2013) Oxidative stress during pregnancy in the sheep. Reprod Domest Anim Zuchthyg 48:353–357. https://doi.org/10.1111/rda.12141
Myatt L, Webster RP (2009) Vascular biology of preeclampsia. J Thromb Haemost 7:375–384. https://doi.org/10.1111/j.1538-7836.2008.03259.x
Myatt L, Rosenfield RB, Eis AL, Brockman DE, Greer I, Lyall F (1996) Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension (Dallas TX) 1979 28:488–493. https://doi.org/10.1161/01.hyp.28.3.488
Myatt L, Eis AL, Brockman DE, Kossenjans W, Greer I, Lyall F (1997) Inducible (type II) nitric oxide synthase in human placental villous tissue of normotensive, pre-eclamptic and intrauterine growth-restricted pregnancies. Placenta 18:261–268. https://doi.org/10.1016/s0143-4004(97)80060-4
Myers J, Mires G, Macleod M, Baker P (2005) In preeclampsia, the circulating factors capable of altering in vitro endothelial function precede clinical disease. Hypertension (Dallas TX) 1979(45):258–263. https://doi.org/10.1161/01.HYP.0000153461.58298.a4
Nakatsuka M, Takata M, Tada K, Asagiri K, Habara T, Noguchi S, Kudo T (2002) A long-term transdermal nitric oxide donor improves uteroplacental circulation in women with preeclampsia. J. Ultrasound Med 21:831–836. https://doi.org/10.7863/jum.2002.21.8.831
Napso T, Yong HEJ, Lopez-Tello J, Sferruzzi-Perri AN (2018) The role of placental hormones in mediating maternal adaptations to support pregnancy and lactation. Front Physiol 9:1091. https://doi.org/10.3389/fphys.2018.01091
Nascimento RA, Possomato-Vieira JS, Gonçalves-Rizzi VH, Bonacio GF, Rizzi E, Dias-Junior CA (2018) Hypertension, augmented activity of matrix metalloproteinases-2 and -9 and angiogenic imbalance in hypertensive pregnancy are attenuated by doxycycline. Eur J Pharmacol 840:60–69. https://doi.org/10.1016/j.ejphar.2018.10.017
Nascimento RA, Possomato-Vieira JS, Bonacio GF, Rizzi E, Dias-Junior CA (2019) Reductions of circulating nitric oxide are followed by hypertension during pregnancy and increased activity of matrix metalloproteinases-2 and -9 in rats. Cell 8:E1402. https://doi.org/10.3390/cells8111402
Nelson SH, Steinsland OS, Suresh MS, Lee NM (1998) Pregnancy augments nitric oxide-dependent dilator response to acetylcholine in the human uterine artery. Hum Reprod Oxf Engl 13:1361–1367. https://doi.org/10.1093/humrep/13.5.1361
Nelson SH, Steinsland OS, Wang Y, Yallampalli C, Dong YL, Sanchez JM (2000) Increased nitric oxide synthase activity and expression in the human uterine artery during pregnancy. Circ Res 87:406–411. https://doi.org/10.1161/01.res.87.5.406
Nishizawa H, Pryor-Koishi K, Suzuki M, Kato T, Sekiya T, Tada S, Kurahashi H, Udagawa Y (2009) Analysis of nitric oxide metabolism as a placental or maternal factor underlying the etiology of pre-eclampsia. Gynecol Obstet Investig 68:239–247. https://doi.org/10.1159/000238381
Norman JE, Cameron IT (1996) Nitric oxide in the human uterus. Rev Reprod 1:61–68. https://doi.org/10.1530/ror.0.0010061
Ohl J, Lefèbvre-Maunoury C, Wittemer C, Nisand G, Laurent M-C, Hoffmann P (2002) Nitric oxide donors for patients undergoing IVF. A prospective, double-blind, randomized, placebo-controlled trial. Hum Reprod Oxf Engl 17:2615–2620. https://doi.org/10.1093/humrep/17.10.2615
Ornaghi S, Paidas MJ (2017) Novel therapy for the treatment of early-onset preeclampsia. Clin Obstet Gynecol 60:169–182. https://doi.org/10.1097/GRF.0000000000000249
Orshal JM, Khalil RA (2004) Reduced endothelial NO-cGMP-mediated vascular relaxation and hypertension in IL-6-infused pregnant rats. Hypertension (Dallas TX) 1979(43):434–444. https://doi.org/10.1161/01.HYP.0000113044.46326.98
