Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1

Circulation

Volumn 115, Issue 13, 2007, Pages 1789-1797

  Cudmore, Melissa ^a,b   Ahmad, Shakil ^a,b   Al Ani, Bahjat ^a,b   Fujisawa, Takeshi ^a,b   Coxall, Heather ^a,b   Chudasama, Kunal ^a,b   Devey, Luke R ^a   Wigmore, Stephen J ^a   Abbas, Allyah ^a,b   Hewett, Peter W ^a,b   Ahmed, Asif ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

Author keywords

Angiogenesis; Endothelium; Endothelium derived factors; Heme oxygenase 1; Preeclampsia; Pregnancy; Statins

Indexed keywords

ADENOVIRUS VECTOR; ALPHA TOCOPHEROL; ASCORBIC ACID; COMPACTIN; ENDOGLIN; FLUINDOSTATIN; GAMMA INTERFERON; HEME OXYGENASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PLACENTAL GROWTH FACTOR; SIMVASTATIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN E; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; ANTIOXIDANT; CARBON MONOXIDE; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; FLT1 PROTEIN, HUMAN; HEME OXYGENASE; HMOX1 PROTEIN, RAT; HYBRID PROTEIN; LEUKOCYTE ANTIGEN; ORGANOMETALLIC COMPOUND; PLACENTA PROTEIN; PRODUCT PLACENTA GROWTH FACTOR; SMALL INTERFERING RNA; TRICARBONYLDICHLORORUTHENIUM (II) DIMER; VASCULOTROPIN A;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; NONHUMAN; PLACENTA VILLUS; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; UPREGULATION; WILD TYPE; ANIMAL; CELL CULTURE; CELL HYPOXIA; CULTURE MEDIUM; CYTOLOGY; FEMALE; GENE VECTOR; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY; RAT; SOLUBILITY; SWINE; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD; ANTIOXIDANTS; CARBON MONOXIDE; CELL HYPOXIA; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; GENETIC VECTORS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INTERFERON TYPE II; MICE; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; ORGANOMETALLIC COMPOUNDS; OXIDATIVE STRESS; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; RATS; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SOLUBILITY; SWINE; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 34247247725     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.106.660134     Document Type: Article

References (78)

