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Glial Cell Development and Function in Zebrafish Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Glial Cell Development and Function in Zebrafish David A. Lyons1 and William S. Talbot2 1Centre for Neuroregeneration, University of Edinburgh, Edinburgh EH16 4SB, United Kingdom 2Department of Developmental Biology, Stanford University, Stanford, California 94305 Correspondence: [email protected] The zebrafish is a premier vertebrate model system that offers many experimental advantages for in vivo imaging and genetic studies. This review provides an overview of glial cell types in the central and peripheral nervous system of zebrafish. We highlight some recent work that exploited the strengths of the zebrafish system to increase the understanding of the role of Gpr126 in Schwann cell myelination and illuminate the mechanisms controlling oligoden- drocyte development and myelination. We also summarize similarities and differences between zebrafish radial glia and mammalian astrocytes and consider the possibility that their distinct characteristics may represent extremes in a continuum of cell identity. Finally, we focus on the emergence of zebrafish as a model for elucidating the development and function of microglia. These recent studies have highlighted the power of the zebrafish system for analyzing important aspects of glial development and function. ollowing the pioneering work of George Ho and Kane 1990; Hatta et al. 1991; Grunwald FStreisinger in the early 1980s, the zebrafish and Eisen 2002), attracting many researchers has emerged as a premier vertebrate model sys- from other fields to the zebrafish system. Follow- tem (Streisingeret al. 1981). A keystrength of the ing the explosion of interest in the zebrafish in zebrafish is that the embryos and early larvae are the 1990s, advances in many areas have added to transparent, allowing exquisite cellular analysis the strengths of the system, including large-scale of many dynamic processes, including cell mi- screens that identified thousands of new muta- gration, axonal pathfinding, and myelination, tions (Driever et al. 1996; Haffter et al. 1996), among many others (e.g., Gilmour et al. 2002; rapid transgenesis (Kawakami et al. 2004), new Lyons et al. 2005; Czopka et al. 2013). The zebra- methods for imaging and tracking all cells dur- fish also has many advantages for large-scale ge- ing development (Huisken 2012), genetic map- netic studies, including relatively small size and ping and sequencing to identify genes and mu- rapid development, high fecundity, and the abil- tated loci (Postlethwait et al. 1994; Howe et al. ity to manipulate the ploidy of gametes and ear- 2013), optogenetic methods to control neural ly embryos (Kimmel 1989). Through the 1980s activity (Portugues et al. 2013), the advent of and early 1990s, insightful studies of several in- targeted nucleases to create mutations in genes teresting mutations elegantly exploited these ex- of interest (Huang et al. 2011; Sander et al. 2011; perimental advantages (e.g., Kimmel et al. 1989; Bedell et al. 2012; Chang et al. 2013; Hwang et al. Editors: Ben A. Barres, Marc R. Freeman, and Beth Stevens Additional Perspectives on Glia available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a020586 1 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press D.A. Lyons and W.S. Talbot 2013), and small molecule screening approaches including axonal neuregulin signals and their to isolate compounds with novel biological ac- glial ErbB receptors and key Schwann cell tran- tivities in vivo (Peterson and Fishman 2011). scription factors including Sox10, Oct6, Brn2, Many fundamental similarities in physiolo- and Krox20 (Jessen and Mirsky 2005; Nave and gy and body plan unite the zebrafish and other Salzer 2006; Pereira et al. 2012). Analysis of ex- vertebrates (Kimmel 1989). In addition, analy- pression patterns, cell behavior, and mutant sis of genes and genomes has revealed that se- phenotypes in zebrafish indicates that the func- quence, expression, and function of many genes tions of these genes are broadly conserved are conserved among zebrafish and other ver- among vertebrates (e.g., Kegel et al. 2014; re- tebrates (Postlethwait and Talbot 1997; Howe viewed in Raphael and Talbot 2011). et al. 2013). Thus, insights from studies in ze- A number of approaches have identified ze- brafish will apply broadly to other vertebrates, brafish mutations disrupting Schwann cell de- including humans. On the other hand, there velopment and differentiation, including dif- are important genetic, genomic, and physiolog- ferent genetic screens, as well as