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March 2023; 10 (2) Research ArticleOpen Access

CAR-T Cell–Mediated B-Cell Depletion in Central Nervous System Autoimmunity

Sasha Gupta, Milos Simic, Sharon A. Sagan, Chanelle Shepherd, Jason Duecker, Raymond A. Sobel, Ravi Dandekar, Gregory F. Wu, Wesley Wu, John E. Pak, View ORCID ProfileStephen L. Hauser, Wendell Lim, View ORCID ProfileMichael R. Wilson, Scott S. Zamvil
First published January 19, 2023, DOI: https://doi.org/10.1212/NXI.0000000000200080
Sasha Gupta
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Milos Simic
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Sharon A. Sagan
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Chanelle Shepherd
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Jason Duecker
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Raymond A. Sobel
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Ravi Dandekar
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Gregory F. Wu
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Wesley Wu
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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John E. Pak
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Stephen L. Hauser
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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  • ORCID record for Stephen L. Hauser
Wendell Lim
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Michael R. Wilson
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Scott S. Zamvil
From the Department of Neurology (S.G., S.A.S., C.S., R.D., S.L.H., M.R.W., S.S.Z.), Weill Institute for Neurosciences, University of California San Francisco, CA; Department of Cellular Molecular Pharmacology (M.S., J.D., W.L.), University of California San Francisco Cell Design Institute, CA; Veterans Affairs Health Care System (R.A.S.), Department of Pathology, Stanford University School of Medicine, CA; Departments of Neurology and Pathology and Immunology (G.F.W.), Washington University in St. Louis, MO; and Chan Zuckerberg Biohub (W.W., J.E.P.), San Francisco, CA.
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Full PDF
Citation
CAR-T Cell–Mediated B-Cell Depletion in Central Nervous System Autoimmunity
Sasha Gupta, Milos Simic, Sharon A. Sagan, Chanelle Shepherd, Jason Duecker, Raymond A. Sobel, Ravi Dandekar, Gregory F. Wu, Wesley Wu, John E. Pak, Stephen L. Hauser, Wendell Lim, Michael R. Wilson, Scott S. Zamvil
Neurol Neuroimmunol Neuroinflamm Mar 2023, 10 (2) e200080; DOI: 10.1212/NXI.0000000000200080

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    Figure 1 EAE Disease on CAR-T Cell Therapy

    (A) Experimental timeline. (B) Average EAE clinical score after immunization with rhMOG. Multiple t tests revealed p < 0.05 from days 15–26 between WT vs cyclophosphamide (Cy) + anti-CD19 (aCD19) CAR-T cells and from days 21–28 from between Cy alone vs Cy + aCD19 CAR-T cells. Shown is average ± SD. (C) Cerebellar histology 28 days after EAE induction. WT and cyclophosphamide treated mice show typical perivascular mononuclear inflammatory cell foci in the white matter (indicated by arrows), whereas the Cy treated with aCD19 CAR-T cells or control cells are normal. Bar = 100 µm and applies to all. (D) Representative total numbers of meningeal and parenchymal foci within spinal cord and brain per sacrificed mouse shown, 2 mice per group. aCD20 as anti-CD20, Cy as cyclophosphamide, and aCD19 CAR as anti-CD19 CAR-T cell. CAR = chimeric antigen receptor; Cy = cyclophosphamide; EAE = experimental autoimmune encephalomyelitis; MOG = myelin oligodendrocyte protein; WT = wild type.

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    Figure 2 B Cell Depletion Based on Treatment

    (A) Frequency of CD45+CD11b-CD19+ cells, average of 5 mice peripheral blood from 5 µL of tail vein blood as ratio against WT. (B) Frequency of CD45+CD11b-CD19+ cells, average of 2 mouse per disease cohort per compartment which included spleen, inguinal lymph node, and femoral bone marrow, and 1 mouse per CNS (brain and spinal cord) on day 17 postimmunization. Shown is average ± SD. (C) Frequency of CD45+CD11b-CD19+ cells, average of 2 mouse per disease cohort per compartment which included spleen, inguinal lymph node, and femoral bone marrow, and CNS (brain and spinal cord) on day 28 postimmunization. Paired t test, p value <0.05 considered significant (*), if p < 0.009 (**). WT = wild type.

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    Figure 3 Endogenous T Cell Response Based on Treatment

    (A) Frequency of CD45+CD4+IL17+ (Th17) or CD45+CD4+IFNg+ (Th1) cells of 1 mouse per disease cohort from periphery (spleen) or CNS (brain and spinal cord) on day 17 postimmunization. (B) Frequency of CD45+CD4+IL17+ (Th17) or CD45+CD4+IFNg+ (Th1) cells, average of 3 mice per disease cohort from periphery (spleen) or CNS (brain and spinal cord) on day 28 postimmunization (C) Frequency of CD4+CD25+FOXp3+ cells average of 2 mice per disease cohort per compartment on day 28 postimmunization. Shown is average ± SD.

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