Unravelling the theories of pre-eclampsia: Are the protective pathways the new paradigm?

British Journal of Pharmacology

Volumn 172, Issue 6, 2015, Pages 1574-1586

  Ahmed, Asif ^a   Ramma, Wenda ^b  

^a ASTON UNIVERSITY   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 MERCAPTOPYRUVATE SULFURTRANSFERASE; ARGINASE; CARBON MONOXIDE; CYSTATHIONINE GAMMA LYASE; ENDOGLIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE; HEME OXYGENASE 1; HEME OXYGENASE 2; HYDROGEN SULFIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PLACENTAL GROWTH FACTOR; PROTEIN KINASE B; SOLUBLE FMS LIKE TYROSINE KINASE 1; SULFURTRANSFERASE; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR; PLACENTA PROTEIN; VASCULOTROPIN RECEPTOR 1;

ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; GLOMERULAR ENDOTHELIOSIS; HUMAN; HYPOXIA; INFLAMMATION; KIDNEY DISEASE; NONHUMAN; OXIDATIVE STRESS; PREECLAMPSIA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DRUG DESIGN; FEMALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY;

ANIMALS; CARBON MONOXIDE; DRUG DESIGN; FEMALE; HUMANS; HYDROGEN SULFIDE; INFLAMMATION; OXIDATIVE STRESS; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84923810589     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12977     Document Type: Review

References (147)

1. Acevedo CH, Ahmed A, (1998). Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy. J Clin Invest 101: 949-955.
2. Ahmad S, Ahmed A, (2004). Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res 95: 884-891.
3. Ahmad S, Hewett PW, Wang P, Al-Ani B, Cudmore M, Fujisawa T, et al. (2006). Direct evidence for endothelial vascular endothelial growth factor receptor-1 function in nitric oxide-mediated angiogenesis. Circ Res 99: 715-722.
4. Ahmed A, (1997). Heparin-binding angiogenic growth factors in pregnancy. Trophoblast Res 10: 215-258.
5. Ahmed A, (2011). New insights into the etiology of preeclampsia: identification of key elusive factors for the vascular complications. Thromb Res 127S3: S72-S75.
6. Ahmed A, Rahman M, Zhang X, Acevedo CH, Nijjar S, Rushton I, et al. (2000). Induction of placental heme oxygenase-1 is protective against TNFalpha- induced cytotoxicity and promotes vessel relaxation. Mol Med 6: 391-409.
7. Ahmed A, Fujisawa T, Niu XL, Ahmad S, Al-Ani B, Chudasama K, et al. (2009). Angiopoietin-2 confers Atheroprotection in apoE-/- mice by inhibiting LDL oxidation via nitric oxide. Circ Res 104: 1333-1336.
8. Ahmed H, McLaughlin BE, Soong J, Marks GS, Brien JF, Nakatsu K, (2005). The source of endogenous carbon monoxide formation in human placental chorionic villi. Cell Mol Biol (Noisy-Le-Grand) 51: 447-451.
9. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Nuclear hormone receptors. Br J Pharmacol 170: 1652-1675.
10. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Catalytic receptors. Br J Pharmacol 170: 1676-1705.
11. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
12. Aoki Y, Yamamoto T, Fumihisa C, Nakamura A, Asanuma A, Suzuki M, (2012). Effect on the production of soluble endoglin from human choriocarcinoma cells by preeclampsia sera. Am J Reprod Immunol 67: 413-420.
13. Avagliano L, Bulfamante GP, Morabito A, Marconi AM, (2011). Abnormal spiral artery remodelling in the decidual segment during pregnancy: from histology to clinical correlation. J Clin Pathol 64: 1064-1068.
14. Bainbridge SA, Farley AE, McLaughlin BE, Graham CH, Marks GS, Nakatsu K, et al. (2002). Carbon monoxide decreases perfusion pressure in isolated human placenta. Placenta 23: 563-569.
15. Barber A, Robson SC, Myatt L, Bulmer JN, Lyall F, (2001). Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J 15: 1158-1168.
16. Baum M, Schiff E, Kreiser D, Dennery PA, Stevenson DK, Rosenthal T, et al. (2000). End-tidal carbon monoxide measurements in women with pregnancy-induced hypertension and preeclampsia. Am J Obstet Gynecol 183: 900-903.
