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Synaptic vesicles contain small ribonucleic acids (sRNAs) including transfer RNA fragments (trfRNA) and microRNAs (miRNA)

Li, Huinan, Wu, Cheng, Aramayo, Rodolfo, Sachs, Matthew S., Harlow, Mark L.·2015·Scientific Reports
DOI 10.1038/srep14918PMC PMC4597359
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Abstract

Synaptic vesicles (SVs) are neuronal presynaptic organelles that load and release neurotransmitter at chemical synapses. In addition to classic neurotransmitters, we have found that synaptic vesicles isolated from the electric organ of Torpedo californica,a model cholinergic synapse, contain small ribonucleic acids (sRNAs), primarily the 5′ ends of transfer RNAs (tRNAs) termed tRNA fragments (trfRNAs). To test the evolutionary conservation of SV sRNAs we examined isolated SVs from the mouse central nervous system (CNS). We found abundant levels of sRNAs in mouse SVs, including trfRNAs and micro RNAs (miRNAs) known to be involved in transcriptional and translational regulation. This discovery suggests that, in addition to inducing changes in local dendritic excitability through the release of neurotransmitters, SVs may, through the release of specific trfRNAs and miRNAs, directly regulate local protein synthesis. We believe these findings have broad implications for the study of chemical synaptic transmission.

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Figure 1 Cholinergic SVs from the electric organ of Torpedo californica contain RNA. (a) Electron micrograph of negatively stained SVs isolated and enriched from electroplaque tissue. Sample contains abundant ~80 nm vesicles (some marked with arrows). (b) Western-blot analysis of the synaptic vesicles during purification. The SV protein synaptophysin was used as a marker during the enrichment. The isolation procedure includes the collection of the original slurry (Sl), two centrifugation supernatants and pellets (S1, P1 and S2, P2), followed by a sucrose density gradient centrifugation and collection of the SV fluffy layer (FL). Further purification using size-exclusion chromatography yields the final, enriched sample of SVs (SV). Purified vesicles were tested by immunoblot and found to be positive for the ~60 kD vesicle acetylcholine transporter (VAChT). (c) Abundant sRNAs co-enrich with the synaptic vesicles (SV). These sRNAs are stable under high pH (pH10), or in the presence of detergent (DM). After addition of RNase much of the RNA is degraded; however an RNase resistant ~32 nt band persists (RNase). The RNase resistant band of RNA can be degraded in the presence of high pH, detergent, and RNase (pHDR). Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (d) TIRF microscope images of SVs reveals that single SVs contain RNA, as demonstrated by triple-labeling of the SVs with the styryl dye FM4–64, VAChT, and the RNA dye SYTO12. Five representative vesicles shown from a total of 307. Scale bar = 1 μm.
Figure 1 Cholinergic SVs from the electric organ of Torpedo californica contain RNA. (a) Electron micrograph of negatively stained SVs isolated and enriched from electroplaque tissue. Sample contains abundant ~80 nm vesicles (some marked with arrows). (b) Western-blot analysis of the synaptic vesicles during purification. The SV protein synaptophysin was used as a marker during the enrichment. The isolation procedure includes the collection of the original slurry (Sl), two centrifugation supernatants and pellets (S1, P1 and S2, P2), followed by a sucrose density gradient centrifugation and collection of the SV fluffy layer (FL). Further purification using size-exclusion chromatography yields the final, enriched sample of SVs (SV). Purified vesicles were tested by immunoblot and found to be positive for the ~60 kD vesicle acetylcholine transporter (VAChT). (c) Abundant sRNAs co-enrich with the synaptic vesicles (SV). These sRNAs are stable under high pH (pH10), or in the presence of detergent (DM). After addition of RNase much of the RNA is degraded; however an RNase resistant ~32 nt band persists (RNase). The RNase resistant band of RNA can be degraded in the presence of high pH, detergent, and RNase (pHDR). Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (d) TIRF microscope images of SVs reveals that single SVs contain RNA, as demonstrated by triple-labeling of the SVs with the styryl dye FM4–64, VAChT, and the RNA dye SYTO12. Five representative vesicles shown from a total of 307. Scale bar = 1 μm.CC BY · PubMed Central
Figure 2 Cholinergic vesicles isolated from the electric organ of T. californica contain 5′-tRNA fragments. (a) Next-generation sequencing of RNA isolated from RNase treated SVs enriched and affinity purified against VAChT reveals that cholinergic SVs contain 5′ fragments of tRNA. The most abundant fragment (5′-trfRNAGlu) shown in red mapped onto the complete tRNA glutamate (tRNAGluCUC) shown in black. (b) Northern analysis of RNA isolated from SVs verifies that the 5′-trfRNAGlu sequence was not a product of RNase treatment. RNA isolated from SVs purely isolated (SV), at pH10 (pH10), in detergent (DM), treated with RNase (RNase), and treated simultaneously with pH10, detergent, and RNase (pHDR). Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (c) Northern analysis of total RNA (TRIzol) and tRNA enriched RNA (LiCl) isolated from the electric lobe (LB) and electric organ (OG) of T. californica reveals full length tRNAGluCUC and 5′-trfRNAGlu were found in near equal abundance in the electric organ, whereas 5′-trfRNAGlu was more abundant than tRNAGluCUC in the electric lobe.
