Heme oxygenase-1 attenuates hypoxia-induced sFlt-1 and oxidative stress in placental villi through its metabolic products CO and bilirubin

International Journal of Hypertension

Volumn 2012, Issue , 2012, Pages

  George, Eric M ^a   Colson, Drew ^a   Dixon, Jeremy ^a   Palei, Ana C ^a   Granger, Joey P ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; CARBON MONOXIDE; HEME OXYGENASE 1; PROTEIN TYROSINE KINASE; SOLUBLE FMS LIKE TYROSINE KINASE 1; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ATTENUATION; CHORION VILLUS; CONTROLLED STUDY; ENZYME SYNTHESIS; EXPLANT; FEMALE; HYPOXIA; METABOLITE; NONHUMAN; OXIDATIVE STRESS; PLACENTA CIRCULATION; PREECLAMPSIA; PRIORITY JOURNAL; RAT;

EID: 84857882767     PISSN: 20900384     EISSN: 20900392     Source Type: Journal    
DOI: 10.1155/2012/486053     Document Type: Article

References (43)

1. Roberts J. M., Cooper D. W., Pathogenesis and genetics of pre-eclampsia. Lancet 2001 357 9249 53 56 2-s2.0-0035814640 10.1016/S0140-6736(00)03577-7 (Pubitemid 32056505)
2. Roberts J. M., Pearson G., Cutler J., Lindheimer M., Summary of the NHLBI Working Group on research on hypertension during pregnancy. Hypertension 2003 41 3 437 445 2-s2.0-0037341925 10.1161/01.HYP.0000054981.03589.E9 (Pubitemid 36314613)
3. Lim K. H., Zhou Y., Janatpour M., McMaster M., Bass K., Chun S. H., Fisher S. J., Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. American Journal of Pathology 1997 151 6 1809 1818 2-s2.0-0030725043 (Pubitemid 27527944)
4. Brosens I. A., Robertson W. B., Dixon H. G., The role of the spiral arteries in the pathogenesis of preeclampsia. Obstetrics and Gynecology Annual 1972 1 177 191 2-s2.0-0015484546
5. Khong Y., Brosens I., ivo.brosens@med.kuleuven.ac.be Defective deep placentation. Best Practice and Research: Clinical Obstetrics and Gynaecology 2011 25 3 301 311 10.1016/j.bpobgyn.2010.10.012
6. Roberts J. M., Taylor R. N., Musci T. J., Rodgers G. M., Hubel C. A., McLaughlin M. K., Preeclampsia: an endothelial cell disorder. American Journal of Obstetrics and Gynecology 1989 161 5 1200 1204 2-s2.0-0024398644 (Pubitemid 20007682)
7. Gilbert J. S., Ryan M. J., Lamarca B. B., Sedeek M., Murphy S. R., Granger J. P., Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. American Journal of Physiology 2008 294 2 H541 H550 2-s2.0-39149111944 10.1152/ajpheart.01113.2007 (Pubitemid 351253261)
8. Ballermann B. J., Glomerular endothelial cell differentiation. Kidney International 2005 67 5 1668 1671 2-s2.0-17744387572 10.1111/j.1523-1755.2005. 00260.x (Pubitemid 40577697)
9. Wu F. T. H., Stefanini M. O., Gabhann F. M., Kontos C. D., Annex B. H., Popel A. S., A systems biology perspective on sVEGFR1: its biological function, pathogenic role and therapeutic use. Journal of Cellular and Molecular Medicine 2010 14 3 528 552 2-s2.0-77952593669 10.1111/j.1582-4934.2009.00941.x
10. Nagamatsu T., Fujii T., Kusumi M., Zou L., Yamashita T., Osuga Y., Momoeda M., Kozuma S., Taketani Y., Cytotrophoblasts up-regulate soluble Fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004 145 11 4838 4845 2-s2.0-9244257290 10.1210/en.2004-0533 (Pubitemid 39551100)
11. Ahmad S., Ahmed A., Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circulation Research 2004 95 9 884 891 2-s2.0-7244238090 10.1161/01.RES.0000147365.86159.f5 (Pubitemid 39435003)
12. Nevo O., Soleymanlou N., Wu Y., Xu J., Kingdom J., Many A., Zamudio S., Caniggia I., Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. American Journal of Physiology 2006 291 4 R1085 R1093 2-s2.0-33749316052 10.1152/ajpregu.00794.2005 (Pubitemid 44498450)
