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HomeScience ImmunologyVol. 7, No. 75C/EBPβ regulates lipid metabolism and Pparg
isoform 2 expression in alveolar macrophages
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C/EBPΒ REGULATES LIPID METABOLISM AND PPARG ISOFORM 2 EXPRESSION IN ALVEOLAR
MACROPHAGES

Dorothea Dörr https://orcid.org/0000-0001-8575-7560Benedikt Obermayer
https://orcid.org/0000-0002-9116-630XJanuary Mikolaj Weiner
https://orcid.org/0000-0003-1438-7819Karin ZimmermannChiara Anania
https://orcid.org/0000-0003-1549-4157Lisa Katharina WagnerEkaterini Maria Lyras
https://orcid.org/0000-0003-3269-0854Valeriia SapozhnikovaDavid Lara-Astiaso
https://orcid.org/0000-0001-8686-4675Felipe Prósper
https://orcid.org/0000-0001-6115-8790Roland LangDarío G. Lupiáñez
https://orcid.org/0000-0002-3165-036XDieter Beule
https://orcid.org/0000-0002-3284-0632Uta E. HöpkenAchim Leutz
https://orcid.org/0000-0001-8259-927Xand [...]Alexander Mildner
https://orcid.org/0000-0002-2019-8427 alexander.mildner@utu.fi +7 authors
Authors Info & Affiliations
Science Immunology
16 Sep 2022
Vol 7, Issue 75
DOI: 10.1126/sciimmunol.abj0140

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 * Alveolar macrophage development and function
 * Abstract
 * Supplementary Materials
 * REFERENCES AND NOTES


ALVEOLAR MACROPHAGE DEVELOPMENT AND FUNCTION

Alveolar macrophages (AMs) are specialized macrophages that serve several key
functions in the lung. Here, Dörr et al. used transcriptomic, ChIPmentation, and
chromatin accessibility analysis to demonstrate that the transcription factor
CCAAT/enhancer binding protein beta (C/EBPβ) is required for AM development.
C/EBPβ-deficient AMs had defects in proliferation, lipid metabolism, and
phagocytosis, thus causing mice to have symptoms that resemble pulmonary
alveolar proteinosis (PAP). They observed that the long C/EBPβ protein variants
LAP* and LAP, combined with CSF2 signaling, induced specific expression of Pparg
isoform 2, which is a mechanism that they also observed in other CSF2-primed
macrophages. These findings indicate that C/EBPβ is a key regulator of AM
development and lipid metabolism.


ABSTRACT

Pulmonary alveolar proteinosis (PAP) is a syndrome characterized by accumulation
of surfactant lipoproteins within the lung alveoli. Alveolar macrophages (AMs)
are crucial for surfactant clearance, and their differentiation depends on
colony-stimulating factor 2 (CSF2), which regulates the establishment of an
AM-characteristic gene regulatory network. Here, we report that the
transcription factor CCAAT/enhancer binding protein β (C/EBPβ) is essential for
the development of the AM identity, as demonstrated by transcriptome and
chromatin accessibility analysis. Furthermore, C/EBPβ-deficient AMs showed
severe defects in proliferation, phagocytosis, and lipid metabolism,
collectively resulting in a PAP-like syndrome. Mechanistically, the long C/EBPβ
protein variants LAP* and LAP together with CSF2 signaling induced the
expression of Pparg isoform 2 but not Pparg isoform 1, a molecular regulatory
mechanism that was also observed in other CSF2-primed macrophages. These results
uncover C/EBPβ as a key regulator of AM cell fate and shed light on the
molecular networks controlling lipid metabolism in macrophages.


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Volume 7 | Issue 75
September 2022

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ACKNOWLEDGMENTS

We thank V. Malchin, S. Jaksch, and J. Voß for excellent technical support, as
well as the MDC animal facility, especially J. Bergemann, the MDC FACS core
unit, H.-P. Rahn, and the MDC genomic core facility, especially
D. Sunaga-Franze. We thank E. Kowenz-Leutz for the donation of C/EBPβ expression
constructs and I. Amit for support. The Csf2rb−/− line was kindly provided by
M. Sieweke (Center for Regenerative Therapies, Dresden, Germany). We also thank
C. J. L. Elender and J. Favret for technical advice and S. Yona and S. Jung for
discussion. Computation has been performed on the HPC for Research Cluster of
the Berlin Institute of Health.
Funding: D.D. was funded by the international MDC PhD program and received a
travel grant from Boehringer Ingelheim Fonds. A.M. was a Heisenberg fellow
supported by the DFG (MI1328/3-1). A.M. was financially supported by the
InFLAMES Flagship Programme of the Academy of Finland (decision number:
337530). 
Author contributions: D.D. performed most experiments and analysis. B.O. and
J.M.W. were supervised by D.B. and performed bioinformatic analyses. A.M.,
L.K.W., E.M.L., V.S., and K.Z. helped with experiments and analysis. C.A. and
D.G.L. performed ChIPmentation experiments. R.L., D.L.-A., F.P., and U.E.H.
provided mouse lines and technical expertise. A.L. provided financial support,
laboratory space, supervision, discussion, review, and editing. A.M. designed
and supervised the study. D.D. and A.M. wrote the manuscript.
Competing interests: The authors declare that they have no competing interests.
Data and materials availability: All data needed to evaluate the conclusions in
the paper are present in the paper or the Supplementary Materials. Sequencing
data that were generated within this study have been deposited in the GEO
database with the accession code GSE173970. Microarray data of CD11c-Cre Pparg
flox and control AMs used for transcriptomic comparison to Cebpb KO AMs were
downloaded from GEO (GSE60249).


