Role of Actin Filament on Synaptic Vesicle Pooling in Cultured Hippocampal Neuron
1
조회
0
다운로드
1
인용
0
참고문헌
키워드
초록
The synaptic vesicle is a specialized structure in presynaptic terminals that stores various neurotransmitters. The actin filament has been proposed for playing an important role in mobilizing synaptic vesicles. To understand the role of actin filament on synaptic vesicle pooling, we characterized synaptic vesicles and actin filament after treatment of brain-derived neurotrophic factor (BDNF) or Latrunculin A on primary cultured neuron from rat embryo hippocampus. Western blots revealed that BDNF treatment increased the expression of synapsin I protein, but Latrunculin A treatment decreased the synapsin I protein expression. The increased expression of synapsin I after BDNF disappeared by the treatment of Latrunculin A. Three-dimensional (3D) tomography of synapse showed that more synaptic vesicles localized near the active zone and total number of synaptic vesicles increased after treatment of BDNF. But the number of synaptic vesicle was 2.5-fold reduced in presynaptic terminals and the loss of filamentous network was observed after Latrunculin A application. The treatment of Latruculin A after preincubation of BDNF group showed that synaptic vesicle number was similar to that of control group, but filamentous structures were not restored. These data suggest that the actin filament plays a significant role in synaptic vesicles pooling in presynaptic terminals.
Abstract
The synaptic vesicle is a specialized structure in presynaptic terminals that stores various neurotransmitters. The actin filament has been proposed for playing an important role in mobilizing synaptic vesicles. To understand the role of actin filament on synaptic vesicle pooling, we characterized synaptic vesicles and actin filament after treatment of brain-derived neurotrophic factor (BDNF) or Latrunculin A on primary cultured neuron from rat embryo hippocampus. Western blots revealed that BDNF treatment increased the expression of synapsin I protein, but Latrunculin A treatment decreased the synapsin I protein expression. The increased expression of synapsin I after BDNF disappeared by the treatment of Latrunculin A. Three-dimensional (3D) tomography of synapse showed that more synaptic vesicles localized near the active zone and total number of synaptic vesicles increased after treatment of BDNF. But the number of synaptic vesicle was 2.5-fold reduced in presynaptic terminals and the loss of filamentous network was observed after Latrunculin A application. The treatment of Latruculin A after preincubation of BDNF group showed that synaptic vesicle number was similar to that of control group, but filamentous structures were not restored. These data suggest that the actin filament plays a significant role in synaptic vesicles pooling in presynaptic terminals.
참고문헌 (31)
- Bamji S X, "BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions", J. Cell Biol., 174, pp.289~299 (2006)[DOI]
- Benfenati F, "Interaction of free and synaptic vesicle-bound synapsin I with F-actin", Neuron, 8, pp.377~386 (1992)[DOI]
- Bloom O, "Colocalization of synapsin and actin during synaptic vesicle recycling", J. Cell Biol., 161, pp.737~747 (2003)[DOI]
- Capani F, "Selective localization of high concentrations of F-actin in subpopulations of dendritic spines in rat central nervous system: a three-dimensional electron microscopic study", J. Comp. Neurol., 435, pp.156~170 (2001)[DOI]
- Cingolani L A, "Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy", Nat. Rev. Neurosci., 9, pp.344~356 (2008)[DOI]
- Cole A A, "A network of three types of fila- ments organizes synaptic vesicles for storage, mobilization, and docking", J. Neurosci., 36, pp.3222~3230 (2016)[DOI]
- Cole J C, "Disruption of actin impedes transmitter release in snake motor terminals", J. Physiol., 525, pp.579~586 (2000)[DOI]
- Cottrell J R, "Work- ing memory impairment in calcineurin knock-out mice is associated with alterations in synaptic vesicle cycling and disruption of high-fre- quency synaptic and network activity in prefrontal cortex", J. Neurosci., 33, pp.10938~10949 (2013)[DOI]
- Coue M, "Inhibition of actin polymerization by latrunculin A", FEBS Lett., 213, pp.316~318 (1987)[DOI]
- Dillon C, "The actin cytoskeleton: integrating form and function at the synapse", Annu. Rev. Neurosci., 28, pp.25~55 (2005)[DOI]
- Doussau F, "The actin cytoskeleton and neu- rotransmitter release: an overview", Biochimie, 82, pp.353~363 (2000)[DOI]
- Greengard P, "Synaptic vesicle phosphoproteins and regulation of synaptic function", Science, 259, pp.780~785 (1993)[DOI]
- Harlow M L, "The architecture of active zone material at the frog’s neuromuscular junction", Nature, 409, pp.479~484 (2001)[DOI]
- Haucke V, "Protein scaffolds in the coupling of synaptic exocytosis and endocytoisis", Nat. Rev. Neurosci., 12, pp.127~138 (2011)[DOI]
- Jovanovic J N, "Synapsins as mediators of BDNF-enhanced neurotransmitter release", Nat. Neurosci., 3, pp.323~329 (2000)[DOI]
- 김현욱, "Electron Tomography and Synapse Study", Applied Microscopy, 44(3), pp.83~87 (2014), 한국현미경학회
- Kim H W, "Rapid method for electron tomographic reconstruction and three-dimensional modeling of the murine synapse using an automated fiducial marker-free system", Microsc. Microanal., 19, pp.182~187 (2013)
- Michel K, "The presynaptic active zone: a dynamic scaffold that regulates synaptic efficacy", Exp. Cell Res., 335, pp.157~164 (2015)[DOI]
- Morales M, "Actin-dependent regulation of neurotransmitter release at central synapses", Neuron, 27, pp.539~550 (2000)[DOI]
- Nelson J C, "The actin cytoskeleton in presynaptic assembly", Cell Adh. Migr., 7, pp.379~387 (2013)[DOI]
- Pechstein A, "Taking a back seat: synaptic vesicle clustering in presynaptic terminals", Front. Synaptic Neurosci., 15, pp.143~ (2010)
- Richards D A, "Effects of wortmannin and latrunculin A on slow endocytosis at the frog neuromuscular junction", J. Physiol., 557, pp.77~91 (2004)[DOI]
- Rizzoli S O, "Synaptic vesicle pools", Nat. Rev. Neurosci., 6, pp.57~69 (2005)[DOI]
- Ryu J R, "Synaptic compartmentalization by micropatterned masking of a surface adhesive cue in cultured neurons", Biomaterials, 92, pp.46~56 (2016)[DOI]
- Sanchez A L, "BDNF increases synapse density in dendrites of developing tectal neurons in vivo", Development, 133, pp.2477~2486 (2006)[DOI]
- Shinoda Y, "BDNF enhances spontaneous and activity-dependent neurotransmitter release at excitatory terminals but not at inhibitory terminals in hippocampal neurons", Front. Synaptic Neurosci., 6, pp.1~12 (2014)
- Shupliakov O, "Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton", Proc. Natl. Acad. Sci. U S A, 99, pp.14476~14481 (2002)[DOI]
- Shupliakov O, "How synapsin I may cluster synaptic vesicles", Semin. Cell Dev. Biol., 22, pp.393~399 (2011)[DOI]
- Sudhof T C, "The presynaptic active zone", Neuron, 75, pp.11~25 (2012)[DOI]
- Yarmola E G, "Actin-latrunculin A structure and function. Differential modu- lation of actin-binding protein function by latrunculin A", J. Biol. Chem., 275, pp.28120~28127 (2000)
- Zhang W, "Stages of synapse development de- fined by dependence on F-actin", J. Neurosci., 21, pp.5169~5181 (2001)[DOI]
