{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T21:08:05Z","timestamp":1790456885525,"version":"4.1.0"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"8","license":[{"start":{"date-parts":[[2016,10,13]],"date-time":"2016-10-13T00:00:00Z","timestamp":1476316800000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Neurobiol"],"published-print":{"date-parts":[[2017,10]]},"DOI":"10.1007\/s12035-016-0176-9","type":"journal-article","created":{"date-parts":[[2016,10,13]],"date-time":"2016-10-13T08:55:01Z","timestamp":1476348901000},"page":"6609-6623","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":33,"title":["Targeting SUMO-1ylation Contrasts Synaptic Dysfunction in a Mouse Model of Alzheimer\u2019s Disease"],"prefix":"10.1007","volume":"54","author":[{"given":"Serena","family":"Marcelli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Ficulle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Filomena","family":"Iannuzzi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enik\u00f6","family":"K\u00f6vari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Nistic\u00f2","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marco","family":"Feligioni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,10,13]]},"reference":[{"key":"176_CR1","first-page":"77","volume":"3","author":"DM Holtzman","year":"2011","unstructured":"Holtzman DM, Morris JC, Goate AM (2011) Alzheimer\u2019s disease: the challenge of the second century. Sci Transl Med 3:77\u201377sr1","journal-title":"Sci Transl Med"},{"issue":"4","key":"176_CR2","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1007\/BF00308809","volume":"82","author":"H Braak","year":"1991","unstructured":"Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239\u2013259","journal-title":"Acta Neuropathol"},{"issue":"1","key":"176_CR3","doi-asserted-by":"crossref","first-page":"a006189","DOI":"10.1101\/cshperspect.a006189","volume":"1","author":"A Serrano-Pozo","year":"2011","unstructured":"Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT (2011) Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 1(1):a006189","journal-title":"Cold Spring Harb Perspect Med"},{"issue":"4","key":"176_CR4","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1016\/j.bcp.2014.01.015","volume":"88","author":"CR Overk","year":"2014","unstructured":"Overk CR, Masliah E (2014) Pathogenesis of synaptic degeneration in Alzheimer\u2019s disease and Lewy body disease. Biochem Pharmacol 88(4):508\u2013516","journal-title":"Biochem Pharmacol"},{"key":"176_CR5","doi-asserted-by":"crossref","unstructured":"Sheng M, Sabatini BL, S\u00fcdhof TC (2012) Synapses and Alzheimer\u2019s disease. Cold Spring Harb Perspect Biol 4(5)","DOI":"10.1101\/cshperspect.a005777"},{"issue":"4\u20135","key":"176_CR6","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.neuropharm.2010.07.012","volume":"59","author":"GA Krafft","year":"2010","unstructured":"Krafft GA, Klein WL (2010) ADDLs and the signaling web that leads to Alzheimer\u2019s disease. Neuropharmacology 59(4\u20135):230\u2013242","journal-title":"Neuropharmacology"},{"issue":"1","key":"176_CR7","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1038\/nn.2709","volume":"14","author":"M D\u2019Amelio","year":"2011","unstructured":"D\u2019Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, Ferri A, Diamantini A, De Zio D et al (2011) Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer\u2019s disease. Nat Neurosci 14(1):69\u201376","journal-title":"Nat Neurosci"},{"issue":"5","key":"176_CR8","doi-asserted-by":"crossref","first-page":"1488","DOI":"10.2353\/ajpath.2008.080434","volume":"173","author":"N