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Blood vessel-resident macrophages safeguard blood and vessel integrity in zebrafish

ABSTRACT: Macrophages are essential in immune defence, tissue development and maintenance, and are involved in disease onset and progression. Their function is influenced by their microenvironment and origin. While tissue-resident macrophages originate from yolk sac progenitors and persist in some adult tissues through self-renewal, no dedicated macrophage population is known to function within the vast network of blood vessels, despite the importance of maintaining a healthy vascular and blood system. Here, using high spatiotemporal live imaging of zebrafish embryos, we identified a distinctive population of macrophages residing within blood vessels, which we term blood vessel-resident macrophages (bMs). bMs actively survey the bloodstream, clearing foreign particles and unfit cells, and are the first responders to endothelial damage. bMs emerge directly from axial vessels through an atypical endothelial-to-macrophage transition (EMacT), independent of Runx1 and Csf1r, both essential for hematopoiesis and myelopoiesis, respectively. We further demonstrate that bMs are evolutionary conserved in mice. Our data thus unveil the existence of a specialized population of macrophages that function within the vasculature to safeguard blood from foreign threats and maintain blood vessel integrity. These discoveries broaden our understanding of immune surveillance, opening new avenues for treating bloodborne and vascular diseases.

ORGANISM(S): Danio rerio

PROVIDER: GSE296640 | GEO | 2026/03/10

REPOSITORIES: GEO

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Project description:Vascular endothelial and hematopoietic cells hold a close relationship that is initiated during development, but that continuously broadens to include new functions aimed at maintaining homeostasis in the adult organism. Here, we report on a population of aortic intimal resident macrophages (MacAIRs) that is a permanent feature of the inner vessel wall (tunica intima) of the aorta in regions of turbulent flow and that shares the luminal surface with the endothelium. MacAIRs were found to be transcriptionally distinct from other macrophages and closely associated with the endothelium in the absence of pathology. Lineage tracing analysis indicated that adult MacAIRs were derived from definitive hematopoietic lineage precursors that migrated from the ductus arteriosus seeding the aorta immediately post-birth in areas of turbulent flow including the lesser curvature of the aortic arch and branch openings. These aortic resident macrophages expanded via direct cell renewal and continued to grow in aged aortae to also populate regions of laminar flow. Binding of MacAIRs relied heavily on expression of endothelial ICAM that interacts with CD11c on macrophages. Genetic deletion of CD11c significantly impaired anchorage of MacAIRs to the endothelium. To clarify the biological significance of this population of macrophages, we used a dual diphtheria toxin induced-depletion system that efficiently eliminated MacAIRs in adult mice. Utilizing this model, we found that absence of MacAIRs led to progressive fibrin accumulation and formation of microclots that, once dislodged, can cause blockade of vessels and organ failure. In fact, 40% of the animals with genetic-mediated depletion of MacAIRs died within 2 weeks post-depletion suggesting that these macrophages were required to clear fibrin deposits in regions of turbulent blood flow. These findings advance our knowledge of how vascular endothelial cells profit from this unique interaction with macrophages to control hemostasis, prevent intravascular clotting, and ensure vascular health.

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Blood vessel-resident macrophages safeguard blood and vessel integrity in zebrafish

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