reverse genetic ical differences among vertebrates. It is, there- approaches to explore candidate genes, such as fore, important to keep possible differences in krox20 (Dutton et al. 2001; Grant et al. 2005; mind and to recognize that analyzing the diver- Pogoda et al. 2006; Monk et al. 2009). In addi- sity among different species mayenhance overall tion to showing that many genes previously understanding of important processes. For ex- known to have important roles in mammals ample, zebrafish and other teleosts have a much have conserved functions in zebrafish, these more extensive regenerative ability than mam- studies highlighted some new functions of these mals, so that studies of fin, heart, and spinal genes, including, for example, the role of axonal cord regeneration in zebrafish may suggest ave- Nrg1-TypeIII as a guidance cue that directs the nues toward new therapeutic approaches in migration of Schwann cells in growing nerves humans (Gemberling et al. 2013; Becker and (Lyons et al. 2005; Perlin et al. 2011). Moreover, Becker 2014). analysis of mutants lacking Schwann cells has In this review, we provide an overview of defined some interesting functions of the cells different types of glia in the zebrafish, with a themselves, including controlling the timing focus on some recent studies that highlight the of sensory organ differentiation, preventing ac- power of the zebrafish system to analyze differ- cumulation of voltage-gated sodium channels ent aspects of glial development and function. at inappropriate locations along axons, and re- modeling the basement membrane of the skin (Grant et al. 2005; Voaset al. 2009; Raphael et al. SCHWANN CELLS 2010; Lush and Piotrowski 2014). These topics Schwann cells are the myelinating glia of periph- have been reviewed extensively (Raphael and eral nerves (Jessen and Mirsky 2005). Schwann Talbot 2011; Pereira et al. 2012; Glenn and Tal- cell precursors, which derive from the neural bot 2013b). Therefore, we focus here on recent crest, migrate with growing axons as nerves are characterization of Gpr126, a gene with essen- developing. After migration is complete, the tial function in myelination that was defined process of radial sorting begins, during which initially using genetic approaches in zebrafish. Schwann cells associate with individual axons in the bundle of the developing nerve (Jessen Gpr126 and Mirsky 2005; Raphael and Talbot 2011). A promyelinating Schwann cell associates with a A screen for disruptions in myelinating glia large-diameter axon and begins the process of identified a number of mutants lacking mye- myelination, which culminates with the forma- lin basic protein (mbp) expression in Schwann tion of a compact myelin sheath. Many studies cells (Pogoda et al. 2006). Initial phenotypic in mammals have defined important regulators studies showed that most of these mutations of Schwann cell development and myelination, disrupted early stages of Schwann cell develop- 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a020586 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Glial Cell Development and Function in Zebrafish ment. In contrast, two allelic mutations had Ultrastructural analysis of the mutants con- normal expression of early Schwann cell and firmed that Schwann cells are present and asso- axonal markers, despite the absence of mbp ex- ciated with apparently normal axons in gpr126 pression, suggesting that the mutated gene was mutants (Fig. 1A). The Schwann cells in gpr126 essential for the initiation of myelination (Po- mutants did not progress beyond the promyeli- goda et al. 2006). nating stage (Fig. 1A), indicating that Gpr126 Genetic mapping and positional cloning is essential to initiate myelination (Monk et al. showed that these mutations disrupt Gpr126, 2009). Analysis of a Gpr126 knockout mouse an orphan member of the adhesion class of G (Fig. 1A) showed that its function in the initia- protein–coupled receptors (Monk et al. 2009). tion of myelination is conserved in mammals Control gpr126 mutant A B Gpr126 Gs Zebrafish Adcy6 cAMP PKA Mouse CREB oct6 HLT C SP CUB PTX HBD GAIN 1234567 st49 Tyr > Stop Figure 1. The role of Gpr126in Schwann cellmyelination.(A)In zebrafish andmouse, gpr126 mutants lack myelin in peripheral nerves. In control animals, compact myelin is evident in transmission electron micrographs of the posterior lateral line nerve from adult zebrafish (top) and the sciatic nerve of P12 mouse (bottom). In corre- sponding images from gpr126 mutants, Schwann cells associatewith axons but do not form myelin. Scale bars, 0.5 mm. (From Monk et al. 2009; reprinted,
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