Louneva","year":"2008","unstructured":"Louneva N, Cohen JW, Han LY, Talbot K, Wilson RS, Bennett DA, Trojanowski JQ, Arnold SE (2008) Caspase-3 is enriched in postsynaptic densities and increased in Alzheimer\u2019s disease. Am J Pathol 173(5):1488\u20131495","journal-title":"Am J Pathol"},{"issue":"7","key":"176_CR9","doi-asserted-by":"crossref","first-page":"2636","DOI":"10.1523\/JNEUROSCI.4456-09.2010","volume":"30","author":"H-Y Wu","year":"2010","unstructured":"Wu H-Y, Hudry E, Hashimoto T, Kuchibhotla K, Rozkalne A, Fan Z, Spires-Jones T, Xie H et al (2010) Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J Neurosci 30(7):2636\u20132649","journal-title":"J Neurosci"},{"issue":"4","key":"176_CR10","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1007\/s12017-013-8257-7","volume":"15","author":"L Lee","year":"2013","unstructured":"Lee L, Sakurai M, Matsuzaki S, Arancio O, Fraser P (2013) SUMO and Alzheimer\u2019s disease. Neruomol Med 15(4):720\u2013736","journal-title":"Neruomol Med"},{"key":"176_CR11","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/B978-0-12-386041-5.00004-2","volume":"288","author":"KD Sarge","year":"2011","unstructured":"Sarge KD, Park-Sarge O-K (2011) SUMO and its role in human diseases. Int Rev Cell Mol Biol 288:167\u2013183","journal-title":"Int Rev Cell Mol Biol"},{"issue":"4","key":"176_CR12","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s12017-013-8258-6","volume":"15","author":"M Droescher","year":"2013","unstructured":"Droescher M, Chaugule VK, Pichler A (2013) SUMO rules: regulatory concepts and their implication in neurologic functions. Neruomol Med 15(4):639\u2013660","journal-title":"Neruomol Med"},{"issue":"4","key":"176_CR13","doi-asserted-by":"crossref","first-page":"382","DOI":"10.3934\/molsci.2015.4.382","volume":"2","author":"M Feligioni","year":"2015","unstructured":"Feligioni M, Marcelli S, Knock E, Nadeem U, Arancio O, Fraser PE (2015) SUMO modulation of protein aggregation and degradation. AIMS Mol Sci 2(4):382\u2013410","journal-title":"AIMS Mol Sci"},{"issue":"4","key":"176_CR14","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s12017-013-8266-6","volume":"15","author":"M Feligioni","year":"2013","unstructured":"Feligioni M, Nistic\u00f2 R (2013) SUMO: a (oxidative) stressed protein. Neruomol Med 15(4):707\u2013719","journal-title":"Neruomol Med"},{"key":"176_CR15","doi-asserted-by":"crossref","first-page":"7190","DOI":"10.1038\/srep07190","volume":"4","author":"L Lee","year":"2014","unstructured":"Lee L, Dale E, Staniszewski A, Zhang H, Saeed F, Sakurai M, Fa M, Orozco I et al (2014) Regulation of synaptic plasticity and cognition by SUMO in normal physiology and Alzheimer\u2019s disease. Sci. Rep. 4:7190","journal-title":"Sci. Rep."},{"issue":"7142","key":"176_CR16","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1038\/nature05736","volume":"447","author":"S Martin","year":"2007","unstructured":"Martin S, Nishimune A, Mellor JR, Henley JM (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447(7142):321\u2013325","journal-title":"Nature"},{"issue":"7","key":"176_CR17","doi-asserted-by":"crossref","first-page":"1348","DOI":"10.1111\/j.1460-9568.2009.06692.x","volume":"29","author":"M Feligioni","year":"2009","unstructured":"Feligioni M, Nishimune A, Henley JM (2009) Protein SUMOylation modulates calcium influx and glutamate release from presynaptic terminals. Eur J Neurosci 29(7):1348\u20131356","journal-title":"Eur J Neurosci"},{"key":"176_CR18","doi-asserted-by":"crossref","first-page":"10730","DOI":"10.1038\/srep10730","volume":"5","author":"S Matsuzaki","year":"2015","unstructured":"Matsuzaki S, Lee L, Knock E, Srikumar T, Sakurai M, Hazrati L-N, Katayama T, Staniszewski A et al (2015) SUMO1 affects synaptic function, spine density and memory. Sci. Rep. 5:10730","journal-title":"Sci. Rep."