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Gut-Brain Axis of Neurodegenerative Disease
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Gut-Brain Axis of Neurodegenerative Disease

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Neurobiology".

Deadline for manuscript submissions: closed (20 March 2023) | Viewed by 36479

Special Issue Editors

Dr. Alejo J Nevado-Holgado

E-Mail Website
Guest Editor
Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UK
Interests: artificial intelligence; neural networks; big data; electronic health records; drug discovery; multi-omics; genomics; Alzheimer’s disease
Dr. Liu Shi

E-Mail Website
Guest Editor
Department of Psychiatry, University of Oxford Medical Sciences Division, Oxford OX3 9DU, UK
Interests: biomarkers; machine learning; genomics; proteomics; metabolomics; multi-omics; neurodegenerative disease; Alzheimer’s disease; iPSC cells; drug discovery

Special Issue Information

Dear Colleagues,

There is increasing evidence showing that the status of the intestinal environment is closely connected with the function of the central nervous system (CNS). This so-called “gut–brain axis” facilitates the bidirectional communication between the central and enteric nervous and endocrine systems, as well as the regulation of immune responses in the gut and brain. All aspects of this system appear to be heavily influenced by the activity of intestinal microbes.

This Special Issue is focused on the gut–brain axis of neurodegenerative disease. It will include original articles and reviews focusing on aspects related to the gut–brain axis in neurodegenerative disease, including, but are not limited to, Alzheimer’s disease, Parkinson’s disease, and amyotrophic lateral sclerosis.

Dr. Alejo J Nevado-Holgado
Dr. Liu Shi
Guest Editors

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Keywords

  • Alzheimer’s disease
  • Parkinson's disease
  • enteric nervous system
  • microbiome
  • metabolomics
  • biomarkers
  • inflammation
  • gut–brain axis
  • neurodegenerative diseases

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Published Papers (7 papers)

