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Tissue-resident macrophages regulate lymphatic vessel growth and patterning in the developing heart

Thomas J. Cahill, Xin Sun, Christophe Ravaud, Cristina Villa del Campo, Konstantinos Klaourakis, Irina-Elena Lupu, Allegra M. Lord, Cathy Browne, Sten Eirik W. Jacobsen, David R. Greaves, David G. Jackson, Sally A. Cowley, William James, Robin P. Choudhury, View ORCID ProfileJoaquim Miguel Vieira, View ORCID ProfilePaul R. Riley
doi: https://doi.org/10.1101/2020.06.30.179952
Thomas J. Cahill
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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Xin Sun
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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Christophe Ravaud
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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Cristina Villa del Campo
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
3Cardiovascular Development Program, Centro Nacional de Investigaciones Cardiovasculares, CNIC, 28029 Madrid, Spain.
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Konstantinos Klaourakis
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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Irina-Elena Lupu
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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Allegra M. Lord
4Karolinska Institutet, Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Stockholm SE-14186, Sweden.
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Cathy Browne
5Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
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Sten Eirik W. Jacobsen
4Karolinska Institutet, Department of Medicine Huddinge, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Stockholm SE-14186, Sweden.
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David R. Greaves
5Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
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David G. Jackson
6MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DS, UK.
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Sally A. Cowley
5Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
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William James
5Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
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Robin P. Choudhury
7Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford OX3 9DU, UK.
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Joaquim Miguel Vieira
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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  • ORCID record for Joaquim Miguel Vieira
  • For correspondence: joaquim.vieira@dpag.ox.ac.uk paul.riley@dpag.ox.ac.uk
Paul R. Riley
1Burdon-Sanderson Cardiac Science Centre, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
2British Heart Foundation - Oxbridge Centre of Regenerative Medicine, CRM, University of Oxford, Oxford OX1 3PT, UK.
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  • ORCID record for Paul R. Riley
  • For correspondence: joaquim.vieira@dpag.ox.ac.uk paul.riley@dpag.ox.ac.uk
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Abstract

Macrophages are components of the innate immune system with key roles in tissue inflammation and repair. It is now evident that macrophages also support organogenesis, but few studies have characterized their identity, ontogeny and function during heart development. Here, we show that resident macrophages in the subepicardial compartment of the developing heart coincide with the emergence of new lymphatics and interact closely with the nascent lymphatic capillaries. Consequently, global macrophage-deficiency led to extensive vessel disruption with mutant hearts exhibiting shortened and mis-patterned lymphatics. The origin of cardiac macrophages was linked to the yolk sac and fetal liver. Moreover, Csf1r+ and Cx3cr1+ myeloid sub-lineages were found to play essential functions in the remodeling of the lymphatic endothelium. Mechanistically, macrophage hyaluronan was found to be required for lymphatic sprouting by mediating direct macrophage-lymphatic endothelial cell interactions. Together, these findings reveal insight into the role of macrophages as indispensable mediators of lymphatic growth during the development of the mammalian cardiac vasculature.

Summary statement Tissue-resident macrophages are indispensable mediators of lymphatic vessel formation during heart development and function to remodel the vascular plexus.

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Tissue-resident macrophages regulate lymphatic vessel growth and patterning in the developing heart
Thomas J. Cahill, Xin Sun, Christophe Ravaud, Cristina Villa del Campo, Konstantinos Klaourakis, Irina-Elena Lupu, Allegra M. Lord, Cathy Browne, Sten Eirik W. Jacobsen, David R. Greaves, David G. Jackson, Sally A. Cowley, William James, Robin P. Choudhury, Joaquim Miguel Vieira, Paul R. Riley
bioRxiv 2020.06.30.179952; doi: https://doi.org/10.1101/2020.06.30.179952
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Tissue-resident macrophages regulate lymphatic vessel growth and patterning in the developing heart
Thomas J. Cahill, Xin Sun, Christophe Ravaud, Cristina Villa del Campo, Konstantinos Klaourakis, Irina-Elena Lupu, Allegra M. Lord, Cathy Browne, Sten Eirik W. Jacobsen, David R. Greaves, David G. Jackson, Sally A. Cowley, William James, Robin P. Choudhury, Joaquim Miguel Vieira, Paul R. Riley
bioRxiv 2020.06.30.179952; doi: https://doi.org/10.1101/2020.06.30.179952

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