Figure 2 Cholinergic vesicles isolated from the electric organ of T. californica contain 5′-tRNA fragments. (a) Next-generation sequencing of RNA isolated from RNase treated SVs enriched and affinity purified against VAChT reveals that cholinergic SVs contain 5′ fragments of tRNA. The most abundant fragment (5′-trfRNAGlu) shown in red mapped onto the complete tRNA glutamate (tRNAGluCUC) shown in black. (b) Northern analysis of RNA isolated from SVs verifies that the 5′-trfRNAGlu sequence was not a product of RNase treatment. RNA isolated from SVs purely isolated (SV), at pH10 (pH10), in detergent (DM), treated with RNase (RNase), and treated simultaneously with pH10, detergent, and RNase (pHDR). Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (c) Northern analysis of total RNA (TRIzol) and tRNA enriched RNA (LiCl) isolated from the electric lobe (LB) and electric organ (OG) of T. californica reveals full length tRNAGluCUC and 5′-trfRNAGlu were found in near equal abundance in the electric organ, whereas 5′-trfRNAGlu was more abundant than tRNAGluCUC in the electric lobe.CC BY · PubMed Central
Figure 3 5′-trfRNAGlu localize to axons and presynaptic nerve terminals of the electric organ of T. californica. (a) Immunohistochemical labeling of 20-micron thick cryostat sections of the electric organ. Axons and presynaptic terminals labeled with polyclonal antibodies against VAChT (red). The nicotinic acetylcholine receptor rich surface of the electrocyte cells labeled with α-Bungarotoxin (green). (a’) Enlarged region from (a), axon marked with white arrow and presynaptic bouton white arrowhead (b) A similar pattern of labeling is present within in situ hybridization samples of the same tissue. Axons and presynaptic boutons labeled with a probe for 5′-trfRNAGLU (red), and the surface of the electrocyte cells labeled with α-Bungarotoxin (green). (b’) Enlarged region from (b), axon marked with white arrow and presynaptic boutons white arrowheads (a’,b’) scale bar = 5 μm.
Figure 3 5′-trfRNAGlu localize to axons and presynaptic nerve terminals of the electric organ of T. californica. (a) Immunohistochemical labeling of 20-micron thick cryostat sections of the electric organ. Axons and presynaptic terminals labeled with polyclonal antibodies against VAChT (red). The nicotinic acetylcholine receptor rich surface of the electrocyte cells labeled with α-Bungarotoxin (green). (a’) Enlarged region from (a), axon marked with white arrow and presynaptic bouton white arrowhead (b) A similar pattern of labeling is present within in situ hybridization samples of the same tissue. Axons and presynaptic boutons labeled with a probe for 5′-trfRNAGLU (red), and the surface of the electrocyte cells labeled with α-Bungarotoxin (green). (b’) Enlarged region from (b), axon marked with white arrow and presynaptic boutons white arrowheads (a’,b’) scale bar = 5 μm.CC BY · PubMed Central
Figure 4 SVs isolated from the mouse CNS contain sRNAs. (a) Electron micrograph image of negatively stained vesicles isolated from the mouse CNS. Sample contains abundant ~40 nm vesicles (some marked with arrows). (b) Western-blot analysis of the synaptic vesicles during purification. The SV protein synaptophysin was used as a marker during isolation. The isolation procedure includes the collection of the orginal slurry (Sl), two centrifugation supernatants and pellets (S1, P1 and S2, P2), followed by a sucrose density gradient centrifugation and collection of the SV fluffy layer (FL). Further purification using size exclusion chromatography yields the final, isolated sample of SVs (SV). (c) Abundant sRNAs co-enrich with the synaptic vesicles (SV). These sRNAs are stable under high pH (pH10), or in the presence of detergent (DM). After addition of RNase much of the RNA is degraded; however an RNase resistant ~32 nt and lower ~20 nt band persists (RNase). The RNAse resistant band of RNA can be partially degraded in the presence of high pH, detergent, and RNAse (pHDR). (d) Northern analysis of RNA isolated from SVs verifies that the 5′-trfRNAGlu sequence, the second most abundant sequence in mouse CNS SV, was not a product of RNase treatment. RNA isolated from SVs purely isolated (SV), at pH10 (pH10), in detergent (DM), treated with RNase (RNase), and treated simultaneously with pH10, detergent, and RNase (pHDR). In the mouse CNS, both full-length tRNAGluCUC and 5′-trfRNAGlu co-enrich with the SVs, but only 5′-trfRNAGlu is resistant to RNase treatment. (e) The most abundant species of sRNA in mouse was a 5′ fragment of a Y RNA: Ro-associated Y1 (RNY1):5′-fRNY1. Like the 5′-trfRNAGlu, full length and precursor sequences of RNY1 co-enrich with the SVs. (c–e) Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (f) The miRNA and RISC associated protein AGO2 co-enriches with SVs, however it is susceptible to trypsin degradation (0–20 minute exposure) indicating it does not reside within the lumen of the SVs. The SV protein synaptophysin, which has trypsin cleavage domains residing within the lumen of the SVs, is not degraded.