Osol G, Mandala M (2009) Maternal uterine vascular remodeling during pregnancy. Physiol Bethesda Md 24:58–71. https://doi.org/10.1152/physiol.00033.2008
Osol G, Ko NL, Mandalà M (2017) Altered endothelial nitric oxide Signaling as a paradigm for maternal vascular maladaptation in preeclampsia. Curr Hypertens Rep 19:82. https://doi.org/10.1007/s11906-017-0774-6
Osol G, Ko NL, Mandalà M (2019) Plasticity of the maternal vasculature during pregnancy. Annu Rev Physiol 81:89–111. https://doi.org/10.1146/annurev-physiol-020518-114435
Ota H, Igarashi S, Hatazawa J, Tanaka T (1998) Endothelial nitric oxide synthase in the endometrium during the menstrual cycle in patients with endometriosis and adenomyosis. Fertil Steril 69:303–308. https://doi.org/10.1016/s0015-0282(97)00478-0
Pánczél Z, Kukor Z, Supák D, Kovács B, Kecskeméti A, Czizel R, Djurecz M, Alasztics B, Csomó KB, Hrabák A, Valent S (2019) Pravastatin induces NO synthesis by enhancing microsomal arginine uptake in healthy and preeclamptic placentas. BMC Pregnancy Childbirth 19:426. https://doi.org/10.1186/s12884-019-2507-0
Pang Y, Thomas P (2017) Additive effects of low concentrations of estradiol-17β and progesterone on nitric oxide production by human vascular endothelial cells through shared signaling pathways. J Steroid Biochem Mol Biol 165:258–267. https://doi.org/10.1016/j.jsbmb.2016.06.014
Pang Y, Thomas P (2018) Progesterone induces relaxation of human umbilical cord vascular smooth muscle cells through mPRα (PAQR7). Mol Cell Endocrinol 474:20–34. https://doi.org/10.1016/j.mce.2018.02.003
Papapetropoulos A, García-Cardeña G, Madri JA, Sessa WC (1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 100:3131–3139. https://doi.org/10.1172/JCI119868
Pimentel AML, Pereira NR, Costa CA, Mann GE, Cordeiro VSC, de Moura RS, Brunini TMC, Mendes-Ribeiro AC, Resende AC (2013) L-arginine-nitric oxide pathway and oxidative stress in plasma and platelets of patients with pre-eclampsia. Hypertens Res 36:783–788. https://doi.org/10.1038/hr.2013.34
Pinheiro TV, Brunetto S, Ramos JGL, Bernardi JR, Goldani MZ (2016) Hypertensive disorders during pregnancy and health outcomes in the offspring: a systematic review. J Dev Orig Health Dis 7:391–407. https://doi.org/10.1017/S2040174416000209
Ponmozhi G, Keepanasseril A, Mathaiyan J, Manikandan K (2019) Nitric oxide in the prevention of pre-eclampsia (NOPE): a double-blind randomized placebo-controlled trial assessing the efficacy of isosorbide mononitrate in the prevention of pre-eclampsia in high-risk women. J Obstet Gynaecol India 69:103–110. https://doi.org/10.1007/s13224-018-1100-1
Poppas A, Shroff SG, Korcarz CE, Hibbard JU, Berger DS, Lindheimer MD, Lang RM (1997) Serial assessment of the cardiovascular system in normal pregnancy. Role of arterial compliance and pulsatile arterial load. Circulation 95:2407–2415. https://doi.org/10.1161/01.cir.95.10.2407
Possomato-Vieira JS, Khalil RA (2016) Mechanisms of endothelial dysfunction in hypertensive pregnancy and preeclampsia. Adv Pharmacol San Diego Calif 77:361–431. https://doi.org/10.1016/bs.apha.2016.04.008
Possomato-Vieira JS, Chimini JS, da Silva MLS, Dias-Junior CA (2018) Increases in placental nitric oxide, but not nitric oxide-mediated relaxation, underlie the improvement in placental efficiency and antihypertensive effects of hydrogen sulphide donor in hypertensive pregnancy. Clin Exp Pharmacol Physiol 45:1118–1127. https://doi.org/10.1111/1440-1681.13000
Pulgar VM, Yamaleyeva LM, Varagic J, McGee C, Bader M, Dechend R, Brosnihan KB (2015) Functional changes in the uterine artery precede the hypertensive phenotype in a transgenic model of hypertensive pregnancy. Am J Physiol Endocrinol Metab 309:E811–E817. https://doi.org/10.1152/ajpendo.00526.2014
