Cited by 1,011Cardiac electrophysiology and arrhythmiasConnexins and lens biologyCardiac Fibrosis and Remodeling

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Macrophages Facilitate Electrical Conduction in the Heart

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Hulsmans, Maarten, Clauss, Sebastian, Xiao, Ling, Aguirre, Aaron D., King, Kevin R., Hanley, Alan, Hucker, William J., Wülfers, Eike M., Seemann, Gunnar, Courties, Gabriel, Iwamoto, Yoshiko, Sun, Yuan, Savol, Andrej J., Sager, Hendrik B., Lavine, Kory J., Fishbein, Gregory A., Capen, Diane E., Da Silva, Nicolas, Miquerol, Lucile, Wakimoto, Hiroko, Seidman, Christine E., Seidman, Jonathan G., Sadreyev, Ruslan I., Naxerova, Kamila, Mitchell, Richard N., Brown, Dennis, Libby, Peter, Weissleder, Ralph, Swirski, Filip K., Kohl, Peter, Vinegoni, Claudio, Milan, David J., Ellinor, Patrick T., Nahrendorf, Matthias·2017·Cell

DOI 10.1016/j.cell.2017.03.050PMC PMC5474950

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Abstract

Organ-specific functions of tissue-resident macrophages in the steady-state heart are unknown. Here, we show that cardiac macrophages facilitate electrical conduction through the distal atrioventricular node, where conducting cells densely intersperse with elongated macrophages expressing connexin 43. When coupled to spontaneously beating cardiomyocytes via connexin-43-containing gap junctions, cardiac macrophages have a negative resting membrane potential and depolarize in synchrony with cardiomyocytes. Conversely, macrophages render the resting membrane potential of cardiomyocytes more positive and, according to computational modeling, accelerate their repolarization. Photostimulation of channelrhodopsin-2-expressing macrophages improves atrioventricular conduction, whereas conditional deletion of connexin 43 in macrophages and congenital lack of macrophages delay atrioventricular conduction. In the Cd11b DTR mouse, macrophage ablation induces progressive atrioventricular block. These observations implicate macrophages in normal and aberrant cardiac conduction.

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Authors: Hulsmans, M., Clauss, S., Xiao, L., Aguirre, A. D., King, K. R., Hanley, A., Hucker, W. J., Wülfers, E. M., Seemann, G., Courties, G., Iwamoto, Y., Sun, Y., Savol, A. J., Sager, H. B., Lavine, K. J., Fishbein, G. A., Capen, D. E., Da Silva, N., Miquerol, L., Wakimoto, H., Seidman, C. E., Seidman, J. G., Sadreyev, R. I., Naxerova, K., Mitchell, R. N., Brown, D., Libby, P., Weissleder, R., Swirski, F. K., Kohl, P., Vinegoni, C., Milan, D. J., Ellinor, P. T., & Nahrendorf, M.
Affiliations: Harvard University (US)
University of Freiburg (DE)
Washington University in St. Louis (US)
Brigham and Women's Hospital (US)
Centre National de la Recherche Scientifique (FR)
Broad Institute (US)
Corresponding author: Nahrendorf, Matthias
ORCID: Hulsmans, Maarten
Clauss, Sebastian
Xiao, Ling
Aguirre, Aaron D.
King, Kevin R.
Hanley, Alan
Hucker, William J.
Wülfers, Eike M.
Seemann, Gunnar
Courties, Gabriel
Iwamoto, Yoshiko
Sager, Hendrik B.
Lavine, Kory J.
Fishbein, Gregory A.
Capen, Diane E.
Miquerol, Lucile
Wakimoto, Hiroko
Seidman, Christine E.
Seidman, Jonathan G.
Sadreyev, Ruslan I.
Naxerova, Kamila
Mitchell, Richard N.
Brown, Dennis
Libby, Peter
Weissleder, Ralph
Kohl, Peter
Vinegoni, Claudio
Milan, David J.
Ellinor, Patrick T.
Nahrendorf, Matthias
Venue: Cell
Publisher: Elsevier BV
Published: 2017-04
Volume: 169
Issue: 3
Pages: 510-522.e20
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2017.03.050
PMC: PMC5474950
OpenAlex: W2605696370
Cited by: 1,011
References: 53
Citations by year: 2026: 99 · 2025: 110 · 2024: 129 · 2023: 112 · 2022: 108 · 2021: 135 · 2020: 112 · 2019: 92 · 2018: 85 · 2017: 26
FWCI: 66.57
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Arrow@dit (Dublin Institute of Technology) (submittedVersion)
HAL (submittedVersion)
ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) (submittedVersion, cc-by-nc-nd)
eScholarship (California Digital Library) (submittedVersion)
mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
Spiral (Imperial College London) (submittedVersion, cc-by-nc-nd)
Funders: NIH (NS084863, HL128264, HL114477, HL117829, HL092577, HD069623, HL105780, HL096576)
Inflammatory Bowel Disease Grant (DK43351)
Boston Area Diabetes and Endocrinology Research Center (BADERC) Award (DK57521)
Fonds voor Wetenschappelijk Onderzoek-Vlaanderen
Marie Curie International Outgoing Fellowship
7th European Community Framework Program (PIOF-GA-2012-328352)
German Center for Cardiovascular Research (DZHK
American Heart Association (14FTF20380185, 13EIA14220013)
Deutsche Forschungsgemeinschaft (SA1668/2-1)
European Research Council Advanced Grant CardioNect
Baden Wurttemberg Sonderlinie Medizin
Established Investigator Award
Fondation Leducq (14CVD01)
MGH Research Scholar Program
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Keywords: cardiac macrophages, atrioventricular node, cardiac conduction, connexin 43, gap junctions, atrioventricular block, channelrhodopsin-2, macrophage depletion, resting membrane potential, repolarization
MeSH terms: Animals, Female, Heart Atria, Heart Conduction System, Humans, Macrophages, Male, Mice, Inbred C57BL, Middle Aged, Connexin 43, Myocytes, Cardiac, Mice

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