17. Bellamy L, Casas JP, Hingorani AD, Williams DJ, (2007). Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 335: 974.
18. Bendall JK, Alp NJ, Warrick N, Cai S, Adlam D, Rockett K, et al. (2005). Stoichiometric relationships between endothelial tetrahydrobiopterin, endothelial NO synthase (eNOS) activity, and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS overexpression. Circ Res 97: 864-871.
19. Bernardi F, Constantino L, Machado R, Petronilho F, Dal-Pizzol F, (2008). Plasma nitric oxide, endothelin-1, arginase and superoxide dismutase in pre-eclamptic women. J Obstet Gynaecol Res 34: 957-963.
20. Bir SC, Kevil CG, (2013). Sulfane sustains vascular health: insights into cystathionine gamma-lyase function. Circulation 127: 2472-2474.
21. Blackstone E, Roth MB, (2007). Suspended animation-like state protects mice from lethal hypoxia. Shock 27: 370-372.
22. Brosens I, (1964). A study of the spiral arteries of the decidua basalis in normotensive and hypertensive pregnancies. J Obstet Gynaecol Br Commonw 71: 222-230.
23. Brosens IA, (1977). Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynaecol 4: 573-593.
24. Brosens JJ, Pijnenborg R, Brosens IA, (2002). The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 187: 1416-1423.
25. Buhimschi CS, Magloire L, Funai E, Norwitz ER, Kuczynski E, Martin R, et al. (2006). Fractional excretion of angiogenic factors in women with severe preeclampsia. Obstet Gynecol 107: 1103-1113.
26. Burke SD, Karumanchi SA, (2013). Spiral artery remodeling in preeclampsia revisited. Hypertension 62: 1013-1014.
27. Burke SD, Barrette VF, Bianco J, Thorne JG, Yamada AT, Pang SC, et al. (2010). Spiral arterial remodeling is not essential for normal blood pressure regulation in pregnant mice. Hypertension 55: 729-737.
28. Burton GJ, Woods AW, Jauniaux E, Kingdom JC, (2009). Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30: 473-482.
29. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A, (2001). Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol 159: 993-1008.
30. Carty DM, Anderson LA, Freeman DJ, Welsh PI, Brennand JE, Dominiczak AF, et al. (2012). Early pregnancy soluble E-selectin concentrations and risk of preeclampsia. J Hypertens 30: 954-959.
31. Chappell LC, Seed PT, Briley A, Kelly FJ, Hunt BJ, Charnock-Jones DS, et al. (2002). A longitudinal study of biochemical variables in women at risk of preeclampsia. Am J Obstet Gynecol 187: 127-136.
32. Chappell LC, Duckworth S, Seed PT, Griffin M, Myers J, Mackillop L, et al. (2013). Diagnostic accuracy of placental growth factor in women with suspected preeclampsia: a prospective multicenter study. Circulation 128: 2121-2131.
33. Cindrova-Davies T, Herrera EA, Niu Y, Kingdom J, Giussani DA, Burton GJ, (2013). Reduced cystathionine gamma-lyase and increased MicroRNA-21 expression are associated with increased vascular resistance in growth-restricted pregnancies: hydrogen sulfide as a placental vasodilator. Am J Pathol 182: 1448-1458.
34. Coletta C, Papapetropoulos A, Erdelyi K, Olah G, Modis K, Panopoulos P, et al. (2012). Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci U S A 109: 9161-9166.
35. Conde-Agudelo A, Althabe F, Belizan JM, Kafury-Goeta AC, (1999). Cigarette smoking during pregnancy and risk of preeclampsia: a systematic review. Am J Obstet Gynecol 181: 1026-1035.
36. Cotechini T, Komisarenko M, Sperou A, Macdonald-Goodfellow S, Adams MA, Graham CH, (2014). Inflammation in rat pregnancy inhibits spiral artery remodeling leading to fetal growth restriction and features of preeclampsia. J Exp Med 211: 165-179.
37. Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E, (2006). Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 195: 201-207.
38. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, et al. (2007). Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 115: 1789-1797.
39. d'Uscio LV, Baker TA, Mantilla CB, Smith L, Weiler D, Sieck GC, et al. (2001). Mechanism of endothelial dysfunction in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 21: 1017-1022.
