The Triple Alliance: Microbiome, Mitochondria, and Metabolites in the Context of Age-Related Cognitive Decline and Alzheimer’s Disease
Abstract Alzheimer’s disease (AD) is a progressive, age-related neurodegenerative disorder that affects a large proportion of the older population. It currently lacks effective treatments, placing a heavy burden on patients, families, health care systems, and society. This is mainly due to our limit...
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creator | Prajapati, Santosh K Shah, Ria Alford, Nicholas Mishra, Sidharth P Jain, Shalini Hansen, Barbara Sanberg, Paul Molina, Anthony J A Yadav, Hariom |
description | Abstract
Alzheimer’s disease (AD) is a progressive, age-related neurodegenerative disorder that affects a large proportion of the older population. It currently lacks effective treatments, placing a heavy burden on patients, families, health care systems, and society. This is mainly due to our limited comprehension of the pathophysiology of AD progression, as well as the lack of effective drug targets and intervention timing to address the underlying pathology. AD is a multifactorial condition, and emerging evidence suggests that abnormalities in the gut microbiota play a significant role as environmental and multifaceted contributors to AD, although the exact mechanisms are yet to be fully explored. Changes in the composition of microbiota influence host neuronal health through their metabolites. These metabolites regulate intestinal epithelia, blood-brain barrier permeability, and neuroinflammation by affecting mitochondrial function. The decline in the proportion of beneficial microbes and their essential metabolites during aging and AD is directly linked to poor mitochondrial function, although the specific mechanisms remain unclear. In this review, we discuss recent developments in understanding the impact of the microbiome and its metabolites on various cell types, their influence on the integrity of the gut and blood-brain barriers, systemic and brain inflammation, and cell-specific effects in AD pathology. This information is expected to pave the way for a new understanding of the interactions between microbiota and mitochondria in AD, providing a foundation for the development of novel treatments for AD. |
doi_str_mv | 10.1093/gerona/glad226 |
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Alzheimer’s disease (AD) is a progressive, age-related neurodegenerative disorder that affects a large proportion of the older population. It currently lacks effective treatments, placing a heavy burden on patients, families, health care systems, and society. This is mainly due to our limited comprehension of the pathophysiology of AD progression, as well as the lack of effective drug targets and intervention timing to address the underlying pathology. AD is a multifactorial condition, and emerging evidence suggests that abnormalities in the gut microbiota play a significant role as environmental and multifaceted contributors to AD, although the exact mechanisms are yet to be fully explored. Changes in the composition of microbiota influence host neuronal health through their metabolites. These metabolites regulate intestinal epithelia, blood-brain barrier permeability, and neuroinflammation by affecting mitochondrial function. The decline in the proportion of beneficial microbes and their essential metabolites during aging and AD is directly linked to poor mitochondrial function, although the specific mechanisms remain unclear. In this review, we discuss recent developments in understanding the impact of the microbiome and its metabolites on various cell types, their influence on the integrity of the gut and blood-brain barriers, systemic and brain inflammation, and cell-specific effects in AD pathology. This information is expected to pave the way for a new understanding of the interactions between microbiota and mitochondria in AD, providing a foundation for the development of novel treatments for AD.</description><identifier>ISSN: 1079-5006</identifier><identifier>ISSN: 1758-535X</identifier><identifier>EISSN: 1758-535X</identifier><identifier>DOI: 10.1093/gerona/glad226</identifier><identifier>PMID: 37738628</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Aging ; Alzheimer Disease ; Alzheimer's disease ; Blood-brain barrier ; Brain ; Cognitive ability ; Cognitive Dysfunction ; Digestive system ; Gastrointestinal Microbiome ; Gastrointestinal tract ; Humans ; Inflammation ; Intestinal microflora ; Membrane permeability ; Metabolites ; Microbiomes ; Microbiota ; Mitochondria ; Nerve Degeneration ; Neurodegenerative diseases ; Pathology ; Pathophysiology ; THE JOURNAL OF GERONTOLOGY: Biological Sciences ; Therapeutic targets</subject><ispartof>The journals of gerontology. Series A, Biological sciences and medical sciences, 2023-12, Vol.78 (12), p.2187-2202</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of The Gerontological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of The Gerontological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>Copyright Oxford University Press Dec 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c413t-7d7ab6f90c459404a5f8193e3e98b2306c92e01454ffd7fcf41076b1ce2520703</citedby><cites>FETCH-LOGICAL-c413t-7d7ab6f90c459404a5f8193e3e98b2306c92e01454ffd7fcf41076b1ce2520703</cites><orcidid>0000-0003-4504-1597</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37738628$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Duque, Gustavo</contributor><creatorcontrib>Prajapati, Santosh K</creatorcontrib><creatorcontrib>Shah, Ria</creatorcontrib><creatorcontrib>Alford, Nicholas</creatorcontrib><creatorcontrib>Mishra, Sidharth P</creatorcontrib><creatorcontrib>Jain, Shalini</creatorcontrib><creatorcontrib>Hansen, Barbara</creatorcontrib><creatorcontrib>Sanberg, Paul</creatorcontrib><creatorcontrib>Molina, Anthony J A</creatorcontrib><creatorcontrib>Yadav, Hariom</creatorcontrib><title>The Triple Alliance: Microbiome, Mitochondria, and Metabolites in the Context of Age-Related Cognitive Decline and Alzheimer’s Disease</title><title>The journals of gerontology. Series A, Biological sciences and medical sciences</title><addtitle>J Gerontol A Biol Sci Med Sci</addtitle><description>Abstract