Purcell TL, Given R, Chwalisz K, Garfield RE (1999) Nitric oxide synthase distribution during implantation in the mouse. Mol Hum Reprod 5:467–475. https://doi.org/10.1093/molehr/5.5.467
Púzserová A, Kopincová J, Bernátová I (2008) [The role of endothelium and nitric oxide in the regulation of vascular tone]. Cesk Fysiol 57:53–60
Ramesar SV, Mackraj I, Gathiram P, Moodley J (2010) Sildenafil citrate improves fetal outcomes in pregnant, L-NAME treated, Sprague-Dawley rats. Eur J Obstet Gynecol Reprod Biol 149:22–26. https://doi.org/10.1016/j.ejogrb.2009.11.005
Raymond D, Peterson E (2011) A critical review of early-onset and late-onset preeclampsia. Obstet Gynecol Surv 66:497–506. https://doi.org/10.1097/OGX.0b013e3182331028
Redman CW (1991) Current topic: pre-eclampsia and the placenta. Placenta 12:301–308. https://doi.org/10.1016/0143-4004(91)90339-h
Rennie MY, Whiteley KJ, Adamson SL, Sled JG (2016) Quantification of gestational changes in the uteroplacental vascular tree reveals vessel specific hemodynamic roles during pregnancy in mice. Biol Reprod 95:43. https://doi.org/10.1095/biolreprod.116.140681
Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy (2000) Am J Obstet Gynecol 183:S1–S22
Roberts RP, Refuerzo JS, Ferrari F, Ontiveros AE, Tamayo EH, Sibai BM, Blackwell SC, Longo M (2016) Sildenafil treatment in a nonsevere hypertensive murine model lowers blood pressure without reducing fetal growth. Am J Obstet Gynecol 215:386.e1–386.e8. https://doi.org/10.1016/j.ajog.2016.05.002
Rocha-Penha L, Caldeira-Dias M, Tanus-Santos JE, de Carvalho Cavalli R, Sandrim VC (2017) Myeloperoxidase in hypertensive disorders of pregnancy and its relation with nitric oxide. Hypertension (Dallas TX) 1979(69):1173–1180. https://doi.org/10.1161/HYPERTENSIONAHA.116.08854
Roggensack AM, Zhang Y, Davidge ST (1999) Evidence for peroxynitrite formation in the vasculature of women with preeclampsia. Hypertension (Dallas TX) 1979(33):83–89. https://doi.org/10.1161/01.hyp.33.1.83
Rosenfeld CR, Roy T (2014) Prolonged uterine artery nitric oxide synthase inhibition modestly alters basal uteroplacental vasodilation in the last third of ovine pregnancy. Am J Physiol Heart Circ Physiol 307:H1196–H1203. https://doi.org/10.1152/ajpheart.00996.2013
Rosselli M, Imthurn B, Macas E, Keller PJ, Dubey RK (1994) Endogenous nitric oxide modulates endothelin-1 induced contraction of bovine oviduct. Biochem Biophys Res Commun 201:143–148. https://doi.org/10.1006/bbrc.1994.1680
Rosselli M, Keller PJ, Dubey RK (1998) Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum Reprod Update 4:3–24. https://doi.org/10.1093/humupd/4.1.3
Rossmanith WG, Hoffmeister U, Wolfahrt S, Kleine B, McLean M, Jacobs RA, Grossman AB (1999) Expression and functional analysis of endothelial nitric oxide synthase (eNOS) in human placenta. Mol Hum Reprod 5:487–494. https://doi.org/10.1093/molehr/5.5.487
Rytlewski K, Olszanecki R, Korbut R, Zdebski Z (2005) Effects of prolonged oral supplementation with l-arginine on blood pressure and nitric oxide synthesis in preeclampsia. Eur J Clin Investig 35:32–37. https://doi.org/10.1111/j.1365-2362.2005.01445.x
Sánchez-Aranguren LC, Prada CE, Riaño-Medina CE, Lopez M (2014) Endothelial dysfunction and preeclampsia: role of oxidative stress. Front Physiol 5:372. https://doi.org/10.3389/fphys.2014.00372
Sankaralingam S, Xu H, Davidge ST (2010) Arginase contributes to endothelial cell oxidative stress in response to plasma from women with preeclampsia. Cardiovasc Res 85:194–203. https://doi.org/10.1093/cvr/cvp277
