Wild-type bone marrow cells repopulate tissue resident macrophages and reverse the impacts of homozygous CSF1R mutation

Author:

Carter-Cusack DylanORCID,Huang Stephen,Keshvari SaharORCID,Patkar Omkar,Sehgal AnujORCID,Allavena RachelORCID,Byrne Robert,Morgan Paul,Bush Stephen J.ORCID,Summers Kim M.ORCID,Irvine Katharine M.ORCID,Hume David A.ORCID

Abstract

AbstractAdaptation to existence outside the womb is a key event in the life of a mammal. The absence of macrophages in rats with a homozygous mutation in theCsf1rgene (Csf1rko) severely compromises pre-weaning somatic growth and maturation of organ function. Transfer of wild-type bone marrow cells (BMT) at weaning rescues tissue macrophage populations permitting normal development and long-term survival. To dissect the phenotype and function of macrophages in postnatal development, we generated transcriptomic profiles of all major organs of wild-type andCsf1rkorats at weaning and selected organs following rescue by BMT. The transcriptomic profiles revealed subtle effects of macrophage deficiency on development of all major organs. Network analysis revealed a common signature of CSF1R-dependent resident tissue macrophages that includes the components of complement C1Q (C1qa/b/cgenes). Circulating C1Q was almost undetectable inCsf1rkorats and rapidly restored to normal levels following BMT. Tissue-specific macrophage signatures were also identified, notably including sinus macrophage populations in the lymph nodes. Their loss inCsf1rkorats was confirmed by immunohistochemical localisation of CD209B (SIGNR1). By 6-12 weeks,Csf1rkorats succumb to emphysema-like pathology associated with the selective loss of interstitial macrophages and granulocytosis. This pathology was reversed by BMT. Along with physiological rescue, BMT precisely regenerated the abundance and expression profiles of resident macrophages. The exception was the brain, where BM-derived microglia-like cells had a distinct expression profile compared to resident microglia. In addition, the transferred BM failed to restore blood monocyte or CSF1R-positive bone marrow progenitors. These studies provide a model for the pathology and treatment of CSF1R mutations in humans and the innate immune deficiency associated with prematurity.

Publisher

Cold Spring Harbor Laboratory

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