Placenta
Volume 30 , Pages 43-48 , March 2009

Placental Endoplasmic Reticulum Stress and Oxidative Stress in the Pathophysiology of Unexplained Intrauterine Growth Restriction and Early Onset Preeclampsia

  • G.J. Burton

      Affiliations

    • Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 1223 333856; fax: +44 1223 333840.
  • ,
  • H.-W. Yung

      Affiliations

    • Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, UK
  • ,
  • T. Cindrova-Davies

      Affiliations

    • Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, UK
  • ,
  • D.S. Charnock-Jones

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Cambridge, UK

,Accepted 6 November 2008.

References 

  1. Ness RB, Sibai BM. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. Am J Obstet Gynecol. 2006;195:40–49
  2. Brosens I, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol. 1977;84:656–663
  3. Gerretsen G, Huisjes HJ, Elema JD. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol. 1981;88:876–881
  4. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, Van Assche FA. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol. 1994;101:669–674
  5. Lyall F. The human placental bed revisited. Placenta. 2002;23:555–562
  6. Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol. 1986;93:1049–1059
  7. Harris JWS, Ramsey EM. The morphology of human uteroplacental vasculature. Contrib Embryol. 1966;38:43–58
  8. Bartelmez GW. The form and functions of the uterine blood vessels in the rhesus monkey. Contrib Embryol. 1957;36:153–182
  9. Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies. Am J Obstet Gynecol. 2002;187:1416–1423
  10. Burton GJ, Hung T-H. Hypoxia-reoxygenation: a potential source of placental oxidative stress in normal pregnancy and preeclampsia. Fetal Mat Med Rev. 2003;14:97–117
  11. Hung TH, Skepper JN, Burton GJ. In vitro ischemia–reperfusion injury in term human placenta as a model for oxidative stress in pathological pregnancies. Am J Pathol. 2001;159:1031–1043
  12. Brosens I. A study of the spiral arteries of the decidua basalis in normotensive and hypertensive pregnancies. J Obstet Gynaecol Br Cwlth. 1964;71:222–230
  13. Sheppard BL, Bonnar J. The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation. Br J Obstet Gynaecol. 1976;83:948–959
  14. Villar J, Carroli G, Wojdyla D, Abalos E, Giordano D, Ba'aqeel H, et al. Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions?. Am J Obstet Gynecol. 2006;194:921–931
  15. Mayhew TM, Manwani R, Ohadike C, Wijesekara J, Baker PN. The placenta in pre-eclampsia and intrauterine growth restriction: studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances. Placenta. 2007;28:233–238
  16. Wang Y, Walsh SW. Placental mitochondria as a source of oxidative stress in pre-eclampsia. Placenta. 1998;19:581–586
  17. Hung T-H, Skepper JN, Charnock-Jones DS, Burton GJ. Hypoxia/reoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia. Circ Res. 2002;90:1274–1281
  18. Soleymanlou N, Wu Y, Wang JX, Todros T, Ietta F, Jurisicova A, et al. A novel Mtd splice isoform is responsible for trophoblast cell death in pre-eclampsia. Cell Death Differ. 2005;12:441–452
  19. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest. 2005;115:2656–2664
  20. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol. 2006;38:317–332
  21. Yoshida H. ER stress and diseases. FEBS J. 2007;274:630–658
  22. DeGracia DJ, Montie HL. Cerebral ischemia and the unfolded protein response. J Neurochem. 2004;91:1–8
  23. Cindrova-Davies T, Spasic-Boskovic O, Jauniaux E, Charnock-Jones DS, Burton GJ. Nuclear factor-kappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins. Am J Pathol. 2007;170:1511–1520
  24. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, et al. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol. 2008;173:451–462
  25. Brewer JW, Hendershot LM, Sherr CJ, Diehl JA. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc Natl Acad Sci U S A. 1999;96:8505–8510
  26. Widdows K, Drewlo S, Baczyk D, Kingdom J, Ansari T. Stereological evidence for reduced cytotrophoblast proliferation in severe IUGR. Placenta. 2008;29:A.99
  27. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E, et al. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem. 2003;278:32124–32131
  28. Leung DN, Smith SC, To KF, Sahota DS, Baker PN. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol. 2001;184:1249–1250
