Heme oxygenase inhibition increases blood pressure in pregnant rats

American Journal of Hypertension

Volumn 26, Issue 7, 2013, Pages 924-930

  George, Eric M ^a   Hosick, Peter A ^a   Stec, David E ^a   Granger, Joey P ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

blood pressure; heme oxygenase; hypertension; NADPH oxidase; preeclampsia; pregnancy; sFlt 1

Indexed keywords

CD135 ANTIGEN; HEME OXYGENASE; LUCIGENIN; MESOPORPHYRIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; CHEMOLUMINESCENCE; CONTROLLED STUDY; DOUBLE ANTIBODY SANDWICH ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GESTATIONAL AGE; MEAN ARTERIAL PRESSURE; NONHUMAN; OXIDATIVE STRESS; PLACENTA CIRCULATION; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT;

BLOOD PRESSURE; HEME OXYGENASE; HYPERTENSION; NADPH OXIDASE; PREECLAMPSIA; PREGNANCY; SFLT-1.;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; FEMALE; HEME OXYGENASE-1; OXIDATIVE STRESS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, CARDIOVASCULAR; PREGNANCY, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84878854626     PISSN: 08957061     EISSN: 19417225     Source Type: Journal    
DOI: 10.1093/ajh/hpt045     Document Type: Article

References (40)

