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Novel Mechanisms of Neurodegeneration in Multiple Sclerosis Models

Date

2022-08-17

Journal Title

Journal ISSN

Volume Title

Publisher

ORCID

0000-0002-5538-7770

Type

Thesis

Degree Level

Doctoral

Abstract

Neurodegeneration, the progressive loss of function or structure to neurons and axons, underlies permanent disability in multiple sclerosis (MS); yet its mechanisms are incompletely understood. Historically, the autoimmune response in MS was thought to target myelin products causing demyelination but recent data indicates autoimmunity to several intraneuronal antigens, including the RNA binding protein (RBP) heterogenous nuclear ribonucleoprotein A1 (hnRNP A1), as contributors to neurodegeneration. Previous research identified that anti-hnRNP A1 antibodies are taken up by neuron-like cells in vitro resulting in hnRNP A1 mislocalization and stress granule formation. Anti-hnRNP A1 antibody addition to mice with experimental autoimmune encephalomyelitis (EAE) resulted in exacerbated clinical disease, and increased neurodegeneration, the mechanisms of which are unknown. We hypothesized that anti-hnRNP A1 antibodies would be taken up by neurons, induce hnRNP A1 dysfunction in the form of its nuclear-cytoplasmic mislocalization, stress granule formation, and altered RNA expression, which might trigger neurodegeneration in models of MS. We tested this hypothesis by treating mice with EAE, primary embryonic cortical neurons, or neuronal cell lines with anti-hnRNP A1 antibodies (which overlap with the immunodominant epitope of MS IgG) and examining them for antibody localization and markers of hnRNP A1 dysfunction and neurodegeneration over time. We found that in in vivo and in vitro MS models, anti-hnRNP A1 antibodies (compared to IgG control) are preferentially taken up by clathrinmediated endocytosis, induce hnRNP A1 cytoplasmic-mislocalization followed by subsequent stress granule formation and altered RNA expression. This anti-hnRNP A1 antibody-mediated hnRNP A1 dysfunction then triggers the activation of necroptosis (a cell death pathway) and subsequent neurodegeneration (characterized by loss of neurons and neurites). These findings implicate an autoantibody response characteristic of MS as an important contributor to neurodegeneration and permanent disability. Further, it demonstrates the importance of RBP dysfunction as an underlying mechanism of neurodegeneration. Taken together, we identified a novel antibody-mediated mechanism of neurodegeneration, which may be targeted to inhibit neurodegeneration and prevent permanent disability in persons living with MS.

Description

Keywords

Multiple Sclerosis, Heterogenous nuclear ribonucleoprotein A1 (hnRNP A1), Autoimmunity, RNA binding protein dysfunction, experimental autoimmune encephalomyelitis (EAE)

Citation

Degree

Doctor of Philosophy (Ph.D.)

Department

Medicine

Program

Health Sciences

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DOI

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