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Cardiac-immune microniches programme macrophage states in the regenerating heart

Abstract:
Adult zebrafish regenerate their hearts after injury, a process that requires macrophages, yet how local tissue microenvironments instruct macrophage states and function remains unclear. Here we combine single cell RNA sequencing with Visium and high-resolution MERFISH spatial transcriptomics to map the cardio-immune landscape of homeostatic and regenerating zebrafish hearts. We identify a mpeg1.1+ compartment comprising macrophages, dendritic, B and NK-like cells, and show that injury establishes a macrophage-centred immune environment with transcriptional programmes spanning resident surveillance, damage sensing, inflammation, antigen presentation, resolution and metabolic support. Communication-aware spatial modelling reveals that these states are not randomly distributed but organised into discrete structural-immune microniches across the injury region, each defined by stereotyped cellular compositions and ligand-receptor circuits. Within a fibroblast-macrophage microniche, we uncover an il34-csf1ra-egr1 axis in which col12a1a+ il34+ fibroblasts promote an egr1 pro-regenerative macrophage state that couples fibrosis, vascular integrity and epicardial signalling. We show that disruption of this axis by csf1ra loss of function reduces macrophage-, endothelial- and epicardial-rich microniches, amplifying fibroblast-driven domains that shift macrophages towards stress and long-sustained inflammatory programmes, thereby biasing early injury response towards a pro-fibrotic state. Our work establishes spatially defined cardio-immune microniches as key organisers of macrophage function and regenerative outcome, providing a mechanistic framework and actionable targets for reprogramming cardiac repair.
Publication status:
Published
Peer review status:
Not peer reviewed

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Preprint server copy:
10.64898/2026.03.05.709830

Authors

More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Sub department:
IDRM (DPAG)
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Sub department:
IDRM (DPAG)
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Sub department:
IDRM (DPAG)
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Sub department:
IDRM (DPAG)
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy and Genetics
Sub department:
IDRM (DPAG)
Role:
Author


More from this funder
Funder identifier:
https://ror.org/02wdwnk04
Grant:
FS/IBSRF/21/25088
RE/18/3/34214
More from this funder
Funder identifier:
https://ror.org/052gg0110


Preprint server:
bioRxiv
Publication date:
2026-03-07
DOI:


Language:
English
Pubs id:
2395937
Local pid:
pubs:2395937
Deposit date:
2026-05-13
ARK identifier:

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