40. Dai B, Liu T, Zhang B, Zhang X, Wang Z, (2013). The polymorphism for endothelial nitric oxide synthase gene, the level of nitric oxide and the risk for pre-eclampsia: a meta-analysis. Gene 519: 187-193.
41. Davidge ST, (1998). Oxidative stress and altered endothelial cell function in preeclampsia. Semin Reprod Endocrinol 16: 65-73.
42. Denschlag D, Marculescu R, Unfried G, Hefler LA, Exner M, Hashemi A, et al. (2004). The size of a microsatellite polymorphism of the haem oxygenase 1 gene is associated with idiopathic recurrent miscarriage. Mol Hum Reprod 10: 211-214.
43. Djurovic S, Clausen T, Wergeland R, Brosstad F, Berg K, Henriksen T, (2002). Absence of enhanced systemic inflammatory response at 18 weeks of gestation in women with subsequent pre-eclampsia. BJOG 109: 759-764.
44. Doridot L, Passet B, Mehats C, Rigourd V, Barbaux S, Ducat A, et al. (2013). Preeclampsia-like symptoms induced in mice by fetoplacental expression of STOX1 are reversed by aspirin treatment. Hypertension 61: 662-668.
45. Doridot L, Chatre L, Ducat A, Vilotte JL, Lombes A, Mehats C, et al. (2014). Nitroso-redox balance and mitochondrial homeostasis are regulated by STOX1, a pre-eclampsia-associated gene. Antioxid Redox Signal 21: 819-834.
46. Dulak J, Deshane J, Jozkowicz A, Agarwal A, (2008). Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation 117: 231-241.
47. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, et al. (2007). Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A 104: 15560-15565.
48. Farina A, Sekizawa A, de Sanctis P, Purwosunu Y, Okai T, Cha DH, et al. (2008). Gene expression in chorionic villous samples at 11 weeks' gestation from women destined to develop preeclampsia. Prenat Diagn 28: 956-961.
49. Feinberg RF, Kliman HJ, Cohen AW, (1991). Preeclampsia, trisomy 13, and the placental bed. Obstet Gynecol 78: 505-508.
50. George EM, Cockrell K, Aranay M, Csongradi E, Stec DE, Granger JP, (2011). Induction of heme oxygenase 1 attenuates placental ischemia-induced hypertension. Hypertension 57: 941-948.
51. Gonzalez C, Cruz MA, Gallardo V, Lagos M, Varela J, Albornoz J, et al. (1995). Nitric oxide and prostaglandin systems inhibition on the isolated perfused human placenta from normal and preeclamptic pregnancies. Gynecol Obstet Invest 40: 244-248.
52. Gude NM, King RG, Brennecke SP, (1990). Role of endothelium-derived nitric oxide in maintenance of low fetal vascular resistance in placenta. Lancet 336: 1589-1590.
53. Hayden LJ, Goeden H, Roth SH, (1990). Growth and development in the rat during sub-chronic exposure to low levels of hydrogen sulfide. Toxicol Ind Health 6: 389-401.
54. Heitzer T, Schlinzig T, Krohn K, Meinertz T, Munzel T, (2001). Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation 104: 2673-2678.
55. Holwerda KM, Bos EM, Rajakumar A, Ris-Stalpers C, van Pampus MG, Timmer A, et al. (2012). Hydrogen sulfide producing enzymes in pregnancy and preeclampsia. Placenta 33: 518-521.
56. Holwerda KM, Burke SD, Faas MM, Zsengeller Z, Stillman IE, Kang PM, et al. (2014). Hydrogen sulfide attenuates sFlt1-induced hypertension and renal damage by upregulating vascular endothelial growth factor. J Am Soc Nephrol 25: 717-725.
57. Hu R, Lu J, You X, Zhu X, Hui N, Ni X, (2011). Hydrogen sulfide inhibits the spontaneous and oxytocin-induced contractility of human pregnant myometrium. Gynecol Endocrinol 27: 900-904.
58. Hubel CA, (1999). Oxidative stress in the pathogenesis of preeclampsia. Proc Soc Exp Biol Med 222: 222-235.
59. Huppertz B, Weiss G, Moser G, (2014). Trophoblast invasion and oxygenation of the placenta: measurements versus presumptions. J Reprod Immunol 101-102: 74-79.
