Invaginating Presynaptic Terminals in Neuromuscular Junctions, Photoreceptor Terminals, and Other Synapses of Animals

Petralia, Ronald S.; Wang, Yaxian; Mattson, Mark P.; Yao, Pamela J.

doi:10.1007/s12017-017-8445-y

Cited by 9 publications

(30 citation statements)

References 352 publications

(676 reference statements)

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“…Phagocytosis has been proposed as a mchanism for invagination of a pre-synaptic terminal into the post-synaptic process; our work supports an indirect role for phagocytosis (Petralia et al, 2017).…”

Section: Folds In the Muscle Membrane Caused By Formation Of Drpr-depsupporting

confidence: 73%

“…Our work suggests that in addition to activity Drpr dependent phagocytosis contributes to ghost bouton formation; the evidence that these do become mature boutons being the persistent bilateral organization of proteins in many boutons at the NMJ. It is not unexpected that an invagination should be able to trap a neurite, as there are numerous examples of synapses in which the presynaptic terminal invaginates into the post-synaptic process, including the Drosophila NMJ (Petralia et al, 2017;Prokop, 1999). Indeed, during initial NMJ development in the Drosophila embryo, boutons are embedded in a shallow indentation in the muscle (Prokop, 1999).…”

Section: Folds In the Muscle Membrane Caused By Formation Of Drpr-depmentioning

confidence: 99%

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The engulfment receptor Draper organizes the postsynaptic spectrin cytoskeleton into corrals containing synaptic proteins and promotes synaptic renewal

Wang

Kim

Yoo

et al. 2019

Preprint

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2 SummaryThe spectrin cytoskeleton is required for development of the Drosophila neuromuscular junction (NMJ) but its role is unclear. Here we show that the muscle spectrin lattice functions to corral membrane-associated synaptic proteins and limit their lateral mobility. Drosophila adducin, Hts, is required for integrity of the spectrin cytoskeleton and disruption of Hts function results in failure of the corrals. The spectrin cytoskeleton is itself patterned at the muscle membrane by the engulfment receptor Draper (Drpr) through regulation of Hts. We find patches of membrane where the spectrin cytoskeleton is organized into bilaterally symmetric patterns, which coincide with a field of Drprdependent structures similar to phagocytic pseudopods. The bilaterally symmetric patterns are likely created by folds of the muscle membrane in the pseudopods. We present evidence that the folds trap nascent boutons of motor neurons, leading to boutons with a bilaterally symmetric organization of the postsynaptic membrane. Drpr thus acts as a sensor of synaptic damage that promotes synaptogenesis.

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Section: Folds In the Muscle Membrane Caused By Formation Of Drpr-depsupporting

confidence: 73%

Section: Folds In the Muscle Membrane Caused By Formation Of Drpr-depmentioning

confidence: 99%

The engulfment receptor Draper organizes the postsynaptic spectrin cytoskeleton into corrals containing synaptic proteins and promotes synaptic renewal

Wang

Kim

Yoo

et al. 2019

Preprint

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“…A photoreceptor terminal-synaptic ribbon (r) contacts a deep invagination containing postsynaptic processes ( category 2 ) from horizontal (h) and bipolar (b) neurons, as well as projections from the terminal. Rod terminals in mammals usually have a single invaginated ribbon/active zone with two horizontal and two bipolar cell processes, as well as “fingers” of rod cytoplasm, while cone terminals have multiple invaginated ribbon/active zones, each with two horizontal and 1–2 bipolar cell processes (Rao-Mirotznik et al, 1995 ; Sterling and Demb, 2004 ; Petralia et al, 2017 ). The horizontal cell processes also may act as invaginating presynaptic terminals ( category 3 ) since they send a retrograde signal to the photoreceptor terminal, mediating a feedback mechanism.…”

Section: Examples Of Invaginating Structures At Mammalian Synapsesmentioning

confidence: 99%

“…A modest variety of invaginating presynaptic terminal structures occur, including in developing auditory nerve endbulbs on neuron somas in the cat, vestibular nerve terminals on neuron somas of the rat lateral vestibular nucleus, crested dendrites in the rat interpeduncular nucleus, and cup-shaped spines (see Petralia et al, 2017 ); also, terminals often partially invaginate (deep indention) into neuron somas in the monkey lateral geniculate nucleus (Saavedra et al, 1968 ). The crested dendrite is a unique dendritic structure containing several crest spines joined with invaginating presynaptic terminals, found in the interpeduncular nucleus of the rat (Murray et al, 1979 ).…”

