Heme oxygenase-1 is not decreased in preeclamptic placenta and does not negatively regulate placental soluble fms-like tyrosine kinase-1 or soluble endoglin secretion

Hypertension

Volumn 66, Issue 5, 2015, Pages 1073-1081

  Tong, Stephen ^a   Kaitu'u Lino, Tu'uhevaha J ^a   Onda, Kenji ^a,b   Beard, Sally ^a   Hastie, Roxanne ^a   Binder, Natalie K ^a   Cluver, Cathy ^a,c   Tuohey, Laura ^a   Whitehead, Clare ^a   Brownfoot, Fiona ^a   De Silva, Manarangi ^a   Hannan, Natalie J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

FLT1 protein, human; heme oxygenase 1; placenta; preeclampsia; pregnancy

Indexed keywords

ENDOGLIN; FUMARIC ACID DIMETHYL ESTER; HEME OXYGENASE 1; MESSENGER RNA; PLACENTA PROTEIN; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN TIN; ROSIGLITAZONE; SOLUBLE FMS LIKE TYROSINE KINASE 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN;

ADULT; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CLINICAL ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; EXPLANT; FEMALE; GENE SILENCING; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; PLACENTA; PLACENTA TISSUE; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SYNCYTIOTROPHOBLAST; TROPHOBLAST; UMBILICAL CORD; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING; CASE CONTROL STUDY; CELL CULTURE; CYTOLOGY; ENDOTHELIUM; METABOLISM; PREGNANCY; TISSUE CULTURE TECHNIQUE;

ANTIGENS, CD; CASE-CONTROL STUDIES; CELLS, CULTURED; ENDOTHELIUM; FEMALE; GESTATIONAL AGE; HEME OXYGENASE-1; HUMANS; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, CELL SURFACE; RNA, MESSENGER; TISSUE CULTURE TECHNIQUES; TROPHOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84943383659     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.05847     Document Type: Article

References (35)

