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Fetus-derived IGF2 matches placental development to fetal demand

View ORCID ProfileIonel Sandovici, Aikaterini Georgopoulou, View ORCID ProfileAntonia S. Hufnagel, Samira N. Schiefer, View ORCID ProfileFátima Santos, Katharina Hoelle, Brian Y.H. Lam, View ORCID ProfileGiles S.H. Yeo, Keith Burling, View ORCID ProfileJorge López-Tello, View ORCID ProfileMoritz Reiterer, View ORCID ProfileAbigail L. Fowden, View ORCID ProfileGraham J. Burton, View ORCID ProfileAmanda N. Sferruzzi-Perri, View ORCID ProfileCristina M. Branco, Miguel Constância
doi: https://doi.org/10.1101/520536
Ionel Sandovici
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
2University of Cambridge Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Institute of Metabolic Science, Addenbrookes Hospital, Cambridge CB2 0QQ
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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  • For correspondence: is299@cam.ac.uk jmasmc2@cam.ac.uk
Aikaterini Georgopoulou
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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Antonia S. Hufnagel
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
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Samira N. Schiefer
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
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Fátima Santos
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
4Epigenetics Programme, Babraham Institute, Cambridge CB22 3AT, United Kingdom
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Katharina Hoelle
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
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Brian Y.H. Lam
2University of Cambridge Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Institute of Metabolic Science, Addenbrookes Hospital, Cambridge CB2 0QQ
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Giles S.H. Yeo
2University of Cambridge Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Institute of Metabolic Science, Addenbrookes Hospital, Cambridge CB2 0QQ
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Keith Burling
2University of Cambridge Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Institute of Metabolic Science, Addenbrookes Hospital, Cambridge CB2 0QQ
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Jorge López-Tello
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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Moritz Reiterer
5Physiological Laboratory, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
6Centre for Cancer research and Cell Biology, Queen’s University Belfast, Belfast BT9 7AE, United Kingdom
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Abigail L. Fowden
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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Graham J. Burton
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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Amanda N. Sferruzzi-Perri
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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Cristina M. Branco
5Physiological Laboratory, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
6Centre for Cancer research and Cell Biology, Queen’s University Belfast, Belfast BT9 7AE, United Kingdom
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Miguel Constância
1Department of Obstetrics and Gynaecology and National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge CB2 0SW, United Kingdom
2University of Cambridge Metabolic Research Laboratories and MRC Metabolic Diseases Unit, Institute of Metabolic Science, Addenbrookes Hospital, Cambridge CB2 0QQ
3Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, United Kingdom
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  • For correspondence: is299@cam.ac.uk jmasmc2@cam.ac.uk
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Abstract

Growth of a fetus is dependent upon the functional capacity of its placenta, but how the latter is matched to fetal demands is currently unknown. Critically, there is continuous expansion of the feto-placental microvasculature throughout pregnancy, along with morphogenic modifications in the overlying trophoblast epithelium. Here we demonstrate, through fetal and trophoblast specific genetic manipulations in the mouse, that signalling by IGF2 from the feto-placental endothelium and endocrine actions of circulating fetal IGF2 are required. We provide evidence that endothelial and fetal-derived IGF2 plays an important role in trophoblast morphogenesis, acting through Gcm1 and Synb. The effects on placental microvasculature expansion are mediated through IGF2R and angiopoietin-Tie2/TEK signalling. Thus, our study reveals a direct role for IGF2-IGF2R axis on matching fetal demand to placental supply and establishes the principle that hormone-like signals from the fetus play important roles in the control of placental vascularization and trophoblast morphogenesis, findings that have potential clinical implications.

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Posted January 16, 2019.
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Fetus-derived IGF2 matches placental development to fetal demand
Ionel Sandovici, Aikaterini Georgopoulou, Antonia S. Hufnagel, Samira N. Schiefer, Fátima Santos, Katharina Hoelle, Brian Y.H. Lam, Giles S.H. Yeo, Keith Burling, Jorge López-Tello, Moritz Reiterer, Abigail L. Fowden, Graham J. Burton, Amanda N. Sferruzzi-Perri, Cristina M. Branco, Miguel Constância
bioRxiv 520536; doi: https://doi.org/10.1101/520536
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Fetus-derived IGF2 matches placental development to fetal demand
Ionel Sandovici, Aikaterini Georgopoulou, Antonia S. Hufnagel, Samira N. Schiefer, Fátima Santos, Katharina Hoelle, Brian Y.H. Lam, Giles S.H. Yeo, Keith Burling, Jorge López-Tello, Moritz Reiterer, Abigail L. Fowden, Graham J. Burton, Amanda N. Sferruzzi-Perri, Cristina M. Branco, Miguel Constância
bioRxiv 520536; doi: https://doi.org/10.1101/520536

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