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

Volumn 65, Issue 4, 2015, Pages 855-862

  Onda, Kenji ^a,b   Tong, Stephen ^a   Nakahara, Anzu ^b   Kondo, Mei ^b   Monchusho, Hideaki ^b   Hirano, Toshihiko ^b   Kaitu'u Lino, Tu'uhevaha ^a   Beard, Sally ^a   Binder, Natalie ^a   Tuohey, Laura ^a   Brownfoot, Fiona ^a   Hannan, Natalie J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

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

Author keywords

heme oxygenase 1; preeclampsia; sFLT 1 protein, human; sofalcone

Indexed keywords

ENDOGLIN; ENDOTHELIN 1; ERYTHROID DERIVED 2 LIKE NUCLEAR FACTOR; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE CYSTEINE LIGASE CATALYTIC SUBUNIT; HEME OXYGENASE 1; MESSENGER RNA; NAD(P)H QUINONE ACCEPTOR OXIDOREDUCTASE 1; NUCLEAR FACTOR; OXIDOREDUCTASE; PROTEIN TYROSINE KINASE; PROTOPORPHYRIN COBALT; SOFALCONE; SOLUBLE ENDOGLIN; SOLUBLE FMS LIKE TYROSINE KINASE 1; THIOREDOXIN; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; CHALCONE DERIVATIVE; RNA; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ARTICLE; CELL ADHESION; CELL ISOLATION; CELL VIABILITY; CELL VIABILITY ASSAY; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MONOCYTE; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSACTIVATION; TROPHOBLAST; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; FEMALE; GENETICS; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PRE-ECLAMPSIA; PREGNANCY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CHALCONES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEME OXYGENASE-1; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PRE-ECLAMPSIA; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TROPHOBLASTS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84929130226     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.04781     Document Type: Article

References (38)

1. Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R. Pre-eclampsia. Lancet. 2010; 376: 631-644. doi: 10.1016/S0140-6736(10)60279-6
2. 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
3. Venkatesha S, Toporsian M, Lam C, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006; 12: 642-649. doi: 10.1038/nm1429
4. 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
5. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev. 2008; 60: 79-127. doi: 10.1124/pr.107.07104
6. Suzuki T, Motohashi H, Yamamoto M. Toward clinical application of the Keap1-Nrf2 pathway. Trends Pharmacol Sci. 2013; 34: 340-346. doi: 10.1016/j.tips.2013.04.005
7. 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
8. 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
9. Matsuo Y, Seki A, Yakabi K, Saziki R, Arai I, Isobe Y, Aihara H. Effect of 2'-carboxymethoxy-4,4'-bis(3-methyl-2-butenyloxy)chalcone (SU-88) on gastric local blood flow. Arzneimittelforschung. 1983; 33: 242-243
10. Murakami S, Yamada H, Muramatsu M, Aihara H, Suwa T, Kishimoto S, Mori Y. Effect of sofalcone on gastric mucous glycoprotein in experimental gastritis induced by sodium taurocholate. Res Commun Chem Pathol Pharmacol. 1988; 62: 461-482
11. Shibuya A, Onda K, Kawahara H, Uchiyama Y, Nakayama H, Omi T, Nagaoka M, Matsui H, Hirano T. Sofalcone, a gastric mucosa protective agent, increases vascular endothelial growth factor via the Nrf2-heme-oxygenase-1 dependent pathway in gastric epithelial cells. Biochem Biophys Res Commun. 2010; 398: 581-584. doi: 10.1016/j. bbrc.2010.06.124
12. Kaitu'u-Lino TJ, Hastie R, Cannon P, Lee S, Stock O, Hannan NJ, Hiscock R, Tong S. Stability of absolute copy number of housekeeping genes in preeclamptic and normal placentas, as measured by digital PCR. Placenta. 2014; 35: 1106-1109. doi: 10.1016/j.placenta.2014.10.003
13. Drewlo S, Levytska K, Kingdom J. Revisiting the housekeeping genes of human placental development and insufficiency syndromes. Placenta. 2012; 33: 952-954. doi: 10.1016/j.placenta.2012.09.007
14. Fraser R, Whitley GS, Johnstone AP, Host AJ, Sebire NJ, Thilaganathan B, Cartwright JE. Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J Pathol. 2012; 228: 322-332. doi: 10.1002/path.4057
15. Sunderland NS, Thomson SE, Heffernan SJ, Lim S, Thompson J, Ogle R, McKenzie P, Kirwan PJ, Makris A, Hennessy A. Tumor necrosis factor α induces a model of preeclampsia in pregnant baboons (Papio hamadryas). Cytokine. 2011; 56: 192-199. doi: 10.1016/j.cyto.2011.06.003
16. Cindrova-Davies T, Sanders DA, Burton GJ, Charnock-Jones DS. Soluble FLT1 sensitizes endothelial cells to inflammatory cytokines by antagonizing VEGF receptor-mediated signalling. Cardiovasc Res. 2011; 89: 671-679. doi: 10.1093/cvr/cvq346
17. Warrington JP, George EM, Palei AC, Spradley FT, Granger JP. Recent advances in the understanding of the pathophysiology of preeclampsia. Hypertension. 2013; 62: 666-673. doi: 10.1161/HYPERTENSIONAHA.113.00588
18. 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
19. George EM, Granger JP. Heme oxygenase in pregnancy and preeclampsia. Curr Opin Nephrol Hypertens. 2013; 22: 156-162. doi: 10.1097/MNH.0b013e32835d19f7
20. Tanaka H, Nakamura S, Onda K, Tazaki T, Hirano T. Sofalcone, an antiulcer chalcone derivative, suppresses inflammatory crosstalk between macrophages and adipocytes and adipocyte differentiation: implication of heme-oxygenase-1 induction. Biochem Biophys Res Commun. 2009; 381: 566-571. doi: 10.1016/j.bbrc.2009.02.086
21. Ahmed A, Cudmore MJ. Can the biology of VEGF and haem oxygenases help solve pre-eclampsia?. Biochem Soc Trans. 2009; 37: 1237-1242
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. 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. doi: 10.1155/2012/486053
24. Dickinson DA, Levonen AL, Moellering DR, Arnold EK, Zhang H, Darley-Usmar VM, Forman HJ. Human glutamate cysteine ligase gene regulation through the electrophile response element. Free Radic Biol Med. 2004; 37: 1152-1159. doi: 10.1016/j.freeradbiomed.2004.06.011
25. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol. 2010; 80: 1895-1903. doi: 10.1016/j.bcp.2010.07.014
26. Hawkes HJ, Karlenius TC, Tonissen KF. Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements. Biochim Biophys Acta. 2014; 1840: 303-314. doi: 10.1016/j.bbagen.2013.09.013
27. Dinkova-Kostova AT, Talalay P. NAD(P)H: quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys. 2010; 501: 116-123. doi: 10.1016/j.abb.2010.03.019
28. Kim YC, Masutani H, Yamaguchi Y, Itoh K, Yamamoto M, Yodoi J. Hemin-induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors. J Biol Chem. 2001; 276: 18399-18406. doi: 10.1074/jbc. M100103200
29. Sahlin L, Ostlund E, Wang H, Holmgren A, Fried G. Decreased expression of thioredoxin and glutaredoxin in placentae from pregnancies with pre-eclampsia and intrauterine growth restriction. Placenta. 2000; 21: 603-609. doi: 10.1053/plac.2000.0554
30. Vanderlelie J, Venardos K, Clifton VL, Gude NM, Clarke FM, Perkins AV. Increased biological oxidation and reduced anti-oxidant enzyme activity in pre-eclamptic placentae. Placenta. 2005; 26: 53-58. doi: 10.1016/j. placenta.2004.04.002
31. Kweider N, Fragoulis A, Rosen C, Pecks U, Rath W, Pufe T, Wruck CJ. Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): implications for preeclampsia. J Biol Chem. 2011; 286: 42863-42872. doi: 10.1074/jbc.M111.286880
32. Gutkowska J, Granger JP, Lamarca BB, Danalache BA, Wang D, Jankowski M. Changes in cardiac structure in hypertension produced by placental ischemia in pregnant rats: effect of tumor necrosis factor blockade. J Hypertens. 2011; 29: 1203-1212. doi: 10.1097/HJH.0b013e3283468392
33. Hannan NJ, Paiva P, Dimitriadis E, Salamonsen LA. Models for study of human embryo implantation: choice of cell lines?. Biol Reprod. 2010; 82: 235-245. doi: 10.1095/biolreprod.109.077800
34. Kaitu'u-Lino TJ, Tong S, Beard S, Hastie R, Tuohey T, 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
35. Yamada T, Tanaka Y, Nakane S, Sasajima M, Ohzeki M. Reproduction studies of 2'-carboxymethoxy-4,4'-bis(3-methyl-2-butenyloxy)chalcone (1) fertility study in rats. Pharmacometrics. 1980; 19: 515-523
36. Yamada T, Tanaka Y, Hosoda K, Nakane S, Sasajima M, Ohzeki M. Reproduction studies of 2'-carboxymethoxy-4,4'-bis(3-methyl-2-butenyloxy) chalcone (2) teratogenicity study in rats. Pharmacometrics. 1980; 19: 525-535
37. Yamada T, Tanaka Y, Suzuki H, Nogariya T, Nakane S, Sasajima M, Ohzeki M. Reproduction studies of 2'-carboxymethoxy-4,4'-bis(3-methyl-2-butenyloxy)chalcone (4) perinatal and postnatal study in rats. Pharmacometrics. 1980; 19: 543-553
38. Yamada T, Tanaka Y, Nogariya T, Nakane S, Sasajima M, Ohzeki M. Reproduction studies of 2'-carboxymethoxy-4,4'-bis(3-methyl-2-butenyloxy) chalcone (3) teratogenicity study in rabbits. Pharmacometrics. 1980; 19: 537-542