The Kinesin Motor KIF3A Is a Component of the Presynaptic Ribbon in Vertebrate Photoreceptors

Mureşan, Virgil; Lyass, Asya; Schnapp, Bruce J.

doi:10.1523/jneurosci.19-03-01027.1999

Cited by 160 publications

(144 citation statements)

References 68 publications

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“…The first is KIF3A, a member of the kinesin superfamily and a component of the kinesin II motor protein holoenzyme (Kondo et al, 1994;Hirokawa and Takemura, 2004;Muresan et al, 1999). The concept of the ribbon as a molecular motor shuttling vesicles to the active zone was originally proposed by Bunt (1971), and the immunocytochemical localization of KIF3A to the ribbon is compatible with this long-standing hypothesis.…”

Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 90%

“…The concept of the ribbon as a molecular motor shuttling vesicles to the active zone was originally proposed by Bunt (1971), and the immunocytochemical localization of KIF3A to the ribbon is compatible with this long-standing hypothesis. However, KIF3A is not exclusively localized to synaptic ribbons: it is also found on some synaptic vesicles (Muresan et al, 1998(Muresan et al, , 1999 as well as on many cargo vesicles in the brain, where it mediates anterograde fast axonal transport (Kondo et al, 1994;Yamazaki et al, 1995;Hirokawa and Takemura, 2004). Thus, a possible function of KIF3A may be to transport active zone structures from the soma to the active zone (e.g., Garner et al, 2000;Kondo et al, 1994;Muresan et al, 1998Muresan et al, , 1999.…”

Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 99%

“…However, KIF3A is not exclusively localized to synaptic ribbons: it is also found on some synaptic vesicles (Muresan et al, 1998(Muresan et al, , 1999 as well as on many cargo vesicles in the brain, where it mediates anterograde fast axonal transport (Kondo et al, 1994;Yamazaki et al, 1995;Hirokawa and Takemura, 2004). Thus, a possible function of KIF3A may be to transport active zone structures from the soma to the active zone (e.g., Garner et al, 2000;Kondo et al, 1994;Muresan et al, 1998Muresan et al, , 1999. To date there is no functional evidence to support the view that molecular motors are involved in vesicle movements in the vicinity of the active zone (reviewed in Lenzi and von Gersdorff, 2001;Heidelberger et al, 2002).…”

Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 99%

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Synaptic transmission at retinal ribbon synapses

Heidelberger

Thoreson

Witkovsky

2005

Progress in Retinal and Eye Research

209

231

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The molecular organization of ribbon synapses in photoreceptors and ON bipolar cells is reviewed in relation to the process of neurotransmitter release. The interactions between ribbon synapseassociated proteins, synaptic vesicle fusion machinery and the voltage-gated calcium channels that gate transmitter release at ribbon synapses are discussed in relation to the process of synaptic vesicle exocytosis. We describe structural and mechanistic specializations that permit the ON bipolar cell to release transmitter at a much higher rate than the photoreceptor does, under in vivo conditions. We also consider the modulation of exocytosis at photoreceptor synapses, with an emphasis on the regulation of calcium channels.

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Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 90%

Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 99%

Section: Ribbon Synapse-associated Proteinsmentioning

confidence: 99%

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Synaptic transmission at retinal ribbon synapses

Heidelberger

Thoreson

Witkovsky

2005

Progress in Retinal and Eye Research

209

231

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“…There were clearly many GluR4-IR Glur2/3-IR puncta in these layers that were not found on the ChAT-IR processes, presumably the sites of excitatory synapses onto ganglion cells or unlabeled amacrine cells. The retinas were also labeled with antibodies to kinesin II, a protein present at the synaptic ribbons of bipolar cells (Muresan et al, 1999;Li et al, 2001). Virtually all of the GluR4-IR (Fig.…”

