The nervous system of vertebrates is made of up of complex networks of nerve cells that send signals to one another. In addition to these cells, there are a number of supporting cells that help nerves carry out their role. Schwann cells, for example, help nerve cells to transmit information faster by wrapping their long extensions in a fatty membrane called myelin. When myelin is not produced properly, this can disturb the signals between nerve cells, leading to neurological defects.

Schwann cells mature simultaneously with nerve cells in the embryo. However, it was not fully understood how Schwann cells generate myelin during development. To investigate, Wiltbank et al. studied the embryos of zebrafish, which, unlike other vertebrates, are transparent and develop outside of the womb. These qualities make it easier to observe how cells in the nervous system grow in real-time using a microscope.

First, the team analyzed genetic data collected from the embryo of zebrafish and mice to search for genes that are highly abundant in Schwann cells during development. This led to the discovery of a gene called cd59, which codes for a protein that also interacts with the immune system. To find out whether Schwann cells rely on cd59, Wiltbank et al. deleted the cd59 gene in zebrafish embryos. Without cd59, the Schwann cells produced too many copies of themselves and this, in turn, impaired the appropriate production of myelin.

Since the protein encoded by cd59 normally balances inflammation levels, it was possible that losing this gene overactivated the immune system in the zebrafish embryos. In support of this hypothesis, when the cd59 mutant embryos were treated with an anti-inflammatory drug, this corrected Schwann cell overproduction and restored myelin formation.

Taken together, these findings reveal how inflammation helps determine the number of Schwann cells produced during development, and that cd59 prevents this process from getting carried away. This suggests that the nervous system and immune system may work together to build the nervous system. In the future, it will be interesting to investigate whether cd59 acts in a similar way during the development of the human nervous system.

Myelin is a highly specialized, lipid-rich membrane that insulates axons in the nervous system to enhance neurotransmission (Ritchie, 1982) while preserving axon health (Stadelmann et al., 2019). Myelin is produced and maintained by myelinating glial cells such as motor exit point glia (Fontenas and Kucenas, 2021; Fontenas and Kucenas, 2018; Smith et al., 2014) and myelinating Schwann cells (SCs; Figure 1A; Ackerman and Monk, 2016; BEN GEREN, 1954; Jessen and Mirsky, 2005) in the peripheral nervous system (PNS) as well as oligodendrocytes (OLs) in the central nervous system (CNS) (Figure 1B; Ackerman and Monk, 2016; Maturana, 1960; Nave and Werner, 2014; Peters, 1960a; Peters, 1960b). Normal myelin and myelinating glial cell development facilitate an efficient and effective nervous system, ensuring precise motor, sensory, and cognitive function (Almeida and Lyons, 2017; Berger et al., 2006; Stadelmann et al., 2019; Wei et al., 2019). When this process is impaired, as seen with inherited disorders that cause abnormal myelination, patients present with neurological dysfunction that often leads to severe physical and intellectual disabilities (Berger et al., 2006; Stadelmann et al., 2019; van der Knaap and Bugiani, 2017; Wei et al., 2019).

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Figure 1—source data 1

Source data for cd59 bulk, RNAseq expression depicted in Figure 1C.

Data contributed to scatter plot of cd59 expression (TPM) in oligodendrocyte lineage cells (OLCs), Schwann cells (SCs), and neurons (N) at 72 hours post fertilization (hpf) (left; mean ± SEM: OLC: 2145.1 ± 1215.1, SC: 40.1 ± 16.3; N: 240.5 ± 173.3; data point = replicate) as well as SCs at 36 and 72 hpf (right; mean ± SEM: 36 hpf: 0.0 ± 0.0, 72 hpf: 40.2 ± 16.3; data point = replicate).