Santiago-Font JA, Amaral LM, Faulkner J, Ibrahim T, Vaka VR, Cunningham MW, LaMarca B (2016) Serelaxin improves the pathophysiology of placental ischemia in the reduced uterine perfusion pressure rat model of preeclampsia. Am J Physiol Regul Integr Comp Physiol 311:R1158–R1163. https://doi.org/10.1152/ajpregu.00192.2016
Schiessl B, Mylonas I, Hantschmann P, Kuhn C, Schulze S, Kunze S, Friese K, Jeschke U (2005) Expression of endothelial NO synthase, inducible NO synthase, and estrogen receptors alpha and beta in placental tissue of normal, preeclamptic, and intrauterine growth-restricted pregnancies. J Histochem Cytochem 53:1441–1449. https://doi.org/10.1369/jhc.4A6480.2005
Schleussner E, Lehmann T, Kähler C, Schneider U, Schlembach D, Groten T (2014) Impact of the nitric oxide-donor pentaerythrityl-tetranitrate on perinatal outcome in risk pregnancies: a prospective, randomized, double-blinded trial. J Perinat Med 42:507–514. https://doi.org/10.1515/jpm-2013-0212
Schmidt HH, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F (1992) Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40:1439–1456. https://doi.org/10.1177/40.10.1382087
Schoolcraft WB, Surrey ES, Gardner DK (2001) Embryo transfer: techniques and variables affecting success. Fertil Steril 76:863–870. https://doi.org/10.1016/s0015-0282(01)02731-5
Seely EW, Ecker J (2011) Clinical practice. Chronic hypertension in pregnancy. N Engl J Med 365:439–446. https://doi.org/10.1056/NEJMcp0804872
Seely EW, Ecker J (2014) Chronic hypertension in pregnancy. Circulation 129:1254–1261. https://doi.org/10.1161/CIRCULATIONAHA.113.003904
Shaheen G, Jahan S, Ul Ain Q, Ullah A, Afsar T, Almajwal A, Alam I, Razak S (2020) Placental endothelial nitric oxide synthase expression and role of oxidative stress in susceptibility to preeclampsia in Pakistani women. Mol Genet Genomic Med 8:e1191. https://doi.org/10.1002/mgg3.1191
Shao R, Zhang SX, Weijdegård B, Zou S, Egecioglu E, Norström A, Brännström M, Billig H (2010) Nitric oxide synthases and tubal ectopic pregnancies induced by chlamydia infection: basic and clinical insights. Mol Hum Reprod 16:907–915. https://doi.org/10.1093/molehr/gaq063
Sharp A, Cornforth C, Jackson R, Harrold J, Turner MA, Kenny LC, Baker PN, Johnstone ED, Khalil A, von Dadelszen P, Papageorghiou AT, Alfirevic Z, STRIDER group (2018) Maternal sildenafil for severe fetal growth restriction (STRIDER): a multicentre, randomised, placebo-controlled, double-blind trial. Lancet Child Adolesc Health 2:93–102. https://doi.org/10.1016/S2352-4642(17)30173-6
Shen M, Tan H, Zhou S, Smith GN, Walker MC, Wen SW (2017) Trajectory of blood pressure change during pregnancy and the role of pre-gravid blood pressure: a functional data analysis approach. Sci Rep 7:6227. https://doi.org/10.1038/s41598-017-06606-0
Shu W, Li H, Gong H, Zhang M, Niu X, Ma Y, Zhang X, Cai W, Yang G, Wei M, Yang N, Li Y (2018) Evaluation of blood vessel injury, oxidative stress and circulating inflammatory factors in an L-NAME-induced preeclampsia-like rat model. Exp Ther Med 16:585–594. https://doi.org/10.3892/etm.2018.6217
Sibai BM (2002) Chronic hypertension in pregnancy. Obstet Gynecol 100:369–377. https://doi.org/10.1016/s0029-7844(02)02128-2
Soares MJ, Chakraborty D, Karim Rumi MA, Konno T, Renaud SJ (2012) Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta 33:233–243. https://doi.org/10.1016/j.placenta.2011.11.026
Soares MJ, Chakraborty D, Kubota K, Renaud SJ, Rumi MAK (2014) Adaptive mechanisms controlling uterine spiral artery remodeling during the establishment of pregnancy. Int J Dev Biol 58:247–259. https://doi.org/10.1387/ijdb.140083ms