1. Sibai B, Dekker G, Kupferminc M., Pre-eclampsia. Lancet 2005 365 785 799. doi: 10.1016/S0140-6736(05)17987-2
2. Young BC, Levine RJ, Karumanchi SA., Pathogenesis of preeclampsia. Annu Rev Pathol 2010 5 173 192. doi: 10.1146/annurev-pathol-121808-102149
3. 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. doi: 10.1056/NEJMoa031884
4. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA, CPEP Study Group Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006 355 992 1005. doi: 10.1056/NEJMoa055352
5. 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. doi: 10.1172/JCI17189
6. Venkatesha S, Toporsian M, Lam C, Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006 12 642 649. doi: 10.1038/nm1429
7. Gozzelino R, Jeney V, Soares MP., Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010 50 323 354. doi: 10.1146/annurev.pharmtox.010909.105600
8. Leinonen HM, Kansanen E, Pölönen P, Heinäniemi M, Levonen AL., Role of the Keap1-Nrf2 pathway in cancer. Adv Cancer Res 2014 122 281 320. doi: 10.1016/B978-0-12-420117-0.00008-6
9. Anuranjani, Bala M., Concerted action of Nrf2-ARE pathway, MRN complex, HMGB1 and inflammatory cytokines-implication in modification of radiation damage. Redox biology 2014 2 832 846. doi: 10.1016/j.redox.2014.02.008
10. Koskenkorva-Frank TS, Weiss G, Koppenol WH, Burckhardt S., The complex interplay of iron metabolism, reactive oxygen species, and reactive nitrogen species: insights into the potential of various iron therapies to induce oxidative and nitrosative stress. Free Radic Biol Med 2013 65 1174 1194. doi: 10.1016/j.freeradbiomed.2013.09.001
11. 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. doi: 10.1161/CIRCULATIONAHA.106.660134
12. Robillard PY, Dekker G, Chaouat G., Fourteen years of debate and workshops on the immunology of preeclampsia. Where are we now after the 2012 workshop? J Reprod Immunol 2014 101-102 62 69. doi: 10.1016/j.jri.2013.06.003
13. Ahmed A., New insights into the etiology of preeclampsia: identification of key elusive factors for the vascular complications. Thromb Res 2011 127 Suppl 3 S72 S75. doi: 10.1016/S0049-3848(11)70020-2
14. Levytska K, Kingdom J, Baczyk D, Drewlo S., Heme oxygenase-1 in placental development and pathology. Placenta 2013 34 291 298. doi: 10.1016/j.placenta.2013.01.004
15. Powe CE, Levine RJ, Karumanchi SA., Preeclampsia, a disease of the maternal endothelium: The role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 2011 123 2856 2869. doi: 10.1161/CIRCULATIONAHA.109.853127
16. Mutter WP, Karumanchi SA., Molecular mechanisms of preeclampsia. Microvasc Res 2008 75 1 8. doi: 10.1016/j.mvr.2007.04.009
17. Wang A, Rana S, Karumanchi SA., Preeclampsia: The role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 2009 24 147 158. doi: 10.1152/physiol.00043.2008
18. Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, Dulak J., Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2008 10 1767 1812. doi: 10.1089/ars.2008.2043
19. Gu Y, Lewis DF, Wang Y., Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008 93 260 266. doi: 10.1210/jc.2007-1550
20. Zhou CC, Ahmad S, Mi T, Abbasi S, Xia L, Day MC, Ramin SM, Ahmed A, Kellems RE, Xia Y., Autoantibody from women with preeclampsia induces soluble Fms-like tyrosine kinase-1 production via angiotensin type 1 receptor and calcineurin/nuclear factor of activated T-cells signaling. Hypertension 2008 51 1010 1019. doi: 10.1161/HYPERTENSIONAHA.107.097790
21. Silasi M, Cohen B, Karumanchi SA, Rana S., Abnormal placentation, angiogenic factors, and the pathogenesis of preeclampsia. Obstet Gynecol Clin North Am 2010 37 239 253. doi: 10.1016/j.ogc.2010.02.013
22. Ramma W, Ahmed A., Therapeutic potential of statins and the induction of heme oxygenase-1 in preeclampsia. J Reprod Immunol 2014 101-102 153 160. doi: 10.1016/j.jri.2013.12.120
23. 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
24. Chigusa Y, Tatsumi K, Kondoh E, Fujita K, Nishimura F, Mogami H, Konishi I., Decreased lectin-like oxidized LDL receptor 1 (LOX-1) and low Nrf2 activation in placenta are involved in preeclampsia. J Clin Endocrinol Metab 2012 97 E1862 E1870. doi: 10.1210/jc.2012-1268
25. American College of Obstetricians and Gynecologists; Task force on Hypertension in Pregnancy Hypertension in Pregnancy. 2013. http://www.acog.org/Resources-And-Publications/Task-Force-and-Work-Group-Reports/Hypertension-in-Pregnancy. Accessed September 1, 2014
26. Kaitu'u-Lino TJ, Tong S, Beard S, Hastie R, Tuohey L, Brownfoot F, Onda K, Hannan NJ., Characterization of protocols for primary trophoblast purification, optimized for functional investigation of sFlt-1 and soluble endoglin. Pregnancy Hypertens 2014 4 287 295. doi: 10.1016/j.preghy.2014.09.003
27. Whale AS, Huggett JF, Cowen S, Speirs V, Shaw J, Ellison S, Foy CA, Scott DJ., Comparison of microfluidic digital PCR and conventional quantitative PCR for measuring copy number variation. Nucleic Acids Res 2012 40 e82. doi: 10.1093/nar/gks203
28. Jebbink J, Keijser R, Veenboer G, Van der Post J, Ris-Stalpers C, Afink G., Expression of placental FLT1 transcript variants relates to both gestational hypertensive disease and fetal growth. Hypertension 2011 58 70 76. doi: 10.1161/HYPERTENSIONAHA.110.164079
29. 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
30. Onda K, Tong S, Nakahara A, Kondo M, Monchusho H, Hirano T, Kaitu'u-Lino T, Beard S, Binder N, Tuohey L, Brownfoot F, Hannan NJ., Sofalcone upregulates the nuclear factor (erythroid-derived 2)-like 2/heme oxygenase-1 pathway, reduces soluble fms-like tyrosine kinase-1, and quenches endothelial dysfunction: potential therapeutic for preeclampsia. Hypertension 2015 65 855 862. doi: 10.1161/HYPERTENSIONAHA.114.04781
31. Brownfoot F, Hannan N, Binder N, Walker S, Cannon P, Hastie R, Onda K, Kaitu'u-Lino T., Effects of pravastatin on human placenta, endothelium, and women with severe preeclampsia [Epub ahead of print]. Hypertension 2015 66 687 697. doi: 10.1161/HYPERTENSIONAHA.115.05445
32. Roberts JM, Redman CW., Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 1993 341 1447 1451
33. 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. doi: 10.1002/path.2946
34. Linzke N, Schumacher A, Woidacki K, Croy BA, Zenclussen AC., Carbon monoxide promotes proliferation of uterine natural killer cells and remodeling of spiral arteries in pregnant hypertensive heme oxygenase-1 mutant mice. Hypertension 2014 63 580 588. doi: 10.1161/HYPERTENSIONAHA.113.02403
35. Zenclussen ML, Linzke N, Schumacher A, Fest S, Meyer N, Casalis PA, Zenclussen AC., Heme oxygenase-1 is critically involved in placentation, spiral artery remodeling, and blood pressure regulation during murine pregnancy. Front Pharmacol 2014 5 291. doi: 10.3389/fphar.2014.00291