A Role for Nrf2 in Redox Signalling of the Invasive Extravillous Trophoblast in Severe Early Onset IUGR Associated with Preeclampsia

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Kweider, Nisreen ^a   Huppertz, Berthold ^b   Wruck, Christoph Jan ^a   Beckmann, Rainer ^a   Rath, Werner ^c   Pufe, Thomas ^a   Kadyrov, Mamed ^a,d  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d MEDIAN Kliniken   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; CYTOKERATIN 7; PARAFFIN; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN;

ADULT; ARTICLE; CELL INVASION; CESAREAN SECTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; CYTOTROPHOBLAST; DISEASE ASSOCIATION; DISEASE SEVERITY; ENDOMETRIUM; FEMALE; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYSTERECTOMY; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; LEYDIG CELL; MYOMETRIUM; ONSET AGE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PLACENTA CIRCULATION; PREECLAMPSIA; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TROPHOBLAST;

ADULT; FEMALE; FETAL GROWTH RETARDATION; HUMANS; IMMUNOHISTOCHEMISTRY; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; PRE-ECLAMPSIA; PREGNANCY; TROPHOBLASTS; UTERUS;

EID: 84867307268     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047055     Document Type: Article

References (48)

1. Myatt L, (1992) Control of vascular resistance in the human placenta. Placenta 13: 329-341.
2. Pijnenborg R, Bland JM, Robertson WB, Brosens I, (1983) Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4: 397-413.
3. Pijnenborg R, Dixon G, Robertson WB, Brosens I, (1980) Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1: 3-19.
4. Huppertz B, (2003) Extravillous trophoblast: proliferation and invasion during pregnancy. Pathologica 95: 231-232.
5. Kaufmann P, Black S, Huppertz B, (2003) Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69: 1-7.
6. Pijnenborg R, Vercruysse L, Brosens I, (2011) Deep placentation. Best Pract Res Clin Obstet Gynaecol 25: 273-285.
7. Burton GJ, Woods AW, Jauniaux E, Kingdom JC, (2009) Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30: 473-482.
8. Schiessl B, Innes BA, Bulmer JN, Otun HA, Chadwick TJ, et al. (2009) Localization of angiogenic growth factors and their receptors in the human placental bed throughout normal human pregnancy. Placenta 30: 79-87.
9. Fretts RC, Boyd ME, Usher RH, Usher HA, (1992) The changing pattern of fetal death, 1961-1988. Obstet Gynecol 79: 35-39.
10. Kadyrov M, Schmitz C, Black S, Kaufmann P, Huppertz B, (2003) Pre-eclampsia and maternal anaemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast. Placenta 24: 540-548.
11. Kadyrov M, Kingdom JC, Huppertz B, (2006) Divergent trophoblast invasion and apoptosis in placental bed spiral arteries from pregnancies complicated by maternal anemia and early-onset preeclampsia/intrauterine growth restriction. Am J Obstet Gynecol 194: 557-563.
12. Huppertz B, Peeters LL, (2005) Vascular biology in implantation and placentation. Angiogenesis 8: 157-167.
13. Roberts JM, Redman CW, (1993) Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 341: 1447-1451.
14. Huppertz B, (2008) Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 51: 970-975.
15. Maynard SE, Min JY, Merchan J, Lim KH, Li J, et al. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658.
16. Kulkarni AV, Mehendale SS, Yadav HR, Kilari AS, Taralekar VS, et al. (2010) Circulating angiogenic factors and their association with birth outcomes in preeclampsia. Hypertens Res 33: 561-567.
17. Sitras V, Paulssen RH, Gronaas H, Leirvik J, Hanssen TA, et al. (2009) Differential placental gene expression in severe preeclampsia. Placenta 30: 424-433.
18. Majima HJ, Nakanishi-Ueda T, Ozawa T, (2002) 4-hydroxy-2-nonenal (4-HNE) staining by anti-HNE antibody. Methods Mol Biol 196: 31-34.
19. Poli G, Schaur RJ, Siems WG, Leonarduzzi G, (2008) 4-hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med Res Rev 28: 569-631.
20. Hung TH, Skepper JN, Burton GJ, (2001) In vitro ischemia-reperfusion injury in term human placenta as a model for oxidative stress in pathological pregnancies. Am J Pathol 159: 1031-1043.
21. Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, et al. (2007) Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol 171: 1168-1179.
22. Lee JM, Johnson JA, (2004) An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37: 139-143.
