Regulation of Dendritic Protein Synthesis by Miniature Synaptic Events

Sutton, Michael A.; Wall, Nicholas R.; Aakalu, Girish; Schuman, Erin M.

doi:10.1126/science.1096202

Cited by 235 publications

(222 citation statements)

References 29 publications

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“…Scaling in those cases has additional similarities to intermediate-and long-term facilitation: Both types of plasticity can involve postsynaptic Ca 2+ (8,23,33), protein synthesis (8,23,34), AMPA receptor insertion (7,8,16,33), and modulation of the presynaptic probability of release (10)(11)(12)15). However, scaling has an opposite sign of action compared with facilitation (during scaling, spontaneous release acts to decrease protein synthesis and synaptic strength).…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have shown that spontaneous release also contributes to several other synaptic effects, including some cases of homeostatic scaling (7)(8)(9)(10)(11)(12)(13)(14). Scaling in those cases has additional similarities to intermediate-and long-term facilitation: Both types of plasticity can involve postsynaptic Ca 2+ (8,23,33), protein synthesis (8,23,34), AMPA receptor insertion (7,8,16,33), and modulation of the presynaptic probability of release (10)(11)(12)15).…”

Section: Discussionmentioning

confidence: 99%

“…In the last few years, we have learned that spontaneous release can contribute to postsynaptic firing (2, 3), regulation of postsynaptic kinase pathways (4), and maintenance of postsynaptic dendritic spines and receptors (5,6). Spontaneous release has also been found to contribute to some cases of homeostatic scaling of synaptic strength (7)(8)(9)(10)(11)(12)(13)(14). Here we report a role of spontaneous transmitter release in the induction of a learning-related form of synaptic plasticity, longterm facilitation produced by serotonin (5HT) in Aplysia.…”

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confidence: 99%

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Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

Jin

Puthanveettil

Udo

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Long-term plasticity can differ from short-term in recruiting the growth of new synaptic connections, a process that requires the participation of both the presynaptic and postsynaptic components of the synapse. How does information about synaptic plasticity spread from its site of origin to recruit the other component? The answer to this question is not known in most systems. We have investigated the possible role of spontaneous transmitter release as such a transsynaptic signal. Until recently, relatively little has been known about the functions of spontaneous release. In this paper, we report that spontaneous release is critical for the induction of a learning-related form of synaptic plasticity, long-term facilitation in Aplysia. In addition, we have found that this signaling is engaged quite early, during an intermediate-term stage that is the first stage to involve postsynaptic as well as presynaptic molecular mechanisms. In a companion paper, we show that spontaneous release from the presynaptic neuron acts as an orthograde signal to recruit the postsynaptic mechanisms of intermediate-term facilitation and initiates a cascade that can culminate in synaptic growth with additional stimulation during long-term facilitation. Spontaneous release could make a similar contribution to learning-related synaptic plasticity in mammals.serotonin | cell culture | miniature excitatory postsynaptic current | octopamine | botulinum toxin S pontaneous transmitter release was discovered 60 y ago by Fatt and Katz (1), who found that it represents the quantal unit of transmitter release evoked by a presynaptic action potential. However, until recently, relatively little has been known about other possible functions of spontaneous release. In the last few years, we have learned that spontaneous release can contribute to postsynaptic firing (2, 3), regulation of postsynaptic kinase pathways (4), and maintenance of postsynaptic dendritic spines and receptors (5, 6). Spontaneous release has also been found to contribute to some cases of homeostatic scaling of synaptic strength (7-14). Here we report a role of spontaneous transmitter release in the induction of a learning-related form of synaptic plasticity, longterm facilitation produced by serotonin (5HT) in Aplysia.Long-term plasticity can differ from short-term in recruiting the growth of new synaptic connections, a process that requires the participation of both the presynaptic and postsynaptic components of the synapse (15-21). Because short-term plasticity often involves only one component of the synapse (22-24), the question arises: How does information about synaptic plasticity spread from its site of origin to recruit the other component of the synapse? Studies of synaptic growth during development have revealed a fairly elaborate program of pre-and postsynaptic changes involving a variety of orthograde and retrograde messengers (25), including activity-dependent or spontaneous release of the transmitter itself (26-30). We have now investigated the possible role of spo...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

