Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals
Identifieur interne : 000067 ( Pmc/Checkpoint ); précédent : 000066; suivant : 000068Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals
Auteurs : Dinara Bulgari ; Chaoming Zhou ; Randall S. Hewes ; David L. Deitcher ; Edwin S. LevitanSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2014.
Abstract
Neuropeptides, which affect mood and behavior, are synthesized in the soma and delivered to nerve terminals for storage and release. Yet, among identified neurons, there is great variation in the abundance of neuropeptides in terminals. Demonstrated transcriptional regulation of neuropeptide synthesis supports the view that presynaptic neuropeptide stores are proportional to synthesis-driven delivery of neuropeptide-containing vesicles to terminals. However, we show that nerve terminals with dramatically different neuropeptide stores are supported by identical vesicle delivery and differ instead in efficiency of vesicle capture. Vesicle capture in the terminal is under transcriptional control and influences vesicle distribution and replacement as well as neuropeptide accumulation for release. Thus, vesicle capture is a major determinant of nerve terminal function.
Url:
DOI: 10.1073/pnas.1322170111
PubMed: 24550480
PubMed Central: 3948302
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Hewes</name><affiliation><nlm:aff wicri:cut="; and" id="aff2">Department of Biology,<institution>University of Oklahoma</institution>, Norman,<addr-line>OK</addr-line> 73019</nlm:aff></affiliation></author><author><name sortKey="Deitcher, David L" sort="Deitcher, David L" uniqKey="Deitcher D" first="David L." last="Deitcher">David L. Deitcher</name><affiliation><nlm:aff id="aff3">Department of Neurobiology and Behavior,<institution>Cornell University</institution>, Ithaca,<addr-line>NY</addr-line> 14853</nlm:aff></affiliation></author><author><name sortKey="Levitan, Edwin S" sort="Levitan, Edwin S" uniqKey="Levitan E" first="Edwin S." last="Levitan">Edwin S. Levitan</name><affiliation><nlm:aff id="aff1">Department of Pharmacology and Chemical Biology,<institution>University of Pittsburgh</institution>, Pittsburgh,<addr-line>PA</addr-line> 15261;</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24550480</idno><idno type="pmc">3948302</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3948302</idno><idno type="RBID">PMC:3948302</idno><idno type="doi">10.1073/pnas.1322170111</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000B86</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B86</idno><idno type="wicri:Area/Pmc/Curation">000B61</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000B61</idno><idno type="wicri:Area/Pmc/Checkpoint">000067</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000067</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals</title><author><name sortKey="Bulgari, Dinara" sort="Bulgari, Dinara" uniqKey="Bulgari D" first="Dinara" last="Bulgari">Dinara Bulgari</name><affiliation><nlm:aff id="aff1">Department of Pharmacology and Chemical Biology,<institution>University of Pittsburgh</institution>, Pittsburgh,<addr-line>PA</addr-line> 15261;</nlm:aff></affiliation></author><author><name sortKey="Zhou, Chaoming" sort="Zhou, Chaoming" uniqKey="Zhou C" first="Chaoming" last="Zhou">Chaoming Zhou</name><affiliation><nlm:aff id="aff1">Department of Pharmacology and Chemical Biology,<institution>University of Pittsburgh</institution>, Pittsburgh,<addr-line>PA</addr-line> 15261;</nlm:aff></affiliation></author><author><name sortKey="Hewes, Randall S" sort="Hewes, Randall S" uniqKey="Hewes R" first="Randall S." last="Hewes">Randall S. Hewes</name><affiliation><nlm:aff wicri:cut="; and" id="aff2">Department of Biology,<institution>University of Oklahoma</institution>, Norman,<addr-line>OK</addr-line> 73019</nlm:aff></affiliation></author><author><name sortKey="Deitcher, David L" sort="Deitcher, David L" uniqKey="Deitcher D" first="David L." last="Deitcher">David L. Deitcher</name><affiliation><nlm:aff id="aff3">Department of Neurobiology and Behavior,<institution>Cornell University</institution>, Ithaca,<addr-line>NY</addr-line> 14853</nlm:aff></affiliation></author><author><name sortKey="Levitan, Edwin S" sort="Levitan, Edwin S" uniqKey="Levitan E" first="Edwin S." last="Levitan">Edwin S. Levitan</name><affiliation><nlm:aff id="aff1">Department of Pharmacology and Chemical Biology,<institution>University of Pittsburgh</institution>, Pittsburgh,<addr-line>PA</addr-line> 15261;</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Neuropeptides, which affect mood and behavior, are synthesized in the soma and delivered to nerve terminals for storage and release. Yet, among identified neurons, there is great variation in the abundance of neuropeptides in terminals. Demonstrated transcriptional regulation of neuropeptide synthesis supports the view that presynaptic neuropeptide stores are proportional to synthesis-driven delivery of neuropeptide-containing vesicles to terminals. However, we show that nerve terminals with dramatically different neuropeptide stores are supported by identical vesicle delivery and differ instead in efficiency of vesicle capture. Vesicle capture in the terminal is under transcriptional control and influences vesicle distribution and replacement as well as neuropeptide accumulation for release. Thus, vesicle capture is a major determinant of nerve terminal function.