Ultrastructural characteristics of oligodendrocyte precursor cells in the early postnatal mouse optic nerve observed by serial block-face scanning electron microscopy

Abstract

Oligodendrocyte precursor cells (OPC) arise from restricted regions of the central nervous system (CNS) and differentiate into myelin-forming cells after migration, but their ultrastructural characteristics have not been fully elucidated. This study examined the three-dimensional ultrastructure of OPCs in comparison with other glial cells in the early postnatal optic nerve by serial block-face scanning electron microscopy. We examined 70 putative OPCs (pOPC) that were distinct from other glial cells according to established morphological criteria. The pOPCs were unipolar in shape with relatively few processes, and their Golgi apparatus were localized in the perinuclear region with a single cisterna. Astrocytes abundant in the optic nerve were distinct from pOPCs and had a greater number of processes and more complicated Golgi apparatus morphology. All pOPCs and astrocytes contained a pair of centrioles (basal bodies). Among them, 45% of pOPCs extended a short cilium, and 20% of pOPCs had centrioles accompanied by vesicles, whereas all astrocytes with basal bodies had cilia with invaginated ciliary pockets. These results suggest that the fine structures of pOPCs during the developing and immature stages may account for their distinct behavior. Additionally, the vesicular transport of the centrioles, along with a short cilium length, suggests active ciliogenesis in pOPCs.

Uncovering cilia function in glial development

“…Deviations from steady state function, either from injury or cellular stress, cause astrocytes to become reactive and adopt a specific morphological and functional response (Escartin et al, 2021). Astrocytes are ciliated; the analysis of developing astrocytes by electron micrograph (EM) imaging reveals that all astrocytes have a primary cilium (Ono et al, 2022). Indeed, developing astrocytes possess cilia from precursor stages through adulthood (Kasahara et al, 2014).…”

“…Astrocytes are ciliated; the analysis of developing astrocytes by electron micrograph (EM) imaging reveals that all astrocytes have a primary cilium (Ono et al., 2022). Indeed, developing astrocytes possess cilia from precursor stages through adulthood (Kasahara et al., 2014).…”

“…Importantly, OPCs lose cilia as they differentiate (Falcón‐Urrutia et al., 2015). Structural analyses of OPC cilia show that the basal body is located near the membrane, and OPCs have surface cilia, suggesting that OPC cilia form through extracellular ciliogenesis (Ono et al., 2022). OPCs express several genes associated with ciliary signaling, most of which have not been functionally explored (Zhang et al., 2014).…”

“…Cilia are not detected in microglia by conventional immunostaining markers in vivo (Sipos et al., 2018). EM imaging in the developing optic tract conclusively shows that microglia do not have a primary cilium (Ono et al., 2022). Microglia do retain a centriole pair, which provide the foundation for cilia in many cell types, but in some cases stand alone.…”

Leukemia inhibitory factor shortens primary cilia by upregulating C‐C motif chemokine 2 in human neural stem/progenitor cells

“…Then, to evaluate primary cilia more precisely, it is better to label cilia with centrioles, because basal body is a marker for the existence of primary cilia (Satir & Christensen, 2007). Furthermore, because primary cilia of NSPCs are known to have characteristic structures including ciliary remnant and ciliary pockets, the analyses with three‐dimensional scanning electron microscopy (3D‐SEM) might offer more novel and valuable insights (Ono et al, 2022; Paridaen et al, 2013). Nonetheless, our study found LIF‐induced shortening of primary cilia via increasing CCL2 expression and revealed a novel mechanism of the regulation of primary cilia in human NSPCs.…”