{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:25:56Z","timestamp":1790835956076,"version":"4.1.0"},"reference-count":46,"publisher":"The Company of Biologists","issue":"6","license":[{"start":{"date-parts":[[2024,5,9]],"date-time":"2024-05-09T00:00:00Z","timestamp":1715212800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000915","name":"Richard King Mellon Foundation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100000915","id-type":"DOI","asserted-by":"crossref"}]},{"name":"AFM-T\u00e9l\u00e9thon","award":["24997"],"award-info":[{"award-number":["24997"]}]},{"DOI":"10.13039\/100014989","name":"Chan Zuckerberg Initiative","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100014989","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Snyder\u2013Robinson Foundation"},{"DOI":"10.13039\/100018232","name":"Orphan Disease Center, Perelman School of Medicine, University of Pennsylvania","doi-asserted-by":"crossref","award":["MDBR-20-135-SRS"],"award-info":[{"award-number":["MDBR-20-135-SRS"]}],"id":[{"id":"10.13039\/100018232","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100010559","name":"Children's Hospital of Pittsburgh","doi-asserted-by":"crossref","award":["YIAP 2019"],"award-info":[{"award-number":["YIAP 2019"]}],"id":[{"id":"10.13039\/100010559","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100007921","name":"University of Pittsburgh","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100007921","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["DP2-AR081047"],"award-info":[{"award-number":["DP2-AR081047"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R01-AR078872"],"award-info":[{"award-number":["R01-AR078872"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R01-HD110500"],"award-info":[{"award-number":["R01-HD110500"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R01 CA235863"],"award-info":[{"award-number":["R01 CA235863"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,6,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Snyder\u2013Robinson syndrome (SRS) is a rare X-linked recessive disorder caused by a mutation in the SMS gene, which encodes spermine synthase, and aberrant polyamine metabolism. SRS is characterized by intellectual disability, thin habitus, seizure, low muscle tone\/hypotonia and osteoporosis. Progress towards understanding and treating SRS requires a model that recapitulates human gene variants and disease presentations. Here, we evaluated molecular and neurological presentations in the G56S mouse model, which carries a missense mutation in the Sms gene. The lack of SMS protein in the G56S mice resulted in increased spermidine\/spermine ratio, failure to thrive, short stature and reduced bone density. They showed impaired learning capacity, increased anxiety, reduced mobility and heightened fear responses, accompanied by reduced total and regional brain volumes. Furthermore, impaired mitochondrial oxidative phosphorylation was evident in G56S cerebral cortex, G56S fibroblasts and Sms-null hippocampal cells, indicating that SMS may serve as a future therapeutic target. Collectively, our study establishes the suitability of the G56S mice as a preclinical model for SRS and provides a set of molecular and functional outcome measures that can be used to evaluate therapeutic interventions for SRS.<\/jats:p>","DOI":"10.1242\/dmm.050639","type":"journal-article","created":{"date-parts":[[2024,3,11]],"date-time":"2024-03-11T04:08:31Z","timestamp":1710130111000},"source":"Crossref","is-referenced-by-count":27,"title":["Impaired polyamine metabolism causes behavioral and neuroanatomical defects in a mouse model of Snyder\u2013Robinson syndrome"],"prefix":"10.1242","volume":"17","author":[{"given":"Oluwaseun","family":"Akinyele","sequence":"first","affiliation":[{"name":"University of Pittsburgh School of Medicine 1 Division of Genetic and Genomic Medicine, Department of Pediatrics , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anushe","family":"Munir","sequence":"additional","affiliation":[{"name":"University of Pittsburgh School of Medicine 1 Division of Genetic and Genomic Medicine, Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"School of Public Health, University of Pittsburgh 2 Department of Human Genetics , , Pittsburgh , PA 15261, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie A.","family":"Johnson","sequence":"additional","affiliation":[{"name":"University of Pittsburgh School of Medicine 1 Division of Genetic and Genomic Medicine, Department of Pediatrics , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan S.","family":"Perez","sequence":"additional","affiliation":[{"name":"University of Pittsburgh School of Medicine 1 Division of Genetic and Genomic Medicine, Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"School of Public Health, University of Pittsburgh 2 Department of Human Genetics , , Pittsburgh , PA 15261, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Gao","sequence":"additional","affiliation":[{"name":"Children's Neuroscience Institute 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"University of Pittsburgh School of Medicine 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jackson R.","family":"Foley","sequence":"additional","affiliation":[{"name":"Johns Hopkins School of Medicine 4 Sidney Kimmel Comprehensive Cancer Center , , Baltimore, MD 21224 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashley","family":"Nwafor","sequence":"additional","affiliation":[{"name":"Johns Hopkins School of Medicine 4 Sidney Kimmel Comprehensive Cancer Center , , Baltimore, MD 21224 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yijen","family":"Wu","sequence":"additional","affiliation":[{"name":"University of Pittsburgh School of Medicine 5 Department of Developmental