Oligodendrocyte precursor cells generate pituicytes in vivo during neurohypophysis development

Abstract

In the vertebrate brain, much remains to be understood concerning the origin of glial cell diversity and the potential lineage relationships between the various types of glia. Besides astrocytes and myelin-forming oligodendrocytes, other macroglial cell populations are found in discrete areas of the central nervous system (CNS). They share functional features with astrocytes and oligodendrocytes but also display specific characteristics. Such specialized cells, called pituicytes, are located in the neurohypophysis (NH). Our work focuses on the lineage of the pituicytes during rodent development. First, we show that cells identified with a combination of oligodendrocyte precursor cell (OPC) markers are present in the developing rat NH. In culture, neonatal NH progenitors also share major functional characteristics with OPCs, being both migratory and bipotential, i.e. able to give rise to type 2 astrocytes and oligodendrocytes. We then observe that, either in vitro or after transplantation into myelin-deficient Shiverer brain, pieces of NH generate myelinating oligodendrocytes, confirming the oligodendrogenic potentiality of NH cells. However, no mature oligodendrocyte can be found in the NH. This led us to hypothesize that the OPCs present in the developing NH might be generating other glial cells, especially the pituicytes. Consistent with this hypothesis, the OPCs appear during NH development before pituicytes differentiate. Finally, we establish a lineage relationship between olig1+ cells, most likely OPCs, and the pituicytes by fate-mapping experiments using genetically engineered mice. This constitutes the first demonstration that OPCs generate glial cells other than oligodendrocytes in vivo.

Single-cell molecular and cellular architecture of the mouse neurohypophysis

“…Importantly, previous reports have described the existence of OPCs in the NH (Miyata, 2017;Virard et al, 2006Virard et al, , 2008. We did not detect OPCs in the present study, however, this could be due to low abundance of these cells in our tissue.…”

“…Alternatively, because Virard et al relied on Pdgfra as a sole OPC marker, it is possible that they misidentified VLMCs as OPCs. Notably, Virard et al reported that these Pdgfra + cells were shown to be pituicyte progenitors in their study (Virard et al, 2006). Similarly, other studies reported that VLMC display multipotent stem cell niche function in the CNS and other organs suggesting that they may play a similar roles in NH function (Nakagomi and Matsuyama, 2017;Ueharu et al, 2018).…”

Enriched environment promotes adult neural progenitor cell mobilization in mouse demyelination models

“…Proteolipid protein (plp) in situ hybridization was performed as described in Virard et al . (2006).…”

Isolation of tumour stem-like cells from benign tumours

“…Lineage analysis and transcriptional control studies in developing pituitary gland generated knowledge about pituitary tissue stem cells and their functions (Zhu and Rosenfeld, 2004;Lee et al, 2005;Virard et al, 2006;Zhu et al, 2006). Vankelecom and colleagues isolated murine pituitary cells from side populations that can be clonally expanded and share many stem cell characteristics Krylyshkina et al, 2005;Vankelecom, 2007).…”