Cited by 142Neuroinflammation and Neurodegeneration MechanismsMultiple Sclerosis Research StudiesTryptophan and brain disorders

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The Emerging Role of Central and Peripheral Immune Systems in Neurodegenerative Diseases

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Zang, Xin, Chen, Si, Zhu, JunYao, Ma, Junwen, Zhai, Yongzhen·2022·Frontiers in Aging Neuroscience

DOI 10.3389/fnagi.2022.872134PMC PMC9082639

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Abstract

For decades, it has been widely believed that the blood–brain barrier (BBB) provides an immune privileged environment in the central nervous system (CNS) by blocking peripheral immune cells and humoral immune factors. This view has been revised in recent years, with increasing evidence revealing that the peripheral immune system plays a critical role in regulating CNS homeostasis and disease. Neurodegenerative diseases are characterized by progressive dysfunction and the loss of neurons in the CNS. An increasing number of studies have focused on the role of the connection between the peripheral immune system and the CNS in neurodegenerative diseases. On the one hand, peripherally released cytokines can cross the BBB, cause direct neurotoxicity and contribute to the activation of microglia and astrocytes. On the other hand, peripheral immune cells can also infiltrate the brain and participate in the progression of neuroinflammatory and neurodegenerative diseases. Neurodegenerative diseases have a high morbidity and disability rate, yet there are no effective therapies to stop or reverse their progression. In recent years, neuroinflammation has received much attention as a therapeutic target for many neurodegenerative diseases. In this review, we highlight the emerging role of the peripheral and central immune systems in neurodegenerative diseases, as well as their interactions. A better understanding of the emerging role of the immune systems may improve therapeutic strategies for neurodegenerative diseases.

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Figure 1 Microglia perform surveillance functions of the extracellular environment of the brain in the resting state. In the presence of stressors, microglia can be activated into two states, which have been traditionally divided into M1 (classical activation) and M2 (alternative activation). Binding of receptors on microglia to Th1 cytokines drives microglia polarization to the M1 phenotype, leading to increased inflammation and oxidative stress as well as BBB dysfunction. In contrast, Th2 cytokines prompt microglia to polarize to the M2 phenotype. M2 phenotype microglia promote tissue repair and regeneration through the production of anti-inflammatory cytokines and neurotrophic factors for to exert neuroprotective effects.CC BY · PubMed Central

Figure 2 In pathological conditions, damaged neurons release autoantigens to activate resting microglia, which differentiate into the pro-inflammatory phenotype of M1. The M1 phenotype microglia secrete pro-inflammatory factors(IL-6, TNF-α, IFN-γ) to activate astrocytes, which induce the activation of A1 phenotype astrocytes. Reactive astrocytes contribute to the formation of glial scarring. It also leads to destruction of the BBB, which in turn leads to infiltration of CNS by peripheral immune cells. Antigens may enter peripheral lymphoid tissue, where they are presented by antigen-presenting cells to naive T cells, which differentiate into antigen-specific T effector cells (Th1, Th2, Th17 or Tregs). These cells then secrete anti-inflammatory or pro-inflammatory factors to regulate neuronal survival. Th1 and Th17 cells cross the BBB, produce neurotoxic and pro-inflammatory factors that interact with glial cells, leading directly to neuroinflammation and damage to motor neurons. Th2 and Tregs migrate from the periphery to the central nervous system and interact with glial cells to function as motor neuron protectors. In addition, antigens can directly stimulate B cells, which are activated to produce pro-inflammatory factors that travel along blood vessels to the brain and participate in neurodegeneration. Activated T cells secrete lymphokines to activate B cells, which proliferate and differentiate into plasma cells. Plasma cells can further produce cytokines and antibodies, such as anti-Aβ or anti-α-synuclein antibodies, which cross the blood-brain barrier into the brain to alleviate neuronal degeneration.CC BY · PubMed Central