13. Levine R. J., Lam C., Qian C., Yu K. F., Maynard S. E., Sachs B. P., Sibai B. M., Epstein F. H., Romero R., Thadhani R., Karumanchi S. A., Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. New England Journal of Medicine 2006 355 10 992 1005 2-s2.0-33748421660 10.1056/NEJMoa055352 (Pubitemid 44343543)
14. Levine R. J., Maynard S. E., Qian C., Lim K. H., England L. J., Yu K. F., Schisterman E. F., Thadhani R., Sachs B. P., Epstein F. H., Sibai B. M., Sukhatme V. P., Karumanchi S. A., Circulating angiogenic factors and the risk of preeclampsia. New England Journal of Medicine 2004 350 7 672 683 2-s2.0-10744227199 10.1056/NEJMoa031884 (Pubitemid 38364626)
15. Maynard S. E., Min J. Y., Merchan J., Lim K. H., Li J., Mondal S., Libermann T. A., Morgan J. P., Sellke F. W., Stillman I. E., Epstein F. H., Sukhatme V. P., Karumanchi S. A., Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction hypertension, and proteinuria in preeclampsia. Journal of Clinical Investigation 2003 111 5 649 658 2-s2.0-0037373006 10.1172/JCI200317189 (Pubitemid 36278583)
16. Gilbert J. S., Babcock S. A., Granger J. P., Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 2007 50 6 1142 1147 2-s2.0-36448996940 10.1161/HYPERTENSIONAHA.107.096594 (Pubitemid 350172938)
17. 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 International 2007 71 10 977 984 2-s2.0-34248341332 10.1038/sj.ki.5002175 (Pubitemid 46741987)
18. Murphy S. R., Lamarca B. B. D., Cockrell K., Granger J. P., Role of endothelin in mediating soluble fms-like tyrosine kinase 1-induced hypertension in pregnant rats. Hypertension 2010 55 2 394 398 2-s2.0-74949098555 10.1161/HYPERTENSIONAHA.109.141473
19. Hung T. H., Skepper J. N., Charnock-Jones D. S., Burton G. J., Hypoxia-reoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia. Circulation Research 2002 90 12 1274 1281 2-s2.0-0037188944 10.1161/01.RES.0000024411.22110.AA (Pubitemid 34787409)
20. Staff A. C., Ranheim T., Khoury J., Henriksen T., Increased contents of phospholipids, cholesterol, and lipid peroxides in decidua basalis in women with preeclampsia. American Journal of Obstetrics and Gynecology 1999 180 3 587 592 2-s2.0-0032981268 10.1016/S0002-9378(99)70259-0 (Pubitemid 29149132)
21. Roggensack A. M., Zhang Y., Davidge S. T., Evidence for peroxynitrite formation in the vasculature of women with preeclampsia. Hypertension 1999 33 1 83 89 2-s2.0-0032891903 (Pubitemid 29061846)
22. Sedeek M., Gilbert J. S., Lamarca B. B., Sholook M., Chandler D. L., Wang Y., Granger J. P., Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. American Journal of Hypertension 2008 21 10 1152 1156 2-s2.0-52449116800 10.1038/ajh.2008.239
23. Sedeek M. H., Wang Y., Granger J. P., Increased oxidative stress in a rat model of preeclampsia. American Journal of Hypertension 2004 17 Issue 5, supplement S142
24. Neuzil J., Stocker R., Bilirubin attenuates radical-mediated damage to serum albumin. FEBS Letters 1993 331 3 281 284 2-s2.0-0027490428 10.1016/0014-5793(93)80353-V (Pubitemid 23287288)
25. Neuzil J., Stocker R., Free and albumin-bound bilirubin are efficient co-antioxidants for α-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. Journal of Biological Chemistry 1994 269 24 16712 16719 2-s2.0-0028239795
26. Wu L., Wang R., Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacological Reviews 2005 57 4 585 630 2-s2.0-29844442868 10.1124/pr.57.4.3 (Pubitemid 43036442)
27. Cudmore M., Ahmad S., Al-Ani B., Fujisawa T., Coxall H., Chudasama K., Devey L. R., Wigmore S. J., Abbas A., Hewett P. W., Ahmed A., Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007 115 13 1789 1797 2-s2.0-34247247725 10.1161/CIRCULATIONAHA.106. 660134 (Pubitemid 46648616)
