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@ARTICLE{Krammer:255141,
author = {Krammer, Christine and Yang, Bishan and Reichl, Sabrina and
Besson-Girard, Simon and Ji, Hao and Bolini, Verena and
Schulte, Corinna and Noels, Heidi and Schlepckow, Kai and
Jocher, Georg and Werner, Georg and Willem, Michael and El
Bounkari, Omar and Kapurniotu, Aphrodite and Gökce, Ozgun
and Weber, Christian and Mohanta, Sarajo and Bernhagen,
Jürgen},
title = {{P}athways linking aging and atheroprotection in
{M}if-deficient atherosclerotic mice.},
journal = {The FASEB journal},
volume = {37},
number = {3},
issn = {0892-6638},
address = {Hoboken, NJ},
publisher = {Wiley},
reportid = {DZNE-2023-00260},
pages = {e22752},
year = {2023},
abstract = {Atherosclerosis is a chronic inflammatory condition of our
arteries and the main underlying pathology of myocardial
infarction and stroke. The pathogenesis is age-dependent,
but the links between disease progression, age, and
atherogenic cytokines and chemokines are incompletely
understood. Here, we studied the chemokine-like inflammatory
cytokine macrophage migration inhibitory factor (MIF) in
atherogenic Apoe-/- mice across different stages of aging
and cholesterol-rich high-fat diet (HFD). MIF promotes
atherosclerosis by mediating leukocyte recruitment, lesional
inflammation, and suppressing atheroprotective B cells.
However, links between MIF and advanced atherosclerosis
across aging have not been systematically explored. We
compared effects of global Mif-gene deficiency in 30-, 42-,
and 48-week-old Apoe-/- mice on HFD for 24, 36, or 42 weeks,
respectively, and in 52-week-old mice on a 6-week HFD.
Mif-deficient mice exhibited reduced atherosclerotic lesions
in the 30/24- and 42/36-week-old groups, but
atheroprotection, which in the applied Apoe-/- model was
limited to lesions in the brachiocephalic artery and
abdominal aorta, was not detected in the 48/42- and
52/6-week-old groups. This suggested that atheroprotection
afforded by global Mif-gene deletion differs across aging
stages and atherogenic diet duration. To characterize this
phenotype and study the underlying mechanisms, we determined
immune cells in the periphery and vascular lesions, obtained
a multiplex cytokine/chemokine profile, and compared the
transcriptome between the age-related phenotypes. We found
that Mif deficiency promotes lesional macrophage and T-cell
counts in younger but not aged mice, with subgroup analysis
pointing toward a role for Trem2+ macrophages. The
transcriptomic analysis identified pronounced MIF- and
aging-dependent changes in pathways predominantly related to
lipid synthesis and metabolism, lipid storage, and brown fat
cell differentiation, as well as immunity, and
atherosclerosis-relevant enriched genes such as Plin1, Ldlr,
Cpne7, or Il34, hinting toward effects on lesional lipids,
foamy macrophages, and immune cells. Moreover, Mif-deficient
aged mice exhibited a distinct plasma cytokine/chemokine
signature consistent with the notion that mediators known to
drive inflamm'aging are either not downregulated or even
upregulated in Mif-deficient aged mice compared with the
corresponding younger ones. Lastly, Mif deficiency favored
formation of lymphocyte-rich peri-adventitial leukocyte
clusters. While the causative contributions of these
mechanistic pillars and their interplay will be subject to
future scrutiny, our study suggests that atheroprotection
due to global Mif-gene deficiency in atherogenic Apoe-/-
mice is reduced upon advanced aging and identifies
previously unrecognized cellular and molecular targets that
could explain this phenotype shift. These observations
enhance our understanding of inflamm'aging and MIF pathways
in atherosclerosis and may have implications for
translational MIF-directed strategies.},
keywords = {Animals / Mice / Macrophage Migration-Inhibitory Factors:
genetics / Macrophage Migration-Inhibitory Factors:
metabolism / Atherosclerosis: metabolism / Chemokines /
Aging / Apolipoproteins E: metabolism / Mice, Knockout /
Mice, Inbred C57BL / Plaque, Atherosclerotic / Membrane
Glycoproteins / Receptors, Immunologic / MIF (Other) / aging
(Other) / artery tertiary lymphoid organ (Other) /
atherosclerosis (Other) / atypical chemokines (Other) /
chemokines (Other) / Macrophage Migration-Inhibitory Factors
(NLM Chemicals) / Chemokines (NLM Chemicals) /
Apolipoproteins E (NLM Chemicals) / Trem2 protein, mouse
(NLM Chemicals) / Membrane Glycoproteins (NLM Chemicals) /
Receptors, Immunologic (NLM Chemicals)},
cin = {AG Haass / AG Lichtenthaler},
ddc = {570},
cid = {I:(DE-2719)1110007 / I:(DE-2719)1110006},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:36794636},
doi = {10.1096/fj.202200056R},
url = {https://pub.dzne.de/record/255141},
}