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Research

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24 pages, 46297 KiB  
Article
Effects of Probiotics on Colitis-Induced Exacerbation of Alzheimer’s Disease in AppNL-G-F Mice
by Bijayani Sahu, Lauren M. Johnson, Mona Sohrabi, Anastasia A. Usatii, Rachel M. J. Craig, Joshua B. Kaelberer, Sathiya Priya Chandrasekaran, Harpreet Kaur, Suba Nookala and Colin K. Combs
Int. J. Mol. Sci. 2023, 24(14), 11551; https://doi.org/10.3390/ijms241411551 - 17 Jul 2023
Cited by 2 | Viewed by 2445
Abstract
Alzheimer’s disease (AD) is characterized by progressive cognitive decline and is a leading cause of death in the United States. Neuroinflammation has been implicated in the progression of AD, and several recent studies suggest that peripheral immune dysfunction may influence the disease. Continuing [...] Read more.
Alzheimer’s disease (AD) is characterized by progressive cognitive decline and is a leading cause of death in the United States. Neuroinflammation has been implicated in the progression of AD, and several recent studies suggest that peripheral immune dysfunction may influence the disease. Continuing evidence indicates that intestinal dysbiosis is an attribute of AD, and inflammatory bowel disease (IBD) has been shown to aggravate cognitive impairment. Previously, we separately demonstrated that an IBD-like condition exacerbates AD-related changes in the brains of the AppNL-G-F mouse model of AD, while probiotic intervention has an attenuating effect. In this study, we investigated the combination of a dietary probiotic and an IBD-like condition for effects on the brains of mice. Male C57BL/6 wild type (WT) and AppNL-G-F mice were randomly divided into four groups: vehicle control, oral probiotic, dextran sulfate sodium (DSS), and DSS given with probiotics. As anticipated, probiotic treatment attenuated the DSS-induced colitis disease activity index in WT and AppNL-G-F mice. Although probiotic feeding significantly attenuated the DSS-mediated increase in WT colonic lipocalin levels, it was less protective in the AppNL-G-F DSS-treated group. In parallel with the intestinal changes, combined probiotic and DSS treatment increased microglial, neutrophil elastase, and 5hmC immunoreactivity while decreasing c-Fos staining compared to DSS treatment alone in the brains of WT mice. Although less abundant, probiotic combined with DSS treatment demonstrated a few similar changes in AppNL-G-F brains with increased microglial and decreased c-Fos immunoreactivity in addition to a slight increase in Aβ plaque staining. Both probiotic and DSS treatment also altered the levels of several cytokines in WT and AppNL-G-F brains, with a unique increase in the levels of TNFα and IL-2 being observed in only AppNL-G-F mice following combined DSS and probiotic treatment. Our data indicate that, while dietary probiotic intervention provides protection against the colitis-like condition, it also influences numerous glial, cytokine, and neuronal changes in the brain that may regulate brain function and the progression of AD. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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14 pages, 2904 KiB  
Article
Neuroprotection by Abdominal Ultrasound in Lipopolysaccharide-Induced Systemic Inflammation
by Wen-Shin Song, Tai-Ho Hung, Shing-Hwa Liu, Yin-Ting Zheng, Hsin-Mei Lin and Feng-Yi Yang
Int. J. Mol. Sci. 2023, 24(11), 9329; https://doi.org/10.3390/ijms24119329 - 26 May 2023
Cited by 3 | Viewed by 1870
Abstract
Systemic inflammation is associated with intestinal inflammation and neuroinflammation by imbalancing the gut–brain axis. Low-intensity pulsed ultrasound (LIPUS) has neuroprotective and anti-inflammatory effects. This study explored LIPUS’s neuroprotective effects against lipopolysaccharide (LPS)-induced neuroinflammation through transabdominal stimulation. Male C57BL/6J mice were intraperitoneally injected with [...] Read more.
Systemic inflammation is associated with intestinal inflammation and neuroinflammation by imbalancing the gut–brain axis. Low-intensity pulsed ultrasound (LIPUS) has neuroprotective and anti-inflammatory effects. This study explored LIPUS’s neuroprotective effects against lipopolysaccharide (LPS)-induced neuroinflammation through transabdominal stimulation. Male C57BL/6J mice were intraperitoneally injected with LPS (0.75 mg/kg) daily for seven days, and abdominal LIPUS was applied to the abdominal area for 15 min/day during the last six days. One day after the last LIPUS treatment, biological samples were collected for microscopic and immunohistochemical analysis. Histological examination showed that LPS administration leads to tissue damage in the colon and brain. Transabdominal LIPUS stimulation attenuated colonic damage, reducing histological score, colonic muscle thickness, and villi shortening. Furthermore, abdominal LIPUS reduced hippocampal microglial activation (labeled by ionized calcium-binding adaptor molecule-1 [Iba-1]) and neuronal cell loss (labeled by microtubule-associated protein 2 [MAP2]). Moreover, abdominal LIPUS attenuated the number of apoptotic cells in the hippocampus and cortex. Altogether, our results indicate that abdominal LIPUS stimulation attenuates LPS-induced colonic inflammation and neuroinflammation. These findings provide new insights into the treatment strategy for neuroinflammation-related brain disorders and may facilitate method development through the gut–brain axis pathway. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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Review