AUTHORS

AFFILIATIONSEXPAND ALL

Dorothea Dörr https://orcid.org/0000-0001-8575-7560
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Institute of Biology, Humboldt University of Berlin, Berlin, Germany.
Roles: Conceptualization, Data curation, Formal analysis, Investigation,
Methodology, Project administration, Validation, Visualization, and Writing -
original draft.
View all articles by this author
Benedikt Obermayer https://orcid.org/0000-0002-9116-630X
Core Unit Bioinformatics, Berlin Institute of Health,
Charité-Universitätsmedizin Berlin, Berlin, Germany.
Roles: Data curation, Formal analysis, Resources, Software, and Visualization.
View all articles by this author
January Mikolaj Weiner https://orcid.org/0000-0003-1438-7819
Core Unit Bioinformatics, Berlin Institute of Health,
Charité-Universitätsmedizin Berlin, Berlin, Germany.
Role: Formal analysis.
View all articles by this author
Karin Zimmermann
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Roles: Formal analysis, Methodology, Resources, Software, Visualization, and
Writing - review & editing.
View all articles by this author
Chiara Anania https://orcid.org/0000-0003-1549-4157
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin Institute for Medical Systems Biology (BIMSB), Epigenetics and Sex
Development Group, Berlin, Germany.
Roles: Investigation and Validation.
View all articles by this author
Lisa Katharina Wagner
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Roles: Investigation, Methodology, and Resources.
View all articles by this author
Ekaterini Maria Lyras https://orcid.org/0000-0003-3269-0854
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Role: Investigation.
View all articles by this author
Valeriia Sapozhnikova
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Role: Investigation.
View all articles by this author
David Lara-Astiaso https://orcid.org/0000-0001-8686-4675
Advanced Genomics Laboratory, Program of Hemato-Oncology, Center for Applied
Medical Research (CIMA), University of Navarra, Pamplona, Spain.
Roles: Methodology and Resources.
View all articles by this author
Felipe Prósper https://orcid.org/0000-0001-6115-8790
Program of Regenerative Medicine, Program of Hemato-Oncology, Center for Applied
Medical Research (CIMA), University of Navarra, Pamplona, Spain.
Instituto de Investigación Sanitaria de Navarra (IdiSNA), Pamplona, Spain.
Roles: Funding acquisition, Investigation, Methodology, Resources, and Writing -
review & editing.
View all articles by this author
Roland Lang
Institute of Clinical Microbiology, Immunology, and Hygiene,
Universitätsklinikum Erlangen, Friedrich-Alexander-Universität
Erlangen-Nürnberg, Erlangen, Germany.
Roles: Resources and Writing - review & editing.
View all articles by this author
Darío G. Lupiáñez https://orcid.org/0000-0002-3165-036X
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin Institute for Medical Systems Biology (BIMSB), Epigenetics and Sex
Development Group, Berlin, Germany.
Role: Investigation.
View all articles by this author
Dieter Beule https://orcid.org/0000-0002-3284-0632
Core Unit Bioinformatics, Berlin Institute of Health,
Charité-Universitätsmedizin Berlin, Berlin, Germany.
Roles: Data curation, Formal analysis, Methodology, Resources, Supervision,
Visualization, and Writing - review & editing.
View all articles by this author
Uta E. Höpken
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Roles: Resources and Writing - review & editing.
View all articles by this author
Achim Leutz https://orcid.org/0000-0001-8259-927X
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Institute of Biology, Humboldt University of Berlin, Berlin, Germany.
Roles: Conceptualization, Funding acquisition, Project administration,
Resources, Supervision, Validation, and Writing - review & editing.
View all articles by this author
Alexander Mildner* https://orcid.org/0000-0002-2019-8427
alexander.mildner@utu.fi
Max-Delbrück-Center for Molecular Medicine in Helmholtz Association (MDC),
Berlin, Germany.
Institute of Biomedicine, Medicity University of Turku, Turku, Finland.
InFLAMES Research Flagship Center, University of Turku, Turku, Finland.
Roles: Conceptualization, Funding acquisition, Investigation, Methodology,
Project administration, Resources, Supervision, Validation, Visualization,
Writing - original draft, and Writing - review & editing.
View all articles by this author

FUNDING INFORMATION

Deutsche Forschungsgemeinschaft: MI1328/3-1

NOTES

*
Corresponding author. Email: alexander.mildner@utu.fi


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