23. Wruck CJ, Fragoulis A, Gurzynski A, Brandenburg LO, Kan YW, et al. (2011) Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis 70: 844-850.
24. Wruck CJ, Gotz ME, Herdegen T, Varoga D, Brandenburg LO, et al. (2008) Kavalactones protect neural cells against amyloid beta peptide-induced neurotoxicity via extracellular signal-regulated kinase 1/2-dependent nuclear factor erythroid 2-related factor 2 activation. Mol Pharmacol 73: 1785-1795.
25. Mann GE, Niehueser-Saran J, Watson A, Gao L, Ishii T, et al. (2007) Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: implications for atherosclerosis and preeclampsia. Sheng Li Xue Bao 59: 117-127.
26. Wruck CJ, Huppertz B, Bose P, Brandenburg LO, Pufe T, et al. (2009) Role of a fetal defence mechanism against oxidative stress in the aetiology of preeclampsia. Histopathology 55: 102-106.
27. Loset M, Mundal SB, Johnson MP, Fenstad MH, Freed KA, et al. (2011) A transcriptional profile of the decidua in preeclampsia. Am J Obstet Gynecol 204: 84 e81-27.
28. Vuckovic M, Ponting J, Terman BI, Niketic V, Seif MW, et al. (1996) Expression of the vascular endothelial growth factor receptor, KDR, in human placenta. J Anat 188 (Pt 2): 361-366.
29. Shiraishi S, Nakagawa K, Kinukawa N, Nakano H, Sueishi K, (1996) Immunohistochemical localization of vascular endothelial growth factor in the human placenta. Placenta 17: 111-121.
30. Clark DE, Smith SK, Sharkey AM, Charnock-Jones DS, (1996) Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod 11: 1090-1098.
31. Kweider N, Fragoulis A, Rosen C, Pecks U, Rath W, et al. (2011) Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): implications for preeclampsia. J Biol Chem 286: 42863-42872.
32. Cooper JC, Sharkey AM, McLaren J, Charnock-Jones DS, Smith SK, (1995) Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil 105: 205-213.
33. Kadyrov M, Kosanke G, Kingdom J, Kaufmann P, (1998) Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet 352: 1747-1749.
34. ACOG practice bulletin, (2002) Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 99: 159-167.
35. Kinzler WL, Vintzileos AM, (2008) Fetal growth restriction: a modern approach. Curr Opin Obstet Gynecol 20: 125-131.
36. Detre S, Saclani Jotti G, Dowsett M, (1995) A "quickscore" method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. J Clin Pathol 48: 876-878.
37. Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L, (1985) Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol 92: 23-30.
38. Hung TH, Burton GJ, (2006) Hypoxia and reoxygenation: a possible mechanism for placental oxidative stress in preeclampsia. Taiwan J Obstet Gynecol 45: 189-200.
39. Robson SC, Simpson H, Ball E, Lyall F, Bulmer JN, (2002) Punch biopsy of the human placental bed. Am J Obstet Gynecol 187: 1349-1355.
40. Martin AM, Bindra R, Curcio P, Cicero S, Nicolaides KH, (2001) Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler at 11-14 weeks of gestation. Ultrasound Obstet Gynecol 18: 583-586.
41. Albaiges G, Missfelder-Lobos H, Parra M, Lees C, Cooper D, et al. (2003) Comparison of color Doppler uterine artery indices in a population at high risk for adverse outcome at 24 weeks' gestation. Ultrasound Obstet Gynecol 21: 170-173.
42. Chen ZH, Saito Y, Yoshida Y, Sekine A, Noguchi N, et al. (2005) 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2. J Biol Chem 280: 41921-41927.
43. Chigusa Y, Tatsumi K, Kondoh E, Fujita K, Nishimura F, et al. (2012) Decreased Lectin-Like Oxidized LDL Receptor 1 (LOX-1) and Low Nrf2 Activation in Placenta Are Involved in Preeclampsia. J Clin Endocrinol Metab.
44. Ahmed A, Li XF, Dunk C, Whittle MJ, Rushton DI, et al. (1995) Colocalisation of vascular endothelial growth factor and its Flt-1 receptor in human placenta. Growth Factors 12: 235-243.
45. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, et al. (2002) 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 160: 1405-1423.
46. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, et al. (2004) Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683.
47. Barber A, Robson SC, Myatt L, Bulmer JN, Lyall F, (2001) Heme oxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J 15: 1158-1168.
48. Perkins AV, (2006) Endogenous anti-oxidants in pregnancy and preeclampsia. Aust N Z J Obstet Gynaecol 46: 77-83.