{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T21:22:22Z","timestamp":1790716942580,"version":"4.1.0"},"reference-count":32,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2020,3,23]],"date-time":"2020-03-23T00:00:00Z","timestamp":1584921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"Brain Protein Aging and Dementia Control","award":["26117004"],"award-info":[{"award-number":["26117004"]}]},{"name":"Mext KAKENHI","award":["15K09310"],"award-info":[{"award-number":["15K09310"]}]},{"name":"Integrated Research on Neuropsychiatric Disorders"},{"name":"Integrated Research on Depression, Dementia and Development Disorders"},{"name":"Strategic Research Program for Brain Sciences"},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Practical Research Project for Rare\/Intractable Diseases","award":["JP18ek0109320"],"award-info":[{"award-number":["JP18ek0109320"]}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,4,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Alterations of RNA metabolism caused by mutations in RNA-binding protein genes, such as transactivating DNA-binding protein-43 (TDP-43) and fused in sarcoma (FUS), have been implicated in the pathogenesis of amyotrophic lateral sclerosis (ALS). Unlike the accumulation of TDP43, which is accepted as a pathological hall mark of sporadic ALS (sALS), FUS pathology in sALS is still under debate. Although immunoreactive inclusions of FUS have been detected in sALS patients previously, the technical limitation of signal detection, including the necessity of specific antigen retrieval, restricts our understanding of FUS-associated ALS pathology. In this study, we applied a novel detection method using a conventional antigen retrieval technique with Sudan Black B treatment to identify FUS-positive inclusions in sALS patients. We classified pathological motor neurons into 5 different categories according to the different aggregation characteristics of FUS and TDP-43. Although the granular type was more dominant for inclusions with TDP-43, the skein-like type was more often observed in FUS-positive inclusions, suggesting that these 2 proteins undergo independent aggregation processes. Moreover, neurons harboring FUS-positive inclusions demonstrated substantially reduced expression levels of dynactin-1, a retrograde motor protein, indicating that perturbation of nucleocytoplasmic transport is associated with the formation of cytoplasmic inclusions of FUS in sALS.<\/jats:p>","DOI":"10.1093\/jnen\/nlaa003","type":"journal-article","created":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T14:15:34Z","timestamp":1583504134000},"page":"370-377","source":"Crossref","is-referenced-by-count":40,"title":["Characteristic Features of FUS Inclusions in Spinal Motor Neurons of Sporadic Amyotrophic Lateral Sclerosis"],"prefix":"10.1093","volume":"79","author":[{"given":"Kensuke","family":"Ikenaka","sequence":"first","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"},{"name":"Department of Neurology, Osaka University Graduate School of Medicine , Suita, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shinsuke","family":"Ishigaki","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"},{"name":"Research Division of Dementia and Neurodegenerative Disease, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yohei","family":"Iguchi","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kaori","family":"Kawai","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yusuke","family":"Fujioka","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Yokoi","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rehab F","family":"Abdelhamid","sequence":"additional","affiliation":[{"name":"Department of Neurology, Osaka University Graduate School of Medicine , Suita, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seiichi","family":"Nagano","sequence":"additional","affiliation":[{"name":"Department of Neurology, Osaka University Graduate School of Medicine , Suita, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hideki","family":"Mochizuki","sequence":"additional","affiliation":[{"name":"Department of Neurology, Osaka University Graduate School of Medicine , Suita, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masahisa","family":"Katsuno","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gen","family":"Sobue","sequence":"additional","affiliation":[{"name":"Department of Neurology, Nagoya University Graduate School of Medicine , Nagoya, Japan"},{"name":"Research Division of Dementia and Neurodegenerative Disease, Nagoya University Graduate School of Medicine , Nagoya, Japan"},{"name":"Aichi Medical University , Aichi, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,3,23]]},"reference":[{"key":"2024032523313698000_nlaa003-B1","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1016\/j.bbrc.2006.10.093","article-title":"TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis","volume":"351","author":"Arai","year":"2006","journal-title":"Biochem Biophys Res