Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy

Pringle, K. G.; Kind, K. L.; Sferruzzi-Perri, A. N.; Thompson, J. G.; Roberts, C. T.

doi:10.1093/humupd/dmp046

Cited by 259Pregnancy and preeclampsia studiesReproductive System and PregnancyNeonatal and fetal brain pathology

Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy

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Pringle, K. G., Kind, K. L., Sferruzzi-Perri, A. N., Thompson, J. G., Roberts, C. T.·2010·Human Reproduction Update

DOI 10.1093/humupd/dmp046PMC PMC2880912

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Abstract

In the first trimester the extravillous cytotrophoblast cells occlude the uterine spiral arterioles creating a low oxygen environment early in pregnancy, which is essential for pregnancy success. Paradoxically, shallow trophoblast invasion and defective vascular remodelling of the uterine spiral arteries in the first trimester may result in impaired placental perfusion and chronic placental ischemia and hypoxia later in gestation leading to adverse pregnancy outcomes. The hypoxia inducible factors (HIFs) are key mediators of the response to low oxygen. We aimed to elucidate mechanisms of regulation of HIFs and the role these may play in the control of placental differentiation, growth and function in both normal and pathological pregnancies. The Pubmed database was consulted for identification of the most relevant published articles. Search terms used were oxygen, placenta, trophoblast, pregnancy, HIF and hypoxia. The HIFs are able to function throughout all aspects of normal and abnormal placental differentiation, growth and function; during the first trimester (physiologically low oxygen), during mid-late gestation (where there is adequate supply of blood and oxygen to the placenta) and in pathological pregnancies complicated by placental hypoxia/ischemia. During normal pregnancy HIFs may respond to complex alterations in oxygen, hormones, cytokines and growth factors to regulate placental invasion, differentiation, transport and vascularization. In the ever-changing environment created during pregnancy, the HIFs appear to act as key mediators of placental development and function and thereby are likely to be important contributors to both normal and adverse pregnancy outcomes.

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Preeclampsia, miscarriages, preterm labour, birth defects, endometriosis, tubal factor infertility, intrauterine growth retardation, and stillbirth have been linked to insufficient trophoblast invasion, development, vascular remodeling, and impaired placental development and function.
“Preeclampsia, miscarriages, preterm labour, birth defects, endometriosis and tubal factor infertility, intrauterine growth retardation and stillbirth have been linked to insufficient trophoblast invasion, development, vascular remodeling and impaired placental development and function (Jauniaux et al., 2003, Szczepanska et al., 2003, Pringle et al, 2010)”
From Iron, Oxidative Stress and Health (2012) · cites this paper as Pringle et al, 2010
The Introduction links impaired placental invasion, development and function to miscarriage, pre-eclampsia, intrauterine growth restriction, pre-term labour with intact membranes, and stillbirth. It does not link birth defects, endometriosis, or tubal factor infertility to these placental problems; the Placental oxygenation section supports the trophoblast-invasion and vascular-remodelling link for some of the listed outcomes. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Maternal blood flow to the intervillous spaces commences only around 11 weeks of gestation.
“Maternal blood flow to the intervillous spaces commences only around 11 weeks of gestation (Pringle et al, 2010).”
From Iron, Oxidative Stress and Health (2012) · cites this paper as Pringle et al, 2010
HIF-1 provides a very rapid mechanism for responding within seconds or minutes to acute changes in oxygenation, whereas HIF-2 is thought to mediate longer-term adaptations to relatively modest changes.
“HIF-1 thus provides a very rapid mechanism for responding within seconds or minutes to acute changes in oxygenation, whereas HIF-2 is thought to mediate longer-term adaptations to relatively modest changes (444).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [444]
HIFs can be stabilized by factors other than hypoxia, including reactive oxygen and nitrogen species, angiotensin, growth factors and cytokines.
“Interpretation of these data is difficult given that it is now realized that HIFs can be stabilized by factors other than hypoxia, including reactive oxygen and nitrogen species, angiotensin, growth factors and cytokines (433, 444), many of which are changing during early pregnancy.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [444]

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“Maternal blood flow to the intervillous spaces commences only around 11 weeks of gestation (Pringle et al, 2010).”
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Authors: Pringle, K. G., Kind, K. L., Sferruzzi-Perri, A. N., Thompson, J. G., & Roberts, C. T.
Affiliations: Hunter Medical Research Institute (AU)
The University of Adelaide (AU)
University of Cambridge (GB)
Corresponding author: Roberts, C. T.
ORCID: Pringle, K. G.
Kind, K. L.
Sferruzzi-Perri, A. N.
Thompson, J. G.
Roberts, C. T.
Venue: Human Reproduction Update
Publisher: Oxford University Press (OUP)
Published: 2009-11-19
Volume: 16
Issue: 4
Pages: 415-431
ISSN: 1355-4786 (ISSN-L)
1460-2369
DOI: 10.1093/humupd/dmp046
PMC: PMC2880912
OpenAlex: W2138670825
Cited by: 259
References: 208
Citations by year: 2026: 10 · 2025: 9 · 2024: 14 · 2023: 25 · 2022: 14 · 2021: 26 · 2020: 13 · 2019: 15 · 2018: 14 · 2017: 19 · 2016: 10 · 2015: 14 · 2014: 18 · 2013: 16 · 2012: 21
FWCI: 2.24
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
Locations: Human Reproduction Update (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
Figshare (submittedVersion, cc-by-nc)
NOVA (University of Newcastle Australia) (submittedVersion, cc-by-nc)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Keywords: hypoxia-inducible factor, placental hypoxia, trophoblast invasion, uterine spiral arteries, placental ischemia, placental differentiation, placental development, adverse pregnancy outcomes, first trimester, placental vascularization, oxygen regulation
MeSH terms: Endothelial PAS Domain-Containing Protein 1, Animals, Hypoxia, Female, Humans, Oxygen, Placenta, Placentation, Pregnancy, Pregnancy Trimester, First, Pregnancy Trimester, Third, Trophoblasts, Mice, Rats, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit

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Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy

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