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21 pages, 474 KiB  
Review
From the Gut to the Brain: The Role of Enteric Glial Cells and Their Involvement in the Pathogenesis of Parkinson’s Disease
by Alba Montalbán-Rodríguez, Raquel Abalo and Laura López-Gómez
Int. J. Mol. Sci. 2024, 25(2), 1294; https://doi.org/10.3390/ijms25021294 - 20 Jan 2024
Cited by 5 | Viewed by 3657
Abstract
The brain–gut axis has been identified as an important contributor to the physiopathology of Parkinson’s disease. In this pathology, inflammation is thought to be driven by the damage caused by aggregation of α-synuclein in the brain. Interestingly, the Braak’s theory proposes that α-synuclein [...] Read more.
The brain–gut axis has been identified as an important contributor to the physiopathology of Parkinson’s disease. In this pathology, inflammation is thought to be driven by the damage caused by aggregation of α-synuclein in the brain. Interestingly, the Braak’s theory proposes that α-synuclein misfolding may originate in the gut and spread in a “prion-like” manner through the vagus nerve into the central nervous system. In the enteric nervous system, enteric glial cells are the most abundant cellular component. Several studies have evaluated their role in Parkinson’s disease. Using samples obtained from patients, cell cultures, or animal models, the studies with specific antibodies to label enteric glial cells (GFAP, Sox-10, and S100β) seem to indicate that activation and reactive gliosis are associated to the neurodegeneration produced by Parkinson’s disease in the enteric nervous system. Of interest, Toll-like receptors, which are expressed on enteric glial cells, participate in the triggering of immune/inflammatory responses, in the maintenance of intestinal barrier integrity and in the configuration of gut microbiota; thus, these receptors might contribute to Parkinson’s disease. External factors like stress also seem to be relevant in its pathogenesis. Some authors have studied ways to reverse changes in EGCs with interventions such as administration of Tryptophan-2,3-dioxygenase inhibitors, nutraceuticals, or physical exercise. Some researchers point out that beyond being activated during the disease, enteric glial cells may contribute to the development of synucleinopathies. Thus, it is still necessary to further study these cells and their role in Parkinson’s disease. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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21 pages, 1599 KiB  
Review
Gut Microbiota and Alzheimer’s Disease: How to Study and Apply Their Relationship
by Ngoc Minh Nguyen, Jungsook Cho and Choongho Lee
Int. J. Mol. Sci. 2023, 24(4), 4047; https://doi.org/10.3390/ijms24044047 - 17 Feb 2023
Cited by 18 | Viewed by 7414
Abstract
Gut microbiota (GM), the microorganisms in the gastrointestinal tract, contribute to the regulation of brain homeostasis through bidirectional communication between the gut and the brain. GM disturbance has been discovered to be related to various neurological disorders, including Alzheimer’s disease (AD). Recently, the [...] Read more.
Gut microbiota (GM), the microorganisms in the gastrointestinal tract, contribute to the regulation of brain homeostasis through bidirectional communication between the gut and the brain. GM disturbance has been discovered to be related to various neurological disorders, including Alzheimer’s disease (AD). Recently, the microbiota-gut-brain axis (MGBA) has emerged as an enticing subject not only to understand AD pathology but also to provide novel therapeutic strategies for AD. In this review, the general concept of the MGBA and its impacts on the development and progression of AD are described. Then, diverse experimental approaches for studying the roles of GM in AD pathogenesis are presented. Finally, the MGBA-based therapeutic strategies for AD are discussed. This review provides concise guidance for those who wish to obtain a conceptual and methodological understanding of the GM and AD relationship with an emphasis on its practical application. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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24 pages, 5257 KiB  
Review
What Are the Key Gut Microbiota Involved in Neurological Diseases? A Systematic Review
by Bruno Bonnechère, Najaf Amin and Cornelia van Duijn
Int. J. Mol. Sci. 2022, 23(22), 13665; https://doi.org/10.3390/ijms232213665 - 8 Nov 2022
Cited by 22 | Viewed by 5182
Abstract
There is a growing body of evidence highlighting there are significant changes in the gut microbiota composition and relative abundance in various neurological disorders. We performed a systematic review of the different microbiota altered in a wide range of neurological disorders (Alzheimer’s disease [...] Read more.