28. George E. M., Cockrell K., Aranay M., Csongradi E., Stec D. E., Granger J. P., jgranger@umc.edu Induction of heme oxygenase 1 attenuates placental ischemia-induced hypertension. Hypertension 2011 57 5 941 948 10.1161/HYPERTENSIONAHA.111.169755
29. George E. M., Cockrell K., Adair T. H., Granger J. P., Regulation of sFlt-1 and VEGF secretion by adenosine under hypoxic conditions in rat placental villous explants. American Journal of Physiology 2010 299 6 R1629 R1633 2-s2.0-78649873524 10.1152/ajpregu.00330.2010
30. Caniggia I., Taylor C. V., Ritchie J. W. K., Lye S. J., Letarte M., Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 1997 138 11 4977 4988 2-s2.0-0030778822 10.1210/en.138.11.4977 (Pubitemid 27460938)
31. Clark J. E., Naughton P., Shurey S., Green C. J., Johnson T. R., Mann B. E., Foresti R., Motterlini R., Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circulation research 2003 93 2 e2 e8 2-s2.0-0041733077
32. Rudolph C., Adam G., Simm A., Determination of copy number of c-Myc protein per cell by quantitative Western blotting. Analytical Biochemistry 1999 269 1 66 71 2-s2.0-0033541670 10.1006/abio.1999.3095 (Pubitemid 29174263)
33. Peshavariya H. M., Dusting G. J., Selemidis S., Analysis of dihydroethidium fluorescence for the detection of intracellular and extracellular superoxide produced by NADPH oxidase. Free Radical Research 2007 41 6 699 712 2-s2.0-34249789273 10.1080/10715760701297354 (Pubitemid 46845591)
34. Walker J. J., Pre-eclampsia. Lancet 2000 356 9237 1260 1265 2-s2.0-0034619029
35. Zandi-Nejad K., Luyckx V. A., Brenner B. M., Adult hypertension and kidney disease: the role of fetal programming. Hypertension 2006 47 3 502 508 2-s2.0-33644983131 10.1161/01.HYP.0000198544.09909.1a (Pubitemid 43843866)
36. Cao J., Inoue K., Li X., Drummond G., Abraham N. G., Physiological significance of heme oxygenase in hypertension. International Journal of Biochemistry and Cell Biology 2009 41 5 1025 1033 2-s2.0-59649087087 10.1016/j.biocel.2008.10.025
37. Botros F. T., Schwartzman M. L., Stier C. T., Goodman A. I., Abraham N. G., Increase in heme oxygenase-1 levels ameliorates renovascular hypertension. Kidney International 2005 68 6 2745 2755 2-s2.0-32844464040 10.1111/j.1523-1755. 2005.00745.x (Pubitemid 43251019)
38. Sabaawy H. E., Zhang F., Nguyen X., ElHosseiny A., Nasjletti A., Schwartzman M., Dennery P., Kappas A., Abraham N. G., Human heme oxygenase-1 gene transfer lowers blood pressure and promotes growth in spontaneously hypertensive rats. Hypertension 2001 38 2 210 215 2-s2.0-0035569053 (Pubitemid 34224746)
39. Yang L., Quan S., Nasjletti A., Laniado-Schwartzman M., Abraham N. G., Heme oxygenase-1 gene expression modulates angiotensin II-induced increase in blood pressure. Hypertension 2004 43 6 1221 1226 2-s2.0-2542434044 10.1161/01.HYP.0000126287.62060.e6 (Pubitemid 38691743)
40. Morita T., Kourembanas S., Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. Journal of Clinical Investigation 1995 96 6 2676 2682 2-s2.0-0028838293
41. Panchenko M. V., Farber H. W., Korn J. H., Induction of heme oxygenase-1 by hypoxia and free radicals in human dermal fibroblasts. American Journal of Physiology 2000 278 1 C92 C101 2-s2.0-0033952364 (Pubitemid 30101899)
42. Motterlini R., Foresti R., Bassi R., Calabrese V., Clark J. E., Green C. J., Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. Journal of Biological Chemistry 2000 275 18 13613 13620 2-s2.0-0034607632 10.1074/jbc.275.18.13613 (Pubitemid 30257429)
43. Carraway M. S., Ghio A. J., Carter J. D., Piantadosi C. A., Expression of heme oxygenase-1 in the lung in chronic hypoxia. American Journal of Physiology 2000 278 4 L806 L812 2-s2.0-0034058383 (Pubitemid 30220042)