Commun"},{"key":"2024032523313698000_nlaa003-B2","doi-asserted-by":"crossref","first-page":"1668","DOI":"10.1126\/science.1154584","article-title":"TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis","volume":"319","author":"Sreedharan","year":"2008","journal-title":"Science"},{"key":"2024032523313698000_nlaa003-B3","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1111\/j.1440-1789.2009.01029.x","article-title":"TDP-43 is consistently co-localized with ubiquitinated inclusions in sporadic and Guam amyotrophic lateral sclerosis but not in familial amyotrophic lateral sclerosis with and without SOD1 mutations","volume":"29","author":"Maekawa","year":"2009","journal-title":"Neuropathology"},{"key":"2024032523313698000_nlaa003-B4","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1038\/ng.132","article-title":"TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis","volume":"40","author":"Kabashi","year":"2008","journal-title":"Nat Genet"},{"key":"2024032523313698000_nlaa003-B5","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1126\/science.1134108","article-title":"Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis","volume":"314","author":"Neumann","year":"2006","journal-title":"Science"},{"key":"2024032523313698000_nlaa003-B6","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1126\/science.1165942","article-title":"Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6","volume":"323","author":"Vance","year":"2009","journal-title":"Science"},{"key":"2024032523313698000_nlaa003-B7","doi-asserted-by":"crossref","first-page":"2922","DOI":"10.1093\/brain\/awp214","article-title":"A new subtype of frontotemporal lobar degeneration with FUS pathology","volume":"132","author":"Neumann","year":"2009","journal-title":"Brain"},{"key":"2024032523313698000_nlaa003-B8","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1007\/s00401-009-0581-5","article-title":"Abundant FUS-immunoreactive pathology in neuronal intermediate filament inclusion disease","volume":"118","author":"Neumann","year":"2009","journal-title":"Acta Neuropathol"},{"key":"2024032523313698000_nlaa003-B9","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1002\/ana.22051","article-title":"FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis","volume":"67","author":"Deng","year":"2010","journal-title":"Ann Neurol"},{"key":"2024032523313698000_nlaa003-B10","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1038\/s41591-018-0140-5","article-title":"Modeling sporadic ALS in iPSC-derived motor neurons identifies a potential therapeutic agent","volume":"24","author":"Fujimori","year":"2018","journal-title":"Nat Med"},{"key":"2024032523313698000_nlaa003-B11","doi-asserted-by":"crossref","first-page":"2572","DOI":"10.1093\/brain\/awz217","article-title":"Widespread FUS mislocalization is a molecular hallmark of amyotrophic lateral sclerosis","volume":"142","author":"Tyzack","year":"2019","journal-title":"Brain"},{"key":"2024032523313698000_nlaa003-B12","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1111\/j.1365-2990.2012.01274.x","article-title":"Nuclear carrier and RNA-binding proteins in frontotemporal lobar degeneration associated with fused in sarcoma (FUS) pathological changes","volume":"39","author":"Davidson","year":"2013","journal-title":"Neuropathol Appl Neurobiol"},{"key":"2024032523313698000_nlaa003-B13","doi-asserted-by":"crossref","first-page":"2235.e11","DOI":"10.1016\/j.neurobiolaging.2013.04.004","article-title":"Mutations in protein N-arginine methyltransferases are not the cause of FTLD-FUS","volume":"34","author":"Ravenscroft","year":"2013","journal-title":"Neurobiol Aging"},{"key":"2024032523313698000_nlaa003-B14","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1186\/1750-1326-7-53","article-title":"Expression of fused in sarcoma mutations in mice recapitulates the neuropathology of FUS proteinopathies and provides insight into disease pathogenesis","volume":"7","author":"Verbeeck","year":"2012","journal-title":"Mol Neurodegener"},{"key":"2024032523313698000_nlaa003-B15","doi-asserted-by":"crossref","first-page":"e47056","DOI":"10.1371\/journal.pone.0047056","article-title":"FUS-NLS\/Transportin 1 complex structure provides insights into the nuclear targeting mechanism of FUS and the implications in ALS","volume":"7","author":"Niu","year":"2012","journal-title":"PLoS One"},{"key":"2024032523313698000_nlaa003-B16","doi-asserted-by":"crossref","first-page":"2676","DOI":"10.1093\/hmg\/ddt117","article-title":"ALS mutant FUS disrupts nuclear localization and sequesters wild-type FUS within cytoplasmic stress granules","volume":"22","author":"Vance","year":"2013","journal-title":"Hum Mol Genet"},{"key":"2024032523313698000_nlaa003-B17","doi-asserted-by":"crossref","first-page":"e1868","DOI":"10.1212\/WNL.0000000000007311","article-title":"Increase of arginine dimethylation correlates with the progression and prognosis of ALS","volume":"92","author":"Ikenaka","year":"2019","journal-title":"Neurology"},{"key":"2024032523313698000_nlaa003-B18","doi-asserted-by":"crossref","first-page":"e54511","DOI":"10.1371\/journal.pone.0054511","article-title":"dnc-1\/dynactin 1 knockdown disrupts transport of autophagosomes and induces motor neuron degeneration","volume":"8","author":"Ikenaka","year":"2013","journal-title":"PLoS