Transmission at rod and cone ribbon synapses in the retina

Thoreson, Wallace B.

doi:10.1007/s00424-021-02548-9

Cited by 27 publications

(27 citation statements)

References 251 publications

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“…The reason for this increased basal synaptic vesicle turnover most likely is the previously reported increased levels of basal, presynaptic Ca 2+ [ 25 ]. Vesicle fusion in rod photoreceptor synapses is exquisitely sensitive to Ca 2+ [ 106 , 107 ]. Elevated basal presynaptic Ca 2+ likely can also account for the increased basal endocytosis, as previously observed also in other synapses [ 104 , 108 , 109 , 110 ].…”

Section: Discussionmentioning

confidence: 99%

Early Changes in Exo- and Endocytosis in the EAE Mouse Model of Multiple Sclerosis Correlate with Decreased Synaptic Ribbon Size and Reduced Ribbon-Associated Vesicle Pools in Rod Photoreceptor Synapses

Kesharwani

Schwarz

Dembla

et al. 2021

IJMS

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Multiple sclerosis (MS) is an inflammatory disease of the central nervous system that finally leads to demyelination. Demyelinating optic neuritis is a frequent symptom in MS. Recent studies also revealed synapse dysfunctions in MS patients and MS mouse models. We previously reported alterations of photoreceptor ribbon synapses in the experimental auto-immune encephalomyelitis (EAE) mouse model of MS. In the present study, we found that the previously observed decreased imunosignals of photoreceptor ribbons in early EAE resulted from a decrease in synaptic ribbon size, whereas the number/density of ribbons in photoreceptor synapses remained unchanged. Smaller photoreceptor ribbons are associated with fewer docked and ribbon-associated vesicles. At a functional level, depolarization-evoked exocytosis as monitored by optical recording was diminished even as early as on day 7 after EAE induction. Moreover compensatory, post-depolarization endocytosis was decreased. Decreased post-depolarization endocytosis in early EAE correlated with diminished synaptic enrichment of dynamin3. In contrast, basal endocytosis in photoreceptor synapses of resting non-depolarized retinal slices was increased in early EAE. Increased basal endocytosis correlated with increased de-phosphorylation of dynamin1. Thus, multiple endocytic pathways in photoreceptor synapse are differentially affected in early EAE and likely contribute to the observed synapse pathology in early EAE.

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Section: Discussionmentioning

confidence: 99%

Early Changes in Exo- and Endocytosis in the EAE Mouse Model of Multiple Sclerosis Correlate with Decreased Synaptic Ribbon Size and Reduced Ribbon-Associated Vesicle Pools in Rod Photoreceptor Synapses

Kesharwani

Schwarz

Dembla

et al. 2021

IJMS

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“…To ensure the supply of SVs for continuous release in response to fluctuating light stimuli, photoreceptors evolved a specialized release machinery, the ribbon-type synapse. 5 , 6 One of the unique properties of this synapse is the presence of the synaptic ribbon, an organelle anchored at the active zone (AZ), which tethers large numbers of SVs and consequently regulates the number of SVs present at the AZ. The elementary building block of synaptic ribbons is the protein ribeye.…”

mentioning

confidence: 99%

Functional and Structural Development of Mouse Cone Photoreceptor Ribbon Synapses

Davison

Gierke

Brandstätter

et al. 2022

Invest. Ophthalmol. Vis. Sci.

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Purpose Cone photoreceptors of the retina use a sophisticated ribbon-containing synapse to convert light-dependent changes in membrane potential into release of synaptic vesicles (SVs). We aimed to study the functional and structural maturation of mouse cone photoreceptor ribbon synapses during postnatal development and to investigate the role of the synaptic ribbon in SV release. Methods We performed patch-clamp recordings from cone photoreceptors and their postsynaptic partners, the horizontal cells during postnatal retinal development to reveal the functional parameters of the synapses. To investigate the occurring structural changes, we applied immunocytochemistry and electron microscopy. Results We found that immature cone photoreceptor terminals were smaller, they had fewer active zones (AZs) and AZ-anchored synaptic ribbons, and they produced a smaller Ca 2+ current than mature photoreceptors. The number of postsynaptic horizontal cell contacts to synaptic terminals increased with age. However, tonic and spontaneous SV release at synaptic terminals stayed similar during postnatal development. Multiquantal SV release was present in all age groups, but mature synapses produced larger multiquantal events than immature ones. Remarkably, at single AZs, tonic SV release was attenuated during maturation and showed an inverse relationship with the appearance of anchored synaptic ribbons. Conclusions Our developmental study suggests that the presence of synaptic ribbons at the AZs attenuates tonic SV release and amplifies multiquantal SV release. However, spontaneous SV release may not depend on the presence of synaptic ribbons or voltage-sensitive Ca 2+ channels at the AZs.

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“…Kif3a may have a weak binding affinity or a transient interaction with Tulp1, or either protein may require post-translational modifications in order to interact. Second, the other components of the Kinesin-2 motor complex are not expressed in photoreceptor terminals questioning the functional significance of Kif3a at the synapse [28,59]. In fact, there is evidence that presynaptic transport vesicles may use different Kinesin family members [60].…”

Section: Discussionmentioning

confidence: 99%

Photoreceptor Compartment-Specific TULP1 Interactomes

Ebke

Sinha

Pauer

et al. 2021

Preprint

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Photoreceptors are highly compartmentalized cells with large amounts of proteins synthesized in the inner segment (IS) and transported to the outer segment (OS) and synaptic terminal. Tulp1 is a photoreceptor-specific protein localized to the IS and synapse. In the absence of Tulp1, sev-eral OS-specific proteins are mislocalized and synaptic vesicle recycling is impaired. To better understand the involvement of Tulp1 in protein trafficking, our approach was to physically iso-late Tulp1-containing photoreceptor compartments by serial tangential sectioning of retinas and to identify compartment-specific Tulp1 binding partners by immunoprecipitation followed by liquid chromatography tandem mass spectrometry. Our results indicate that Tulp1 has two dis-tinct interactomes. We report the identification of: 1) an IS-specific interaction between Tulp1 and the motor protein Kinesin family member 3a (Kif3a), 2) a synaptic-specific interaction be-tween Tulp1 and the scaffold protein Ribeye, and 3) an interaction between Tulp1 and the cyto-skeletal protein Microtubule-associated protein 1B (MAP1B) in both compartments. Immuno-localization studies in the wild-type retina indicate that Tulp1 and its binding partners co-localize to their respective compartments. Our observations are compatible with Tulp1 functioning in protein trafficking in multiple photoreceptor compartments, likely as an adapter molecule linking vesicles to molecular motors and the cytoskeletal scaffold.

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Transmission at rod and cone ribbon synapses in the retina

Cited by 27 publications

References 251 publications

Early Changes in Exo- and Endocytosis in the EAE Mouse Model of Multiple Sclerosis Correlate with Decreased Synaptic Ribbon Size and Reduced Ribbon-Associated Vesicle Pools in Rod Photoreceptor Synapses

Early Changes in Exo- and Endocytosis in the EAE Mouse Model of Multiple Sclerosis Correlate with Decreased Synaptic Ribbon Size and Reduced Ribbon-Associated Vesicle Pools in Rod Photoreceptor Synapses

Functional and Structural Development of Mouse Cone Photoreceptor Ribbon Synapses

Photoreceptor Compartment-Specific TULP1 Interactomes

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