Cellular architecture of evolving neuroinflammatory lesions and multiple sclerosis pathology
Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by model...
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| Published in | Cell Vol. 187; no. 8; pp. 1990 - 2009.e19 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Inc
11.04.2024
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| Abstract | Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single-cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease-associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single-cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub-compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single-cell resolution, our study unveils the intricate cellular dynamics underlying MS.
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•ISS elucidates cellular dynamics of EAE model and architecture of human MS lesions•Active EAE lesions propagate in a centrifugal manner•EAE DA-glia are induced independently of lesions and dynamically resolved•Spatial preferences of glial states drive MS lesion compartmentalization
Spatial mapping of mouse and human multiple sclerosis neuropathology at a single-cell resolution unveils the cellular architecture and dynamics underlying disease evolution. |
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| AbstractList | Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single-cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease-associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single-cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub-compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single-cell resolution, our study unveils the intricate cellular dynamics underlying MS.Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single-cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease-associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single-cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub-compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single-cell resolution, our study unveils the intricate cellular dynamics underlying MS. Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single-cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease-associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single-cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub-compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single-cell resolution, our study unveils the intricate cellular dynamics underlying MS. Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single -cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single -cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease -associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single -cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub -compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single -cell resolution, our study unveils the intricate cellular dynamics underlying MS. Multiple sclerosis (MS) is a neurological disease characterized by multifocal lesions and smoldering pathology. Although single-cell analyses provided insights into cytopathology, evolving cellular processes underlying MS remain poorly understood. We investigated the cellular dynamics of MS by modeling temporal and regional rates of disease progression in mouse experimental autoimmune encephalomyelitis (EAE). By performing single-cell spatial expression profiling using in situ sequencing (ISS), we annotated disease neighborhoods and found centrifugal evolution of active lesions. We demonstrated that disease-associated (DA)-glia arise independently of lesions and are dynamically induced and resolved over the disease course. Single-cell spatial mapping of human archival MS spinal cords confirmed the differential distribution of homeostatic and DA-glia, enabled deconvolution of active and inactive lesions into sub-compartments, and identified new lesion areas. By establishing a spatial resource of mouse and human MS neuropathology at a single-cell resolution, our study unveils the intricate cellular dynamics underlying MS. [Display omitted] •ISS elucidates cellular dynamics of EAE model and architecture of human MS lesions•Active EAE lesions propagate in a centrifugal manner•EAE DA-glia are induced independently of lesions and dynamically resolved•Spatial preferences of glial states drive MS lesion compartmentalization Spatial mapping of mouse and human multiple sclerosis neuropathology at a single-cell resolution unveils the cellular architecture and dynamics underlying disease evolution. |
| Author | Zheng, Chao Guerreiro-Cacais, André O. Langseth, Christoffer M. Kukanja, Petra Avenel, Christophe Agirre, Eneritz Tiklová, Katarina Hilscher, Markus M. Raman, Amitha Rubio Rodríguez-Kirby, Leslie A. Yokota, Chika Nilsson, Mats Olsson, Tomas Castelo-Branco, Gonçalo |
| Author_xml | – sequence: 1 givenname: Petra surname: Kukanja fullname: Kukanja, Petra email: petra.kukanja@ki.se organization: Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden – sequence: 2 givenname: Christoffer M. surname: Langseth fullname: Langseth, Christoffer M. email: christoffer.langseth@scilifelab.se organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 3 givenname: Leslie A. surname: Rubio Rodríguez-Kirby fullname: Rubio Rodríguez-Kirby, Leslie A. organization: Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden – sequence: 4 givenname: Eneritz surname: Agirre fullname: Agirre, Eneritz organization: Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden – sequence: 5 givenname: Chao surname: Zheng fullname: Zheng, Chao organization: Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden – sequence: 6 givenname: Amitha surname: Raman fullname: Raman, Amitha organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 7 givenname: Chika surname: Yokota fullname: Yokota, Chika organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 8 givenname: Christophe surname: Avenel fullname: Avenel, Christophe organization: Department of Information Technology, Uppsala University, 752 37 Uppsala, Sweden – sequence: 9 givenname: Katarina surname: Tiklová fullname: Tiklová, Katarina organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 10 givenname: André O. surname: Guerreiro-Cacais fullname: Guerreiro-Cacais, André O. organization: Center for Molecular Medicine, Department of Clinical Neuroscience, Karolinska Institutet, Karolinska University Hospital, 171 76 Solna, Sweden – sequence: 11 givenname: Tomas surname: Olsson fullname: Olsson, Tomas organization: Center for Molecular Medicine, Department of Clinical Neuroscience, Karolinska Institutet, Karolinska University Hospital, 171 76 Solna, Sweden – sequence: 12 givenname: Markus M. surname: Hilscher fullname: Hilscher, Markus M. organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 13 givenname: Mats surname: Nilsson fullname: Nilsson, Mats email: mats.nilsson@scilifelab.se organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Solna, 17154 Stockholm, Sweden – sequence: 14 givenname: Gonçalo surname: Castelo-Branco fullname: Castelo-Branco, Gonçalo email: goncalo.castelo-branco@ki.se organization: Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden |
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| Keywords | Serpina3n SERPINA3 in situ sequencing experimental autoimmune encephalomyelitis disease-associated glia neuroinflammation multiple sclerosis MS single-cell EAE spatial sequencing neuropathology |
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| SubjectTerms | disease-associated glia EAE encephalomyelitis experimental autoimmune experimental autoimmune encephalomyelitis in situ sequencing multiple sclerosis neuroinflammation neuroinflammation disease-associated glia neuropathology SERPINA3 Serpina3n single-cell spatial sequencing |
| Title | Cellular architecture of evolving neuroinflammatory lesions and multiple sclerosis pathology |
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