{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T00:08:24Z","timestamp":1792800504323,"version":"4.5.0"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,10,30]],"date-time":"2019-10-30T00:00:00Z","timestamp":1572393600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,10,30]],"date-time":"2019-10-30T00:00:00Z","timestamp":1572393600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["NIH\/NINDS R01NS086810"],"award-info":[{"award-number":["NIH\/NINDS R01NS086810"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["NIH\/NINDS R01NS099280"],"award-info":[{"award-number":["NIH\/NINDS R01NS099280"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100002243","name":"National Ataxia Foundation","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/100002243","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["acta neuropathol commun"],"published-print":{"date-parts":[[2019,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    CGG repeat expansions in\n                    <jats:italic>FMR1<\/jats:italic>\n                    cause the neurodegenerative disorder Fragile X-associated Tremor\/Ataxia Syndrome (FXTAS). Ubiquitinated neuronal intranuclear inclusions (NIIs) are the neuropathological hallmark of FXTAS. Both sense strand derived CGG repeats and antisense strand derived CCG repeats support non-AUG initiated (RAN) translation of homopolymeric proteins in potentially 6 different reading frames. However, the relative abundance of these proteins in FXTAS brains and their co-localization with each other and NIIs is lacking. Here we describe rater-blinded assessment of immunohistochemical and immunofluorescence staining with newly generated antibodies to different CGG RAN translation products in FXTAS and control brains as well as co-staining with ubiquitin, p62\/SQSTM1, and ubiquilin 2. We find that both FMRpolyG and a second CGG repeat derived RAN translation product, FMRpolyA, accumulate in aggregates in FXTAS brains. FMRpolyG is a near-obligate component of both ubiquitin-positive and p62-positive NIIs in FXTAS, with occurrence of aggregates in 20% of all hippocampal neurons and\u2009&gt;\u200990% of all inclusions. A subset of these inclusions also stain positive for the ALS\/FTD associated protein ubiquilin 2. Ubiquitinated inclusions and FMRpolyG+ aggregates are rarer in cortex and cerebellum. Intriguingly, FMRpolyG staining is also visible in control neuronal nuclei. In contrast to FMRpolyG, staining for FMRpolyA and CCG antisense derived RAN translation products were less abundant and less frequent components of ubiquitinated inclusions. In conclusion, RAN translated FMRpolyG is a common component of ubiquitin and p62 positive inclusions in FXTAS patient brains.\n                  <\/jats:p>","DOI":"10.1186\/s40478-019-0782-7","type":"journal-article","created":{"date-parts":[[2019,10,30]],"date-time":"2019-10-30T16:44:07Z","timestamp":1572453847000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":51,"title":["Neuropathology of RAN translation proteins in fragile X-associated tremor\/ataxia syndrome"],"prefix":"10.1186","volume":"7","author":[{"given":"Amy","family":"Krans","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Geena","family":"Skariah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bryana","family":"Bayly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4781-6376","authenticated-orcid":false,"given":"Peter K.","family":"Todd","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,10,30]]},"reference":[{"key":"782_CR1","first-page":"105","volume-title":"Handbook of clinical neurology","author":"H Paulson","year":"2018","unstructured":"Paulson H (2018) Chapter 9 - repeat expansion diseases. In: Geschwind DH, Paulson HL, Klein C (eds) Handbook of clinical neurology. Elsevier, City, pp 105\u2013123"},{"key":"782_CR2","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1016\/j.neuron.2013.02.022","volume":"77","author":"DL Nelson","year":"2013","unstructured":"Nelson DL, Orr HT, Warren ST (2013) The unstable repeats--three evolving faces of neurological disease. Neuron 77:825\u2013843. \n                    https:\/\/doi.org\/10.1016\/j.neuron.2013.02.022","journal-title":"Neuron"},{"key":"782_CR3","doi-asserted-by":"publisher","unstructured":"Nguyen L, Cleary JD, Ranum LPW (2019) Repeat-associated non-ATG translation: molecular mechanisms and contribution to neurological disease. Ann Rev Neurosci. \n                    