1. Seely EW, Solomon CG. Insulin resistance and its potential role in pregnancy-induced hypertension. J Clin Endocrinol Metab. 2003;88:2393-2398.
2. Rodie VA, Freeman DJ, Sattar N, Greer IA. Pre-eclampsia and cardiovascular disease: metabolic syndrome of pregnancy? Atherosclerosis. 2004;175:189-202.
3. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
4. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592-1594.
5. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet. 2005;365:785-799.
6. Smith GC, Pell JP, Walsh D. Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet. 2001;357:2002-2006.
7. Vatten LJ, Romundstad PR, Holmen TL, Hsieh CC, Trichopoulos D, Stuver SO. Intrauterine exposure to preeclampsia and adolescent blood pressure, body size, and age at menarche in female offspring. Obstet Gynecol. 2003;101:529-533.
8. Ahmed A. Heparin-binding angiogenic growth factors in pregnancy. Trophoblast Res. 1997;10:215-258.
9. Yuan HT, Haig D, Ananth Karumanchi S. Angiogenic factors in the pathogenesis of preeclampsia. Curr Top Dev Biol. 2005;71:297-312.
10. 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.
11. Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, Blink AL, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Urinary placental growth factor and risk of preeclampsia. JAMA. 2005;293:77-85.
12. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med. 2006;355:992-1005.
13. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, Mazor M. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med. 2005;17:3-18.
14. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab. 2003;88:2348-2351.
15. Hertig A, Berkane N, Lefevre G, Toumi K, Marti HP, Capeau J, Uzan S, Rondeau E. Maternal serum sFlt1 concentration is an early and reliable predictive marker of preeclampsia. Clin Chem. 2004;50:1702-1703.
16. Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. 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. 2006;195:201-207.
17. Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, Kalluri R. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem. 2003;278:12605-12608.
18. 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.
19. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12:642-649.
20. 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.
21. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase: characterization of the enzyme. J Biol Chem. 1969;244:6388-6394.
22. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A. 1989;86:99-103.
23. Duckers HJ, Boehm M, True AL, Yet SF, San H, Park JL, Clinton Webb R, Lee ME, Nabel GJ, Nabel EG. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med. 2001;7:693-698.
24. Melo LG, Agrawal R, Zhang L, Rezvani M, Mangi AA, Ehsan A, Griese DP, Dell'Acqua G, Mann MJ, Oyama J, Yet SF, Layne MD, Perrella MA, Dzau VJ. Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation. 2002;105:602-607.
25. Katori M, Anselmo DM, Busuttil RW, Kupiec-Weglinski JW. A novel strategy against ischemia and reperfusion injury: cytoprotection with heme oxygenase system. Transpl Immunol. 2002;9:227-233.
26. Zhang X, Shan P, Jiang D, Noble PW, Abraham NG, Kappas A, Lee PJ. Small interfering RNA targeting heme oxygenase-1 enhances ischemia-reperfusion-induced lung apoptosis. J Biol Chem. 2004;279:10677-10684.
27. Tsuchihashi S, Fondevila C, Kupiec-Weglinski JW. Heme oxygenase system in ischemia and reperfusion injury. Ann Transplant. 2004;9:84-87.
28. Maines MD, Mayer RD, Ewing JF, McCoubrey WK Jr. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: possible role of heme as both promotor of tissue damage and regulator of HSP32. J Pharmacol Exp Ther. 1993;264:457-462.
29. Bainbridge SA, Smith GN. HO in pregnancy. Free Radic Biol Med. 2005;38:979-988.
30. Alexandreanu IC, Lawson DM. Effects of chronic administration of a heme oxygenase substrate or inhibitor on progression of the estrous cycle, pregnancy and lactation of Sprague-Dawley rats. Life Sci. 2002;72:153-162.
31. Zenclussen AC, Fest S, Joachim R, Klapp BF, Arck PC. Introducing a mouse model for pre-eclampsia: adoptive transfer of activated Th1 cells leads to pre-eclampsia-like symptoms exclusively in pregnant mice. Eur J Immunol. 2004;34:377-387.
