Evidence of Placental Translation Inhibition and Endoplasmic Reticulum Stress in the Etiology of Human Intrauterine Growth Restriction

Yung, Hong-wa; Calabrese, Stefania; Hynx, Debby; Hemmings, Brian A.; Cetin, Irene; Charnock-Jones, D. Stephen; Burton, Graham J.

doi:10.2353/ajpath.2008.071193

Cited by 388Pregnancy and preeclampsia studiesEndoplasmic Reticulum Stress and DiseaseBirth, Development, and Health

Evidence of Placental Translation Inhibition and Endoplasmic Reticulum Stress in the Etiology of Human Intrauterine Growth Restriction

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Yung, Hong-wa, Calabrese, Stefania, Hynx, Debby, Hemmings, Brian A., Cetin, Irene, Charnock-Jones, D. Stephen, Burton, Graham J.·2008·The American Journal of Pathology

DOI 10.2353/ajpath.2008.071193PMC PMC2475782

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Abstract

Unexplained intrauterine growth restriction of the fetus (IUGR) results from impaired placental development, frequently associated with maternal malperfusion. Some cases are complicated further by preeclampsia (PE+IUGR). Here, we provide the first evidence that placental protein synthesis inhibition and endoplasmic reticulum (ER) stress play key roles in IUGR pathophysiology. Increased phosphorylation of eukaryotic initiation factor 2alpha suggests suppression of translation initiation in IUGR placentas, with a further increase in PE+IUGR cases. Consequently, AKT levels were reduced at the protein, but not mRNA, level. Additionally, levels of other proteins in the AKT-mammalian target of rapamycin pathway were decreased, and there was associated dephosphorylation of 4E-binding protein 1 and activation of glycogen synthase kinase 3beta. Cyclin D1 and the eukaryotic initiation factor 2B epsilon subunit were also down-regulated, providing additional evidence for this placental phenotype. The central role of AKT signaling in placental growth regulation was confirmed in Akt1 null mice, which display IUGR. In addition, we demonstrated ultrastructural and molecular evidence of ER stress in human IUGR and PE+IUGR placentas, providing a potential mechanism for eukaryotic initiation factor 2alpha phosphorylation. In confirmation, induction of low-grade ER stress in trophoblast-like cell lines reduced cellular proliferation. PE+IUGR placentas showed elevated ER stress with the additional expression of the pro-apoptotic protein C/EBP-homologous protein/growth arrest and DNA damage 153. These findings may account for the increased microparticulate placental debris in the maternal circulation of these cases, leading to endothelial cell activation and impairing placental development.

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UPR signaling cascades are activated in placentas from cases of growth restriction and early-onset pre-eclampsia, but no data are yet available for pregnancies complicated by maternal obesity or other metabolic disorders.
“These cascades are activated in placentas from cases of growth restriction and early-onset pre-eclampsia (595, 596), but no data are yet available for pregnancies complicated by maternal obesity or other metabolic disorders.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [596]
UPR activation can be replicated in trophoblast cell lines by hypoxia-reoxygenation, with activation of the three pathways dependent on the severity of the stress.
“These findings can be replicated in trophoblast cell lines by exposure to hypoxiareoxygenation, with activation of the three pathways being dependent on the severity of the stress (596).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [596]
More severe UPR activation is seen in human placentas from growth-restricted pregnancies, particularly early-onset pre-eclampsia.
“More severe activation is seen in human placentas from growth-restricted pregnancies (596), and particularly in cases of early-onset pre-eclampsia (595).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [596]
A reduction of AKT and mTOR at the protein level, and reduced phosphorylation of mTOR, TSC1/2, 4E-BP1 and GSK-3β, have been reported in growth restricted human placentas associated with maternal vascular compromise, but there was no effect on S6Ks and eEF2K.
“Equally, a reduction of AKT and mTOR at the protein level, and reduced phosphorylation of mTOR, TSC1/2, 4E-BP1 and GSK-3β have been reported in growth restricted human placentas associated with maternal vascular compromise, but there was no effect on S6Ks and eEF2K (596).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [596]
Evidence of more severe translational arrest has been reported in placentas from growth restricted pregnancies of maternal vascular origin when placental weight is significantly reduced.
“Evidence of more severe translational arrest has been reported in placentas from growth restricted pregnancies of maternal vascular origin when placental weight is significantly reduced (596).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [596]

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Schweikhart G, Kaufmann P: [Problems of distinction of normal, art- eficial and pathological structures in mature human placental villi. I Ultrastructure of the syncytiotrophoblast (author's transl)] Arch Gynakol 1977, 222:213-230

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Endoplasmic reticulum stress disrupts placental morphogenesis: implications for human intrauterine growth restriction
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Placental Stress, Protein Synthesis Inhibition, and Growth Restriction.
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No evidence of the unfolded protein response in the placenta of two rodent models of preeclampsia and intrauterine growth restriction
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Authors: Yung, H.-W., Calabrese, S., Hynx, D., Hemmings, B. A., Cetin, I., Charnock-Jones, D. S., & Burton, G. J.
Affiliations: University of Cambridge (GB)
University of Milan (IT)
Friedrich Miescher Institute (CH)
Corresponding author: Burton, Graham J.
ORCID: Yung, Hong-wa
Cetin, Irene
Burton, Graham J.
Venue: The American Journal of Pathology
Publisher: Elsevier BV
Published: 2008-08
Volume: 173
Issue: 2
Pages: 451-462
ISSN: 0002-9440 (ISSN-L)
DOI: 10.2353/ajpath.2008.071193
PMC: PMC2475782
OpenAlex: W2140865853
Cited by: 388
References: 78
Citations by year: 2026: 9 · 2025: 21 · 2024: 22 · 2023: 14 · 2022: 20 · 2021: 34 · 2020: 26 · 2019: 26 · 2018: 22 · 2017: 29 · 2016: 23 · 2015: 22 · 2014: 20 · 2013: 21 · 2012: 34
FWCI: 17.26
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: American Journal Of Pathology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
Funders: Wellcome Trust (069027)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: fetal growth restriction, preeclampsia, endoplasmic reticulum stress, Akt signaling, mTOR signaling, 4E-binding protein 1, glycogen synthase kinase-3β, cyclin D1, trophoblast proliferation, CHOP/GADD153, placental apoptosis, endothelial activation, placental development
MeSH terms: Glycogen Synthase Kinase 3 beta, Animals, Cell Line, Endoplasmic Reticulum, Female, Fetal Growth Retardation, Humans, Phosphoproteins, Phosphorylation, Placenta, Pre-Eclampsia, Pregnancy, Protein Kinases, Protein Biosynthesis, Down-Regulation, Eukaryotic Initiation Factor-2, Mice, Knockout, Cell Cycle Proteins, Cyclin D1, Glycogen Synthase Kinase 3, Adaptor Proteins, Signal Transducing, Cell Proliferation, Proto-Oncogene Proteins c-akt, Mice, Transcription Factor CHOP, TOR Serine-Threonine Kinases

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Evidence of Placental Translation Inhibition and Endoplasmic Reticulum Stress in the Etiology of Human Intrauterine Growth Restriction

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