60. Johal T, Lees CC, Everett TR, Wilkinson IB, (2014). The nitric oxide pathway and possible therapeutic options in pre-eclampsia. Br J Clin Pharmacol 78: 244-257.
61. Kaartokallio T, Klemetti MM, Timonen A, Uotila J, Heinonen S, Kajantie E, et al. (2014). Microsatellite polymorphism in the heme oxygenase-1 promoter is associated with nonsevere and late-onset preeclampsia. Hypertension 64: 172-177.
62. Kabbinavar F, Hurwitz HI, Fehrenbacher L, Meropol NJ, Novotny WF, Lieberman G, et al. (2003). Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21: 60-65.
63. Kabil O, Vitvitsky V, Xie P, Banerjee R, (2011). The quantitative significance of the transsulfuration enzymes for H2S production in murine tissues. Antioxid Redox Signal 15: 363-372.
64. Kery V, Bukovska G, Kraus JP, (1994). Transsulfuration depends on heme in addition to pyridoxal 5-phosphate. Cystathionine beta-synthase is a heme protein. J Biol Chem 269: 25283-25288.
65. Khalil AA, Tsikas D, Akolekar R, Jordan J, Nicolaides KH, (2013). Asymmetric dimethylarginine, arginine and homoarginine at 11-13 weeks' gestation and preeclampsia: a case-control study. J Hum Hypertens 27: 38-43.
66. Kharb S, (2000). Vitamin E and C in preeclampsia. Eur J Obstet Gynecol Reprod Biol 93: 37-39.
67. Khong TY, de Wolf F, Robertson WB, Brosens I, (1986). Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 93: 1049-1059.
68. Kondo K, Bhushan S, King AL, Prabhu SD, Hamid T, Koenig S, et al. (2013). H(2)S protects against pressure overload-induced heart failure via upregulation of endothelial nitric oxide synthase. Circulation 127: 1116-1127.
69. Kreiser D, Baum M, Seidman DS, Fanaroff A, Shah D, Hendler I, et al. (2004). End tidal carbon monoxide levels are lower in women with gestational hypertension and pre-eclampsia. J Perinatol 24: 213-217.
70. Kronborg CS, Gjedsted J, Vittinghus E, Hansen TK, Allen J, Knudsen UB, (2011). Longitudinal measurement of cytokines in pre-eclamptic and normotensive pregnancies. Acta Obstet Gynecol Scand 90: 791-796.
71. Kukor Z, Valent S, Toth M, (2000). Regulation of nitric oxide synthase activity by tetrahydrobiopterin in human placentae from normal and pre-eclamptic pregnancies. Placenta 21: 763-772.
72. Kumasawa K, Ikawa M, Kidoya H, Hasuwa H, Saito-Fujita T, Morioka Y, et al. (2011). Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc Natl Acad Sci U S A 108: 1451-1455.
73. LaMarca BD, Ryan MJ, Gilbert JS, Murphy SR, Granger JP, (2007). Inflammatory cytokines in the pathophysiology of hypertension during preeclampsia. Curr Hypertens Rep 9: 480-485.
74. Learmont JG, Poston L, (1996). Nitric oxide is involved in flow-induced dilation of isolated human small fetoplacental arteries. Am J Obstet Gynecol 174: 583-588.
75. Leffler CW, Parfenova H, Jaggar JH, Wang R, (2006). Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J Appl Physiol (1985) 100: 1065-1076.
76. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, et al. (2004). Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683.
77. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, et al. (2006). Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 355: 992-1005.
78. Li F, Hagaman JR, Kim HS, Maeda N, Jennette JC, Faber JE, et al. (2012). eNOS deficiency acts through endothelin to aggravate sFlt-1-induced pre-eclampsia-like phenotype. J Am Soc Nephrol 23: 652-660.
79. Lin MI, Fulton D, Babbitt R, Fleming I, Busse R, Pritchard KA Jr, et al. (2003). Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production. J Biol Chem 278: 44719-44726.
80. Linzke N, Schumacher A, Woidacki K, Croy BA, Zenclussen AC, (2014). Carbon monoxide promotes proliferation of uterine natural killer cells and remodeling of spiral arteries in pregnant hypertensive heme oxygenase-1 mutant mice. Hypertension 63: 580-588.
