Ribbon synapses in zebrafish hair cells

Abstract

The basic architecture and functionality of ribbon synapses of mechanosensitive hair cells are well conserved among vertebrates. Forward and reverse genetic methods in zebrafish (Danio rerio) have identified components that are critical for the development and function of ribbon synapses. This review will focus on the findings of these genetic approaches, and discuss some emergent concepts on the role of the ribbon body and calcium in synapse development, and how perturbations in synaptic vesicles lead to a loss of temporal fidelity at ribbon synapses.

Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome

“…Our data suggest that the electroreceptor ribbon synapse is glutamatergic, and functions in the same way as the hair cell ribbon synapse (Safieddine et al, 2012; Nicolson, 2015; Wichmann and Moser, 2015; Moser and Starr, 2016), with glutamate being loaded into synaptic vesicles by Vglut3, and otoferlin-dependent exocytosis being triggered by the activation of Ca v 1.3 channels, potentially including the auxiliary beta subunit Ca v β 2 , as in cochlear inner hair cells (Neef et al, 2009). In contrast, retinal and pineal photoreceptors express Vglut1 and Vglut2 and neuronal SNAREs, and retinal photoreceptors depend on Ca v 1.4 (see e.g.…”

“…These tether glutamate-filled synaptic vesicles and stabilize L-type voltage-gated calcium channels at the plasma membrane (Ca v 1.3 in hair cells; Ca v 1.4, in retinal photoreceptors; Joiner and Lee, 2015), enabling rapid and sustained glutamate release in response to activation of these calcium channels by membrane depolarization (Matthews and Fuchs, 2010; Pangršič et al, 2012; Safieddine et al, 2012; Nicolson, 2015; Wichmann and Moser, 2015; Moser and Starr, 2016). Electroreceptors also have synaptic ribbons of varying morphology (Northcutt, 1986; Bodznick and Montgomery, 2005): in paddlefish, they were described as synaptic ‘sheets’ (Jorgensen et al, 1972).…”

Innervation regulates synaptic ribbons in lateral line mechanosensory hair cells

“…For example, in mature auditory hair cells ribbons are ellipsoid, whereas in mature photoreceptor cells they appear as sheets (Sterling and Matthews, 2005;Nouvian et al, 2006). Transmission electron microscopy (TEM) shows that in mature zebrafish mechanosensory lateral line hair cells, ribbons at the synapse are spherical with a diameter of about 300 nm (Sidi et al, 2004;Obholzer et al, 2008;Nicolson, 2015) (Fig. 1A).…”

“…Ribbons (also known as dense bodies) are electron-dense structures that tether glutamate-containing synaptic vesicles and are found at synapses of sensory cells that respond to a broad range of stimulus intensities, such as mechanosensory hair cells of the auditory and lateral line system (in fish and amphibians), retinal photoreceptor and bipolar cells, and pineal cells (reviewed in Moser et al, 2006;Nouvian et al, 2006;Matthews and Fuchs, 2010;Yu and Goodrich, 2014;Nicolson, 2015). They are thought to store a ready-releasable pool of synaptic vesicles and coordinate synchronous vesiclerelease at the synapse (Khimich et al, 2005;Buran et al, 2010;Matthews and Fuchs, 2010;Maxeiner et al, 2016).…”

“…Because of the ability to generate mutants through forward genetic screens in zebrafish and the accessibility of lateral line hair cells, this system has become valuable in discovering the molecular mechanisms that oversee hair cell development and ribbon synapse formation (Nicolson et al, 1998;Nicolson, 2005Nicolson, , 2015.…”