Comparison of the ontogeny of the vesicular glutamate transporter 3 (VGLUT3) with VGLUT1 and VGLUT2 in the rat retina

Abstract

Glutamate is the major excitatory neurotransmitter in the retina, and most glutamatergic neurons express one of the three known vesicular glutamate transporters (VGLUT1, 2, or 3). However, the expression profiles of these transporters vary greatly in the retina. VGLUT1 is expressed by photoreceptor and bipolar cell terminals, and VGLUT2 appears to be predominately expressed by ganglion cells, and perhaps Müller cells, cone photoreceptor terminals, and horizontal cells in some species. The discovery of a third vesicular glutamate transporter, VGLUT3, has brought about speculation concerning its role and function based on its expression in amacrine cells. To address this we studied the postnatal development of VGLUT3 from day 0 through adult in the rat retina, and compared this with the expression patterns of VGLUT1 and VGLUT2. VGLUT3 expression was restricted to a population of amacrine cells. Expression of VGLUT3 was first observed at postnatal day 10 (P10) in the soma and some processes, which extensively arborized in both the ON and OFF sublamina of the IPL by P15. In contrast, VGLUT1 and VGLUT2 expression appeared earlier than VGLUT3; with VGLUT1 initially detected at P5 in photoreceptor terminals and P6 in bipolar terminals, and VGLUT2 immunoreactivity initially detected at P0 in ganglion cell bodies, and remained prominent throughout all stages of development. Interestingly, VGLUT3 has extensive somatic expression throughout development, which could be involved in non-synaptic modulation by glutamate in developing retina, and could influence trophic and extra-synaptic neuronal signaling by glutamate in the inner retina.

Relationship between rat retinal degeneration and potassium channel KCNQ5 expression

“…The SD rat retinas showed that VGluT1 immunoreactivity followed previously reported patterns (Gong et al, 2006;Stella et al, 2008) (Fig. 4A).…”

“…VGluT1 is a marker of all the photoreceptor terminals in the OPL, and also of the bipolar cell terminals in both the ON and OFF laminae of the IPL (Gong et al, 2006;Stella et al, 2008). The SD rat retinas showed that VGluT1 immunoreactivity followed previously reported patterns (Gong et al, 2006;Stella et al, 2008) (Fig.…”

“…VGluT1 is located in the glutamatergic vesicular membrane of the photoreceptors synapses and output synapses of bipolar cells in the IPL of the mammalian retina (Gong et al, 2006;Stella et al, 2008). The co-localization of both proteins KCNQ5 and VGluT1 take place in the synaptic terminals of auditory neurons in brainstem nuclei (Garcia-Pino et al, 2010).…”

Vesicular glutamate transporter 2 (VGLUT2) is co-stored with PACAP in projections from the rat melanopsin-containing retinal ganglion cells

“…Expression of VGLUT2 in retinal ganglion cells has previously been shown in rodents (Fujiyama et al 2003;Johnson et al 2004Johnson et al , 2007Stella et al 2008), and co-localization of VGLUT2 mRNA and melanopsin-ir in the ipRGCs has recently been demonstrated in mice (Johnson et al 2007). In the present study, we used PACAP as a marker for the melanopsin-expressing ipRGCs and their projections, and demonstrated colocalization of PACAP and VGLUT2 in these cells and their nerve terminals in the rat SCN, IGL, and OPN.…”

“…To date, three isoforms of VGLUT have been identified, characterized and named VGLUT1, 2, and 3 (reviewed in Takamori 2006). Previous studies in rodents have demonstrated the presence of VGLUT2 mRNA and protein in RGCs (Fujiyama et al 2003;Johnson et al 2004Johnson et al , 2007Stella et al 2008) and colocalization of VGLUT2 and melanopsin in ipRGCs of the mouse retina (Johnson et al 2007). VGLUT2 has been identified in visual target areas of the CNS (Fujiyama et al 2003;Kaneko et al 2002;Kiss et al 2007Kiss et al , 2008Land et al 2004;Sakata-Haga et al 2001;Varoqui et al 2002), but not shown in distinct target areas of the ipRGCs.…”