Abstract
In the testis, interstitial macrophages are thought to be derived from the yolk sac during fetal development, and later replaced by bone marrow-derived macrophages. By contrast, the peritubular macrophages have been reported to emerge first in the postnatal testis and solely represent descendants of bone marrow-derived monocytes. Here, we define new monocyte and macrophage types in the fetal and postnatal testis using high-dimensional single-cell analyses. Our results show that interstitial macrophages have a dominant contribution from fetal liver-derived precursors, while peritubular macrophages are generated already at birth from embryonic precursors. We find that bone marrow-derived monocytes do not substantially contribute to the replenishment of the testicular macrophage pool even after systemic macrophage depletion. The presence of macrophages prenatally, but not postnatally, is necessary for normal spermatogenesis. Our multifaceted data thus challenge the current paradigms in testicular macrophage biology by delineating their differentiation, homeostasis and functions.
Highlights
In the testis, interstitial macrophages are thought to be derived from the yolk sac during fetal development, and later replaced by bone marrow-derived macrophages
We demonstrate that under normal physiological conditions, tissue-resident macrophages in the adult testis are derived from embryonic precursors and that postnatally the macrophages are dispensable for spermatogenesis
We report here that high-dimensional single-cell analyses reveal the presence of many more monocyte and macrophage types in the testis than previously appreciated
Summary
Interstitial macrophages are thought to be derived from the yolk sac during fetal development, and later replaced by bone marrow-derived macrophages. We define new monocyte and macrophage types in the fetal and postnatal testis using high-dimensional single-cell analyses. It is thought that the peritubular macrophages are derived from circulating, bone-marrow-derived monocytes[31], and that the interstitial macrophages originate from fetal, yolk-sac-derived cells but are replaced by bone-marrow-derived macrophages after birth[23]. We demonstrate that under normal physiological conditions, tissue-resident macrophages in the adult testis are derived from embryonic precursors and that postnatally the macrophages are dispensable for spermatogenesis. These findings profoundly alter our understanding of the heterogeneity, origins, and functions of macrophages in the testis, and reveal their unique adaptations when compared to tissue-resident macrophages at other locations
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