81. Liu X, Pan L, Zhuo Y, Gong Q, Rose P, Zhu Y, (2010). Hypoxia-inducible factor-1alpha is involved in the pro-angiogenic effect of hydrogen sulfide under hypoxic stress. Biol Pharm Bull 33: 1550-1554.
82. Lowe DT, (2000). Nitric oxide dysfunction in the pathophysiology of preeclampsia. Nitric Oxide 4: 441-458.
83. Lowe SA, Brown MA, Dekker GA, Gatt S, McLintock CK, McMahon LP, et al. (2009). Guidelines for the management of hypertensive disorders of pregnancy 2008. Aust N Z J Obstet Gynaecol 49: 242-246.
84. Lyall F, Barber A, Myatt L, Bulmer JN, Robson SC, (2000). Hemeoxygenase expression in human placenta and placental bed implies a role in regulation of trophoblast invasion and placental function. FASEB J 14: 208-219.
85. Lyall F, Robson SC, Bulmer JN, (2013). Spiral artery remodeling and trophoblast invasion in preeclampsia and fetal growth restriction: relationship to clinical outcome. Hypertension 62: 1046-1054.
86. MacDonald SE, Walker M, Ramshaw H, Godwin M, Chen XK, Smith G, (2007). Hypertensive disorders of pregnancy and long-term risk of hypertension: what do Ontario prenatal care providers know, and what do they communicate? J Obstet Gynaecol Can 29: 705-710.
87. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, et al. (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.
88. McCarthy FP, Drewlo S, Kingdom J, Johns EJ, Walsh SK, Kenny LC, (2011). Peroxisome proliferator-activated receptor-{gamma} as a potential therapeutic target in the treatment of preeclampsia. Hypertension 58: 280-286.
89. Mehendale R, Hibbard J, Fazleabas A, Leach R, (2007). Placental angiogenesis markers sFlt-1 and PlGF: response to cigarette smoke. Am J Obstet Gynecol 197: 363, e1-5.
90. 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.
91. Miyagami S, Koide K, Sekizawa A, Ventura W, Yotsumoto J, Oishi S, et al. (2013). Physiological changes in the pattern of placental gene expression early in the first trimester. Reprod Sci 20: 710-714.
92. Moncada S, (1997). Nitric oxide in the vasculature: physiology and pathophysiology. Ann N Y Acad Sci 811: 60-67, discussion 67-9.
93. Mustafa AK, Gadalla MM, Snyder SH, (2009). Signaling by gasotransmitters. Sci Signal 2: re2.
94. Myatt L, Brewer A, Brockman DE, (1991). The action of nitric oxide in the perfused human fetal-placental circulation. Am J Obstet Gynecol 164: 687-692.
95. Naljayan MV, Karumanchi SA, (2013). New developments in the pathogenesis of preeclampsia. Adv Chronic Kidney Dis 20: 265-270.
96. Nayeri UA, Buhimschi IA, Laky CA, Cross SN, Duzyj CM, Ramma W, et al. (2014). Antenatal corticosteroids impact the inflammatory rather than the antiangiogenic profile of women with preeclampsia. Hypertension 63: 1285-1292.
97. Odrcich MJ, Graham CH, Kimura KA, McLaughlin BE, Marks GS, Nakatsu K, et al. (1998). Heme oxygenase and nitric oxide synthase in the placenta of the guinea-pig during gestation. Placenta 19: 509-516.
98. Ozler A, Turgut A, Sak ME, Evsen MS, Soydinc HE, Evliyaoglu O, et al. (2012). Serum levels of neopterin, tumor necrosis factor-alpha and Interleukin-6 in preeclampsia: relationship with disease severity. Eur Rev Med Pharmacol Sci 16: 1707-1712.
99. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, et al. (2009). Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci U S A 106: 21972-21977.
100. Patel P, Vatish M, Heptinstall J, Wang R, Carson RJ, (2009). The endogenous production of hydrogen sulphide in intrauterine tissues. Reprod Biol Endocrinol 7: 10.
101. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl. Acids Res. 42 (Database Issue): D1098-1106.