https://cdn.elifesciences.org/articles/76640/elife-76640-fig1-data1-v2.xlsx

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Despite the importance of myelin, we still lack a complete understanding of myelin and myelinating glial cell development. With the recent boon of transcriptomic and proteomic analyses, many genes and proteins have been highlighted as differentially expressed during myelinating glial cell development, yet their precise functions remain unknown. For example, cd59, a gene that encodes for a small, glycosylphosphotidylinositol (GPI)-anchored glycoprotein, is a particularly interesting candidate for exploration. This gene features in several RNA sequencing (RNAseq) and proteomic analyses of zebrafish and rodent myelinating glial cells (Gerber et al., 2021; Howard et al., 2021; Marisca et al., 2020; Marques et al., 2018; Marques et al., 2016; Piller et al., 2021; Saunders et al., 2019; Siems et al., 2021; Wolbert et al., 2020; Zhu et al., 2019), all of which demonstrate high expression of cd59 in developing oligodendrocyte lineage cells (OLCs) and SCs. cd59 continues to be expressed in juvenile and adult zebrafish (Saunders et al., 2019; Siems et al., 2021; Sun et al., 2013) and becomes the fourth most abundant CNS myelin protein in adult zebrafish (Siems et al., 2021). Phylogenetic analysis demonstrates that Cd59 is conserved within vertebrate evolution (Siems et al., 2021), and accordingly, CD59 protein is also found in developing and adult human myelin (Erne et al., 2002; Koski et al., 2002; Scolding et al., 1998; Zajicek et al., 1995). Collectively, these data indicate that cd59 is a key component of the genetic program that orchestrates myelinating glial cell development. However, despite this knowledge of Cd59 expression, little is known about the function of Cd59 in the developing nervous system.

Outside of the nervous system, Cd59 is best known as a complement inhibitory protein. Complement is a molecular cascade within the innate immune system that aids in cell lysis of invading pathogens or aberrant cells in the body (Merle et al., 2015). This process lacks specificity and requires inhibitory proteins, such as Cd59, to protect healthy cells from lytic death (Davies et al., 1989). Cd59, specifically, acts at the end of the complement cascade where it binds to complement proteins 8 and 9 (C8 and C9, respectively) to prevent the polymerization of C9 and the subsequent formation of lytic pores (also known as membrane attack complexes [MACs] or terminal complement complexes [TCCs]) in healthy cell membranes (Meri et al., 1990; Ninomiya and Sims, 1992; Rollins et al., 1991). This interaction is important throughout the adult body, including the nervous system, where CD59a is neuroprotective in models of multiple sclerosis (Mead et al., 2004) and neuromyelitis optica (Yao and Verkman, 2017). Beyond complement-inhibitory functions, Cd59 can also facilitate vesicle signaling in insulin-producing pancreatic cells (Golec et al., 2019; Krus et al., 2014), suppress cell proliferation in T cells responding to a viral infection (Longhi et al., 2005) or smooth muscle cells in models of atherosclerosis (Li et al., 2013), and orchestrate proximal-distal cell identity during limb regeneration (Echeverri and Tanaka, 2005). Like complement inhibition, these processes are critical to normal nervous system function (Almeida et al., 2021; Baron and Hoekstra, 2010; Reiter and Bongarzone, 2020; White and Krämer-Albers, 2014). However, it is unclear exactly what role Cd59 is playing in myelinating glial cell development.

Though the precise function is unknown, it is clear that CD59 does impact human nervous system development. Patients with CD59 dysfunction, such as those with congenital CD59 deficiency (Haliloglu et al., 2015; Höchsmann and Schrezenmeier, 2015; Karbian et al., 2018; Solmaz et al., 2020) or germline paroxysmal nocturnal hemoglobinuria (Johnston et al., 2012), present with polyneuropathies during infancy and continue to have nervous system dysfunction throughout their lives. Intriguingly, these neurological symptoms persist even with complement inhibition, the most common treatment for congenital CD59 deficiency (Höchsmann and Schrezenmeier, 2015). Together, these observations further indicate that CD59 has an additional role in the developing nervous system and requires further investigation.

