Cellular and molecular attributes of neural stem cell niches in adult zebrafish brain

Abstract

Adult neurogenesis is a complex, presumably conserved phenomenon in vertebrates with a broad range of variations regarding neural progenitor/stem cell niches, cellular composition of these niches, migratory patterns of progenitors and so forth among different species. Current understanding of the reasons underlying the inter-species differences in adult neurogenic potential, the identification and characterization of various neural progenitors, characterization of the permissive environment of neural stem cell niches and other important aspects of adult neurogenesis is insufficient. In the last decade, zebrafish has emerged as a very useful model for addressing these questions. In this review, we have discussed the present knowledge regarding the neural stem cell niches in adult zebrafish brain as well as their cellular and molecular attributes. We have also highlighted their similarities and differences with other vertebrate species. In the end, we shed light on some of the known intrinsic and extrinsic factors that are assumed to regulate the neurogenic process in adult zebrafish brain. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1188-1205, 2017.

Conserved and Divergent Features of Adult Neurogenesis in Zebrafish

“…We will focus in this review on adult neurogenesis in the zebrafish telencephalon, which hosts the territories homologous to two main neurogenic niches of adult rodents: the sub-ependymal zone of the lateral ventricle (SEZ) and the sub-granular zone (SGZ) of the dentate gyrus of the hippocampus [for completeness on other territories, the reader is referred to other recent reviews or articles ( Than-Trong and Bally-Cuif, 2015 ; Anand and Mondal, 2017 ; Lindsey et al, 2018 )]. Following a process of eversion, likely involving both morphogenetic cell shape changes and anisotropic growth, the ventricle of the zebrafish dorsal telencephalon (pallium) becomes exposed dorsally, covered by an enlarged choroid plexus, with its dorsal midline flipped to lateral positions ( Folgueira et al, 2012 ).…”

“…The fundamental importance of NSCs stimulated an explosive research field during the last 20-years, and, more recently, the development of a new study model: the zebrafish adult brain. The large amount of adult NSCs in this system, their widespread distribution and varied properties, and their reactivity toward regeneration, all propelled the zebrafish model to the forefront of adult NSC research, as a complementary and synergistic model to rodents (Anand and Mondal, 2017;Lindsey et al, 2018;Zambusi and Ninkovic, 2020). The time to reach sexual maturity in zebrafish (3 months) and the adult lifespan also approximate those of mouse, allowing to draw direct temporal parallels.…”

Hedgehog Signaling Regulates Neurogenesis in the Larval and Adult Zebrafish Hypothalamus

“…Similar to more dorsal neurogenic zones, hypothalamic proliferation requires highly coordinated regulation of cell proliferation and differentiation within a discrete population of progenitors. Cell-cell signaling systems that regulate nervous system development such as the Notch, Fibroblast Growth Factor (FGF), Wnt, Hedgehog (Hh), and Bone Morphogenetic (BMP) signaling pathways play a key role in controlling adult neurogenesis (Kizil et al, 2012;Petrova and Joyner, 2014;Anand and Mondal, 2017;Obernier and Alvarez-Buylla, 2019). Heterogeneity in both neural stem cell populations and in cell-cell signaling systems helps control the range of differentiated cell types that are produced in stem cell niches (Marz et al, 2010;Chaker et al, 2016;Lim and Alvarez-Buylla, 2016;Ceci et al, 2018).…”

“…While Hh signaling has been shown to be a key component of hypothalamic-pituitary axis development during embryogenesis (Kondoh et al, 2000;Guner et al, 2008;Blackshaw et al, 2010;Bergeron et al, 2011;Muthu et al, 2016), a role in the post-embryonic and adult hypothalamus has not been documented. The zebrafish brain, which maintains up to 16 proliferative zones throughout life, has proven to be a powerful model for studying adult neurogenesis (Grandel et al, 2006;Schmidt et al, 2013;Anand and Mondal, 2017). Work in the zebrafish has defined a role for notch signaling in the telencephalon (Chapouton et al, 2010;Chapouton et al, 2011;Rothenaigner et al, 2011) and uncovered a key role for Wnt signaling in hypothalamic neurogenesis, with Wnt signaling being required for the formation of distinct neuronal subtypes and disruptions in Wnt-mediated hypothalamic proliferation leading to reduced growth and behavioral effects (Wang et al, 2012;Duncan et al, 2016;).…”

Nerve growth factor is expressed and stored in central neurons of adult zebrafish

“…Among teleost fish, zebrafish ( Danio rerio ) is widely used as model species for developmental genetic studies and functional mechanisms of numerous genes responsible for human diseases (D'Angelo et al., ,b). In addition, zebrafish brain has been largely utilized in numerous studies devoted to adult neurogenesis (Pellegrini et al., ; Diotel et al., ; Coumailleau et al., ; Than‐Trong & Bally‐Cuif, ; Anand & Mondal, ) and regenerative ability after injury (Cosacak et al., ; Alunni & Bally‐Cuif, ; Cacialli et al., ,b).…”