102. Podmore ID, Griffiths HR, Herbert KE, Mistry N, Mistry P, Lunec J, (1998). Vitamin C exhibits pro-oxidant properties. Nature 392: 559.
103. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH, (2006). Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet 367: 1145-1154.
104. Ramesar SV, Mackraj I, Gathiram P, Moodley J, (2011). Sildenafil citrate decreases sFlt-1 and sEng in pregnant l-NAME treated Sprague-Dawley rats. Eur J Obstet Gynecol Reprod Biol 157: 136-140.
105. Ramma W, Ahmed A, (2011). Is inflammation the cause of pre-eclampsia? Biochem Soc Trans 39: 1619-1627.
106. Ramma W, Buhimschi IA, Zhao G, Dulay AT, Nayeri UA, Buhimschi CS, et al. (2012). The elevation in circulating anti-angiogenic factors is independent of markers of neutrophil activation in preeclampsia. Angiogenesis 15: 341-348.
107. Rana S, Karumanchi SA, Lindheimer MD, (2014). Angiogenic factors in diagnosis, management, and research in preeclampsia. Hypertension 63: 198-202.
108. Redman CW, (1992). Immunological aspects of pre-eclampsia. Baillieres Clin Obstet Gynaecol 6: 601-615.
109. Redman CW, Sargent IL, (2005). Latest advances in understanding preeclampsia. Science 308: 1592-1594.
110. Redman CW, Sacks GP, Sargent IL, (1999). Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 180: 499-506.
111. Rizos D, Eleftheriades M, Batakis E, Rizou M, Haliassos A, Hassiakos D, et al. (2012). Levels of asymmetric dimethylarginine throughout normal pregnancy and in pregnancies complicated with preeclampsia or had a small for gestational age baby. J Matern Fetal Neonatal Med 25: 1311-1315.
112. Rizzo G, Arduini D, Romanini C, (1993). Uterine artery Doppler velocity waveforms in twin pregnancies. Obstet Gynecol 82: 978-983.
113. Roberge S, Nicolaides KH, Demers S, Villa P, Bujold E, (2013). Prevention of perinatal death and adverse perinatal outcome using low-dose aspirin: a meta-analysis. Ultrasound Obstet Gynecol 41: 491-499.
114. Roberts JM, Hubel CA, (2009). The two stage model of preeclampsia: variations on the theme. Placenta 30 (Suppl. A): S32-S37.
115. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK, (1989). Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 161: 1200-1204.
116. Robinson H, Wray S, (2012). A new slow releasing, H(2)S generating compound, GYY4137 relaxes spontaneous and oxytocin-stimulated contractions of human and rat pregnant myometrium. PLoS ONE 7: e46278.
117. Rossi AC, Mullin PM, (2011). Prevention of pre-eclampsia with low-dose aspirin or vitamins C and E in women at high or low risk: a systematic review with meta-analysis. Eur J Obstet Gynecol Reprod Biol 158: 9-16.
118. Rubbo H, Batthyany C, Radi R, (2000). Nitric oxide-oxygen radicals interactions in atherosclerosis. Biol Res 33: 167-175.
119. 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.
120. Schiff E, Barkai G, Ben-Baruch G, Mashiach S, (1990). Low-dose aspirin does not influence the clinical course of women with mild pregnancy-induced hypertension. Obstet Gynecol 76: 742-744.
121. Sidhu R, Singh M, Samir G, Carson RJ, (2001). L-cysteine and sodium hydrosulphide inhibit spontaneous contractility in isolated pregnant rat uterine strips in vitro. Pharmacol Toxicol 88: 198-203.
122. Sidle EH, Casselman R, Smith GN, (2007). Effect of cigarette smoke on placental antioxidant enzyme expression. Am J Physiol Regul Integr Comp Physiol 293: R754-R758.
123. Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A, (2004). The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol 286: F425-F441.
124. Smith GC, Pell JP, Walsh D, (2001). Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 357: 2002-2006.
125. Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, et al. (2003). Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem 278: 12605-12608.
126. Tao BB, Liu SY, Zhang CC, Fu W, Cai WJ, Wang Y, et al. (2013). VEGFR2 functions as an H2S-targeting receptor protein kinase with its novel Cys1045-Cys1024 disulfide bond serving as a specific molecular switch for hydrogen sulfide actions in vascular endothelial cells. Antioxid Redox Signal 19: 448-464.