Soobryan N, Murugesan S, Phoswa W, Gathiram P, Moodley J, Mackraj I (2017) The effects of sildenafil citrate on uterine angiogenic status and serum inflammatory markers in an L-NAME rat model of pre-eclampsia. Eur J Pharmacol 795:101–107. https://doi.org/10.1016/j.ejphar.2016.12.010
Staley JR, Bradley J, Silverwood RJ, Howe LD, Tilling K, Lawlor DA, Macdonald-Wallis C (2015) Associations of blood pressure in pregnancy with offspring blood pressure trajectories during childhood and adolescence: findings from a prospective study. J Am Heart Assoc 4:e001422. https://doi.org/10.1161/JAHA.114.001422
Stanley JL, Andersson IJ, Poudel R, Rueda-Clausen CF, Sibley CP, Davidge ST, Baker PN (2012) Sildenafil citrate rescues fetal growth in the catechol-O-methyl transferase knockout mouse model. Hypertension (Dallas TX) 1979(59):1021–1028. https://doi.org/10.1161/HYPERTENSIONAHA.111.186270
Stergiotou I, Crispi F, Valenzuela-Alcaraz B, Bijnens B, Gratacos E (2013) Patterns of maternal vascular remodeling and responsiveness in early- versus late-onset preeclampsia. Am J Obstet Gynecol 209:558.e1–558.e14. https://doi.org/10.1016/j.ajog.2013.07.030
Stuart JJ, Tanz LJ, Missmer SA, Rimm EB, Spiegelman D, James-Todd TM, Rich-Edwards JW (2018) Hypertensive disorders of pregnancy and maternal cardiovascular disease risk factor development: an observational cohort study. Ann Intern Med 169:224–232. https://doi.org/10.7326/M17-2740
Sutton EF, Rogan SC, Lopa S, Sharbaugh D, Muldoon MF, Catov JM (2020) Early pregnancy blood pressure elevations and risk for maternal and neonatal morbidity. Obstet Gynecol 136:129–139. https://doi.org/10.1097/AOG.0000000000003885
Suzuki T, Ikeda Y, Yoshikawa H, Tanaka K, Morita H, Yamamoto M, Takizawa T (2009) Gestational changes in production of NO and expression of NOS mRNA isoforms in the rat placenta. J Vet Med Sci 71:495–498. https://doi.org/10.1292/jvms.71.495
Tabatabaee HR, Zahedi A, Etemad K, Valadbeigi T, Mahdavi S, Enayatrad M, Almasi SZ, Yaghoobi H, Zolfizadeh F, Hajipour M (2020) Risk of stillbirth in women with gestational diabetes and high blood pressure. Iran J Public Health 49:773–781
Takiuti NH, Carvalho MH, Kahhale S, Nigro D, Barbeiro HV, Zugaib M (1999) The effect of chronic nitric oxide inhibition on vascular reactivity and blood pressure in pregnant rats. Sao Paulo Med J Rev Paul Med 117:197–204. https://doi.org/10.1590/s1516-31801999000500004
Tanbe AF, Khalil RA (2010) Circulating and vascular bioactive factors during hypertension in pregnancy. Curr Bioact Compd 6:60–75. https://doi.org/10.2174/157340710790711737
Telfer JF, Irvine GA, Kohnen G, Campbell S, Cameron IT (1997) Expression of endothelial and inducible nitric oxide synthase in non-pregnant and decidualized human endometrium. Mol Hum Reprod 3:69–75. https://doi.org/10.1093/molehr/3.1.69
Tomimatsu T, Mimura K, Endo M, Kumasawa K, Kimura T (2017) Pathophysiology of preeclampsia: an angiogenic imbalance and long-lasting systemic vascular dysfunction. Hypertens Res 40:305–310. https://doi.org/10.1038/hr.2016.152
Tooher J, Thornton C, Makris A, Ogle R, Korda A, Hennessy A (2017) All hypertensive disorders of pregnancy increase the risk of future cardiovascular disease. Hypertension (Dallas TX) 1979(70):798–803. https://doi.org/10.1161/HYPERTENSIONAHA.117.09246
Torgersen KL, Curran CA (2006) A systematic approach to the physiologic adaptations of pregnancy. Crit Care Nurs Q 29:2–19. https://doi.org/10.1097/00002727-200601000-00002
Tranquilli AL, Dekker G, Magee L, Roberts J, Sibai BM, Steyn W, Zeeman GG, Brown MA (2014) The classification, diagnosis and management of the hypertensive disorders of pregnancy: a revised statement from the ISSHP. Pregnancy Hypertens 4:97–104. https://doi.org/10.1016/j.preghy.2014.02.001