Jin

Puthanveettil

Udo

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…None of these cells are considered to have an unusually large cytoplasmic volume or storage function. It is well known, however, that localized protein synthesis is critical for synaptic plasticity and maintenance (Sutton and Schuman, 2005;Sutton et al, 2004;Wiersma-Meems et al, 2005). Furthermore, neuronal signal transmission may require a high level of protein synthesis; however, a requirement for more ribosomes per se does not completely explain the life-long sustained high level of pre-rRNA synthesis.…”

Section: Discussionmentioning

confidence: 99%

Mapping ribosomal RNA transcription activity in the mouse eye

Qian

Lavker

Tseng

2006

Developmental Dynamics

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All cells must make ribosomes, in which rRNA transcription is the rate-limiting step; however, some cells may require more ribosomes than others. Cell-type specific regulation of rRNA synthesis has been largely ignored in the past, because of the inability to measure rRNA transcription rate in situ. Here we map rRNA transcription activity in individual cells in mouse ocular tissues detected by a novel in situ hybridization technique, which detects the full-length transcripts (47S pre-rRNA) as well as various rRNA processing intermediates. In the adult mouse eye, the corneal and lens epithelia and some retinal neurons contain a higher level of 47S pre-rRNA and rRNA processing intermediates, which are regulated developmentally in neonates prior to eye opening. In the cornea and lens epithelia, the higher rRNA level of 47S rRNA correlates with cell proliferation, which is consistent with the notion that dividing cells require more protein synthesis. Interestingly, in some retinal neurons, the high level of 47S pre-rRNA does not correlate with mature rRNA accumulation or protein synthesis, suggesting the existence of unappreciated biochemical needs of these cells.

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“…Schuman and colleagues created a dendritic translation reporter by flanking the coding sequence for GFP with the 5 0 and 3 0 untranslated regions (UTR) of the a subunit of Ca 2þ /calmodulindependent kinase II (aCaMKII) (Fig. 3A.1) (Aakalu et al 2001;Sutton et al 2004). The 3 0 UTR of aCaMKII has been shown to be sufficient for dendritic localization of the mRNA in neurons.…”

Section: Fluorescent Protein Reportersmentioning

confidence: 99%

Imaging Translation in Single Cells Using Fluorescent Microscopy

Chao

Yoon

Singer

2012

Cold Spring Harbor Perspectives in Biology

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The regulation of translation provides a mechanism to control not only the abundance of proteins, but also the precise time and subcellular location that they are synthesized. Much of what is known concerning the molecular basis for translational control has been gleaned from experiments (e.g., luciferase assays and polysome analysis) that measure average changes in the protein synthesis of a population of cells, however, mechanistic insights can be obscured in ensemble measurements. The development of fluorescent microscopy techniques and reagents has allowed translation to be studied within its cellular context. Here we highlight recent methodologies that can be used to study global changes in protein synthesis or regulation of specific mRNAs in single cells. Imaging of translation has provided direct evidence for local translation of mRNAs at synapses in neurons and will become an important tool for studying translational control.

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Regulation of Dendritic Protein Synthesis by Miniature Synaptic Events

Abstract: Methods Cell Culture and MicroscopyDissociated postnatal (P1-2) rat hippocampal neuron cultures, plated at a density of 230-460/ mm 2 , were prepared as previously described (1). In all experiments, neurons were used following 14-23

Cited by 235 publications

References 29 publications

Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

Mapping ribosomal RNA transcription activity in the mouse eye

Imaging Translation in Single Cells Using Fluorescent Microscopy

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