},{"key":"176_CR19","first-page":"63","volume":"5","author":"R Nistic\u00f2","year":"2014","unstructured":"Nistic\u00f2 R, Ferraina C, Marconi V, Blandini F, Negri L, Egebjerg J, Feligioni M (2014) Age-related changes of protein SUMOylation balance in the A\u03b2PP Tg2576 mouse model of Alzheimer\u2019s disease. Front Pharmacol 5:63","journal-title":"Front Pharmacol"},{"key":"176_CR20","doi-asserted-by":"crossref","first-page":"9035","DOI":"10.1038\/srep09035","volume":"5","author":"R Nistic\u00f2","year":"2015","unstructured":"Nistic\u00f2 R, Florenzano F, Mango D, Ferraina C, Grilli M, Di Prisco S, Nobili A, Saccucci S et al (2015) Presynaptic c-Jun N-terminal Kinase 2 regulates NMDA receptor-dependent glutamate release. Sci Rep 5:9035","journal-title":"Sci Rep"},{"issue":"3","key":"176_CR21","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1016\/j.bbrc.2009.10.065","volume":"390","author":"H Lu","year":"2009","unstructured":"Lu H, Liu B, You S, Xue Q, Zhang F, Cheng J, Yu B (2009) The activity-dependent stimuli increase SUMO modification in SHSY5Y cells. Biochem Biophys Res Commun 390(3):872\u2013876","journal-title":"Biochem Biophys Res Commun"},{"issue":"4","key":"176_CR22","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1016\/j.cell.2006.06.046","volume":"126","author":"B Gong","year":"2006","unstructured":"Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, Staniszewski A, Moolman D, Zhang H et al (2006) Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126(4):775\u2013788","journal-title":"Cell"},{"issue":"10","key":"176_CR23","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.molmed.2007.08.002","volume":"13","author":"JM Gump","year":"2007","unstructured":"Gump JM, Dowdy SF (2007) TAT transduction: the molecular mechanism and therapeutic prospects. Trends Mol Med 13(10):443\u2013448","journal-title":"Trends Mol Med"},{"issue":"12","key":"176_CR24","doi-asserted-by":"crossref","first-page":"e28185","DOI":"10.1371\/journal.pone.0028185","volume":"6","author":"M Feligioni","year":"2011","unstructured":"Feligioni M, Brambilla E, Camassa A, Sclip A, Arnaboldi A, Morelli F, Antoniou X, Borsello T (2011) Crosstalk between JNK and SUMO signaling pathways: deSUMOylation is protective against H2O2-induced cell injury. PLoS One 6(12):e28185","journal-title":"PLoS One"},{"issue":"7","key":"176_CR25","doi-asserted-by":"crossref","first-page":"4740","DOI":"10.1074\/jbc.M111.321141","volume":"287","author":"JR Gareau","year":"2012","unstructured":"Gareau JR, Reverter D, Lima CD (2012) Determinants of small ubiquitin-like modifier 1 (SUMO1) protein specificity, E3 ligase, and SUMO-RanGAP1 binding activities of nucleoporin RanBP2. J Biol Chem 287(7):4740\u20134751","journal-title":"J Biol Chem"},{"issue":"4","key":"176_CR26","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1111\/j.1750-3639.2008.00147.x","volume":"18","author":"I Alafuzoff","year":"2008","unstructured":"Alafuzoff I, Arzberger T, Al-Sarraj S, Bodi I, Bogdanovic N, Braak H, Bugiani K, Del-Tredici K et al (2008) Staging of neurofibrillary pathology in Alzheimer\u2019s disease: a study of the BrainNet Europe consortium. Brain Pathol 18(4):484\u2013496","journal-title":"Brain Pathol"},{"issue":"1","key":"176_CR27","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/1750-1326-4-48","volume":"4","author":"GM