https:\/\/doi.org\/10.1146\/annurev-neuro-070918-050405","DOI":"10.1146\/annurev-neuro-070918-050405"},{"key":"782_CR4","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1111\/nyas.12693","volume":"1338","author":"PJ Hagerman","year":"2015","unstructured":"Hagerman PJ, Hagerman RJ (2015) Fragile X-associated tremor\/ataxia syndrome. Ann N Y Acad Sci 1338:58\u201370. \n                    https:\/\/doi.org\/10.1111\/nyas.12693","journal-title":"Ann N Y Acad Sci"},{"key":"782_CR5","doi-asserted-by":"publisher","first-page":"2018","DOI":"10.1002\/mds.21493","volume":"22","author":"E Berry-Kravis","year":"2007","unstructured":"Berry-Kravis E, Abrams L, Coffey SM, Hall DA, Greco C, Gane LW, Grigsby J, Bourgeois JA, Finucane B, Jacquemont S et al (2007) Fragile X-associated tremor\/ataxia syndrome: clinical features, genetics, and testing guidelines. Mov Disord 22:2018\u20132030, quiz 2140. \n                    https:\/\/doi.org\/10.1002\/mds.21493","journal-title":"Mov Disord"},{"key":"782_CR6","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1086\/302720","volume":"66","author":"F Tassone","year":"2000","unstructured":"Tassone F, Hagerman RJ, Taylor AK, Gane LW, Godfrey TE, Hagerman PJ (2000) Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am J Hum Genet 66:6\u201315. \n                    https:\/\/doi.org\/10.1086\/302720","journal-title":"Am J Hum Genet"},{"key":"782_CR7","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1002\/(SICI)1096-8628(20000313)91:2<144::AID-AJMG14>3.0.CO;2-V","volume":"91","author":"F Tassone","year":"2000","unstructured":"Tassone F, Hagerman RJ, Taylor AK, Mills JB, Harris SW, Gane LW, Hagerman PJ (2000) Clinical involvement and protein expression in individuals with the FMR1 premutation. Am J Med Genet 91:144\u2013152","journal-title":"Am J Med Genet"},{"key":"782_CR8","doi-asserted-by":"publisher","first-page":"1760","DOI":"10.1093\/brain\/awf184","volume":"125","author":"CM Greco","year":"2002","unstructured":"Greco CM, Hagerman RJ, Tassone F, Chudley AE, Del Bigio MR, Jacquemont S, Leehey M, Hagerman PJ (2002) Neuronal intranuclear inclusions in a new cerebellar tremor\/ataxia syndrome among fragile X carriers. Brain 125:1760\u20131771","journal-title":"Brain"},{"key":"782_CR9","doi-asserted-by":"publisher","first-page":"e43","DOI":"10.1136\/jmg.2003.012518","volume":"41","author":"F Tassone","year":"2004","unstructured":"Tassone F, Hagerman RJ, Garcia-Arocena D, Khandjian EW, Greco CM, Hagerman PJ (2004) Intranuclear inclusions in neural cells with premutation alleles in fragile X associated tremor\/ataxia syndrome. J Med Genet 41:e43","journal-title":"J Med Genet"},{"key":"782_CR10","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1093\/brain\/awh683","volume":"129","author":"CM Greco","year":"2006","unstructured":"Greco CM, Berman RF, Martin RM, Tassone F, Schwartz PH, Chang A, Trapp BD, Iwahashi C, Brunberg J, Grigsby J et al (2006) Neuropathology of fragile X-associated tremor\/ataxia syndrome (FXTAS). Brain 129:243\u2013255. \n                    https:\/\/doi.org\/10.1093\/brain\/awh683","journal-title":"Brain"},{"key":"782_CR11","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1007\/s12311-016-0776-y","volume":"15","author":"J Ariza","year":"2016","unstructured":"Ariza J, Rogers H, Monterrubio A, Reyes-Miranda A, Hagerman PJ, Martinez-Cerdeno V (2016) A majority of FXTAS cases present with Intranuclear inclusions within Purkinje cells. Cerebellum 15:546\u2013551. \n                    https:\/\/doi.org\/10.1007\/s12311-016-0776-y","journal-title":"Cerebellum"},{"key":"782_CR12","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1093\/brain\/awh650","volume":"129","author":"CK Iwahashi","year":"2006","unstructured":"Iwahashi CK, Yasui DH, An HJ, Greco CM, Tassone F, Nannen K, Babineau B, Lebrilla CB, Hagerman RJ, Hagerman PJ (2006) Protein composition of the intranuclear inclusions of FXTAS. Brain 129:256\u2013271. \n                    https:\/\/doi.org\/10.1093\/brain\/awh650","journal-title":"Brain"},{"key":"782_CR13","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1016\/j.neuron.2007.07.020","volume":"55","author":"P Jin","year":"2007","unstructured":"Jin P, Duan R, Qurashi A, Qin Y, Tian D, Rosser TC, Liu H, Feng Y, Warren ST (2007) Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor\/ataxia syndrome. Neuron 55:556\u2013564. \n                    https:\/\/doi.org\/10.1016\/j.neuron.2007.07.020","journal-title":"Neuron"},{"key":"782_CR14","doi-asserted-by":"publisher","first-page":"1248","DOI":"10.1038\/emboj.2010.21","volume":"29","author":"C