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24550480</article-id><article-id pub-id-type="pmc">3948302</article-id><article-id pub-id-type="publisher-id">201322170</article-id><article-id pub-id-type="doi">10.1073/pnas.1322170111</article-id><article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Neuroscience</subject></subj-group></subj-group></article-categories><title-group><article-title>Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals</article-title><alt-title alt-title-type="short">Vesicle capture produces large neuropeptide stores</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bulgari</surname><given-names>Dinara</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhou</surname><given-names>Chaoming</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hewes</surname><given-names>Randall S.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Deitcher</surname><given-names>David L.</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Levitan</surname><given-names>Edwin S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><aff id="aff1"><sup>a</sup>Department of Pharmacology and Chemical Biology,<institution>University of Pittsburgh</institution>, Pittsburgh,<addr-line>PA</addr-line> 15261;</aff><aff id="aff2"><sup>b</sup>Department of Biology,<institution>University of Oklahoma</institution>, Norman,<addr-line>OK</addr-line> 73019; and</aff><aff id="aff3"><sup>c</sup>Department of Neurobiology and Behavior,<institution>Cornell University</institution>, Ithaca,<addr-line>NY</addr-line> 14853</aff></contrib-group><author-notes><corresp id="cor1"><sup>1</sup>To whom correspondence should be addressed. E-mail: <email>elevitan@pitt.edu</email>.</corresp><fn fn-type="edited-by"><p>Edited by Eve Marder, Brandeis University, Waltham, MA, and approved January 24, 2014 (received for review November 26, 2013)</p></fn><fn fn-type="con"><p>Author contributions: D.B. and E.S.L. designed research; D.B. performed research; C.Z., R.S.H., and D.L.D. contributed new reagents/analytic tools; D.B. and E.S.L. analyzed data; and D.B. and E.S.L. wrote the paper.</p></fn></author-notes><pub-date pub-type="ppub"><day>4</day><month>3</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>18</day><month>2</month><year>2014</year></pub-date><volume>111</volume><issue>9</issue><fpage>3597</fpage><lpage>3601</lpage><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201322170.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Neuropeptides, which affect mood and behavior, are synthesized in the soma and delivered to nerve terminals for storage and release. Yet, among identified neurons, there is great variation in the abundance of neuropeptides in terminals. Demonstrated transcriptional regulation of neuropeptide synthesis supports the view that presynaptic neuropeptide stores are proportional to synthesis-driven delivery of neuropeptide-containing vesicles to terminals. However, we show that nerve terminals with dramatically different neuropeptide stores are supported by identical vesicle delivery and differ instead in efficiency of vesicle capture. Vesicle capture in the terminal is under transcriptional control and influences vesicle distribution and replacement as well as neuropeptide accumulation for release. Thus, vesicle capture is a major determinant of nerve terminal function.</p></abstract><abstract><p>Neurons vary in their capacity to produce, store, and release neuropeptides packaged in dense-core vesicles (DCVs). Specifically, neurons used for cotransmission have terminals that contain few DCVs and many small synaptic vesicles, whereas neuroendocrine neuron terminals contain many DCVs. Although the mechanistic basis for presynaptic variation is unknown, past research demonstrated transcriptional control of neuropeptide synthesis suggesting that supply from the soma limits presynaptic neuropeptide accumulation. Here neuropeptide release is shown to scale with presynaptic neuropeptide stores in identified <italic>Drosophila</italic> cotransmitting and neuroendocrine terminals. However, the dramatic difference in DCV number in these terminals occurs with similar anterograde axonal transport and DCV half-lives. Thus, differences in presynaptic neuropeptide stores are not explained by DCV delivery from the soma or turnover. Instead, greater neuropeptide accumulation in neuroendocrine terminals is promoted by dramatically more efficient presynaptic DCV capture. Greater capture comes with tradeoffs, however, as fewer uncaptured DCVs are available to populate distal boutons and replenish neuropeptide stores following release. Finally, expression of the Dimmed transcription factor in cotransmitting neurons increases presynaptic DCV capture. Therefore, DCV capture in the terminal is genetically controlled and determines neuron-specific variation in peptidergic function.</p></abstract><kwd-group><kwd>nerve terminal</kwd><kwd>secretory granule</kwd><kwd>neurotransmission</kwd><kwd>LDCV</kwd></kwd-group><counts><page-count count="5"></page-count></counts></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Bulgari, Dinara" sort="Bulgari, Dinara" uniqKey="Bulgari D" first="Dinara" last="Bulgari">Dinara Bulgari</name><name sortKey="Deitcher, David L" sort="Deitcher, David L" uniqKey="Deitcher D" first="David L." last="Deitcher">David L. Deitcher</name><name sortKey="Hewes, Randall S" sort="Hewes, Randall S" uniqKey="Hewes R" first="Randall S." last="Hewes">Randall S. Hewes</name><name sortKey="Levitan, Edwin S" sort="Levitan, Edwin S" uniqKey="Levitan E" first="Edwin S." last="Levitan">Edwin S. Levitan</name><name sortKey="Zhou, Chaoming" sort="Zhou, Chaoming" uniqKey="Zhou C" first="Chaoming" last="Zhou">Chaoming Zhou</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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