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Article ; Online: Regulation of stress granule formation in human oligodendrocytes.

Pernin, Florian / Cui, Qiao-Ling / Mohammadnia, Abdulshakour / Fernandes, Milton G F / Hall, Jeffery A / Srour, Myriam / Dudley, Roy W R / Zandee, Stephanie E J / Klement, Wendy / Prat, Alexandre / Salapa, Hannah E / Levin, Michael C / Moore, G R Wayne / Kennedy, Timothy E / Vande Velde, Christine / Antel, Jack P

Nature communications

2024 Volume 15, Issue 1, Page(s) 1524

Abstract: Oligodendrocyte (OL) injury and subsequent loss is a pathologic hallmark of multiple sclerosis (MS). Stress granules (SGs) are membrane-less organelles containing mRNAs stalled in translation and considered as participants of the cellular response to ... ...

Abstract	Oligodendrocyte (OL) injury and subsequent loss is a pathologic hallmark of multiple sclerosis (MS). Stress granules (SGs) are membrane-less organelles containing mRNAs stalled in translation and considered as participants of the cellular response to stress. Here we show SGs in OLs in active and inactive areas of MS lesions as well as in normal-appearing white matter. In cultures of primary human adult brain derived OLs, metabolic stress conditions induce transient SG formation in these cells. Combining pro-inflammatory cytokines, which alone do not induce SG formation, with metabolic stress results in persistence of SGs. Unlike sodium arsenite, metabolic stress induced SG formation is not blocked by the integrated stress response inhibitor. Glycolytic inhibition also induces persistent SGs indicating the dependence of SG formation and disassembly on the energetic glycolytic properties of human OLs. We conclude that SG persistence in OLs in MS reflects their response to a combination of metabolic stress and pro-inflammatory conditions.
MeSH term(s)	Humans ; Cytoplasmic Granules/metabolism ; Stress Granules ; Oligodendroglia ; Cytokines/metabolism ; Stress, Physiological ; Multiple Sclerosis/metabolism
Chemical Substances	Cytokines
Language	English
Publishing date	2024-02-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-45746-6
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Article: Disease-associated astrocyte epigenetic memory promotes CNS pathology.

Lee, Hong-Gyun / Rone, Joseph M / Li, Zhaorong / Akl, Camilo Faust / Shin, Seung Won / Lee, Joon-Hyuk / Flausino, Lucas E / Pernin, Florian / Chao, Chun-Cheih / Kleemann, Kilian L / Srun, Lena / Illouz, Tomer / Giovannoni, Federico / Charabati, Marc / Sanmarco, Liliana M / Kenison, Jessica E / Piester, Gavin / Zandee, Stephanie E J / Antel, Jack /

Rothhammer, Veit / Wheeler, Michael A / Prat, Alexandre / Clark, Iain C / Quintana, Francisco J

bioRxiv : the preprint server for biology

2024

Abstract: Astrocytes play important roles in the central nervous system (CNS) physiology and pathology. Indeed, astrocyte subsets defined by specific transcriptional activation states contribute to the pathology of neurologic diseases, including multiple sclerosis ...

Abstract	Astrocytes play important roles in the central nervous system (CNS) physiology and pathology. Indeed, astrocyte subsets defined by specific transcriptional activation states contribute to the pathology of neurologic diseases, including multiple sclerosis (MS) and its pre-clinical model experimental autoimmune encephalomyelitis (EAE)
Language	English
Publishing date	2024-01-05
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.04.574196
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Article ; Online: Disease-associated astrocyte epigenetic memory promotes CNS pathology.

Rothhammer, Veit / Wheeler, Michael A / Prat, Alexandre / Clark, Iain C / Quintana, Francisco J

Nature

2024 Volume 627, Issue 8005, Page(s) 865–872

Abstract: Disease-associated astrocyte subsets contribute to the pathology of neurologic diseases, including multiple sclerosis and experimental autoimmune ... ...

