{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T04:58:31Z","timestamp":1792213111399,"version":"4.4.0"},"reference-count":39,"publisher":"Oxford University Press (OUP)","issue":"8","license":[{"start":{"date-parts":[[2024,4,20]],"date-time":"2024-04-20T00:00:00Z","timestamp":1713571200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82071430"],"award-info":[{"award-number":["82071430"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82371878"],"award-info":[{"award-number":["82371878"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["92249302"],"award-info":[{"award-number":["92249302"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Shanghai Municipal Natural Science Foundation General Program","award":["22ZR1466400"],"award-info":[{"award-number":["22ZR1466400"]}]},{"DOI":"10.13039\/501100012476","name":"Fundamental Research Funds","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100012476","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Central Universities"},{"name":"Science Innovation 2030 \u2013 Brain Science and Brain-Inspired Intelligence Technology Major Project","award":["#2021ZD0201100"],"award-info":[{"award-number":["#2021ZD0201100"]}]},{"name":"Science Innovation 2030 \u2013 Brain Science and Brain-Inspired Intelligence Technology Major Project","award":["2021ZD0201104"],"award-info":[{"award-number":["2021ZD0201104"]}]},{"DOI":"10.13039\/100007225","name":"Ministry of Science and Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007225","id-type":"DOI","asserted-by":"publisher"}]},{"name":"ALS Society of Canada and Canadian Consortium on Neurodegeneration in Aging"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Amyotrophic lateral sclerosis (ALS) is a severe motor neuron disease with uncertain genetic predisposition in most sporadic cases. The spatial architecture of cell types and gene expression are the basis of cell\u2013cell interactions, biological function and disease pathology, but are not well investigated in the human motor cortex, a key ALS-relevant brain region. Recent studies indicated single nucleus transcriptomic features of motor neuron vulnerability in ALS motor cortex. However, the brain regional vulnerability of ALS-associated genes and the genetic link between region-specific genes and ALS risk remain largely unclear.<\/jats:p>\n               <jats:p>Here, we developed an entropy-weighted differential gene expression matrix-based tool (SpatialE) to identify the spatial enrichment of gene sets in spatial transcriptomics. We benchmarked SpatialE against another enrichment tool (multimodal intersection analysis) using spatial transcriptomics data from both human and mouse brain tissues. To investigate regional vulnerability, we analysed three human motor cortex and two dorsolateral prefrontal cortex tissues for spatial enrichment of ALS-associated genes. We also used Cell2location to estimate the abundance of cell types in ALS-related cortex layers. To dissect the link of regionally expressed genes and ALS risk, we performed burden analyses of rare loss-of-function variants detected by whole-genome sequencing in ALS patients and controls, then analysed differential gene expression in the TargetALS RNA-sequencing dataset.<\/jats:p>\n               <jats:p>SpatialE showed more accurate and specific spatial enrichment of regional cell type markers than multimodal intersection analysis in both mouse brain and human dorsolateral prefrontal cortex. Spatial transcriptomic analyses of human motor cortex showed heterogeneous cell types and spatial gene expression profiles. We found that 260 manually curated ALS-associated genes are significantly enriched in layer 5 of the motor cortex, with abundant expression of upper motor neurons and layer 5 excitatory neurons. Burden analyses of rare loss-of-function variants in Layer 5-associated genes nominated NOMO1 as a novel ALS-associated gene in a combined sample set of 6814 ALS patients and 3324 controls (P = 0.029). Gene expression analyses in CNS tissues revealed downregulation of NOMO1 in ALS, which is consistent with a loss-of-function disease mechanism. In conclusion, our integrated spatial transcriptomics and genomic analyses identified regional brain vulnerability in ALS and the association of a layer 5 gene (NOMO1) with ALS risk.<\/jats:p>","DOI":"10.1093\/brain\/awae123","type":"journal-article","created":{"date-parts":[[2024,4,21]],"date-time":"2024-04-21T01:13:50Z","timestamp":1713662030000},"page":"2826-2841","source":"Crossref","is-referenced-by-count":10,"title":["Spatial enrichment and genomic analyses reveal the link of <i>NOMO1<\/i> with amyotrophic lateral sclerosis"],"prefix":"10.1093","volume":"147","author":[{"given":"Jingyan","family":"Guo","sequence":"first","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2569-0269","authenticated-orcid":false,"given":"Linya","family":"You","sequence":"additional","affiliation":[{"name":"Department of Human Anatomy and Histoembryology, School of Basic Medical Sciences, Fudan University , 200032, Shanghai , China"},{"name":"Key Laboratory of Medical Computing and Computer Assisted Intervention of Shanghai , 200032, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Zhou","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiali","family":"Hu","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahao","family":"Li","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanli","family":"Yang","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuelin","family":"Tang","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"},{"name":"Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto , Toronto, ON M5T 0S8 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3073-6444","authenticated-orcid":false,"given":"Yimin","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Neurology and National Center for Neurological Disorders, Huashan Hospital, Fudan University , 200040, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuqi","family":"Gu","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Dong","sequence":"additional","affiliation":[{"name":"Department of Neurology and National Center for Neurological Disorders, Huashan Hospital, Fudan University , 200040, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Neurology and National Center for Neurological Disorders, Huashan Hospital, Fudan University , 200040, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Sato","sequence":"additional","affiliation":[{"name":"Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto , Toronto, ON M5T 0S8 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lorne","family":"Zinman","sequence":"additional","affiliation":[{"name":"Sunnybrook Health Sciences Centre , Toronto, ON M4N 3M5 , Canada"},{"name":"Division of Neurology, University of Toronto , Toronto, ON M5S 3H2 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ekaterina","family":"Rogaeva","sequence":"additional","affiliation":[{"name":"Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto , Toronto, ON M5T 0S8 , Canada"},{"name":"Division of Neurology, University of Toronto , Toronto, ON M5S 3H2 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2748-395X","authenticated-orcid":false,"given":"Jian","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neurology and National Center for Neurological Disorders, Huashan Hospital, Fudan University , 200040, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Neurology and National Center for Neurological Disorders, Huashan Hospital, Fudan University , 200040, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4491-8927","authenticated-orcid":false,"given":"Ming","family":"Zhang","sequence":"additional","affiliation":[{"name":"The First Rehabilitation Hospital of Shanghai, Department of Medical Genetics, School of Medicine, Tongji University , 200090, Shanghai , China"},{"name":"State Key Laboratory of Cardiology and Medical Innovation Center, Shanghai East Hospital, School of Medicine, Tongji University , 200120, Shanghai , China"},{"name":"Clinical Center for Brain and Spinal Cord Research, School of Medicine, Tongji University , 200331, Shanghai , China"},{"name":"Institute for Advanced Study, Tongji University , 200092, Shanghai , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,4,20]]},"reference":[{"key":"2024080113035736100_awae123-B1","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":"2024080113035736100_awae123-B2","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1056\/NEJMra1603471","article-title":"Amyotrophic lateral 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