Sellier","year":"2010","unstructured":"Sellier C, Rau F, Liu Y, Tassone F, Hukema RK, Gattoni R, Schneider A, Richard S, Willemsen R, Elliott DJ et al (2010) Sam68 sequestration and partial loss of function are associated with splicing alterations in FXTAS patients. EMBO J 29:1248\u20131261. \n                    https:\/\/doi.org\/10.1038\/emboj.2010.21","journal-title":"EMBO J"},{"key":"782_CR15","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1016\/j.neuron.2007.07.021","volume":"55","author":"OA Sofola","year":"2007","unstructured":"Sofola OA, Jin P, Qin Y, Duan R, Liu H, de Haro M, Nelson DL, Botas J (2007) RNA-binding proteins hnRNP A2\/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 55:565\u2013571. \n                    https:\/\/doi.org\/10.1016\/j.neuron.2007.07.021","journal-title":"Neuron"},{"key":"782_CR16","doi-asserted-by":"publisher","first-page":"103","DOI":"10.4161\/rna.1.2.1035","volume":"1","author":"F Tassone","year":"2004","unstructured":"Tassone F, Iwahashi C, Hagerman PJ (2004) FMR1 RNA within the intranuclear inclusions of fragile X-associated tremor\/ataxia syndrome (FXTAS). RNA Biol 1:103\u2013105","journal-title":"RNA Biol"},{"key":"782_CR17","doi-asserted-by":"publisher","first-page":"869","DOI":"10.1016\/j.celrep.2013.02.004","volume":"3","author":"C Sellier","year":"2013","unstructured":"Sellier C, Freyermuth F, Tabet R, Tran T, He F, Ruffenach F, Alunni V, Moine H, Thibault C, Page A et al (2013) Sequestration of DROSHA and DGCR8 by expanded CGG RNA repeats alters microRNA processing in fragile X-associated tremor\/ataxia syndrome. Cell Rep 3:869\u2013880. \n                    https:\/\/doi.org\/10.1016\/j.celrep.2013.02.004","journal-title":"Cell Rep"},{"key":"782_CR18","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1097\/NEN.0b013e31821d3194","volume":"70","author":"MR Hunsaker","year":"2011","unstructured":"Hunsaker MR, Greco CM, Tassone F, Berman RF, Willemsen R, Hagerman RJ, Hagerman PJ (2011) Rare intranuclear inclusions in the brains of 3 older adult males with fragile x syndrome: implications for the spectrum of fragile x-associated disorders. J Neuropathol Exp Neurol 70:462\u2013469. \n                    https:\/\/doi.org\/10.1097\/NEN.0b013e31821d3194","journal-title":"J Neuropathol Exp Neurol"},{"key":"782_CR19","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1016\/S0896-6273(03)00533-6","volume":"39","author":"P Jin","year":"2003","unstructured":"Jin P, Zarnescu DC, Zhang F, Pearson CE, Lucchesi JC, Moses K, Warren ST (2003) RNA-mediated neurodegeneration caused by the fragile X premutation rCGG repeats in Drosophila. Neuron 39:739\u2013747","journal-title":"Neuron"},{"key":"782_CR20","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.brainres.2018.02.006","volume":"1693","author":"MR Glineburg","year":"2018","unstructured":"Glineburg MR, Todd PK, Charlet-Berguerand N, Sellier C (2018) Repeat-associated non-AUG (RAN) translation and other molecular mechanisms in fragile X tremor Ataxia syndrome. Brain Res 1693:43\u201354. \n                    https:\/\/doi.org\/10.1016\/j.brainres.2018.02.006","journal-title":"Brain Res"},{"key":"782_CR21","doi-asserted-by":"publisher","first-page":"2133","DOI":"10.1093\/hmg\/ddx108","volume":"26","author":"H Castro","year":"2017","unstructured":"Castro H, Kul E, Buijsen RAM, Severijnen L, Willemsen R, Hukema RK, Stork O, Santos M (2017) Selective rescue of heightened anxiety but not gait ataxia in a premutation 90CGG mouse model of fragile X-associated tremor\/ataxia syndrome. Hum Mol Genet 26:2133\u20132145. \n                    https:\/\/doi.org\/10.1093\/hmg\/ddx108","journal-title":"Hum Mol Genet"},{"key":"782_CR22","doi-asserted-by":"publisher","first-page":"4948","DOI":"10.1093\/hmg\/ddv216","volume":"24","author":"RK Hukema","year":"2015","unstructured":"Hukema RK, Buijsen RA, Schonewille M, Raske C, Severijnen LA, Nieuwenhuizen-Bakker I, Verhagen RF, van Dessel L, Maas A, Charlet-Berguerand N et al (2015) Reversibility of neuropathology and motor deficits in an inducible mouse model for FXTAS. Hum Mol Genet 24:4948\u20134957. \n                    https:\/\/doi.org\/10.1093\/hmg\/ddv216","journal-title":"Hum Mol Genet"},{"key":"782_CR23","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1016\/j.molcel.2016.02.034","volume":"62","author":"MG Kearse","year":"2016","unstructured":"Kearse MG, Green KM, Krans A, Rodriguez CM, Linsalata AE, Goldstrohm AC, Todd PK (2016) CGG repeat-associated non-AUG