There is a growing body of evidence highlighting there are significant changes in the gut microbiota composition and relative abundance in various neurological disorders. We performed a systematic review of the different microbiota altered in a wide range of neurological disorders (Alzheimer’s disease (AD), Parkinson’s disease (PD), multiple sclerosis (MS), amyotrophic lateral sclerosis, and stroke). Fifty-two studies were included representing 5496 patients. At the genus level, the most frequently involved microbiota are Akkermansia, Faecalibacterium, and Prevotella. The overlap between the pathologies was strongest for MS and PD, sharing eight genera (Akkermansia, Butyricicoccus, Bifidobacterium, Coprococcus, Dorea, Faecalibacterium, Parabacteroides, and Prevotella) and PD and stroke, sharing six genera (Enterococcus, Faecalibacterium, Lactobacillus, Parabacteroides, Prevotella, and Roseburia). The identification signatures overlapping for AD, PD, and MS raise the question of whether these reflect a common etiology or rather common consequence of these diseases. The interpretation is hampered by the low number and low power for AD, ALS, and stroke with ample opportunity for false positive and false negative findings. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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49 pages, 5237 KiB  
Review
The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment
by Angelica Varesi, Lucrezia Irene Maria Campagnoli, Foroogh Fahmideh, Elisa Pierella, Marcello Romeo, Giovanni Ricevuti, Marchesi Nicoletta, Salvatore Chirumbolo and Alessia Pascale
Int. J. Mol. Sci. 2022, 23(20), 12289; https://doi.org/10.3390/ijms232012289 - 14 Oct 2022
Cited by 34 | Viewed by 10308
Abstract
The bidirectional interaction between the gut microbiota (GM) and the Central Nervous System, the so-called gut microbiota brain axis (GMBA), deeply affects brain function and has an important impact on the development of neurodegenerative diseases. In Parkinson’s disease (PD), gastrointestinal symptoms often precede [...] Read more.
The bidirectional interaction between the gut microbiota (GM) and the Central Nervous System, the so-called gut microbiota brain axis (GMBA), deeply affects brain function and has an important impact on the development of neurodegenerative diseases. In Parkinson’s disease (PD), gastrointestinal symptoms often precede the onset of motor and non-motor manifestations, and alterations in the GM composition accompany disease pathogenesis. Several studies have been conducted to unravel the role of dysbiosis and intestinal permeability in PD onset and progression, but the therapeutic and diagnostic applications of GM modifying approaches remain to be fully elucidated. After a brief introduction on the involvement of GMBA in the disease, we present evidence for GM alterations and leaky gut in PD patients. According to these data, we then review the potential of GM-based signatures to serve as disease biomarkers and we highlight the emerging role of probiotics, prebiotics, antibiotics, dietary interventions, and fecal microbiota transplantation as supportive therapeutic approaches in PD. Finally, we analyze the mutual influence between commonly prescribed PD medications and gut-microbiota, and we offer insights on the involvement also of nasal and oral microbiota in PD pathology, thus providing a comprehensive and up-to-date overview on the role of microbial features in disease diagnosis and treatment. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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25 pages, 2179 KiB  
Review
Impact of Nutrition, Microbiota Transplant and Weight Loss Surgery on Dopaminergic Alterations in Parkinson’s Disease and Obesity
by Sevag Hamamah, Andras Hajnal and Mihai Covasa
Int. J. Mol. Sci. 2022, 23(14), 7503; https://doi.org/10.3390/ijms23147503 - 6 Jul 2022
Cited by 11 | Viewed by 4195
Abstract
Parkinson’s disease (PD), the second most common neurodegenerative disorder worldwide, is characterized by dopaminergic neuron degeneration and α-synuclein aggregation in the substantia nigra pars compacta of the midbrain. Emerging evidence has shown that dietary intake affects the microbial composition in the gut, which [...] Read more.
Parkinson’s disease (PD), the second most common neurodegenerative disorder worldwide, is characterized by dopaminergic neuron degeneration and α-synuclein aggregation in the substantia nigra pars compacta of the midbrain. Emerging evidence has shown that dietary intake affects the microbial composition in the gut, which in turn contributes to, or protects against, the degeneration of dopaminergic neurons in affected regions of the brain. More specifically, the Mediterranean diet and Western diet, composed of varying amounts of proteins, carbohydrates, and fats, exert contrasting effects on PD pathophysiology via alterations in the gut microbiota and dopamine levels. Interestingly, the negative changes in the gut microbiota of patients with PD parallel changes that are seen in individuals that consume a Western diet, and are opposite to those that adhere to a Mediterranean diet. In this review, we first examine the role of prominent food groups on dopamine bioavailability, how they modulate the composition and function of the gut microbiota and the subsequent effects on PD and obesity pathophysiology. We then highlight evidence on how microbiota transplant and weight loss surgery can be used as therapeutic tools to restore dopaminergic deficits through optimizing gut microbial composition. In the process, we revisit dietary metabolites and their role in therapeutic approaches involving dopaminergic pathways. Overall, understanding the role of nutrition on dopamine bioavailability and gut microbiota in dopamine-related pathologies such as PD will help develop more precise therapeutic targets to rescue dopaminergic deficits in neurologic and metabolic disorders. Full article
(This article belongs to the Special Issue Gut-Brain Axis of Neurodegenerative Disease)
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