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“In addition, the results of animal studies of AD suggest that neutrophils may be associated with the destruction of the BBB (Baik et al., 2014).”
Background
Metabolic alterations in Parkinson’s disease astrocytes
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NF‐κB activation in astrocytes drives a stage‐specific beneficial neuroimmunological response in ALS
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Understanding the Role of T Cells in CNS Homeostasis
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Peripheral monocytes are functionally altered and invade the CNS in ALS patients
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The role of glial cells in multiple sclerosis disease progression
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“These therapies primarily target the peripheral immune system and therefore have limited effectiveness in the treatment of progressive MS (Healy et al., 2022).”
Background
Active immunization against alpha-synuclein ameliorates the degenerative pathology and prevents demyelination in a model of multiple system atrophy
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NK cells clear α-synuclein and the depletion of NK cells exacerbates synuclein pathology in a mouse model of α-synucleinopathy
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Mast cells and neutrophils mediate peripheral motor pathway degeneration in ALS
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Cytotoxic CD8 + T lymphocytes expressing ALS-causing SOD1 mutant selectively trigger death of spinal motoneurons
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New oligodendrocytes exhibit more abundant and accurate myelin regeneration than those that survive demyelination
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Traditional Chinese Medicine: Role in Reducing β-Amyloid, Apoptosis, Autophagy, Neuroinflammation, Oxidative Stress, and Mitochondrial Dysfunction of Alzheimer’s Disease
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Self-citation
The Gut-Microglia Connection: Implications for Central Nervous System Diseases
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The heme-regulated inhibitor is a cytosolic sensor of protein misfolding that controls innate immune signaling
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A deficiency in CCR2+ monocytes: the hidden side of Alzheimer’s disease
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Insights into T‐cell dysfunction in Alzheimer's disease
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γδ T Cells Regulate the Extent and Duration of Inflammation in the Central Nervous System by a Fas Ligand-Dependent Mechanism
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Astrocytic VEGFA : An essential mediator in blood–brain‐barrier disruption in Parkinson's disease
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Peripherally induced brain tissue–resident memory CD8+ T cells mediate protection against CNS infection
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The immunomodulatory oligodendrocyte
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Innate Immune Cells: Monocytes, Monocyte-Derived Macrophages and Microglia as Therapeutic Targets for Alzheimer’s Disease and Multiple Sclerosis
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Accumulation of cytotoxic T cells in the aged CNS leads to axon degeneration and contributes to cognitive and motor decline
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Depletion of NK Cells Improves Cognitive Function in the Alzheimer Disease Mouse Model
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Regulation of myeloid cell phagocytosis by LRRK2 via WAVE2 complex stabilization is altered in Parkinson’s disease
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Activation of pial and dural macrophages and dendritic cells by cortical spreading depression
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Innate Immunity: A Common Denominator between Neurodegenerative and Neuropsychiatric Diseases
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Interplay between Brain Pericytes and Endothelial Cells in Dementia
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NKG2D-Mediated Cytotoxicity toward Oligodendrocytes Suggests a Mechanism for Tissue Injury in Multiple Sclerosis
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Gut bacterial composition in a mouse model of Parkinson’s disease
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Analyses of phenotypic and functional characteristics of CX3CR1‐expressing natural killer cells
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Microglia enhanced the angiogenesis, migration and proliferation of co-cultured RMECs
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Authors: Zang, X., Chen, S., Zhu, J., Ma, J., & Zhai, Y.
Affiliations: Sheng Jing Hospital (CN)
Fourth Affiliated Hospital of China Medical University (CN)
Corresponding author: Zhai, Yongzhen
ORCID: Chen, Si
Zhu, JunYao
Zhai, Yongzhen
Venue: Frontiers in Aging Neuroscience
Publisher: Frontiers Media SA
Published: 2022-04-25
Volume: 14
Pages: 872134-872134
ISSN: 1663-4365 (ISSN-L)
DOI: 10.3389/fnagi.2022.872134
PMC: PMC9082639
OpenAlex: W4224441906
Cited by: 139
References: 221
Citations by year: 2026: 35 · 2025: 49 · 2024: 35 · 2023: 17 · 2022: 3
FWCI: 2.76
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Frontiers in Aging Neuroscience (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: neurodegenerative diseases, neuroinflammation, blood-brain barrier, peripheral immune system, central nervous system, cytokines, microglial activation, astrocytes, immune privilege, neurodegeneration therapy

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The Emerging Role of Central and Peripheral Immune Systems in Neurodegenerative Diseases

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