Here, utilizing the zebrafish model, we examined the role of Cd59 in the developing nervous system. In this study, we found that cd59 is highly expressed in a subset of developing SCs in addition to mature OLs and myelinating and nonmyelinating SCs. We chose to focus on SCs and found that cd59 mutant zebrafish have excessive SC proliferation. These mutants also have impaired myelin and node of Ranvier development. Finally, we demonstrate that complement activity increases in cd59 mutants and that unregulated inflammation contributes to SC overproliferation and mutant larvae may also have aberrant myelin and node of Ranvier formation. Overall, this data demonstrates that developmental inflammation stimulates SC proliferation and that this process is balanced by Cd59 to ensure normal SC and myelinated nerve development.

Myelination during nervous system development is essential for neural function, providing trophic and structural support to axons as well as quickening electrical conduction (Ritchie, 1982; Stadelmann et al., 2019). Consequently, impairment of this process can be devastating to patient quality of life (Stadelmann et al., 2019; van der Knaap and Bugiani, 2017). For this reason, the genetic mechanisms that orchestrate myelinating glial cell development requires continued exploration. Over the past few decades, we and others have noted expression of cd59 that is conserved in developing myelinating glial cells across multiple organisms, including zebrafish, rodents, and humans (Gerber et al., 2021; Howard et al., 2021; Marisca et al., 2020; Marques et al., 2018; Marques et al., 2016; Piller et al., 2021; Saunders et al., 2019; Siems et al., 2021; Sun et al., 2013; Wolbert et al., 2020; Zajicek et al., 1995; Zhu et al., 2019). Despite these observations, there had been little exploration into the function of Cd59 in the developing nervous system. In this study, we demonstrate that cd59 is expressed in a subset of developing SCs as well as mature OLs and SCs, revealing transcriptional heterogeneity among myelinating glial cells during development. Focusing on SCs, we demonstrated that Cd59 regulates SC proliferation induced by developmental inflammation. Furthermore, embryos with Cd59 dysfunction may have abnormal myelin and node of Ranvier formation during development. Overall, these findings illuminate the intersection of the innate immune system and glial cells and how they collaborate to establish a functioning nervous system during development.