Section: Examples Of Invaginating Structures At Mammalian Synapsesmentioning

confidence: 99%

“…In contrast, active zone-associated invaginating structures can be derived from postsynaptic processes that include postsynaptic spines and spine-like structures, or from part or all of the presynaptic terminal. We have previously described three categories of invaginating structures in all animals (Petralia et al, 2015 , 2016 , 2017 ). In this short review, we focus on the three categories in mammals, and update the literature.…”

Section: Introductionmentioning

confidence: 99%

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Invaginating Structures in Mammalian Synapses

Petralia¹,

Wang²,

Mattson

et al. 2018

Front. Synaptic Neurosci.

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Invaginating structures at chemical synapses in the mammalian nervous system exist in presynaptic axon terminals, postsynaptic spines or dendrites, and glial processes. These invaginating structures can be divided into three categories. The first category includes slender protrusions invaginating into axonal terminals, postsynaptic spines, or glial processes. Best known examples of this category are spinules extending from postsynaptic spines into presynaptic terminals in forebrain synapses. Another example of this category are protrusions from inhibitory presynaptic terminals invaginating into postsynaptic neuronal somas. Regardless of the direction and location, the invaginating structures of the first category do not have synaptic active zones within the invagination. The second category includes postsynaptic spines invaginating into presynaptic terminals, whereas the third category includes presynaptic terminals invaginating into postsynaptic spines or dendrites. Unlike the first category, the second and third categories have active zones within the invagination. An example of the second category are mossy terminal synapses of the hippocampal CA3 region, in which enlarged spine-like structures invaginate partly or entirely into mossy terminals. An example of the third category is the neuromuscular junction (NMJ) where substantial invaginations of the presynaptic terminals invaginate into the muscle fibers. In the retina, rod and cone synapses have invaginating processes from horizontal and bipolar cells. Because horizontal cells act both as post and presynaptic structures, their invaginating processes represent both the second and third category. These invaginating structures likely play broad yet specialized roles in modulating neuronal cell signaling.

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Insights into Electroreceptor Development and Evolution from Molecular Comparisons with Hair Cells

Baker

Modrell

2018

Integrative and Comparative Biology

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The vertebrate lateral line system comprises a mechanosensory division, with neuromasts containing hair cells that detect local water movement ("distant touch"); and an electrosensory division, with electrosensory organs that detect the weak, low-frequency electric fields surrounding other animals in water (primarily used for hunting). The entire lateral line system was lost in the amniote lineage with the transition to fully terrestrial life; the electrosensory division was lost independently in several lineages, including the ancestors of frogs and of teleost fishes. (Electroreception with different characteristics subsequently evolved independently within two teleost lineages.) Recent gene expression studies in a non-teleost actinopterygian fish suggest that electroreceptor ribbon synapses employ the same transmission mechanisms as hair cell ribbon synapses, and show that developing electrosensory organs express transcription factors essential for hair cell development, including Atoh1 and Pou4f3. Previous hypotheses for electroreceptor evolution suggest either that electroreceptors and hair cells evolved independently in the vertebrate ancestor from a common ciliated secondary cell, or that electroreceptors evolved from hair cells. The close developmental and putative physiological similarities implied by the gene expression data support the latter hypothesis, i.e., that electroreceptors evolved in the vertebrate ancestor as a "sister cell-type" to lateral line hair cells.

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Invaginating Presynaptic Terminals in Neuromuscular Junctions, Photoreceptor Terminals, and Other Synapses of Animals

Cited by 9 publications

References 352 publications

The engulfment receptor Draper organizes the postsynaptic spectrin cytoskeleton into corrals containing synaptic proteins and promotes synaptic renewal

The engulfment receptor Draper organizes the postsynaptic spectrin cytoskeleton into corrals containing synaptic proteins and promotes synaptic renewal

Invaginating Structures in Mammalian Synapses

Insights into Electroreceptor Development and Evolution from Molecular Comparisons with Hair Cells

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