Shankar","year":"2009","unstructured":"Shankar GM, Walsh DM (2009) Alzheimer\u2019s disease: synaptic dysfunction and Abeta. Mol Neurodegener 4(1):48","journal-title":"Mol Neurodegener"},{"issue":"3","key":"176_CR28","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1007\/s12035-012-8324-3","volume":"46","author":"R Nistic\u00f2","year":"2012","unstructured":"Nistic\u00f2 R, Pignatelli M, Piccinin S, Mercuri NB, Collingridge G (2012) Targeting synaptic dysfunction in Alzheimer\u2019s disease therapy. Mol Neurobiol 46(3):572\u2013587","journal-title":"Mol Neurobiol"},{"issue":"1","key":"176_CR29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1515\/REVNEURO.2009.20.1.1","volume":"20","author":"V Nimmrich","year":"2009","unstructured":"Nimmrich V, Ebert U (2009) Is Alzheimer\u2019s disease a result of presynaptic failure? Synaptic dysfunctions induced by oligomeric beta-amyloid. Rev Neurosci 20(1):1\u201312","journal-title":"Rev Neurosci"},{"issue":"11 Suppl 18","key":"176_CR30","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1017\/S1092852900014164","volume":"10","author":"PT Francis","year":"2005","unstructured":"Francis PT (2005) The interplay of neurotransmitters in Alzheimer\u2019s disease. CNS Spectr 10(11 Suppl 18):6\u20139","journal-title":"CNS Spectr"},{"issue":"3","key":"176_CR31","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.neulet.2011.07.045","volume":"502","author":"LE McMillan","year":"2011","unstructured":"McMillan LE, Brown JT, Henley JM, Cimarosti H (2011) Profiles of SUMO and ubiquitin conjugation in an Alzheimer\u2019s disease model. Neurosci Lett 502(3):201\u2013208","journal-title":"Neurosci Lett"},{"issue":"2","key":"176_CR32","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.chembiol.2009.01.009","volume":"16","author":"I Fukuda","year":"2009","unstructured":"Fukuda I, Ito A, Hirai G, Nishimura S, Kawasaki H, Saitoh H, Kimura K-I, Sodeoka M et al (2009) Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 16(2):133\u2013140","journal-title":"Chem Biol"},{"key":"176_CR33","doi-asserted-by":"crossref","unstructured":"I. M. Janssen, S. Sturtz, G. Skipka, A. Zentner, M. Velasco Garrido, M. V Garrido, and MV. Garrido R. Busse, \u201cGinkgo biloba In Alzheimer\u2019s disease: a systematic review.,\u201d Wien Med Wochenschr, vol. 160, no. 21\u201322, pp. 539\u2013546, 2010.","DOI":"10.1007\/s10354-010-0844-8"},{"issue":"51","key":"176_CR34","doi-asserted-by":"crossref","first-page":"43871","DOI":"10.1074\/jbc.M111.297515","volume":"286","author":"A Sclip","year":"2011","unstructured":"Sclip A, Antoniou X, Colombo A, Camici GG, Pozzi L, Cardinetti D, Feligioni M, Veglianese P et al (2011) C-Jun N-terminal kinase regulates soluble A\u03b2 oligomers and cognitive impairment in AD mouse model. J Biol Chem 286(51):43871\u201343880","journal-title":"J Biol Chem"},{"key":"176_CR35","doi-asserted-by":"crossref","first-page":"245","DOI":"10.3389\/fncel.2015.00245","volume":"9","author":"M Mellone","year":"2015","unstructured":"Mellone M, Stanic J, Hernandez LF, Iglesias E, Zianni E, Longhi A, Prigent A, Picconi B et al (2015) NMDA receptor GluN2A\/GluN2B subunit ratio as synaptic trait of levodopa-induced dyskinesias: from experimental models to patients. Front Cell Neurosci 9:245","journal-title":"Front Cell Neurosci"},{"issue":"5284","key":"176_CR36","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1126\/science.274.5284.99","volume":"274","author":"K Hsiao","year":"1996","unstructured":"Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274(5284):99\u2013102","journal-title":"Science"},{"issue":"7","key":"176_CR37","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1517\/17460441.2015.1041913","volume":"10","author":"D