Considering the importance of myelination, our investigation revealed some interesting myelin defects in response to cd59 dysfunction. With the increase in SC proliferation in cd59 mutant embryos, we hypothesized that the myelin sheath lengths would shorten in order to accommodate the excess SCs and maintain the same amount of myelin on the nerve. Unexpectedly, we noted that with Cd59 dysfunction, the myelin sheath length was unaffected. Additionally, myelin volume was reduced, which may be related to a nonsignificant decrease in the average number myelin wraps around each axon. At this point, it is unclear if the decrease in myelin volume is directly due to Cd59 dysfunction, secondary to SC excess, or simply an indirect consequence of developmental inflammation. That said, from these data we can imagine a couple of potential hypotheses as to why myelin volume is decreased. First, it is possible that Cd59, in addition to regulating SC proliferation, is also necessary for myelinogenesis. Past investigations demonstrate that CD59a helps facilitate vesicle signaling, which is important during insulin release and is implicated in diabetic patients (Golec et al., 2019; Krus et al., 2014). Within the nervous system, vesicle-dependent signaling is also important for myelin formation as well as trafficking within the myelin sheath (Baron and Hoekstra, 2010; Reiter and Bongarzone, 2020; White and Krämer-Albers, 2014). Electron micrographs show that CD59a is positioned throughout the myelin sheath in oligodendrocytes (Siems et al., 2021). Notably, CD59a molecules are observed deep within compacted myelin (Siems et al., 2021). Because Cd59 is unlikely to encounter complement when it is so isolated from the extracellular environment, it is possible that Cd59 is playing an additional role in mature myelinating glial cells, possibly by regulating vesicle signaling within the myelin sheath. In future work, it will be interesting to identify if Cd59 has any direct role in SC and/or oligodendrocyte myelinogenesis. That said, it is important to note that cd59 mutant SCs continue to express molecules necessary for SC development and subsequent myelination, including sox10, mbp, and krox20 (Bremer et al., 2011; Gould et al., 1995; Jessen and Mirsky, 2005; Takada et al., 2010; Topilko et al., 1994), as well as produce myelin at the appropriate developmental stage. Therefore, these SCs are able to make myelin without Cd59. These facts considered, it is also possible that Cd59 is not directly involved in SC myelinogenesis. With this in mind, another possibility is that the excess SCs themselves are responsible for the reduction in myelin through a contact inhibition mechanism. In support of this idea, prior work in vitro demonstrates that SCs produce a glycoprotein called contactinhibin when the cells reach a high density (Casella et al., 2000). Contactinhibin and its receptor, contactinhibin receptor, mediate contact-dependent inhibition of growth in SCs and fibroblasts (Casella et al., 2000; Gradl et al., 1995; Wieser et al., 1990), demonstrating that SCs have methods to restrict overgrowth under homeostatic conditions. Interestingly, contactinhibin also interacts with vimentin (Wieser et al., 1990), which is known to collaborate with TACE to negatively regulate NRG1 type III expression and subsequent myelin production (Triolo et al., 2012). Without vimentin and TACE, SCs hypermyelinate nerves (Triolo et al., 2012). Considering these findings, it is possible that overproliferation of SCs in cd59 mutant larvae leads to activation of these growth-inhibiting molecules, such as contactinhibin, vimentin, and TACE, and consequently decreases NRG1 type III expression and myelinogenesis. Finally, as mentioned previously, it is also possible that Cd59 or Cd59-regulated SC proliferation has nothing to do with changes in myelin development. Dex treatment indicates that developmental inflammation (or possibly other effects of glucocorticoid signaling) contributes to abnormal myelin formation in cd59 mutant larvae. Therefore, it is possible that this altered myelination is an indirect effect of developmental inflammation and not relevant to Cd59 or Cd59-regulated SC proliferation, indicating that we have more to learn about the role of developmental inflammation in myelinogenesis. Utilizing the cd59 mutant model established in this article, future studies can investigate these hypotheses to learn more about the molecular mechanisms that regulate myelin development.

While evaluating myelination, we were also curious about the SCs that were not contributing to myelination. Because the number of myelinated axons as well as myelin sheath length is similar between wildtype and mutant nerves, this indicates that the extra SCs are not producing myelin. It is unclear if this extra population of SCs are NMSCs or undifferentiated iSCs, which is a question worth exploring in a future study. Fortunately, a recent transcriptomic analysis of developing SCs revealed several new markers in which to better differentiate iSCs, NMSCs, and MSCs (Tasdemir-Yilmaz et al., 2021), which have historically been difficult to distinguish. Using these new cell-specific markers, future investigations will be able to determine the fate of these extra SCs on cd59 mutant nerves.

Beyond changes in myelination, in this study we showed that Cd59-limited proliferation is elicited by developmental inflammation. This finding provokes many interesting questions. First, these data reiterate the idea that the innate immune system and genes traditionally active in immune cells are first used during development to guide nervous system assembly and formation. In the CNS, there is evidence that complement aids in stimulating synaptic pruning of developing dendrites, directing cell polarity in the ventricular zone, guiding cortical neuron migration, and fostering neural progenitor cell proliferation (Coulthard et al., 2018; Coulthard et al., 2017; Denny et al., 2013; Gorelik et al., 2017; Magdalon et al., 2020; Paolicelli et al., 2011; Stevens et al., 2007). Similarly, inflammasome signaling was recently shown to be a necessary asset in Purkinje neuron development and mutations in this pathway are associated with increased DNA damage and behavioral deficits (Lammert et al., 2020). Finally, microglia, the resident innate immune cell of the CNS, have several roles in CNS development, including phagocytosing cell debris as well as pruning developing synapses and myelin (Hughes and Appel, 2020; Mazaheri et al., 2014; Silva et al., 2021; Stevens et al., 2007; Villani et al., 2019). To our knowledge, our study is the first examination of the role of inflammation and complement signaling in PNS development beyond the NCC stage (Carmona-Fontaine et al., 2011). These data prompt future exploration into this relationship between the nervous and immune systems during PNS formation.

