Involvement of the Golgi apparatus in sorting of materials to opposite ends of frog rod retinal photoreceptors

Schmied, Robert; Holtzman, Eric

doi:10.1002/neu.480200303

Cited by 21 publications

(6 citation statements)

References 80 publications

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“…Studies on the developmental expression of synaptophysin and synaptoporin in the central nervous system revealed that these proteins are present not only in mature terminals but also in outgrowing axons (Bergmann et al, 1991Scarfone et al, 1991;Ovtscharoff et al, 1993; this study) and, unexpectedly, in the cytoplasmic bridge connecting retinal photoreceptor cell bodies with the rod component (Schmied and Holtzman, 1989), in dendrites of the continuously regenerating olfactory receptor neurons and, transiently, in dendrites of developing hippocampal pyramidal neurons (this study). While synaptic vesicles in outgrowing axons could serve as a reservoir for subsequent synaptogenesis, synaptic vesicle membrane antigens in developing dendrites are unlikely to contribute to synaptic organelles.…”

Section: Discussionmentioning

confidence: 58%

Differential Expression of Synaptophysin and Synaptoporin During Pre‐ and Postnatal Development of the Rat Hippocampal Network

Grabs

Bergmann

Schuster

et al. 1994

Eur J of Neuroscience

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The closely related synaptic vesicle membrane proteins synaptophysin and synaptoporin are abundant in the hippocampal formation of the adult rat. But the prenatal hippocampal formation contains only synaptophysin, which is first detected at embryonic day 17 (E17) in perikarya and axons of the pyramidal neurons. At E21 synaptophysin immunoreactivity extends into the apical dendrites of these cells and in newly formed terminals contacting these dendrites. The transient presence of synaptophysin in axons and dendrites suggests a functional involvement of synaptophysin in fibre outgrowth of developing pyramidal neurons. Synaptoporin expression parallels the formation of dentate granule cell synaptic contacts with pyramidal neurons: the amount of hippocampal synaptoporin, determined in immunoblots and by synaptoporin immunostaining of developing mossy fibre terminals, increases during the first postnatal week. Moreover, in the adult, synaptoporin is found exclusively in the mossy fibre terminals present in the hilar region of the dentate gyrus and the regio inferior of the cornu ammonis. In contrast, synaptophysin is present in all synaptic fields of the hippocampal formation, including the mossy fibre terminals, where it colocalizes with synaptoporin in the same boutons. Our data indicate that granule neuron terminals differ from all other terminals of the hippocampal formation by the presence of both synaptoporin and synaptophysin. This difference, observed in the earliest synaptic contacts in the postnatal hippocampus and persisting into adult life, suggests distinct functions of synaptoporin in these nerve terminals.

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Section: Discussionmentioning

confidence: 58%

Differential Expression of Synaptophysin and Synaptoporin During Pre‐ and Postnatal Development of the Rat Hippocampal Network

Grabs

Bergmann

Schuster

et al. 1994

Eur J of Neuroscience

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“…3F,G) microscopy. This region probably corresponds to the location of the Golgi apparatus, where synaptic vesicle membrane biogenesis, and thus accumulatipn of SVPs, may occur (Tixier-Vidal et al, 1988;Janetzko et al, 1989;Schmied and Holtzman, 1989). This was supported by double-labeling experiments showing colocalization of SV2 or synaptophysin immunoreactivity and binding of WGA, a Golgi marker, in the perinuclear region (data not shown).…”

Section: Resultsmentioning

confidence: 75%

Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro

1993

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To assess the regenerative capability of the photoreceptor synapse, we have isolated and cultured photoreceptors from the mature salamander retina. Both rod and cone photoreceptors were able to regenerate processes within 3 d of plating. Cells extended numerous actin-containing filopodia as well as a few neuritic processes. The neurites contained microtubules and formed synaptic vesicle-filled varicosities, as shown by immunostaining for tubulin and synaptic vesicle proteins and by electron microscopy. Furthermore, regenerated varicosities were capable of depolarization-induced vesicle labeling, suggesting that they can recycle synaptic vesicles and release neurotransmitter by synaptic vesicle exocytosis. Differences were observed between rod and cone cell synaptic regeneration in vitro, which resembled structural differences between their synaptic terminals in situ: rod cells formed multiple synaptic vesicle-filled varicosities along neurites at a distance from the soma, whereas cone cells tended to accumulate synaptic vesicles within the soma. The regeneration of neurites and synaptic vesicle-filled varicosities was abolished by microtubule depolymerizing agents, suggesting a role for microtubule-based vesicle transport in the formation of varicosities. Finally, process outgrowth and varicosity formation were independent of cell-cell contact and, indeed, proceeded in the complete absence of other cells. These findings suggest not only that differentiated photoreceptors are capable of synaptic renewal but that the regeneration of presynaptic-like terminals is an intrinsic ability of rod and cone cells.

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“…The disordered Golgi in nrc a14 photoreceptors would be predicted to cause a defect in trafficking newly synthesized synaptic proteins. Prior to reaching their destinations, many apical and basal proteins both pass through the trans Golgi [46]. However, the ability of nrc a14 cone photoreceptors to maintain proper apical trafficking despite altered Golgi morphology suggests that the disruption of protein transport of newly synthesized proteins is not the primary defect.…”

Section: Discussionmentioning

confidence: 99%

Synaptojanin 1 Is Required for Endolysosomal Trafficking of Synaptic Proteins in Cone Photoreceptor Inner Segments

et al. 2014

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Highly polarized cells such as photoreceptors require precise and efficient strategies for establishing and maintaining the proper subcellular distribution of proteins. The signals and molecular machinery that regulate trafficking and sorting of synaptic proteins within cone inner segments is mostly unknown. In this study, we show that the polyphosphoinositide phosphatase Synaptojanin 1 (SynJ1) is critical for this process. We used transgenic markers for trafficking pathways, electron microscopy, and immunocytochemistry to characterize trafficking defects in cones of the zebrafish mutant, nrca14, which is deficient in phosphoinositide phosphatase, SynJ1. The outer segments and connecting cilia of nrca14 cone photoreceptors are normal, but RibeyeB and VAMP2/synaptobrevin, which normally localize to the synapse, accumulate in the nrca14 inner segment. The structure of the Endoplasmic Reticulum in nrca14 mutant cones is normal. Golgi develop normally, but later become disordered. Large vesicular structures accumulate within nrca14 cone photoreceptor inner segments, particularly after prolonged incubation in darkness. Cone inner segments of nrc a14 mutants also have enlarged acidic vesicles, abnormal late endosomes, and a disruption in autophagy. This last pathway also appears exacerbated by darkness. Taken altogether, these findings show that SynJ1 is required in cones for normal endolysosomal trafficking of synaptic proteins.

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Involvement of the Golgi apparatus in sorting of materials to opposite ends of frog rod retinal photoreceptors

Cited by 21 publications

References 80 publications

Differential Expression of Synaptophysin and Synaptoporin During Pre‐ and Postnatal Development of the Rat Hippocampal Network

Differential Expression of Synaptophysin and Synaptoporin During Pre‐ and Postnatal Development of the Rat Hippocampal Network

Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro

Synaptojanin 1 Is Required for Endolysosomal Trafficking of Synaptic Proteins in Cone Photoreceptor Inner Segments

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