Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions

Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral artery remodeling. Failures in uterine spiral artery remodeling are linked to diseases of pregnancy. This prompted an investigation of the in...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 108; no. 39; pp. 16295 - 16300
Main Authors Chakraborty, Damayanti, Rumi, M. A. Karim, Konno, Toshihiro, Soares, Michael J
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 27.09.2011
National Acad Sciences
Subjects
Animals
Arteries
Biological Sciences
Cell Lineage
Cells
Differentiation
Endothelium
Female
Genotype & phenotype
Hypoxia
Hypoxia-inducible factor 1 alpha
Hypoxia-Inducible Factor 1, alpha Subunit - physiology
Hypoxia-inducible factors
Killer Cells, Natural - physiology
Natural killer cells
Oxygen
Oxygen - metabolism
Oxygen tension
phenotype
Placenta
Placenta - blood supply
Placenta - cytology
Placenta - metabolism
Placentation
Pregnancy
Proteins
Rats
Rats, Sprague-Dawley
Reflexes
Renovations
Signal Transduction
Stem cells
Stroma
trophoblast
Trophoblasts
Trophoblasts - cytology
Uterus
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Abstract Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral artery remodeling. Failures in uterine spiral artery remodeling are linked to diseases of pregnancy. This prompted an investigation of the involvement of NK cells in placentation. NK cell depletion decreased the delivery of proangiogenic factors and delayed uterine spiral artery development, leading to decreased oxygen tension at the placentation site, stabilized hypoxia-inducible factor 1A protein, and redirected trophoblast differentiation to an invasive phenotype. Trophoblast cells replaced the endothelium of uterine spiral arteries extending the depth of the placental vascular bed and accelerating vessel remodeling. Hypoxia-regulated trophoblast lineage decisions, including expansion of invasive trophoblast, could be reproduced in vitro by using rat trophoblast stem cells and were dependent on hypoxia-inducible factor signaling. We conclude that NK cells guide hemochorial placentation through controlling a hypoxia-sensitive adaptive reflex regulating trophoblast lineage decisions.
AbstractList Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral artery remodeling. Failures in uterine spiral artery remodeling are linked to diseases of pregnancy. This prompted an investigation of the involvement of NK cells in placentation. NK cell depletion decreased the delivery of proangiogenic factors and delayed uterine spiral artery development, leading to decreased oxygen tension at the placentation site, stabilized hypoxia-inducible factor 1A protein, and redirected trophoblast differentiation to an invasive phenotype. Trophoblast cells replaced the endothelium of uterine spiral arteries extending the depth of the placental vascular bed and accelerating vessel remodeling. Hypoxia-regulated trophoblast lineage decisions, including expansion of invasive trophoblast, could be reproduced in vitro by using rat trophoblast stem cells and were dependent on hypoxia-inducible factor signaling. We conclude that NK cells guide hemochorial placentation through controlling a hypoxia-sensitive adaptive reflex regulating trophoblast lineage decisions.
Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral artery remodeling. Failures in uterine spiral artery remodeling are linked to diseases of pregnancy. This prompted an investigation of the involvement of NK cells in placentation. NK cell depletion decreased the delivery of proangiogenic factors and delayed uterine spiral artery development leading to decreased oxygen tension at the placentation site/stabilized hypoxia-inducible factor 1A protein, and redirected trophoblast differentiation to an invasive phenotype. Trophoblast cells replaced the endothelium of uterine spiral arteries extending the depth of the placental vascular bed and accelerating vessel remodeling. Hypoxia-regulated trophoblast lineage decisions, including expansion of invasive trophoblast, could be reproduced in vitro by using rat trophoblast stem cells and were dependent on hypoxia-inducible factor signaling. We conclude that NK cells guide hemochorial placentation through controlling a hypoxiasensitive adaptive reflex regulating trophoblast lineage decisions.
Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral artery remodeling. Failures in uterine spiral artery remodeling are linked to diseases of pregnancy. This prompted an investigation of the involvement of NK cells in placentation. NK cell depletion decreased the delivery of proangiogenic factors and delayed uterine spiral artery development, leading to decreased oxygen tension at the placentation site, stabilized hypoxia-inducible factor 1A protein, and redirected trophoblast differentiation to an invasive phenotype. Trophoblast cells replaced the endothelium of uterine spiral arteries extending the depth of the placental vascular bed and accelerating vessel remodeling. Hypoxia-regulated trophoblast lineage decisions, including expansion of invasive trophoblast, could be reproduced in vitro by using rat trophoblast stem cells and were dependent on hypoxia-inducible factor signaling. We conclude that NK cells guide hemochorial placentation through controlling a hypoxia-sensitive adaptive reflex regulating trophoblast lineage decisions. [PUBLICATION ABSTRACT]
Author Konno, Toshihiro
Rumi, M. A. Karim
Chakraborty, Damayanti
Soares, Michael J
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Author contributions: D.C., M.A.K.R., and M.J.S. designed research; D.C., M.A.K.R., T.K., and M.J.S. performed research; D.C., M.A.K.R., T.K., and M.J.S. analyzed data; and D.C. and M.J.S. wrote the paper.
Edited* by R. Michael Roberts, University of Missouri-Columbia, Columbia, MO, and approved August 15, 2011 (received for review June 13, 2011)
1Present address: Laboratory of Animal Breeding, Graduate School of Agricultural and Life Science, University of Tokyo, Tokyo 113-8657 Japan.
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Snippet Natural killer (NK) cells are recruited into the uterine stroma during establishment of the hemochorial placenta and are proposed regulators of uterine spiral...
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StartPage 16295
SubjectTerms Animals
Arteries
Biological Sciences
Cell Lineage
Cells
Differentiation
Endothelium
Female
Genotype & phenotype
Hypoxia
Hypoxia-inducible factor 1 alpha
Hypoxia-Inducible Factor 1, alpha Subunit - physiology
Hypoxia-inducible factors
Killer Cells, Natural - physiology
Natural killer cells
Oxygen
Oxygen - metabolism
Oxygen tension
phenotype
Placenta
Placenta - blood supply
Placenta - cytology
Placenta - metabolism
Placentation
Pregnancy
Proteins
Rats
Rats, Sprague-Dawley
Reflexes
Renovations
Signal Transduction
Stem cells
Stroma
trophoblast
Trophoblasts
Trophoblasts - cytology
Uterus
Title Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions
URI https://www.jstor.org/stable/41352792
http://www.pnas.org/content/108/39/16295.abstract
https://www.ncbi.nlm.nih.gov/pubmed/21900602
https://www.proquest.com/docview/894733125
https://search.proquest.com/docview/894818455
https://search.proquest.com/docview/907173767
https://pubmed.ncbi.nlm.nih.gov/PMC3182743
Volume 108
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