To further this point, our data indicate that MACs may be involved in enhancing SC proliferation during development. Previous findings in vitro demonstrated that sublytic MACs could stimulate SC proliferation through activation of the MAPK/ERK and PKC pathways (Dashiell et al., 2000; Hila et al., 2001). These and other mitogenic pathways are also activated in other cells that undergo MAC-stimulated proliferation (Tegla et al., 2011b), such as smooth muscle cells, T cells, and oligodendrocytes (Chauhan and Moore, 2011; Rus et al., 1997; Rus et al., 1996; Tegla et al., 2011b; Zwaka et al., 2003). Collectively, these data have established that MACs induce cell proliferation through activation of Gi protein and Ras/Raf1, which go onto activate MEK1 and ERK1 that then facilitate transcription of cell cycle-related genes, such as CDK4 and CDK2 (Dashiell et al., 2000; Niculescu et al., 1999; Niculescu et al., 1997; Tegla et al., 2011b). Simultaneously, PI3K and Akt activate mTOR, P70^S6, and K_V1.3 to induce DNA and protein synthesis that aids in cell cycle activation (Badea et al., 2002; Hila et al., 2001; Rus et al., 2001; Tegla et al., 2011a; Tegla et al., 2011b). At this point, it is unclear whether increased MAC formation in cd59 mutant SCs leads to activation of these pathways in vivo and whether this mechanism contributes to developmental SC proliferation. Utilizing the tools developed in this study, we look forward to future investigations of these pathways and their role in SC development.

During our investigation, we also show that cd59 is expressed in a subset of SCs and OLs and is not expressed in other myelinating glial cells, including MEP glia and SCs that associate with spinal motor nerves. This expression pattern persists at least until 7 dpf in SCs, indicating that developmental heterogeneity lingers in the mature SCs. Furthermore, we show that Cd59 regulates proliferation of sensory SCs on the pLLN but not motor nerve-associated SCs, indicating that these differences in cd59 expression are associated with functional heterogeneity as well. These findings provoke many topics for further investigation. First, how do cd59-positive SCs differ from cd59-negative SCs? Does this imply that a subset of SCs is more sensitive to complement activity, or are there other implications for these expression differences? Related, why do motor SCs lack cd59? Recent RNAseq analysis of developing satellite glial cells (SGCs) and SCs showed that glial cell precursors, SGCs, and iSCs are heterogenous and that this transcriptional diversity depended on the type of nerve/ganglia they associated with (Tasdemir-Yilmaz et al., 2021; Wiltbank and Kucenas, 2021). Motor neurons and sensory neurons are transcriptionally and functionally distinct and likely have different demands of the SCs that they are intimately associated with. Therefore, it follows that sensory SC functionality may require Cd59 whereas motor SCs do not. It will be interesting to explore the consequences of this heterogeneity in future investigations.