  29. Smith SC, Baker PN, Symonds EM. Increased placental apoptosis in intrauterine growth restriction. Am J Obstet Gynecol. 1997;177:1395–1401
  30. Allaire AD, Ballenger KA, Wells SR, McMahon MJ, Lessey BA. Placental apoptosis in preeclampsia. Obstet Gynecol. 2000;96:271–276
  31. Ishihara N, Matsuo H, Murakoshi H, Laoag-Fernandez J, Samoto T, Maruo T. Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol. 2002;186:158–166
  32. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, et al. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta. 2006;27:56–61
  33. Redman CWG, Sargent IL. Placental debris, oxidative stress and pre-eclampsia. Placenta. 2000;21:597–602
  34. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Oxford: Oxford Science Publications; 1999;p. 936
  35. Many A, Hubel CA, Roberts JM. Hyperuricemia and xanthine oxidase in preeclampsia, revisited. Am J Obstet Gynecol. 1996;174:288–291
  36. Tu BP, Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol. 2004;164:341–346
  37. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature. 2008;454:455–462
  38. Hung T-H, Charnock-Jones DS, Skepper JN, Burton GJ. Secretion of tumour necrosis factor-a 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
  39. Tjoa ML, Cindrova-Davies T, Spasic-Boskovic O, Bianchi DW, Burton GJ. Trophoblastic oxidative stress and the release of cell-free feto-placental DNA. Am J Pathol. 2006;169:400–404
  40. Cindrova-Davies T. Pre-eclampsia; from placental oxidative stress to maternal endothelial dysfunction. Placenta. 2009;23(Suppl. A):S55–S65
  41. Hubel CA. Oxidative stress in the pathogenesis of preeclampsia. Proc Soc Exp Biol Med. 1999;222:222–235
  42. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol. 2004;122:369–382
  43. Roberts JM, Hubel CA. Is oxidative stress the link in the two-stage model of pre-eclampsia?. Lancet. 1999;354:788–789
  44. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592–1594
  45. Takagi Y, Nikaido T, Toki T, Kita N, Kanai M, Ashida T, et al. Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Arch. 2004;444:49–55
  46. Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, Jauniaux E, et al. Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol. 2007;171:1168–1179
  47. 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
  48. Choi SJ, Oh SY, Kim JH, Sadovsky Y, Roh CR. Increased expression of N-myc downstream-regulated gene 1 (NDRG1) in placentas from pregnancies complicated by intrauterine growth restriction or preeclampsia. Am J Obstet Gynecol. 2007;196(45):e1–e7
  49. Vaiman D, Mondon F, Garces-Duran A, Mignot TM, Robert B, Rebourcet R, et al. Hypoxia-activated genes from early placenta are elevated in preeclampsia, but not in intra-uterine growth retardation. BMC Genomics. 2005;6:111
  50. Sibley CP, Turner MA, Cetin I, Ayuk P, Boyd CAR, D'Souza SW, et al. Placental phenotypes of intrauterine growth. Ped Res. 2005;58:827–832
  51. Shibata E, Hubel CA, Powers RW, von Versen-Hoeynck F, Gammill H, Rajakumar A, et al. Placental system A amino acid transport is reduced in pregnancies with small for gestational age (SGA) infants but not in preeclampsia with SGA infants. Placenta. 2008;29:879–882
  52. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, et al. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab. 2005;90:4895–4903
  53. Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, et al. The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med. 2008;21:25–40
  54. Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, et al. Urinary placental growth factor and risk of preeclampsia. JAMA. 2005;293:77–85
  55. Sekizawa A, Jimbo M, Saito H, Iwasaki M, Matsuoka R, Okai T, et al. Cell-free fetal DNA in the plasma of pregnant women with severe fetal growth restriction. Am J Obstet Gynecol. 2003;188:480–484
  56. Laivuori H, Gallaher MJ, Collura L, Crombleholme WR, Markovic N, Rajakumar A, et al. Relationships between maternal plasma leptin, placental leptin mRNA and protein in normal pregnancy, pre-eclampsia and intrauterine growth restriction without pre-eclampsia. Mol Hum Reprod. 2006;12:551–556
  57. Johnson MR, Anim-Nyame N, Johnson P, Sooranna SR, Steer PJ. Does endothelial cell activation occur with intrauterine growth restriction?. BJOG. 2002;109:836–839

PII: S0143-4004(08)00375-5

doi: 10.1016/j.placenta.2008.11.003

Placenta
Volume 30 , Pages 43-48 , March 2009