Abstract	Disease-associated astrocyte subsets contribute to the pathology of neurologic diseases, including multiple sclerosis and experimental autoimmune encephalomyelitis
MeSH term(s)	Animals ; Female ; Humans ; Male ; Mice ; Acetyl Coenzyme A/metabolism ; Astrocytes/enzymology ; Astrocytes/metabolism ; Astrocytes/pathology ; ATP Citrate (pro-S)-Lyase/metabolism ; Chromatin/genetics ; Chromatin/metabolism ; Chromatin Assembly and Disassembly ; Chromatin Immunoprecipitation Sequencing ; CRISPR-Cas Systems ; Encephalomyelitis, Autoimmune, Experimental/enzymology ; Encephalomyelitis, Autoimmune, Experimental/genetics ; Encephalomyelitis, Autoimmune, Experimental/metabolism ; Encephalomyelitis, Autoimmune, Experimental/pathology ; Epigenetic Memory ; Inflammation/enzymology ; Inflammation/genetics ; Inflammation/metabolism ; Inflammation/pathology ; Multiple Sclerosis/enzymology ; Multiple Sclerosis/genetics ; Multiple Sclerosis/metabolism ; Multiple Sclerosis/pathology ; Single-Cell Gene Expression Analysis ; Transposases/metabolism
Chemical Substances	Acetyl Coenzyme A (72-89-9) ; ATP Citrate (pro-S)-Lyase (EC 2.3.3.8) ; Chromatin ; p300-CBP-associated factor (EC 2.3.1.48) ; Transposases (EC 2.7.7.-)
Language	English
Publishing date	2024-03-20
Publishing country	England
Document type	Journal Article
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-024-07187-5
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Article ; Online: Diverse injury responses of human oligodendrocyte to mediators implicated in multiple sclerosis.

Pernin, Florian / Luo, Julia / Cui, Qiao-Ling / Blain, Manon / Fernandes, Milton G F / Yaqubi, Moein / Srour, Myriam / Hall, Jeff / Dudley, Roy / Jamann, Hélène / Larochelle, Catherine / Zandee, Stephanie E J / Prat, Alexandre / Stratton, Jo Anne / Kennedy, Timothy E / Antel, Jack P

Brain : a journal of neurology

2022

Abstract: Early multiple sclerosis lesions feature relative preservation of oligodendrocyte cell bodies with dying back retraction of their myelinating processes. Cell loss occurs with disease progression. Putative injury mediators include metabolic stress (low ... ...

Abstract	Early multiple sclerosis lesions feature relative preservation of oligodendrocyte cell bodies with dying back retraction of their myelinating processes. Cell loss occurs with disease progression. Putative injury mediators include metabolic stress (low glucose/nutrient), pro-inflammatory mediators (interferon γ and tumor necrosis factor α), and excitotoxins (glutamate). Our objective was to compare the impact of these disease relevant mediators on the injury responses of human mature oligodendrocytes. In the current study, we determined the effects of these mediators on process extension and survival of human brain derived mature oligodendrocytes in vitro and used bulk RNA sequencing to identify distinct effector mechanisms that underlie the responses. All mediators induced significant process retraction of the oligodendrocytes in dissociated cell culture. Only metabolic stress (low glucose/nutrient) conditions resulted in delayed (4-6 days) non-apoptotic cell death. Metabolic effects were associated with induction of the integrated stress response, which can be protective or contribute to cell injury dependent on its level and duration of activation. Addition of Sephin1, an agonist of the integrated stress response induced process retraction under control conditions and further enhanced retraction under metabolic stress conditions. The antagonist ISRIB restored process outgrowth under stress conditions, and if added to already stressed cells, reduced delayed cell death and prolonged the period in which recovery could occur. Inflammatory cytokine functional effects were associated with activation of multiple signaling pathways (including Jak/Stat-1) that regulate process outgrowth, without integrated stress response induction. Glutamate application produced limited transcriptional changes suggesting a contribution of effects directly on cell processes. Our comparative studies indicate the need to consider both the specific injury mediators and the distinct cellular mechanisms of responses to them by human oligodendrocytes to identify effective neuroprotective therapies for multiple sclerosis.
Language	English
Publishing date	2022-02-24
Publishing country	England
Document type	Journal Article
ZDB-ID	80072-7
ISSN	1460-2156 ; 0006-8950
ISSN (online)	1460-2156
ISSN	0006-8950
DOI	10.1093/brain/awac075
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Article ; Online: Mechanisms of metabolic stress induced cell death of human oligodendrocytes: relevance for progressive multiple sclerosis.

