Spermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses
Aging is associated with functional alterations of synapses thought to contribute to age-dependent memory impairment (AMI). While therapeutic avenues to protect from AMI are largely elusive, supplementation of spermidine, a polyamine normally declining with age, has been shown to restore defective p...
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| Veröffentlicht in: | Scientific reports 2019-12, Vol.9 (1), p.19616-12, Article 19616 |
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| creator | Maglione, Marta Kochlamazashvili, Gaga Eisenberg, Tobias Rácz, Bence Michael, Eva Toppe, David Stumpf, Alexander Wirth, Alexander Zeug, André Müller, Franziska E. Moreno-Velasquez, Laura Sammons, Rosanna P. Hofer, Sebastian J. Madeo, Frank Maritzen, Tanja Maier, Nikolaus Ponimaskin, Evgeni Schmitz, Dietmar Haucke, Volker Sigrist, Stephan J. |
| description | Aging is associated with functional alterations of synapses thought to contribute to age-dependent memory impairment (AMI). While therapeutic avenues to protect from AMI are largely elusive, supplementation of spermidine, a polyamine normally declining with age, has been shown to restore defective proteostasis and to protect from AMI in
Drosophila
. Here we demonstrate that dietary spermidine protects from age-related synaptic alterations at hippocampal mossy fiber (MF)-CA3 synapses and prevents the aging-induced loss of neuronal mitochondria. Dietary spermidine rescued age-dependent decreases in synaptic vesicle density and largely restored defective presynaptic MF-CA3 long-term potentiation (LTP) at MF-CA3 synapses (MF-CA3) in aged animals. In contrast, spermidine failed to protect CA3-CA1 hippocampal synapses characterized by postsynaptic LTP from age-related changes in function and morphology. Our data demonstrate that dietary spermidine attenuates age-associated deterioration of MF-CA3 synaptic transmission and plasticity. These findings provide a physiological and molecular basis for the future therapeutic usage of spermidine. |
| doi_str_mv | 10.1038/s41598-019-56133-3 |
| format | Article |
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Drosophila
. Here we demonstrate that dietary spermidine protects from age-related synaptic alterations at hippocampal mossy fiber (MF)-CA3 synapses and prevents the aging-induced loss of neuronal mitochondria. Dietary spermidine rescued age-dependent decreases in synaptic vesicle density and largely restored defective presynaptic MF-CA3 long-term potentiation (LTP) at MF-CA3 synapses (MF-CA3) in aged animals. In contrast, spermidine failed to protect CA3-CA1 hippocampal synapses characterized by postsynaptic LTP from age-related changes in function and morphology. Our data demonstrate that dietary spermidine attenuates age-associated deterioration of MF-CA3 synaptic transmission and plasticity. These findings provide a physiological and molecular basis for the future therapeutic usage of spermidine.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-019-56133-3</identifier><identifier>PMID: 31873156</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378/2591/2592 ; 631/378/2611 ; Age ; Aging ; Aging - drug effects ; Aging - metabolism ; Aging - pathology ; Animals ; CA3 Region, Hippocampal - metabolism ; CA3 Region, Hippocampal - pathology ; Dietary supplements ; Hippocampus ; Humanities and Social Sciences ; Long-term potentiation ; Long-Term Potentiation - drug effects ; Mice ; Mitochondria ; Mossy Fibers, Hippocampal - metabolism ; Mossy Fibers, Hippocampal - pathology ; multidisciplinary ; Science ; Science (multidisciplinary) ; Spermidine ; Spermidine - pharmacology ; Synapses ; Synaptic density ; Synaptic plasticity ; Synaptic transmission ; Synaptic Transmission - drug effects ; Synaptic Vesicles - metabolism ; Synaptic Vesicles - pathology</subject><ispartof>Scientific reports, 2019-12, Vol.9 (1), p.19616-12, Article 19616</ispartof><rights>The Author(s) 2019</rights><rights>2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-446987659f08bb4f386292ae608514aadc8a56412bf8fb7e51bbaa3a175217d43</citedby><cites>FETCH-LOGICAL-c540t-446987659f08bb4f386292ae608514aadc8a56412bf8fb7e51bbaa3a175217d43</cites><orcidid>0000-0003-0525-0714 ; 0000-0002-4570-5130 ; 0000-0003-3559-1130 ; 0000-0002-0756-0014 ; 0000-0001-9858-5841 ; 0000-0002-1933-5332 ; 0000-0003-3119-6993</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6927957/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6927957/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,41096,42165,51551,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31873156$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Maglione, Marta</creatorcontrib><creatorcontrib>Kochlamazashvili, Gaga</creatorcontrib><creatorcontrib>Eisenberg, Tobias</creatorcontrib><creatorcontrib>Rácz, Bence</creatorcontrib><creatorcontrib>Michael, Eva</creatorcontrib><creatorcontrib>Toppe, David</creatorcontrib><creatorcontrib>Stumpf, Alexander</creatorcontrib><creatorcontrib>Wirth, Alexander</creatorcontrib><creatorcontrib>Zeug, André</creatorcontrib><creatorcontrib>Müller, Franziska E.