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July 2020; 7 (4) ArticleOpen Access

Single-cell RNA-seq analysis of human CSF microglia and myeloid cells in neuroinflammation

Ekaterina Esaulova, Claudia Cantoni, Irina Shchukina, View ORCID ProfileKonstantin Zaitsev, Robert C. Bucelli, View ORCID ProfileGregory F. Wu, Maxim N. Artyomov, View ORCID ProfileAnne H. Cross, View ORCID ProfileBrian T. Edelson
First published May 5, 2020, DOI: https://doi.org/10.1212/NXI.0000000000000732
Ekaterina Esaulova
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Claudia Cantoni
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Irina Shchukina
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Konstantin Zaitsev
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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  • ORCID record for Konstantin Zaitsev
Robert C. Bucelli
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Gregory F. Wu
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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  • ORCID record for Gregory F. Wu
Maxim N. Artyomov
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Anne H. Cross
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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  • ORCID record for Anne H. Cross
Brian T. Edelson
From the Department of Pathology and Immunology (E.E., I.S., K.Z., G.F.W., M.N.A., B.T.E.) and Department of Neurology (C.C., R.C.B., G.F.W., A.H.C.), Washington University School of Medicine, St. Louis, MO; and Computer Technologies Department (K.Z.), ITMO University, St. Petersburg, Russia.
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Citation
Single-cell RNA-seq analysis of human CSF microglia and myeloid cells in neuroinflammation
Ekaterina Esaulova, Claudia Cantoni, Irina Shchukina, Konstantin Zaitsev, Robert C. Bucelli, Gregory F. Wu, Maxim N. Artyomov, Anne H. Cross, Brian T. Edelson
Neurol Neuroimmunol Neuroinflamm Jul 2020, 7 (4) e732; DOI: 10.1212/NXI.0000000000000732

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    Figure 1 scRNA-seq characterization of leukocytes from MS, anti-MOG disorder, and HIV

    (A) UMAP of immune cell clusters from the blood (top) and CSF (bottom) of all subjects merged. (B) Characteristic marker gene expression assigned to each cluster displayed by UMAP. (C) Proportional abundance of 20 cell clusters within the blood (purple) and CSF (yellow). Y axis represents the percentage of all cells. cDC = conventional DC; PBMC = peripheral blood mononuclear cell; pDC = plasmacytoid DC; RBC = red blood cell; Tgd = γδ T cells; UMAP = Uniform Manifold Approximation and Projection.

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    Figure 2 Relative expression of myeloid population-defining genes in neuroinflammation

    (A) Expression of canonical microglial genes within the UMAP of CSF immune cell clusters. (B) Heatmap representation of gene expression in blood (purple) and CSF (yellow) myeloid populations. Gene list derived from Sankowski et al.7 (C) Top genes reported by Farhadian et al.3 as specific for “microglia-like cells” (top) and Beltran et al.4 as specific for “monocytes” (bottom) displayed in the UMAP of immune cell clusters in the CSF of all subjects. cDC = conventional DC; PBMC = peripheral blood mononuclear cell; pDC = plasmacytoid DC; UMAP = Uniform Manifold Approximation and Projection.

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    Figure 3 Discrimination of myeloid cell populations in neuroinflammation by gene expression

    Heatmap of 10 genes that discriminate myeloid cell types within the blood (purple) and CSF (yellow). Columns represent individual subjects. cDC = conventional DC; PBMC = peripheral blood mononuclear cell; pDC = plasmacytoid DC.

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    Figure 4 Flow cytometric identification of microglia and myeloid cells within the blood and CSF

    (A and B) Plots were obtained by gating on CD3−CD19− singlets. HLA-DR+BDCA-2hi cells represent pDCs. cDCs are represented as HLA-DR+BDCA-2−CD1chi. Red gates in the third column represent microglia, whereas blue gates represent monocytes. The fourth column shows HLA-DR and Lyve-1 staining of microglia (red) and monocytes (blue). The fifth column shows HLA-DR and Lox-1 staining of microglia (red) and monocytes (blue). (A) Flow cytometry on CSF and blood samples from a subject with RRMS. (B) Flow cytometry on CSF from subjects with anti-MOG disorder (anti-MOG), ALS, IIH, and a healthy control. (C) Mean fluorescence intensity (MFI) of HLA-DR, CD33, Lyve-1, and Lox-1 of CSF monocytes and microglia from subjects. Each pair of connected circles represents one CSF sample. Statistical significance was determined using a paired Student t test. ALS = amyotrophic lateral sclerosis; cDC = conventional DC; IIH = idiopathic intracranial hypertension; MOG = myelin oligodendrocyte glycoprotein; PBMC = peripheral blood mononuclear cell; pDC = plasmacytoid DC.

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