Acta neuropathologica communications

2023 Volume 11, Issue 1, Page(s) 108

Abstract: Oligodendrocyte (OL) injury and loss are central features of evolving lesions in multiple sclerosis. Potential causative mechanisms of OL loss include metabolic stress within the lesion microenvironment. Here we use the injury response of primary human ... ...

Abstract	Oligodendrocyte (OL) injury and loss are central features of evolving lesions in multiple sclerosis. Potential causative mechanisms of OL loss include metabolic stress within the lesion microenvironment. Here we use the injury response of primary human OLs (hOLs) to metabolic stress (reduced glucose/nutrients) in vitro to help define the basis for the in situ features of OLs in cases of MS. Under metabolic stress in vitro, we detected reduction in ATP levels per cell that precede changes in survival. Autophagy was initially activated, although ATP levels were not altered by inhibitors (chloroquine) or activators (Torin-1). Prolonged stress resulted in autophagy failure, documented by non-fusion of autophagosomes and lysosomes. Consistent with our in vitro results, we detected higher expression of LC3, a marker of autophagosomes in OLs, in MS lesions compared to controls. Both in vitro and in situ, we observe a reduction in nuclear size of remaining OLs. Prolonged stress resulted in increased ROS and cleavage of spectrin, a target of Ca
MeSH term(s)	Humans ; Multiple Sclerosis/pathology ; Reactive Oxygen Species/metabolism ; Oligodendroglia/pathology ; Cell Death ; Multiple Sclerosis, Chronic Progressive/pathology ; Adenosine Triphosphate/metabolism
Chemical Substances	Reactive Oxygen Species ; Adenosine Triphosphate (8L70Q75FXE)
Language	English
Publishing date	2023-07-05
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2715589-4
ISSN	2051-5960 ; 2051-5960
ISSN (online)	2051-5960
ISSN	2051-5960
DOI	10.1186/s40478-023-01601-1
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Article ; Online: Identification of astrocyte regulators by nucleic acid cytometry.

Nature

2023 Volume 614, Issue 7947, Page(s) 326–333

Abstract: Multiple sclerosis is a chronic inflammatory disease of the central nervous ... ...

Abstract	Multiple sclerosis is a chronic inflammatory disease of the central nervous system
MeSH term(s)	Animals ; Humans ; Mice ; Astrocytes/metabolism ; Astrocytes/pathology ; Encephalomyelitis, Autoimmune, Experimental ; Gene Expression Regulation ; Mice, Knockout ; Multiple Sclerosis/pathology ; Microfluidics/methods ; Single-Cell Gene Expression Analysis/methods ; Nucleic Acids/analysis ; Gene Editing
Chemical Substances	Xbp1 protein, mouse ; Nucleic Acids ; NR3C2 protein, human ; NCOR2 protein, human ; XBP1 protein, human ; Nr3c2 protein, mouse ; Ncor2 protein, mouse
Language	English
Publishing date	2023-01-04
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-022-05613-0
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Zs.A 26: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Stress Signal ULBP4, an NKG2D Ligand, Is Upregulated in Multiple Sclerosis and Shapes CD8

Carmena Moratalla, Ana / Carpentier Solorio, Yves / Lemaitre, Florent / Farzam-Kia, Negar / Levert, Annie / Zandee, Stephanie E J / Lahav, Boaz / Guimond, Jean Victor / Haddad, Elie / Girard, Marc / Duquette, Pierre / Larochelle, Catherine / Prat, Alexandre / Arbour, Nathalie

Neurology(R) neuroimmunology & neuroinflammation

2021 Volume 9, Issue 1

Abstract: Background and objectives: We posit the involvement of the natural killer group 2D (NKG2D) pathway in multiple sclerosis (MS) pathology via the presence of specific NKG2D ligands (NKG2DLs). We aim to evaluate the expression of NKG2DLs in the CNS and CSF ...