Puzzo","year":"2015","unstructured":"Puzzo D, Gulisano W, Palmeri A, Arancio O (2015) Rodent models for Alzheimer\u2019s disease drug discovery. Expert Opin Drug Discov 10(7):703\u2013711","journal-title":"Expert Opin Drug Discov"},{"issue":"5","key":"176_CR38","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1016\/j.neuropharm.2012.06.049","volume":"63","author":"M Grilli","year":"2012","unstructured":"Grilli M, Summa M, Salamone A, Olivero G, Zappettini S, Di Prisco S, Feligioni M, Usai C et al (2012) In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacology 63(5):916\u2013926","journal-title":"Neuropharmacology"},{"issue":"3","key":"176_CR39","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.neuropharm.2005.09.004","volume":"50","author":"A Pittaluga","year":"2006","unstructured":"Pittaluga A, Feligioni M, Longordo F, Luccini E, Raiteri M (2006) Trafficking of presynaptic AMPA receptors mediating neurotransmitter release: neuronal selectivity and relationships with sensitivity to cyclothiazide. Neuropharmacology 50(3):286\u2013296","journal-title":"Neuropharmacology"},{"issue":"2","key":"176_CR40","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1038\/sj.bjp.0705960","volume":"144","author":"A Pittaluga","year":"2005","unstructured":"Pittaluga A, Segantini D, Feligioni M, Raiteri M (2005) Extracellular protons differentially potentiate the responses of native AMPA receptor subtypes regulating neurotransmitter release. Br J Pharmacol 144(2):293\u2013299","journal-title":"Br J Pharmacol"},{"issue":"7","key":"176_CR41","doi-asserted-by":"crossref","first-page":"9097","DOI":"10.3390\/ijms13079097","volume":"13","author":"TY Lin","year":"2012","unstructured":"Lin TY, Lu CW, Huang SK, Wang SJ (2012) Curcumin inhibits glutamate release from rat prefrontal nerve endings by affecting vesicle mobilization. Int J Mol Sci 13(7):9097\u20139109","journal-title":"Int J Mol Sci"},{"issue":"4","key":"176_CR42","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1111\/j.0953-816X.2004.03209.x","volume":"19","author":"K Tuz","year":"2004","unstructured":"Tuz K, Pe\u00f1a-Segura C, Franco R, Pasantes-Morales H (2004) Depolarization, exocytosis and amino acid release evoked by hyposmolarity from cortical synaptosomes. Eur J Neurosci 19(4):916\u2013924","journal-title":"Eur J Neurosci"},{"issue":"3","key":"176_CR43","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1006\/meth.2001.1186","volume":"24","author":"M Becker-Hapak","year":"2001","unstructured":"Becker-Hapak M, McAllister SS, Dowdy SF (2001) TAT-mediated protein transduction into mammalian cells. Methods 24(3):247\u2013256","journal-title":"Methods"}],"container-title":["Molecular Neurobiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s12035-016-0176-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-016-0176-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-016-0176-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,19]],"date-time":"2024-06-19T22:26:59Z","timestamp":1718836019000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s12035-016-0176-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,13]]},"references-count":43,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2017,10]]}},"alternative-id":["176"],"URL":"https:\/\/doi.org\/10.1007\/s12035-016-0176-9","relation":{},"ISSN":["0893-7648","1559-1182"],"issn-type":[{"value":"0893-7648","type":"print"},{"value":"1559-1182","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,13]]}}}