Troiano NH (2018) Physiologic and hemodynamic changes during pregnancy. AACN Adv Crit Care 29:273–283. https://doi.org/10.4037/aacnacc2018911
Tropea T, De Francesco EM, Rigiracciolo D, Maggiolini M, Wareing M, Osol G, Mandalà M (2015) Pregnancy augments G protein estrogen receptor (GPER) induced vasodilation in rat uterine arteries via the nitric oxide – cGMP signaling pathway. PLoS One 10:e0141997. https://doi.org/10.1371/journal.pone.0141997
Trounson A (1998) Reproduction, fertility and development. Reprod Fertil Dev 10:515–515. https://doi.org/10.1071/rdv10n8_in
Tseng L, Zhang J, Peresleni TY, Goligorsky MS (1996) Cyclic expression of endothelial nitric oxide synthase mRNA in the epithelial glands of human endometrium. J Soc Gynecol Investig 3:33–38. https://doi.org/10.1016/1071-5576(95)00039-9
Turgut NH, Temiz TK, Bagcivan I, Turgut B, Gulturk S, Karadas B (2008) The effect of sildenafil on the altered thoracic aorta smooth muscle responses in rat pre-eclampsia model. Eur J Pharmacol 589:180–187. https://doi.org/10.1016/j.ejphar.2008.04.034
Vaka VR, McMaster KM, Cunningham MW, Ibrahim T, Hazlewood R, Usry N, Cornelius DC, Amaral LM, LaMarca B (2018) Role of mitochondrial dysfunction and reactive oxygen species in mediating hypertension in the reduced uterine perfusion pressure rat model of preeclampsia. Hypertension (Dallas TX) 1979(72):703–711. https://doi.org/10.1161/HYPERTENSIONAHA.118.11290
Veerbeek JHW, Hermes W, Breimer AY, van Rijn BB, Koenen SV, Mol BW, Franx A, de Groot CJM, Koster MPH (2015) Cardiovascular disease risk factors after early-onset preeclampsia, late-onset preeclampsia, and pregnancy-induced hypertension. Hypertension (Dallas TX) 1979(65):600–606. https://doi.org/10.1161/HYPERTENSIONAHA.114.04850
Vignini A, Cecati M, Nanetti L, Raffaelli F, Ciavattini A, Giannubilo SR, Mazzanti L, Saccucci F, Emanuelli M, Tranquilli AL (2016) Placental expression of endothelial and inducible nitric oxide synthase and NO metabolism in gestational hypertension: a case-control study. J Matern-Fetal Neonatal Med 29:576–581. https://doi.org/10.3109/14767058.2015.1011615
von Ehr J, von Versen-Höynck F (2016) Implications of maternal conditions and pregnancy course on offspring’s medical problems in adult life. Arch Gynecol Obstet 294:673–679. https://doi.org/10.1007/s00404-016-4178-7
Wang Y, Zhao S (2010) Vascular biology of the placenta, integrated systems physiology: from molecules to function to disease. Morgan & Claypool Life Sciences, San Rafael
Wannenburg T, Little WC (2010) Chapter 6 – Regulation of cardiac output. In: Jeremias A, Brown DL (eds) Cardiac intensive care, 2nd edn. W.B. Saunders, Philadelphia, pp 61–68. https://doi.org/10.1016/B978-1-4160-3773-6.10006-0
Webster RP, Roberts VHJ, Myatt L (2008) Protein nitration in placenta – functional significance. Placenta 29:985–994. https://doi.org/10.1016/j.placenta.2008.09.003
Weissgerber TL, Milic NM, Milin-Lazovic JS, Garovic VD (2016) Impaired flow-mediated dilation before, during, and after preeclampsia: a systematic review and meta-analysis. Hypertension (Dallas TX) 1979(67):415–423. https://doi.org/10.1161/HYPERTENSIONAHA.115.06554
Whelton PK, Carey RM, Aronow WS, Casey DE, Collins KJ, Dennison Himmelfarb C, DePalma SM, Gidding S, Jamerson KA, Jones DW, MacLaughlin EJ, Muntner P, Ovbiagele B, Smith SC, Spencer CC, Stafford RS, Taler SJ, Thomas RJ, Williams KA, Williamson JD, Wright JT (2018) 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA guideline for the prevention, detection, evaluation, and management of high blood pressure in adults: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 71:e127–e248. https://doi.org/10.1016/j.jacc.2017.11.006