translation utilizes a cap-dependent scanning mechanism of initiation to produce toxic proteins. Mol Cell 62:314\u2013322. \n                    https:\/\/doi.org\/10.1016\/j.molcel.2016.02.034","journal-title":"Mol Cell"},{"key":"782_CR24","doi-asserted-by":"publisher","first-page":"4317","DOI":"10.1093\/hmg\/ddv165","volume":"24","author":"SY Oh","year":"2015","unstructured":"Oh SY, He F, Krans A, Frazer M, Taylor JP, Paulson HL, Todd PK (2015) RAN translation at CGG repeats induces ubiquitin proteasome system impairment in models of fragile X-associated tremor ataxia syndrome. Hum Mol Genet 24:4317\u20134326. \n                    https:\/\/doi.org\/10.1093\/hmg\/ddv165","journal-title":"Hum Mol Genet"},{"key":"782_CR25","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/j.neuron.2016.12.016","volume":"93","author":"C Sellier","year":"2017","unstructured":"Sellier C, Buijsen RA, He F, Natla S, Jung L, Tropel P, Gaucherot A, Jacobs H, Meziane H, Vincent A et al (2017) Translation of expanded CGG repeats into FMRpolyG is pathogenic and may contribute to fragile X tremor Ataxia syndrome. Neuron 93:331\u2013347. \n                    https:\/\/doi.org\/10.1016\/j.neuron.2016.12.016","journal-title":"Neuron"},{"key":"782_CR26","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1016\/j.neuron.2013.03.026","volume":"78","author":"PK Todd","year":"2013","unstructured":"Todd PK, Oh SY, Krans A, He F, Sellier C, Frazer M, Renoux AJ, Chen KC, Scaglione KM, Basrur V et al (2013) CGG repeat-associated translation mediates neurodegeneration in fragile X tremor ataxia syndrome. Neuron 78:440\u2013455. \n                    https:\/\/doi.org\/10.1016\/j.neuron.2013.03.026","journal-title":"Neuron"},{"key":"782_CR27","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1002\/ana.24800","volume":"80","author":"A Krans","year":"2016","unstructured":"Krans A, Kearse MG, Todd PK (2016) Repeat-associated non-AUG translation from antisense CCG repeats in fragile X tremor\/ataxia syndrome. Ann Neurol 80:871\u2013881. \n                    https:\/\/doi.org\/10.1002\/ana.24800","journal-title":"Ann Neurol"},{"key":"782_CR28","doi-asserted-by":"publisher","first-page":"249","DOI":"10.3389\/fgene.2019.00249","volume":"10","author":"G Hoem","year":"2019","unstructured":"Hoem G, Bowitz Larsen K, Overvatn A, Brech A, Lamark T, Sjottem E, Johansen T (2019) The FMRpolyGlycine protein mediates aggregate formation and toxicity independent of the CGG mRNA hairpin in a cellular model for FXTAS. 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Acta Neuropathol Commun 2:162. \n                    https:\/\/doi.org\/10.1186\/s40478-014-0162-2","journal-title":"Acta Neuropathol Commun"},{"key":"782_CR30","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1093\/humrep\/dev280","volume":"31","author":"RA Buijsen","year":"2016","unstructured":"Buijsen RA, Visser JA, Kramer P, Severijnen EA, Gearing M, Charlet-Berguerand N, Sherman SL, Berman RF, Willemsen R, Hukema RK (2016) Presence of inclusions positive for polyglycine containing protein, FMRpolyG, indicates that repeat-associated non-AUG translation plays a role in fragile X-associated primary ovarian insufficiency. 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Acta Neuropathol 127:347\u2013357. \n                    https:\/\/doi.org\/10.1007\/s00401-013-1232-4","journal-title":"Acta Neuropathol"}],"container-title":["Acta Neuropathologica Communications"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s40478-019-0782-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s40478-019-0782-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s40478-019-0782-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,10,28]],"date-time":"2020-10-28T20:32:25Z","timestamp":1603917145000},"score":1,"resource":{"primary":{"URL":"https:\/\/actaneurocomms.biomedcentral.com\/articles\/10.1186\/s40478-019-0782-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,30]]},"references-count":34,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["782"],"URL":"https:\/\/doi.org\/10.1186\/s40478-019-0782-7","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/672444","asserted-by":"object"}]},"ISSN":["2051-5960"],"issn-type":[{"value":"2051-5960","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,30]]},"assertion":[{"value":"14 June 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 July 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 October 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"152"}}