We are also curious if Cd59 function is multifaceted in the nervous system. Our findings demonstrated that Cd59 prevents overproliferation of SCs during development by shielding them from developmental inflammation. Similar observations have been noted in T cells and smooth muscle cells (Li et al., 2013; Longhi et al., 2005). That said, many other functions beyond proliferation control have been documented for CD59. For example, CD59 is required to instruct proximal-distal cell identity, a process that is necessary for proper cell positioning during limb regeneration (Echeverri and Tanaka, 2005). In our study, we noted that floor plate and hypochord cells express cd59. During neural tube development, floor plate cells play an important role in determining cell fate as well as dorsal-ventral patterning in the spinal cord (Hirano et al., 1991; Yu et al., 2013), whereas the hypochord orchestrates midline blood vessel pattering (Cleaver and Krieg, 1998). Considering the role of CD59 in dictating proximal-distal cell identity during limb regeneration (Echeverri and Tanaka, 2005), it would be interesting to see if Cd59 participated in similar signaling pathways in floor plate and hypochord cells. Alternatively, Cd59’s role in dictating proximal-distal cell identity could also be useful during nerve regeneration. Like limb regeneration, there needs to be an appropriate distribution of cells along the proximal-distal axis of the regenerating nerve. With this idea in mind, it would be interesting to examine how Cd59 dysfunction impacts SC distribution after nerve regeneration.

Finally, our study revealed that Cd59 plays a role in nervous system development. Previous case studies of patients with CD59 dysfunction, such as those with germline PNH and congenital CD59 deficiency, noted early-onset neurological dysfunction in these patients (Haliloglu et al., 2015; Höchsmann and Schrezenmeier, 2015; Johnston et al., 2012; Karbian et al., 2018; Solmaz et al., 2020). These neurological symptoms were generally attributed to damage from overactivation of complement and excess inflammation (Höchsmann and Schrezenmeier, 2015). In support of this idea, eculizumab treatment, which inhibits complement protein 5 (C5) and limits formation of MACs, slowed the progression of severe neurological symptoms, including bulbar symptoms, focal seizures, impaired respiration, and muscular hypotonia. However, eculizumab could not restore full neurological function in these patients (Höchsmann and Schrezenmeier, 2015). In light of our recent findings, we propose that CD59 dysfunction could be interfering with nervous system development in these human patients, likely through inflammation-induced overproliferation of SCs and subsequent malformation of myelin and nodes of Ranvier. However, because developmental SC proliferation has completed by the time these patients receive eculizumab (Cravioto, 1965; Höchsmann and Schrezenmeier, 2015), it is likely too late to restore SC proliferation and preserve nerve development. In future case studies of these patients, it would be interesting to confirm with nerve biopsies whether these patients also have excess SCs and abnormal myelin volume like we have observed in our zebrafish model. In support of this idea, neutrophils isolated from patients with PNH also overproliferate (Li et al., 2019), indicating that SCs may do the same. Ultimately, there remain many areas of exploration to fully characterize the role of Cd59 in the developing and mature nervous system.

All data generated and analyzed during this study are included in the manuscript and supporting source files for Figures 1 to 8. All previously published datasets analyzed, including RNAseq and proteomics, are cited in the manuscript.

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Author details

1. Ashtyn T Wiltbank

   1. Neuroscience Graduate Program, University of Virginia, Charlottesville, United States
   2. Program in Fundamental Neuroscience, University of Virginia, Charlottesville, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Resources, Validation, Visualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

2. Emma R Steinson

   Department of Biology, University of Virginia, Charlottesville, United States

   Contribution

   Formal analysis, Investigation, Validation

   Competing interests

   No competing interests declared

3. Stacey J Criswell

   Department of Cell Biology, University of Virginia, Charlottesville, United States

   Contribution

   Methodology

   Competing interests

   No competing interests declared

4. Melanie Piller

   Department of Biology, University of Virginia, Charlottesville, United States

   Contribution

   Data curation, Formal analysis, Visualization, Writing – original draft

   Competing interests

   No competing interests declared

5. Sarah Kucenas

   1. Neuroscience Graduate Program, University of Virginia, Charlottesville, United States
   2. Program in Fundamental Neuroscience, University of Virginia, Charlottesville, United States
   3. Department of Biology, University of Virginia, Charlottesville, United States

   Contribution

   Conceptualization, Funding acquisition, Project administration, Supervision, Validation, Writing – original draft, Writing – review and editing

   For correspondence

   sk4ub@virginia.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1950-751X

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