One"},{"key":"2024032523313698000_nlaa003-B19","first-page":"519","article-title":"Comparison of heat induced antigen retrieval techniques for immune-histochemical estrogen receptor expression in ductal carcinoma of breast in females","volume":"20","author":"Qadir","year":"2010","journal-title":"J Coll Physicians Surg Pak"},{"key":"2024032523313698000_nlaa003-B20","doi-asserted-by":"crossref","first-page":"1565","DOI":"10.1177\/002215540104901210","article-title":"Control of autofluorescence of archival formaldehyde-fixed, paraffin-embedded tissue in confocal laser scanning microscopy (CLSM)","volume":"49","author":"Baschong","year":"2001","journal-title":"J Histochem Cytochem"},{"key":"2024032523313698000_nlaa003-B21","doi-asserted-by":"crossref","first-page":"S204","DOI":"10.1016\/j.neuroimage.2010.06.020","article-title":"Identification of amyloid plaques in retinas from Alzheimer\u2019s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model","volume":"54","author":"Koronyo-Hamaoui","year":"2011","journal-title":"NeuroImage"},{"key":"2024032523313698000_nlaa003-B22","doi-asserted-by":"crossref","first-page":"227","DOI":"10.2353\/ajpath.2007.070182","article-title":"TDP-43 in familial and sporadic frontotemporal lobar degeneration with ubiquitin inclusions","volume":"171","author":"Cairns","year":"2007","journal-title":"Am J Pathol"},{"key":"2024032523313698000_nlaa003-B23","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1007\/s00401-006-0189-y","article-title":"Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43","volume":"113","author":"Davidson","year":"2007","journal-title":"Acta Neuropathol"},{"key":"2024032523313698000_nlaa003-B24","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.jns.2007.12.016","article-title":"Anterior horn cells with abnormal TDP-43 immunoreactivities show fragmentation of the Golgi apparatus in ALS","volume":"269","author":"Fujita","year":"2008","journal-title":"J Neurol Sci"},{"key":"2024032523313698000_nlaa003-B25","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/s00401-008-0396-9","article-title":"Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia","volume":"116","author":"Mori","year":"2008","journal-title":"Acta Neuropathol"},{"key":"2024032523313698000_nlaa003-B26","doi-asserted-by":"crossref","first-page":"2899","DOI":"10.1016\/j.febslet.2008.07.027","article-title":"Abnormal phosphorylation of Ser409\/410 of TDP-43 in FTLD-U and ALS","volume":"582","author":"Inukai","year":"2008","journal-title":"FEBS Lett"},{"key":"2024032523313698000_nlaa003-B27","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1002\/ana.20379","article-title":"Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis","volume":"57","author":"Jiang","year":"2005","journal-title":"Ann Neurol"},{"key":"2024032523313698000_nlaa003-B28","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1097\/nen.0b013e318093ece3","article-title":"Gene expressions specifically detected in motor neurons (dynactin 1, early growth response 3, acetyl-CoA transporter, death receptor 5, and cyclin C) differentially correlate to pathologic markers in sporadic amyotrophic lateral sclerosis","volume":"66","author":"Jiang","year":"2007","journal-title":"J Neuropathol Exp Neurol"},{"key":"2024032523313698000_nlaa003-B29","doi-asserted-by":"crossref","first-page":"532","DOI":"10.3389\/fnins.2019.00532","article-title":"Motor neuron susceptibility in ALS\/FTD","volume":"13","author":"Ragagnin","year":"2019","journal-title":"Front Neurosci"},{"key":"2024032523313698000_nlaa003-B30","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1083\/jcb.115.6.1639","article-title":"Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein","volume":"115","author":"Gill","year":"1991","journal-title":"J Cell Biol"},{"key":"2024032523313698000_nlaa003-B31","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1016\/j.neuron.2010.09.039","article-title":"Molecular motors in neurons: Transport mechanisms and roles in brain function, development, and disease","volume":"68","author":"Hirokawa","year":"2010","journal-title":"Neuron"},{"key":"2024032523313698000_nlaa003-B32","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/ng1123","article-title":"Mutant dynactin in motor neuron disease","volume":"33","author":"Puls","year":"2003","journal-title":"Nat Genet"}],"container-title":["Journal of Neuropathology &amp; Experimental Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/79\/4\/370\/32963331\/nlaa003.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/79\/4\/370\/32963331\/nlaa003.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,25]],"date-time":"2024-03-25T23:45:47Z","timestamp":1711410347000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jnen\/article\/79\/4\/370\/5788520"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,23]]},"references-count":32,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,3,23]]},"published-print":{"date-parts":[[2020,4,1]]}},"URL":"https:\/\/doi.org\/10.1093\/jnen\/nlaa003","relation":{},"ISSN":["0022-3069","1554-6578"],"issn-type":[{"value":"0022-3069","type":"print"},{"value":"1554-6578","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,4]]},"published":{"date-parts":[[2020,3,23]]}}}