32. Acevedo CH, Ahmed A. Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy. J Clin Invest. 1998;101:949-955.
33. Hendler I, Baum M, Kreiser D, Schiff E, Druzin M, Stevenson DK, Seidman DS. End-tidal breath carbon monoxide measurements are lower in pregnant women with uterine contractions. J Perinatol. 2004;24:275-278.
34. Baum M, Schiff E, Kreiser D, Dennery PA, Stevenson DK, Rosenthal T, Seidman DS. End-tidal carbon monoxide measurements in women with pregnancy-induced hypertension and preeclampsia. Am J Obstet Gynecol. 2000;183:900-903.
35. Kreiser D, Baum M, Seidman DS, Fanaroff A, Shah D, Hendler I, Stevenson DK, Schiff E, Druzin ML. End tidal carbon monoxide levels are lower in women with gestational hypertension and pre-eclampsia. J Perinatol. 2004;24:213-217.
36. 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.
37. Lash GE, McLaughlin BE, MacDonald-Goodfellow SK, Smith GN, Brien JF, Marks GS, Nakatsu K, Graham CH. Relationship between tissue damage and heme oxygenase expression in chorionic villi of term human placenta. Am J Physiol Heart Circ Physiol. 2003;284:H160-H167.
38. 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.
39. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A. Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol. 2001;159:993-1008.
40. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest. 1999;103:1047-1054.
41. Ahmad S, Hewett PW, Wang P, Al-Ani B, Cudmore M, Fujisawa T, Haigh JJ, le Noble F, Wang L, Mukhopadhyay D, Ahmed A. Direct evidence for endothelial vascular endothelial growth factor receptor-1 function in nitric oxide-mediated angiogenesis. Circ Res. 2006;99:715-722.
42. Smith G, Dawe RS, Clark C, Evans AT, Comrie MM, Wolf CR, Ferguson J, Ibbotson SH. Quantitative real-time reverse transcription-polymerase chain reaction analysis of drug metabolizing and cytoprotective genes in psoriasis and regulation by ultraviolet radiation. J Invest Dermatol. 2003;121:390-398.
43. Kweon MH, Adhami VM, Lee JS, Mukhtar H. Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem. 2006;281:33761-33772.
44. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A. 1997;94:10919-10924.
45. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A. 1997;94:10925-10930.
46. Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen: a review. Placenta. 2000;21(suppl A):S16-S24.
47. Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res. 2004;95:884-891.
48. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitalo K, Damsky C, Fisher SJ. 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. 2002;160:1405-1423.
49. Baker PN, Krasnow J, Roberts JM, Yeo KT. Elevated serum levels of vascular endothelial growth factor in patients with preeclampsia. Obstet Gynecol. 1995;86:815-821.
50. Hornig C, Barleon B, Ahmad S, Vuorela P, Ahmed A, Weich HA. Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab Invest. 2000;80:443-454.
51. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res. 2002;90:E17-E24.
52. Lain KY, Powers RW, Krohn MA, Ness RB, Crombleholme WR, Roberts JM. Urinary cotinine concentration confirms the reduced risk of preeclampsia with tobacco exposure. Am J Obstet Gynecol. 1999;181(pt 1):1192-1196.
53. Powers RW, Roberts JM, Cooper KM, Gallaher MJ, Frank MP, Harger GF, Ness RB. Maternal serum soluble fms-like tyrosine kinase 1 concentrations are not increased in early pregnancy and decrease more slowly postpartum in women who develop preeclampsia. Am J Obstet Gynecol. 2005;193:185-191.
54. England LJ, Levine RJ, Mills JL, Klebanoff MA, Yu KF, Cnattingius S. Adverse pregnancy outcomes in snuff users. Am J Obstet Gynecol. 2003;189:939-943.
55. Bainbridge SA, Belkacemi L, Dickinson M, Graham CH, Smith GN. Carbon monoxide inhibits hypoxia/reoxygenation-induced apoptosis and secondary necrosis in syncytiotrophoblast. Am J Pathol. 2006;169:774-783.
56. Appleton SD, Marks GS, Nakatsu K, Brien JF, Smith GN, Graham CH. Heme oxygenase activity in placenta: direct dependence on oxygen availability. Am J Physiol Heart Circ Physiol. 2002;282:H2055-H2059.
57. Newby D, Cousins F, Myatt L, Lyall F. Heme oxygenase expression in cultured human trophoblast cells during in vitro differentiation: effects of hypoxia. Placenta. 2005;26:201-209.