Wight E, Küng CF, Moreau P, Takase H, Bersinger NA, Lüscher TF (2000) Aging, serum estradiol levels, and pregnancy differentially affect vascular reactivity of the rat uterine artery. J Soc Gynecol Investig 7:106–113
Wójtowicz A, Zembala-Szczerba M, Babczyk D, Kołodziejczyk-Pietruszka M, Lewaczyńska O, Huras H (2019) Early- and late-onset preeclampsia: a comprehensive cohort study of laboratory and clinical findings according to the new ISHHP criteria. Int J Hypertens 2019:4108271. https://doi.org/10.1155/2019/4108271
Xiao D, Pearce WJ, Zhang L (2001) Pregnancy enhances endothelium-dependent relaxation of ovine uterine artery: role of NO and intracellular Ca(2+). Am J Physiol Heart Circ Physiol 281:H183–H190. https://doi.org/10.1152/ajpheart.2001.281.1.H183
Yang X, Guo L, Li H, Chen X, Tong X (2012) Analysis of the original causes of placental oxidative stress in normal pregnancy and pre-eclampsia: a hypothesis. J Matern-Fetal Neonatal Med 25:884–888. https://doi.org/10.3109/14767058.2011.601367
Yang Y, Wu Z, Meininger CJ, Wu G (2015) L-Leucine and NO-mediated cardiovascular function. Amino Acids 47:435–447. https://doi.org/10.1007/s00726-014-1904-y
Yoshida A, Nakao S, Kobayashi M, Kobayashi H (2000) Flow-mediated vasodilation and plasma fibronectin levels in preeclampsia. Hypertension (Dallas TX) 1979(36):400–404. https://doi.org/10.1161/01.hyp.36.3.400
Yunta C, Vonnahme KA, Mordhost BR, Hallford DM, Lemley CO, Parys C, Bach A (2015) Arginine supplementation between 41 and 146 days of pregnancy reduces uterine blood flow in dairy heifers. Theriogenology 84:43–50. https://doi.org/10.1016/j.theriogenology.2015.02.007
Zafer E, Yenisey C, Kurek Eken M, Ozdemir E, Kurt Omurlu I, Yuksel H (2018) Second trimester maternal serum-amniotic fluid nitric oxide and vascular endothelial growth factor levels in relation to uterine artery Doppler indices in pregnancies with normal outcome. J Obstet Gynaecol J Inst Obstet Gynaecol 38:1088–1092. https://doi.org/10.1080/01443615.2018.1454409
Zawiejska A, Wender-Ozegowska E, Iciek R, Brazert J (2014) Concentrations of endothelial nitric oxide synthase, angiotensin-converting enzyme, vascular endothelial growth factor and placental growth factor in maternal blood and maternal metabolic status in pregnancy complicated by hypertensive disorders. J Hum Hypertens 28:670–676. https://doi.org/10.1038/jhh.2014.42
Zhang H-H, Chen JC, Sheibani L, Lechuga TJ, Chen D-B (2017) Pregnancy augments VEGF-stimulated in vitro angiogenesis and vasodilator (NO and H2S) production in human uterine artery endothelial cells. J Clin Endocrinol Metab 102:2382–2393. https://doi.org/10.1210/jc.2017-00437
Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitalo K, Damsky C, Fisher SJ (2002) Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 160:1405–1423. https://doi.org/10.1016/S0002-9440(10)62567-9
Zullino S, Buzzella F, Simoncini T (2018) Nitric oxide and the biology of pregnancy. Vasc Pharmacol 110:71–74. https://doi.org/10.1016/j.vph.2018.07.004
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Dela Justina, V., dos Passos Júnior, R.R., Lima, V.V., Giachini, F.R. (2023). Evidence of Nitric Oxide Impairment During Hypertensive Pregnancies. In: Gonzalez-Ortiz, M. (eds) Advances in Maternal-Fetal Biomedicine. Advances in Experimental Medicine and Biology, vol 1428. Springer, Cham. https://doi.org/10.1007/978-3-031-32554-0_5
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