</creatorcontrib><creatorcontrib>Moreno-Velasquez, Laura</creatorcontrib><creatorcontrib>Sammons, Rosanna P.</creatorcontrib><creatorcontrib>Hofer, Sebastian J.</creatorcontrib><creatorcontrib>Madeo, Frank</creatorcontrib><creatorcontrib>Maritzen, Tanja</creatorcontrib><creatorcontrib>Maier, Nikolaus</creatorcontrib><creatorcontrib>Ponimaskin, Evgeni</creatorcontrib><creatorcontrib>Schmitz, Dietmar</creatorcontrib><creatorcontrib>Haucke, Volker</creatorcontrib><creatorcontrib>Sigrist, Stephan J.</creatorcontrib><title>Spermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Aging is associated with functional alterations of synapses thought to contribute to age-dependent memory impairment (AMI). While therapeutic avenues to protect from AMI are largely elusive, supplementation of spermidine, a polyamine normally declining with age, has been shown to restore defective proteostasis and to protect from AMI in
Drosophila
. Here we demonstrate that dietary spermidine protects from age-related synaptic alterations at hippocampal mossy fiber (MF)-CA3 synapses and prevents the aging-induced loss of neuronal mitochondria. Dietary spermidine rescued age-dependent decreases in synaptic vesicle density and largely restored defective presynaptic MF-CA3 long-term potentiation (LTP) at MF-CA3 synapses (MF-CA3) in aged animals. In contrast, spermidine failed to protect CA3-CA1 hippocampal synapses characterized by postsynaptic LTP from age-related changes in function and morphology. Our data demonstrate that dietary spermidine attenuates age-associated deterioration of MF-CA3 synaptic transmission and plasticity. These findings provide a physiological and molecular basis for the future therapeutic usage of spermidine.</description><subject>631/378/2591/2592</subject><subject>631/378/2611</subject><subject>Age</subject><subject>Aging</subject><subject>Aging - drug effects</subject><subject>Aging - metabolism</subject><subject>Aging - pathology</subject><subject>Animals</subject><subject>CA3 Region, Hippocampal - metabolism</subject><subject>CA3 Region, Hippocampal - pathology</subject><subject>Dietary supplements</subject><subject>Hippocampus</subject><subject>Humanities and Social Sciences</subject><subject>Long-term potentiation</subject><subject>Long-Term Potentiation - drug effects</subject><subject>Mice</subject><subject>Mitochondria</subject><subject>Mossy Fibers, Hippocampal - metabolism</subject><subject>Mossy Fibers, Hippocampal - pathology</subject><subject>multidisciplinary</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Spermidine</subject><subject>Spermidine - pharmacology</subject><subject>Synapses</subject><subject>Synaptic density</subject><subject>Synaptic plasticity</subject><subject>Synaptic transmission</subject><subject>Synaptic Transmission - drug effects</subject><subject>Synaptic Vesicles - metabolism</subject><subject>Synaptic Vesicles - pathology</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kUtv1TAQhS0EolXpH2CBLLFhY_AzsTdI1RUvqRILYG1NksmtqyQOti_S_fd1m1IKC7yxpfnOGc8cQl4K_lZwZd9lLYyzjAvHTCOUYuoJOZVcGyaVlE8fvU_Iec7XvB4jnRbuOTlRwrZKmOaUwLcV0xyGsCBdUyzYl0zHFGcKe2QJJyg40HxcYC2hpzAVTFBCXDKFQq_CusYe5hUmOsecj3QMHSa2u1CbJmN-QZ6NMGU8v7_PyI-PH77vPrPLr5--7C4uWW80L0zrxtm2MW7ktuv0qGwjnQRsuDVCAwy9BdNoIbvRjl2LRnQdgALRGinaQasz8n7zXQ_djEOPS0kw-TWFGdLRRwj-78oSrvw-_vKNk60zbTV4c2-Q4s8D5uLnkHucJlgwHrKXSnF1u0FT0df_oNfxkJY63h3Fja2WlZIb1ae6m4Tjw2cE97ch-i1EX0P0dyF6VUWvHo_xIPkdWQXUBuRaWvaY_vT-j-0N5DGosA</recordid><startdate>20191223</startdate><enddate>20191223</enddate><creator>Maglione, Marta</creator><creator>Kochlamazashvili, Gaga</creator><creator>Eisenberg, Tobias</creator><creator>Rácz, Bence</creator><creator>Michael, Eva</creator><creator>Toppe, David</creator><creator>Stumpf, Alexander</creator><creator>Wirth, Alexander</creator><creator>Zeug, André</creator><creator>Müller, Franziska E.</creator><creator>Moreno-Velasquez, Laura</creator><creator>Sammons, Rosanna P.</creator><creator>Hofer, Sebastian J.