58. Hung TH, Charnock-Jones DS, Skepper JN, Burton GJ. Secretion of tumor necrosis factor-alpha from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro: a potential mediator of the inflammatory response in preeclampsia. Am J Pathol. 2004;164:1049-1061.
59. Tsuchihashi S, Livhits M, Zhai Y, Busuttil RW, Araujo JA, Kupiec-Weglinski JW. Basal rather than induced heme oxygenase-1 levels are crucial in the antioxidant cytoprotection. J Immunol. 2006;177:4749-4757.
60. Yoneyama Y, Suzuki S, Sawa R, Yoneyama K, Power GG, Araki T. Relation between adenosine and T-helper 1/T-helper 2 imbalance in women with preeclampsia. Obstet Gynecol. 2002;99:641-646.
61. Wilczynski JR, Tchorzewski H, Banasik M, Glowacka E, Wieczorek A, Lewkowicz P, Malinowski A, Szpakowski M, Wilczynski J. Lymphocyte subset distribution and cytokine secretion in third trimester decidua in normal pregnancy and preeclampsia. Eur J Obstet Gynecol Reprod Biol. 2003;109:8-15.
62. Arriaga-Pizano L, Jimenez-Zamudio L, Vadillo-Ortega F, Martinez-Flores A, Herrerias-Canedo T, Hernandez-Guerrero C. The predominant Th1 cytokine profile in maternal plasma of preeclamptic women is not reflected in the choriodecidual and fetal compartments. J Soc Gynecol Investig. 2005;12:335-342.
63. Azizieh F, Raghupathy R, Makhseed M. Maternal cytokine production patterns in women with pre-eclampsia. Am J Reprod Immunol. 2005;54:30-37.
64. Banerjee S, Smallwood A, Moorhead J, Chambers AE, Papageorghiou A, Campbell S, Nicolaides K. Placental expression of interferon-gamma (IFN-gamma) and its receptor IFN-gamma R2 fail to switch from early hypoxic to late normotensive development in preeclampsia. J Clin Endocrinol Metab. 2005;90:944-952.
65. Naldini A, Carraro F, Silvestri S, Bocci V. Hypoxia affects cytokine production and proliferative responses by human peripheral mononuclear cells. J Cell Physiol. 1997;173:335-342.
66. Kitamuro T, Takahashi K, Ogawa K, Udono-Fujimori R, Takeda K, Furuyama K, Nakayama M, Sun J, Fujita H, Hida W, Hattori T, Shirato K, Igarashi K, Shibahara S. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J Biol Chem. 2003;278:9125-9133.
67. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med. 2005;202:1703-1713.
68. Rumbold AR, Crowther CA, Haslam RR, Dekker GA, Robinson JS. Vitamins C and E and the risks of preeclampsia and perinatal complications. N Engl J Med. 2006;354:1796-1806.
69. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH. Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet. 2006;367:1145-1154.
70. Lee TS, Chang CC, Zhu Y, Shyy JY. Simvastatin induces heme oxygenase-1: a novel mechanism of vessel protection. Circulation. 2004;110:1296-1302.
71. Grosser N, Hemmerle A, Berndt G, Erdmann K, Hinkelmann U, Schurger S, Wijayanti N, Immenschuh S, Schroder H. The antioxidant defense protein heme oxygenase 1 is a novel target for statins in endothelial cells. Free Radic Biol Med. 2004;37:2064-2071.
72. Kodama Y, Kitta Y, Nakamura T, Takano H, Umetani K, Fujioka D, Saito Y, Kawabata K, Obata JE, Mende A, Kobayashi T, Kugiyama K. Atorvastatin increases plasma soluble Fms-like tyrosine kinase-1 and decreases vascular endothelial growth factor and placental growth factor in association with improvement of ventricular function in acute myocardial infarction. J Am Coll Cardiol. 2006;48:43-50.
73. Minsker DH, MacDonald JS, Robertson RT, Bokelman DL. Mevalonate supplementation in pregnant rats suppresses the teratogenicity of mevinolinic acid, an inhibitor of 3-hydroxy-3-methylglutaryl-coenzyme a reductase. Teratology. 1983;28:449-456.
74. Freyssinges C, Ducrocq MB. Simvastatin and pregnancy [in French]. Therapie. 1996;51:537-542.
75. Gibb H, Scialli AR. Statin drugs and congenital anomalies. Am J Med Genet A. 2005;135:230-231.
76. Manson JM, Freyssinges C, Ducrocq MB, Stephenson WP. Postmarketing surveillance of lovastatin and simvastatin exposure during pregnancy. Reprod Toxicol. 1996;10:439-446.
77. Pollack PS, Shields KE, Burnett DM, Osborne MJ, Cunningham ML, Stepanavage ME. Pregnancy outcomes after maternal exposure to simvastatin and lovastatin. Birth Defects Res A Clin Mol Teratol. 2005;73:888-896.
78. Wang YP, Yu YH. Expression of endogenous heme oxygenase on surface of placental trophoblasts of pregnant women with intrauterine growth retardation of the fetus. Di Yi Jun Yi Da Xue Xue Bao. 2002;22:637-639.