127. Tenhunen R, Marver HS, Schmid R, (1969). Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem 244: 6388-6394.
128. Teupe C, Richter S, Fisslthaler B, Randriamboavonjy V, Ihling C, Fleming I, et al. (2002). Vascular gene transfer of phosphomimetic endothelial nitric oxide synthase (S1177D) using ultrasound-enhanced destruction of plasmid-loaded microbubbles improves vasoreactivity. Circulation 105: 1104-1109.
129. Tsukatani E, (1983). Etiology of EPH-gestosis from the viewpoint of dynamics of vasoactive prostanoid, lipid peroxides and vitamin E. Nihon Sanka Fujinka Gakkai Zasshi 35: 713-720.
130. Velauthar L, Plana MN, Kalidindi M, Zamora J, Thilaganathan B, Illanes SE, et al. (2014). First-trimester uterine artery Doppler and adverse pregnancy outcome: a meta-analysis involving 55,974 women. Ultrasound Obstet Gynecol 43: 500-507.
131. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, et al. (2006). Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12: 642-649.
132. Villa PM, Kajantie E, Raikkonen K, Pesonen AK, Hamalainen E, Vainio M, et al. (2013). Aspirin in the prevention of pre-eclampsia in high-risk women: a randomised placebo-controlled PREDO Trial and a meta-analysis of randomised trials. BJOG 120: 64-74.
133. Wallenburg HC, Dekker GA, Makovitz JW, Rotmans P, (1986). Low-dose aspirin prevents pregnancy-induced hypertension and pre-eclampsia in angiotensin-sensitive primigravidae. Lancet 1: 1-3.
134. Wang K, Ahmad S, Cai M, Rennie J, Fujisawa T, Crispi F, et al. (2013). Dysregulation of hydrogen sulfide producing enzyme cystathionine gamma-lyase contributes to maternal hypertension and placental abnormalities in preeclampsia. Circulation 127: 2514-2522.
135. Whiteman M, le Trionnaire S, Chopra M, Fox B, Whatmore J, (2011). Emerging role of hydrogen sulfide in health and disease: critical appraisal of biomarkers and pharmacological tools. Clin Sci (Lond) 121: 459-488.
136. Wickens D, Wilkins MH, Lunec J, Ball G, Dormandy TL, (1981). Free radical oxidation (peroxidation) products in plasma in normal and abnormal pregnancy. Ann Clin Biochem 18: 158-162.
137. Wong RJ, Zhao H, Stevenson DK, (2012). A deficiency in haem oxygenase-1 induces foetal growth restriction by placental vasculature defects. Acta Paediatr 101: 827-834.
138. Xenos ES, Stevens SL, Freeman MB, Cassada DC, Goldman MH, (2005). Nitric oxide mediates the effect of fluvastatin on intercellular adhesion molecule-1 and platelet endothelial cell adhesion molecule-1 expression on human endothelial cells. Ann Vasc Surg 19: 386-392.
139. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, et al. (1999). Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103: 129-135.
140. Yan H, Du J, Tang C, (2004). The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats. Biochem Biophys Res Commun 313: 22-27.
141. Yanfei W, Lin S, Junbao D, Chaoshu T, (2006). Impact of L-arginine on hydrogen sulfide/cystathionine-gamma-lyase pathway in rats with high blood flow-induced pulmonary hypertension. Biochem Biophys Res Commun 345: 851-857.
142. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, et al. (2008). H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322: 587-590.
143. You XJ, Xu C, Lu JQ, Zhu XY, Gao L, Cui XR, et al. (2011). Expression of cystathionine beta-synthase and cystathionine gamma-lyase in human pregnant myometrium and their roles in the control of uterine contractility. PLoS ONE 6: e23788.
144. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL, (2006). Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120.
145. Zhao H, Wong RJ, Doyle TC, Nayak N, Vreman HJ, Contag CH, et al. (2008). Regulation of maternal and fetal hemodynamics by heme oxygenase in mice. Biol Reprod 78: 744-751.
146. Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK, (2009). Effect of heme oxygenase-1 deficiency on placental development. Placenta 30: 861-868.
147. Zhao W, Zhang J, Lu Y, Wang R, (2001). The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20: 6008-6016.