Figure 4 SVs isolated from the mouse CNS contain sRNAs. (a) Electron micrograph image of negatively stained vesicles isolated from the mouse CNS. Sample contains abundant ~40 nm vesicles (some marked with arrows). (b) Western-blot analysis of the synaptic vesicles during purification. The SV protein synaptophysin was used as a marker during isolation. The isolation procedure includes the collection of the orginal slurry (Sl), two centrifugation supernatants and pellets (S1, P1 and S2, P2), followed by a sucrose density gradient centrifugation and collection of the SV fluffy layer (FL). Further purification using size exclusion chromatography yields the final, isolated sample of SVs (SV). (c) Abundant sRNAs co-enrich with the synaptic vesicles (SV). These sRNAs are stable under high pH (pH10), or in the presence of detergent (DM). After addition of RNase much of the RNA is degraded; however an RNase resistant ~32 nt and lower ~20 nt band persists (RNase). The RNAse resistant band of RNA can be partially degraded in the presence of high pH, detergent, and RNAse (pHDR). (d) Northern analysis of RNA isolated from SVs verifies that the 5′-trfRNAGlu sequence, the second most abundant sequence in mouse CNS SV, was not a product of RNase treatment. RNA isolated from SVs purely isolated (SV), at pH10 (pH10), in detergent (DM), treated with RNase (RNase), and treated simultaneously with pH10, detergent, and RNase (pHDR). In the mouse CNS, both full-length tRNAGluCUC and 5′-trfRNAGlu co-enrich with the SVs, but only 5′-trfRNAGlu is resistant to RNase treatment. (e) The most abundant species of sRNA in mouse was a 5′ fragment of a Y RNA: Ro-associated Y1 (RNY1):5′-fRNY1. Like the 5′-trfRNAGlu, full length and precursor sequences of RNY1 co-enrich with the SVs. (c–e) Bands of gel underlined (_) indicate a 20-fold reduction of sample loaded. (f) The miRNA and RISC associated protein AGO2 co-enriches with SVs, however it is susceptible to trypsin degradation (0–20 minute exposure) indicating it does not reside within the lumen of the SVs. The SV protein synaptophysin, which has trypsin cleavage domains residing within the lumen of the SVs, is not degraded.CC BY · PubMed Central
Figure 5 Tertiary structure of 5′-trfRNAGlu mimics tRNA anticodon stem and loop. (a) RNAfold was used to calculate the minimum free energy secondary structure of 5′-trfRNAGlu. Base-pair probabilities are shown in a heat map from 0–1; for non-paired nucleotides, heat map indicates probability of being unpaired. (b) The centroid secondary structure is identical to the minimum free energy structure. The heat map shows the positional entropy (from 0–1.1). (c) Secondary structure of 5′-trfRNAGlu showing the pseudo-anticodon region in orange. (d) Tertiary structure of 5′-trfRNAGlu calculated using RNACOMPOSER (red and orange). The tertiary structure was aligned in pymol to a known crystal structure of a tRNA, shown in blue (yeast tRNAPhe 1ehz) The stem and loop structure determined in this manner closely resembled known crystal structures of the tRNA anticodon stem and loop, particularly at the anticodon region (orange). The sequence of this pseudo-anticodon is GGU. Both RNAfold and RNACOMPOSER used with default settings.
Figure 5 Tertiary structure of 5′-trfRNAGlu mimics tRNA anticodon stem and loop. (a) RNAfold was used to calculate the minimum free energy secondary structure of 5′-trfRNAGlu. Base-pair probabilities are shown in a heat map from 0–1; for non-paired nucleotides, heat map indicates probability of being unpaired. (b) The centroid secondary structure is identical to the minimum free energy structure. The heat map shows the positional entropy (from 0–1.1). (c) Secondary structure of 5′-trfRNAGlu showing the pseudo-anticodon region in orange. (d) Tertiary structure of 5′-trfRNAGlu calculated using RNACOMPOSER (red and orange). The tertiary structure was aligned in pymol to a known crystal structure of a tRNA, shown in blue (yeast tRNAPhe 1ehz) The stem and loop structure determined in this manner closely resembled known crystal structures of the tRNA anticodon stem and loop, particularly at the anticodon region (orange). The sequence of this pseudo-anticodon is GGU. Both RNAfold and RNACOMPOSER used with default settings.CC BY · PubMed Central

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Authors
Li, H., Wu, C., Aramayo, R., Sachs, M. S., & Harlow, M. L.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2015-10-08
Volume
5
Issue
1
ISSN
2045-2322
DOI
10.1038/srep14918
PMC
PMC4597359
Cited by
31
References
4
Language
en
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Li, H., Wu, C., Aramayo, R., Sachs, M. S., & Harlow, M. L. (2015). Synaptic vesicles contain small ribonucleic acids (sRNAs) including transfer RNA fragments (trfRNA) and microRNAs (miRNA). Scientific Reports. https://doi.org/10.1038/srep14918