Abstract	Background and objectives: We posit the involvement of the natural killer group 2D (NKG2D) pathway in multiple sclerosis (MS) pathology via the presence of specific NKG2D ligands (NKG2DLs). We aim to evaluate the expression of NKG2DLs in the CNS and CSF of patients with MS and to identify cellular stressors inducing the expression of UL16-binding protein 4 (ULBP4), the only detectable NKG2DL. Finally, we evaluate the impact of ULBP4 on functions such as cytokine production and motility by CD8 Methods: Human postmortem brain samples and CSF from patients with MS and controls were used to evaluate NKG2DL expression. In vitro assays using primary cultures of human astrocytes and neurons were performed to identify stressors inducing ULBP4 expression. Human CD8 Results: We detected mRNA coding for the 8 identified human NKG2DLs in brain samples from patients with MS and controls, but only ULBP4 protein expression was detectable by Western blot. ULBP4 levels were greater in patients with MS, particularly in active and chronic active lesions and normal-appearing white matter, compared with normal-appearing gray matter from MS donors and white and gray matter from controls. Soluble ULBP4 was also detected in CSF of patients with MS and controls, but a smaller shed/soluble form of 25 kDa was significantly elevated in CSF from female patients with MS compared with controls and male patients with MS. Our data indicate that soluble ULBP4 affects various functions of CD8 Discussion: Our study provides new evidence for the involvement of NKG2D and its ligand ULBP4 in MS pathology. Our results point to ULBP4 as a viable target to specifically block 1 component of the NKG2D pathway without altering immune surveillance involving other NKG2DL.
MeSH term(s)	Astrocytes ; Autopsy ; Brain/metabolism ; Brain/pathology ; CD8-Positive T-Lymphocytes ; Carrier Proteins/cerebrospinal fluid ; Carrier Proteins/metabolism ; Cells, Cultured ; Fetus ; Histocompatibility Antigens Class I/cerebrospinal fluid ; Histocompatibility Antigens Class I/metabolism ; Humans ; Membrane Proteins/cerebrospinal fluid ; Membrane Proteins/metabolism ; Multiple Sclerosis/cerebrospinal fluid ; Multiple Sclerosis/immunology ; Multiple Sclerosis/metabolism ; NK Cell Lectin-Like Receptor Subfamily K/metabolism ; Neurons ; Stress, Physiological/immunology ; Stress, Physiological/physiology ; Up-Regulation ; White Matter/metabolism
Chemical Substances	Carrier Proteins ; Histocompatibility Antigens Class I ; KLRK1 protein, human ; Membrane Proteins ; NK Cell Lectin-Like Receptor Subfamily K ; RAET1E protein, human
Language	English
Publishing date	2021-12-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2767740-0
ISSN	2332-7812 ; 2332-7812
ISSN (online)	2332-7812
ISSN	2332-7812
DOI	10.1212/NXI.0000000000001119
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Article ; Online: Droplet-based forward genetic screening of astrocyte-microglia cross-talk.

Wheeler, Michael A / Clark, Iain C / Lee, Hong-Gyun / Li, Zhaorong / Linnerbauer, Mathias / Rone, Joseph M / Blain, Manon / Akl, Camilo Faust / Piester, Gavin / Giovannoni, Federico / Charabati, Marc / Lee, Joon-Hyuk / Kye, Yoon-Chul / Choi, Joshua / Sanmarco, Liliana M / Srun, Lena / Chung, Elizabeth N / Flausino, Lucas E / Andersen, Brian M /

Rothhammer, Veit / Yano, Hiroshi / Illouz, Tomer / Zandee, Stephanie E J / Daniel, Carolin / Artis, David / Prinz, Marco / Abate, Adam R / Kuchroo, Vijay K / Antel, Jack P / Prat, Alexandre / Quintana, Francisco J

Science (New York, N.Y.)

2023 Volume 379, Issue 6636, Page(s) 1023–1030

Abstract: Cell-cell interactions in the central nervous system play important roles in neurologic diseases. However, little is known about the specific molecular pathways involved, and methods for their systematic identification are limited. Here, we developed a ... ...