Biology , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8679-6414","authenticated-orcid":false,"given":"Tracy","family":"Murray-Stewart","sequence":"additional","affiliation":[{"name":"Johns Hopkins School of Medicine 4 Sidney Kimmel Comprehensive Cancer Center , , Baltimore, MD 21224 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"Jr.","given":"Robert A.","family":"Casero","sequence":"additional","affiliation":[{"name":"Johns Hopkins School of Medicine 4 Sidney Kimmel Comprehensive Cancer Center , , Baltimore, MD 21224 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H\u00fclya","family":"Bayir","sequence":"additional","affiliation":[{"name":"Children's Neuroscience Institute 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"University of Pittsburgh School of Medicine 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0747-4589","authenticated-orcid":false,"given":"Dwi U.","family":"Kemaladewi","sequence":"additional","affiliation":[{"name":"University of Pittsburgh School of Medicine 1 Division of Genetic and Genomic Medicine, Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"School of Public Health, University of Pittsburgh 2 Department of Human Genetics , , Pittsburgh , PA 15261, USA"},{"name":"Children's Neuroscience Institute 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"},{"name":"University of Pittsburgh School of Medicine 3 , Department of Pediatrics , , Pittsburgh , PA 15224, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2024,5,9]]},"reference":[{"key":"2024050912002214900_DMM050639C1","doi-asserted-by":"publisher","first-page":"51","DOI":"10.3390\/medsci10030051","article-title":"Understanding the polyamine and mTOR pathway interaction in breast cancer cell growth","volume":"10","author":"Akinyele","year":"2022","journal-title":"Med. Sci."},{"key":"2024050912002214900_DMM050639C2","doi-asserted-by":"publisher","first-page":"eaar2606","DOI":"10.1126\/sciadv.aar2606","article-title":"Oil for the cancer engine: the cross-talk between oncogenic signaling and polyamine metabolism","volume":"4","author":"Arruabarrena-Aristorena","year":"2018","journal-title":"Sci. Adv."},{"key":"2024050912002214900_DMM050639C3","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1152\/physiologyonline.2001.16.3.106","article-title":"Polyamines: new cues in cellular signal transduction","volume":"16","author":"Bachrach","year":"2001","journal-title":"News Physiol. Sci."},{"key":"2024050912002214900_DMM050639C4","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1038\/sj.ejhg.5201072","article-title":"X-linked spermine synthase gene (SMS) defect: the first polyamine deficiency syndrome","volume":"11","author":"Cason","year":"2003","journal-title":"Eur. J. Hum. Genet."},{"key":"2024050912002214900_DMM050639C5","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1007\/s12017-015-8377-3","article-title":"Astrocyte-dependent vulnerability to excitotoxicity in spermine oxidase-overexpressing mouse","volume":"18","author":"Cervetto","year":"2016","journal-title":"Neuromolecular Med."},{"key":"2024050912002214900_DMM050639C6","doi-asserted-by":"publisher","first-page":"942","DOI":"10.1016\/j.bbrc.2009.11.169","article-title":"The effect of spermine on the initiation of mitochondrial protein synthesis","volume":"391","author":"Christian","year":"2010","journal-title":"Biochem. Biophys. Res. 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Genet."},{"key":"2024050912002214900_DMM050639C9","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/j.bbabio.2014.10.007","article-title":"Spermine selectively inhibits high-conductance, but not low-conductance calcium-induced permeability transition pore","volume":"2","author":"Elustondo","year":"2015","journal-title":"Biochim. Biophys. Acta Bioenerg"},{"key":"2024050912002214900_DMM050639C10","doi-asserted-by":"publisher","first-page":"2003","DOI":"10.3969\/j.issn.1673-5374.2013.21.009","article-title":"Oxidative stress, mitochondrial damage and neurodegenerative diseases","volume":"8","author":"Guo","year":"2013","journal-title":"Neural Regen. Res."},{"key":"2024050912002214900_DMM050639C11","doi-asserted-by":"publisher","first-page":"11140","DOI":"10.1073\/pnas.95.19.11140","article-title":"The natural polyamine spermine functions directly as a free radical scavenger","volume":"95","author":"Ha","year":"1998","journal-title":"Proc. Natl. Acad. Sci. 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Chem."},{"key":"2024050912002214900_DMM050639C19","doi-asserted-by":"publisher","first-page":"103777","DOI":"10.1016\/j.ejmg.2019.103777","article-title":"The complete loss of function of the SMS gene results in a severe form of Snyder-Robinson syndrome","volume":"63","author":"Larcher","year":"2020","journal-title":"Eur. J. Med. Genet."},{"key":"2024050912002214900_DMM050639C21","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1093\/nar\/gkaa1165","article-title":"Reconstitution of mammalian mitochondrial translation system capable of correct initiation and long polypeptide synthesis from leaderless mRNA","volume":"49","author":"Lee","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"2024050912002214900_DMM050639C22","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s00726-019-02749-8","article-title":"Epileptic seizures and oxidative stress in a mouse model over-expressing spermine oxidase","volume":"52","author":"Leonetti","year":"2020","journal-title":"Amino Acids"},{"key":"2024050912002214900_DMM050639C23","doi-asserted-by":"publisher","first-page":"16970","DOI":"10.1073\/pnas.1011751107","article-title":"Polyamine pathway contributes to the pathogenesis of Parkinson disease","volume":"107","author":"Lewandowski","year":"2010","journal-title":"Proc. Natl. Acad. Sci. 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