1. Pijnenborg R, Vercruysse L, Brosens I. Deep placentation. Best Pract Res Clin Obstet Gynaecol 2011; 25:273-285.
2. Gilbert JS, Ryan MJ, LaMarca BB, Sedeek M, Murphy SR, Granger JP. Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. Am J Physiol Heart Circ Physiol 2008; 294:H541-H550.
3. Sedeek M, Gilbert JS, LaMarca BB, Sholook M, Chandler DL, Wang Y, Granger JP. Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. Am J Hypertens 2008; 21:1152-1156.
4. Sedeek MW, YP, Granger, JP. Increased oxidative stress in a rat model of preeclampsia. Am J Hypertens 2004; 17:142A.
5. Gilbert JS, Babcock SA, Granger JP. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 2007; 50:1142-1147.
6. Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, Waugh R, McKenzie P, Kirwan P, Hennessy A. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 2007; 71:977-984.
7. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111:649-658.
8. George EM, Colson D, Dixon J, Palei AC, Granger JP. Heme oxygenase-1 attenuates hypoxia-induced sFlt-1 and oxidative stress in placental villi through its metabolic products CO and bilirubin. Int J Hypertens 2012; 2012:486053.
9. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, Ahmed A. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007; 115:1789-1797.
10. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235:1043-1046.
11. McGeary RP, Szyczew AJ, Toth I. Biological properties and therapeutic potential of bilirubin. Mini Rev Med Chem 2003;3:253-256.
12. Botros FT, Schwartzman ML, Stier CT, Jr., Goodman AI, Abraham NG. Increase in heme oxygenase-1 levels ameliorates renovascular hypertension. Kidney Int 2005; 68:2745-2755.
13. Yang L, Quan S, Nasjletti A, Laniado-Schwartzman M, Abraham NG. Heme oxygenase-1 gene expression modulates angiotensin II-induced increase in blood pressure. Hypertension 2004; 43:1221-1226.
14. Idriss NK, Blann AD, Lip GY. Hemoxygenase-1 in cardiovascular disease. J Am Coll Cardiol 2008; 52:971-978.
15. Wu FT, Stefanini MO, Mac Gabhann F, Kontos CD, Annex BH, Popel AS. A systems biology perspective on sVEGFR1: its biological function, pathogenic role and therapeutic use. J Cell Mol Med 2010; 14:528-552.
16. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350:672-683.
17. Tam Tam KB, Lamarca B, Arany M, Cockrell K, Fournier L, Murphy S, Martin JN Jr, Granger JP. Role of reactive oxygen species during hypertension in response to chronic antiangiogenic factor (sFlt-1) excess in pregnant rats. Am J Hypertens 2011; 24:110-113.
18. Zhao H, Azuma J, Kalish F, Wong RJ, Stevenson DK. Maternal heme oxygenase 1 regulates placental vasculature development via angiogenic factors in mice. Biol Reprod 2011; 85:1005-1012.
19. Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK. Effect of heme oxygenase-1 deficiency on placental development. Placenta 2009; 30:861-868.
20. Porteri E, Rodella LF, Rezzani R, Rizzoni D, Paiardi S, de Ciuceis C, Boari GE, Foglio E, Favero G, Rizzardi N, Platto C, Agabiti Rosei E. Role of heme oxygenase in modulating endothelial function in mesenteric small resistance arteries of spontaneously hypertensive rats. Clin Exp Hypertens 2009; 31:560-571.
21. George EM, Cockrell K, Aranay M, Csongradi E, Stec DE, Granger JP. Induction of heme oxygenase 1 attenuates placental ischemia-induced hypertension. Hypertension 2011; 57:941-948.
22. Drummond GS, Kappas A. Sn-mesoporphyrin suppression of hyperbilirubinemia in EHBR/Eis rats, an animal model of Dubin-Johnson syndrome. Pharmacology 1998; 56:158-164.
23. Wong RJ, Zhao H, Stevenson DK. A deficiency in haem oxygenase-1 induces foetal growth restriction by placental vasculature defects. Acta Paediatr 2012; 101:827-834.
24. Barber A, Robson SC, Myatt L, Bulmer JN, Lyall F. Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. Faseb J 2001; 15:1158-1168.
25. Lyall F, Barber A, Myatt L, Bulmer JN, Robson SC. Hemeoxygenase expression in human placenta and placental bed implies a role in regulation of trophoblast invasion and placental function. FASEB J 2000; 14:208-219.
26. McCaig D, Lyall F. Inhibitors of heme oxygenase reduce invasion of human primary cytotrophoblast cells in vitro. Placenta 2009; 30:536-538.
27. Bilban M, Haslinger P, Prast J, Klinglmuller F, Woelfel T, Haider S, Sachs A, Otterbein LE, Desoye G, Hiden U, Wagner O, Knofler M. Identification of novel trophoblast invasion-related genes: heme oxygenase-1 controls motility via peroxisome proliferator-activated receptor gamma. Endocrinology 2009; 150:1000-1013.
28. Zenclussen ML, Casalis PA, El-Mousleh T, Rebelo S, Langwisch S, Linzke N, Volk HD, Fest S, Soares MP, Zenclussen AC. Haem oxygenase-1 dictates intrauterine fetal survival in mice via carbon monoxide. J Pathol 2011; 225:293-304.
29. Dulak J, Jozkowicz A, Foresti R, Kasza A, Frick M, Huk I, Green CJ, Pachinger O, Weidinger F, Motterlini R. Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal 2002; 4:229-240.
30. Loboda A, Jazwa A, Wegiel B, Jozkowicz A, Dulak J. Heme oxygenase-1-dependent and-independent regulation of angiogenic genes expression: effect of cobalt protoporphyrin and cobalt chloride on VEGF and IL-8 synthesis in human microvascular endothelial cells. Cell Mol Biol (Noisy-le-grand) 2005; 51:347-355.
31. Fujii M, Inoguchi T, Sasaki S, Maeda Y, Zheng J, Kobayashi K, Takayanagi R. Bilirubin and biliverdin protect rodents against diabetic nephropathy by downregulating NAD(P)H oxidase. Kidney Int 2010; 78:905-919.
32. Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension 2007; 50:636-642.
33. Lanone S, Bloc S, Foresti R, Almolki A, Taille C, Callebert J, Conti M, Goven D, Aubier M, Dureuil B, El-Benna J, Motterlini R, Boczkowski J. Bilirubin decreases nos2 expression via inhibition of NAD(P)H oxidase: implications for protection against endotoxic shock in rats. FASEB J 2005; 19:1890-1892.
34. Kwak JY, Takeshige K, Cheung BS, Minakami S. Bilirubin inhibits the activation of superoxide-producing NADPH oxidase in a neutrophil cell-free system. Biochim Biophys Acta 1991; 1076:369-373.
35. Briones AM, Touyz RM. Oxidative stress and hypertension: current concepts. Curr Hypertens Rep 2010; 12:135-142.
36. Ahmed A, Cudmore MJ. Can the biology of VEGF and haem oxygenases help solve pre-eclampsia Biochem Soc Trans 2009; 37:1237-1242.
37. Ahmed A, Rahman M, Zhang X, Acevedo CH, Nijjar S, Rushton I, Bussolati B, St John J. Induction of placental heme oxygenase-1 is protective against TNFalpha-induced cytotoxicity and promotes vessel relaxation. Mol Med 2000; 6:391-409.
38. Shrestha Dangol D, Chen HP. Role of hemeoxygenase-2 in pregnancyinduced hypertension. Int J Gynaecol Obstet 2004; 85:44-46.
39. Zenclussen AC, Lim E, Knoeller S, Knackstedt M, Hertwig K, Hagen E, Klapp BF, Arck PC. Heme oxygenases in pregnancy II: HO-2 is downregulated in human pathologic pregnancies. Am J Reprod Immunol 2003; 50:66-76.
40. Stec DE, Hosick PA, Granger JP. Bilirubin, renal hemodynamics, and blood pressure. Front Pharmacol 2012; 3:18.