Section: Composition Of Ampa Subunits On Chat-immunoreactive Amacrinementioning

confidence: 99%

AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

Firth

Massey

et al. 2003

J of Comparative Neurology

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The light response of starburst amacrine cells is initiated by glutamate released from bipolar cells. To identify the receptors that mediate this response, we used a combination of anatomical and physiological techniques. An in vivo, rabbit eyecup was preloaded with [ 3 H]-choline, and the [ 3 H]-acetylcholine (ACh) released into the superfusate was monitored. A photopic, 3 Hz flashing light increased ACh release, and the selective AMPA receptor antagonist, GYKI 53655, blocked this light-evoked response. Nonselective AMPA/kainate agonists increased the release of ACh, but the specific kainate receptor agonist, SYM 2081, did not increase ACh release. Selective AMPA receptor antagonists, GYKI 53655 or GYKI 52466, also blocked the responses to agonists. We conclude that the predominant excitatory input to starburst amacrine cells is mediated by AMPA receptors. We also labeled lightly fixed rabbit retinas with antisera to choline acetyltransferase (ChAT), AMPA receptor subunits GluR1, GluR2/3, or GluR4, and kainate receptor subunits GluR6/7 and KA2. Labeled puncta were observed in the inner plexiform layer with each of these antisera to glutamate receptors, but only GluR2/3-IR puncta and GluR4-IR puncta were found on the ChAT-IR processes. The same was true of starburst cells injected intracellularly with Neurobiotin, and these AMPA receptor subunits were localized to two populations of puncta. The AMPA receptors are expected to desensitize rapidly, enhancing the sensitivity of starburst amacrine cells to moving or other rapidly changing stimuli. Indexing termsglutamate; ionotropic receptors; localization; cholinergic; interneuron; confocal microscopy Starburst amacrine cells are one of the most common types of amacrine cells in rabbit retina (MacNeil et al., 1999), and there are two subtypes. Type a cells have perikarya in the inner nuclear layer, processes ramifying in the outer half of the inner plexiform layer (IPL) in stratum 2 (S2) and OFF responses to light. Type b cells have perikarya displaced to the ganglion cell layer, processes ramifying in stratum 4 (S4) of the IPL and ON responses to light (Famiglietti, 1983;Tauchi and Masland, 1984;Vaney, 1984;Bloomfield and Miller, 1986). In rabbits, starburst amacrine cells are known to receive synaptic inputs from cone (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).Starburst amacrine cells synthesize and release both γ-aminobutyric acid (GABA) and acetylcholine (ACh) when depolarized (Masland and Livingstone, 1976;Massey and Neal, 1979;O'Malley and Masland, 1989). ACh release from the rabbit retina increases at both light onset and light offset and is maximally stimulated by large stimuli at temporal frequencies of 1-4 Hz (Massey and Neal, 1979;Massey and Redburn, 1985;O'Malley and Masland, 1993). The majority of the synaptic output from the starburst cells is onto ganglion cell dendrites (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991 . The agonist α-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) is more potent than kainate or...

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“…Because Ribeye can form cellular aggregates, it may function by assembling other proteins into the ribbons (Schmitz et al, 2000). The ribbons may then be anchored to the presynaptic sites by the scaffolding proteins Bassoon and Piccolo/Aczonin, which are present both in conventional synapses and in ribbon synapses (Grabs et al, 1996;Wang et al, 1997;Brandstatter et al, 1999;Muresan et al, 1999;Von Kriegstein et al, 1999;Dick et al, 2001Dick et al, , 2003Piatigorsky, 2001;Von Kriegstein and Schmitz, 2003). If the primary function of Ribeye is to organize a ribbon, one would predict that its removal would have a fairly specific effect, namely the absence of synaptic ribbons.…”

Section: Introductionmentioning

confidence: 99%

TworibeyeGenes in Teleosts: The Role of Ribeye in Ribbon Formation and Bipolar Cell Development

Wan¹,

Almers²,

Chen³

2005

J. Neurosci.

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Ribeye is the only known protein specific to synaptic ribbon, but its function is unclear. We show that the teleost fish, Fugu and zebrafish, have two ribeye genes, ribeye a and ribeye b. Whole-mount in situ hybridization revealed that ribeye a is expressed in tissues containing synaptic ribbons, including the pineal gland, inner ear, and retina. Ribeye b is absent in the pineal gland. In the retina, ribeye a is expressed in both photoreceptors and bipolar cells, whereas ribeye b is detected only in photoreceptors. To study the function of Ribeye a in retina, we depleted it by morpholino antisense oligos. Fish deficient in Ribeye a lack an optokinetic response and have shorter synaptic ribbons in photoreceptors and fewer synaptic ribbons in bipolar cells. Their bipolar cells still target Syntaxin-3 proteins to the inner plexiform layer and have abundant vsx1 mRNA. However, they lack large synaptic terminals and show increased apoptosis. Rod bipolar cells are fewer in number and/or deficient in PKC␣. Recovery of Ribeye a levels rescues the optokinetic response, increases the number of PKC␣-positive bipolar cells, and stops apoptosis. We conclude that Ribeye a is important for late steps in bipolar cell development.

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The Kinesin Motor KIF3A Is a Component of the Presynaptic Ribbon in Vertebrate Photoreceptors

Cited by 160 publications

References 68 publications

Synaptic transmission at retinal ribbon synapses

Synaptic transmission at retinal ribbon synapses

AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

TworibeyeGenes in Teleosts: The Role of Ribeye in Ribbon Formation and Bipolar Cell Development

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