Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes

Abstract

Chemical synapses equipped with ribbons are tonically active, high-output synapses. The ribbons may play a role in the trafficking of synaptic vesicles. Recent findings in retinal rod cells of BALB/c mice indicate that ribbons are large and smooth in the dark phase, and, due to the formation and release of protrusions, small during the light phase. As a consequence of these changes, ribbons may traffick fewer vesicles in the light than in the dark phases. The aim of the present study was to find out whether the above ribbon changes in this mouse strain are strictly illumination-dependent and which signalling processes may be involved. Here, we show that ribbons form protrusions and release them into the cytoplasm within 30-60 min after lights on, the reverse occurring within 30 min after lights off. Under constant light or constant dark, no circadian rhythm of synaptic ribbon changes is observed. The illumination-dependence of ribbon structure is supported by in vitro experiments showing that in dark-adapted retinas, light induces the same morphological changes as in vivo. In vitro, the effect of light on the ribbons can be counteracted by cyclic guanosine monophosphate and melatonin. In dark-adapted retinas, light effects can be produced by decreasing the calcium ion concentrations in the incubation media. These results suggest that in retinal rod cells, the well known phototransduction signalling mechanisms may be responsible for the ribbon changes presently and previously reported.

Myosin Va is required for normal photoreceptor synaptic activity

“…It could also explain why so many ribbons have an abnormal morphology. It is now well established that the length and gross morphology of the mouse photoreceptor ribbons can change and that this change is directly related to the light cycle (or potentially synaptic activity) (Adly et al, 1999;Balkema et al, 2001;Spiwoks-Becker et al, 2004). Our results suggest that myosin Va might play a role in this dynamic regulation of synaptic ribbon morphology.…”

Multiple RIBEYE–RIBEYE Interactions Create a Dynamic Scaffold for the Formation of Synaptic Ribbons

“…The proposed modular assembly of the synaptic ribbon from individual RIBEYE subunits provides a molecular basis for the ultrastructural plasticity of synaptic ribbons (e.g., changes in size and shape of the ribbon). The binding of externally added RIBEYE to purified synaptic ribbons mimics the growth of synaptic ribbons that occurs in situ, e.g., under darkness in the mouse retina (Balkema et al, 2001;Spiwoks-Becker et al, 2004;Hull et al, 2006). Similarly, RIBEYE-aggregates increased in size over time in light microscopy (supplemental Fig.…”

“…In EM sections, retinal synaptic ribbons usually appear bar-shaped, and inner ear synaptic ribbons are usually spherical structures (for review, see Nouvian et al, 2006). Also in the retina, the assembly of the bar-shaped ribbon is believed to go through spherical ribbon intermediates, the so called synaptic spheres (for review, see Vollrath and Spiwoks-Becker, 1996;Spiwoks-Becker et al, 2004). The dimensions of synaptic ribbons in the retina can vary and are subject to changes, e.g., in response to different stimuli (lighting conditions/circadian rhythm), probably reflecting structural adaptations to different degrees of synaptic activity (for review, see Vollrath and SpiwoksBecker, 1996;Wagner, 1997).…”

Disruption of the Presynaptic Cytomatrix Protein Bassoon Degrades Ribbon Anchorage, Multiquantal Release, and Sound Encoding at the Hair Cell Afferent Synapse

“…Their morphological hallmark is the synaptic ribbon, an electron-dense structure tethering a halo of synaptic vesicles (tom Dieck and Brandstätter, 2006; for review, see Schmitz, 2009;Matthews and Fuchs, 2010;Rutherford and Pangršič, 2012). Several experimental approaches have indicated the functional importance of the ribbon, including biochemical studies of its major component, RIBEYE (Schwarz et al, 2011), genetic manipulation (Dick et al, 2003;Sheets et al, 2011), studies of physiological ribbon dynamics (Remé and Young, 1977;Spiwoks-Becker et al, 2004;Hull et al, 2006;Emran et al, 2010), and acute photodamage (Snellman et al, 2011). Based on such data, two major functions of the ribbon can be hypothesized: (1) establishing and stabilizing a large number of vesicular release sites and Ca 2ϩ channels at the active zone, i.e., a large readily releasable vesicle pool (RRP; Hull et al, 2006; and (2) (Heidelberger et al, 1994;Parsons and Sterling, 2003;Edmonds, 2004;Fuchs, 2005;Matthews and Sterling, 2008;Graydon et al, 2011).…”