</creator><creator>Madeo, Frank</creator><creator>Maritzen, Tanja</creator><creator>Maier, Nikolaus</creator><creator>Ponimaskin, Evgeni</creator><creator>Schmitz, Dietmar</creator><creator>Haucke, Volker</creator><creator>Sigrist, Stephan J.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0525-0714</orcidid><orcidid>https://orcid.org/0000-0002-4570-5130</orcidid><orcidid>https://orcid.org/0000-0003-3559-1130</orcidid><orcidid>https://orcid.org/0000-0002-0756-0014</orcidid><orcidid>https://orcid.org/0000-0001-9858-5841</orcidid><orcidid>https://orcid.org/0000-0002-1933-5332</orcidid><orcidid>https://orcid.org/0000-0003-3119-6993</orcidid></search><sort><creationdate>20191223</creationdate><title>Spermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses</title><author>Maglione, Marta ; Kochlamazashvili, Gaga ; Eisenberg, Tobias ; Rácz, Bence ; Michael, Eva ; Toppe, David ; Stumpf, Alexander ; Wirth, Alexander ; Zeug, André ; Müller, Franziska E. ; Moreno-Velasquez, Laura ; Sammons, Rosanna P. ; Hofer, Sebastian J. ; Madeo, Frank ; Maritzen, Tanja ; Maier, Nikolaus ; Ponimaskin, Evgeni ; Schmitz, Dietmar ; Haucke, Volker ; Sigrist, Stephan J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-446987659f08bb4f386292ae608514aadc8a56412bf8fb7e51bbaa3a175217d43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>631/378/2591/2592</topic><topic>631/378/2611</topic><topic>Age</topic><topic>Aging</topic><topic>Aging - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maglione, Marta</au><au>Kochlamazashvili, Gaga</au><au>Eisenberg, Tobias</au><au>Rácz, Bence</au><au>Michael, Eva</au><au>Toppe, David</au><au>Stumpf, Alexander</au><au>Wirth, Alexander</au><au>Zeug, André</au><au>Müller, Franziska E.</au><au>Moreno-Velasquez, Laura</au><au>Sammons, Rosanna P.</au><au>Hofer, Sebastian J.</au><au>Madeo, Frank</au><au>Maritzen, Tanja</au><au>Maier, Nikolaus</au><au>Ponimaskin, Evgeni</au><au>Schmitz, Dietmar</au><au>Haucke, Volker</au><au>Sigrist, Stephan J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2019-12-23</date><risdate>2019</risdate><volume>9</volume><issue>1</issue><spage>19616</spage><epage>12</epage><pages>19616-12</pages><artnum>19616</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Aging is associated with functional alterations of synapses thought to contribute to age-dependent memory impairment (AMI). While therapeutic avenues to protect from AMI are largely elusive, supplementation of spermidine, a polyamine normally declining with age, has been shown to restore defective proteostasis and to protect from AMI in
Drosophila
. Here we demonstrate that dietary spermidine protects from age-related synaptic alterations at hippocampal mossy fiber (MF)-CA3 synapses and prevents the aging-induced loss of neuronal mitochondria. Dietary spermidine rescued age-dependent decreases in synaptic vesicle density and largely restored defective presynaptic MF-CA3 long-term potentiation (LTP) at MF-CA3 synapses (MF-CA3) in aged animals. In contrast, spermidine failed to protect CA3-CA1 hippocampal synapses characterized by postsynaptic LTP from age-related changes in function and morphology. Our data demonstrate that dietary spermidine attenuates age-associated deterioration of MF-CA3 synaptic transmission and plasticity. These findings provide a physiological and molecular basis for the future therapeutic usage of spermidine.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31873156</pmid><doi>10.1038/s41598-019-56133-3</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-0525-0714</orcidid><orcidid>https://orcid.org/0000-0002-4570-5130</orcidid><orcidid>https://orcid.org/0000-0003-3559-1130</orcidid><orcidid>https://orcid.org/0000-0002-0756-0014</orcidid><orcidid>https://orcid.org/0000-0001-9858-5841</orcidid><orcidid>https://orcid.org/0000-0002-1933-5332</orcidid><orcidid>https://orcid.org/0000-0003-3119-6993</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 631/378/2591/2592 631/378/2611 Age Aging Aging - drug effects Aging - metabolism Aging - pathology Animals CA3 Region, Hippocampal - metabolism CA3 Region, Hippocampal - pathology Dietary supplements Hippocampus Humanities and Social Sciences Long-term potentiation Long-Term Potentiation - drug effects Mice Mitochondria Mossy Fibers, Hippocampal - metabolism Mossy Fibers, Hippocampal - pathology multidisciplinary Science Science (multidisciplinary) Spermidine Spermidine - pharmacology Synapses Synaptic density Synaptic plasticity Synaptic transmission Synaptic Transmission - drug effects Synaptic Vesicles - metabolism Synaptic Vesicles - pathology |
| title | Spermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses |
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