Abstract	Cell-cell interactions in the central nervous system play important roles in neurologic diseases. However, little is known about the specific molecular pathways involved, and methods for their systematic identification are limited. Here, we developed a forward genetic screening platform that combines CRISPR-Cas9 perturbations, cell coculture in picoliter droplets, and microfluidic-based fluorescence-activated droplet sorting to identify mechanisms of cell-cell communication. We used SPEAC-seq (systematic perturbation of encapsulated associated cells followed by sequencing), in combination with in vivo genetic perturbations, to identify microglia-produced amphiregulin as a suppressor of disease-promoting astrocyte responses in multiple sclerosis preclinical models and clinical samples. Thus, SPEAC-seq enables the high-throughput systematic identification of cell-cell communication mechanisms.
MeSH term(s)	Astrocytes/physiology ; Genetic Testing/methods ; High-Throughput Screening Assays ; Microfluidic Analytical Techniques/methods ; Microglia/physiology ; Amphiregulin/genetics ; Autocrine Communication/genetics ; Gene Expression ; Humans
Chemical Substances	Amphiregulin
Language	English
Publishing date	2023-03-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	128410-1
ISSN	1095-9203 ; 0036-8075
ISSN (online)	1095-9203
ISSN	0036-8075
DOI	10.1126/science.abq4822
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Zs.A 27: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Gut-licensed IFNγ

Sanmarco, Liliana M / Wheeler, Michael A / Gutiérrez-Vázquez, Cristina / Polonio, Carolina Manganeli / Linnerbauer, Mathias / Pinho-Ribeiro, Felipe A / Li, Zhaorong / Giovannoni, Federico / Batterman, Katelyn V / Scalisi, Giulia / Zandee, Stephanie E J / Heck, Evelyn S / Alsuwailm, Moneera / Rosene, Douglas L / Becher, Burkhard / Chiu, Isaac M / Prat, Alexandre / Quintana, Francisco J

Nature

2021 Volume 590, Issue 7846, Page(s) 473–479

Abstract: Astrocytes are glial cells that are abundant in the central nervous system (CNS) and that have important homeostatic and disease-promoting ... ...

Abstract	Astrocytes are glial cells that are abundant in the central nervous system (CNS) and that have important homeostatic and disease-promoting functions
MeSH term(s)	Animals ; Apoptosis ; Astrocytes/immunology ; Astrocytes/metabolism ; Biomarkers ; Central Nervous System/immunology ; Encephalomyelitis, Autoimmune, Experimental/immunology ; Encephalomyelitis, Autoimmune, Experimental/prevention & control ; Female ; Gastrointestinal Microbiome/immunology ; Homeostasis ; Humans ; Inflammation/immunology ; Inflammation/prevention & control ; Interferon-gamma/immunology ; Killer Cells, Natural/immunology ; Lysosomal Membrane Proteins/metabolism ; Meninges/cytology ; Meninges/immunology ; Mice ; Mice, Inbred C57BL ; T-Lymphocytes/cytology ; T-Lymphocytes/immunology ; TNF-Related Apoptosis-Inducing Ligand/metabolism
Chemical Substances	Biomarkers ; Lamp1 protein, mouse ; Lysosomal Membrane Proteins ; TNF-Related Apoptosis-Inducing Ligand ; TNFSF10 protein, human ; Tnfsf10 protein, mouse ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2021-01-06
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-020-03116-4
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Article: A Context-Dependent Role for αv Integrins in Regulatory T Cell Accumulation at Sites of Inflammation.

Mair, Iris / Zandee, Stephanie E J / Toor, Iqbal S / Saul, Louise / McPherson, Rhoanne C / Leech, Melanie D / Smyth, Danielle J / O'Connor, Richard A / Henderson, Neil C / Anderton, Stephen M

Frontiers in immunology

2018 Volume 9, Page(s) 264

Abstract: Several inflammatory diseases including multiple sclerosis and inflammatory bowel disease have been associated with dysfunctional and/or reduced numbers of ... ...

Abstract	Several inflammatory diseases including multiple sclerosis and inflammatory bowel disease have been associated with dysfunctional and/or reduced numbers of Foxp3
MeSH term(s)	Animals ; Autoimmune Diseases/immunology ; Colitis/immunology ; Encephalomyelitis, Autoimmune, Experimental/immunology ; Inflammation/immunology ; Integrin alphaV/immunology ; Mice ; Mice, Knockout ; T-Lymphocytes, Regulatory/immunology
Chemical Substances	Integrin alphaV
Language	English
Publishing date	2018-02-26
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2018.00264
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