Alzheimer’s disease (AD) is a progressive, age-related neurodegenerative disorder that affects a large proportion of the older population. It currently lacks effective treatments, placing a heavy burden on patients, families, health care systems, and society. This is mainly due to our limited comprehension of the pathophysiology of AD progression, as well as the lack of effective drug targets and intervention timing to address the underlying pathology. AD is a multifactorial condition, and emerging evidence suggests that abnormalities in the gut microbiota play a significant role as environmental and multifaceted contributors to AD, although the exact mechanisms are yet to be fully explored. Changes in the composition of microbiota influence host neuronal health through their metabolites. These metabolites regulate intestinal epithelia, blood-brain barrier permeability, and neuroinflammation by affecting mitochondrial function. The decline in the proportion of beneficial microbes and their essential metabolites during aging and AD is directly linked to poor mitochondrial function, although the specific mechanisms remain unclear. In this review, we discuss recent developments in understanding the impact of the microbiome and its metabolites on various cell types, their influence on the integrity of the gut and blood-brain barriers, systemic and brain inflammation, and cell-specific effects in AD pathology. This information is expected to pave the way for a new understanding of the interactions between microbiota and mitochondria in AD, providing a foundation for the development of novel treatments for AD.</description><subject>Aging</subject><subject>Alzheimer Disease</subject><subject>Alzheimer's disease</subject><subject>Blood-brain barrier</subject><subject>Brain</subject><subject>Cognitive ability</subject><subject>Cognitive Dysfunction</subject><subject>Digestive system</subject><subject>Gastrointestinal Microbiome</subject><subject>Gastrointestinal tract</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Intestinal microflora</subject><subject>Membrane permeability</subject><subject>Metabolites</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Mitochondria</subject><subject>Nerve Degeneration</subject><subject>Neurodegenerative diseases</subject><subject>Pathology</subject><subject>Pathophysiology</subject><subject>THE JOURNAL OF GERONTOLOGY: Biological Sciences</subject><subject>Therapeutic targets</subject><issn>1079-5006</issn><issn>1758-535X</issn><issn>1758-535X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc9u1DAQxiMEoqVw5YgscQGpaf0nThwuaLWlFKkVElokbpbjTLKuHHuxnQo4ceQVeD2epG53qYALc5mR_ZtPM_MVxVOCjwhu2fEIwTt1PFrVU1rfK_ZJw0XJGf90P9e4aUuOcb1XPIrxEt8Epw-LPdY0TNRU7Bc_VmtAq2A2FtDCWqOchlfowujgO-MnOMx18nrtXR-MOkTK9egCkuq8NQkiMg6lrLD0LsGXhPyAFiOUH8CqBH1-Hp1J5grQCWhrHNz2L-y3NZgJwq_vPyM6MRFUhMfFg0HZCE92-aD4ePpmtTwrz9-_fbdcnJe6IiyVTd-orh5arCveVrhSfBCkZcCgFR1luNYtBUwqXg1D3wx6qPIR6o5ooJziBrOD4vVWdzN3E_QaXArKyk0wkwpfpVdG_v3jzFqO_koSXLe0YiIrvNgpBP95hpjkZKIGa5UDP0dJRS0IEQ3hGX3-D3rp5-DyfpK22RdBKWaZOtpS-egxBhjupiFY3rgsty7Lncu54dmfO9zhv23NwMst4OfN_8SuAQJltW0</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Prajapati, Santosh K</creator><creator>Shah, Ria</creator><creator>Alford, Nicholas</creator><creator>Mishra, Sidharth P</creator><creator>Jain, Shalini</creator><creator>Hansen, Barbara</creator><creator>Sanberg, Paul</creator><creator>Molina, Anthony J A</creator><creator>Yadav, Hariom</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4504-1597</orcidid></search><sort><creationdate>20231201</creationdate><title>The Triple Alliance: Microbiome, Mitochondria, and Metabolites in the Context of Age-Related Cognitive Decline and Alzheimer’s Disease</title><author>Prajapati, Santosh K ; Shah, Ria ; Alford, Nicholas ; Mishra, Sidharth P ; Jain, Shalini ; Hansen, Barbara ; Sanberg, Paul ; Molina, Anthony J A ; Yadav, Hariom</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c413t-7d7ab6f90c459404a5f8193e3e98b2306c92e01454ffd7fcf41076b1ce2520703</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Aging</topic><topic>Alzheimer Disease</topic><topic>Alzheimer's disease</topic><topic>Blood-brain barrier</topic><topic>Brain</topic><topic>Cognitive ability</topic><topic>Cognitive Dysfunction</topic><topic>Digestive system</topic><topic>Gastrointestinal Microbiome</topic><topic>Gastrointestinal tract</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Intestinal microflora</topic><topic>Membrane permeability</topic><topic>Metabolites</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Mitochondria</topic><topic>Nerve Degeneration</topic><topic>Neurodegenerative diseases</topic><topic>Pathology</topic><topic>Pathophysiology</topic><topic>THE JOURNAL OF GERONTOLOGY: Biological Sciences</topic><topic>Therapeutic targets</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Prajapati, Santosh K</creatorcontrib><creatorcontrib>Shah, Ria</creatorcontrib><creatorcontrib>Alford, Nicholas</creatorcontrib><creatorcontrib>Mishra, Sidharth P</creatorcontrib><creatorcontrib>Jain, Shalini</creatorcontrib><creatorcontrib>Hansen, Barbara</creatorcontrib><creatorcontrib>Sanberg, Paul</creatorcontrib><creatorcontrib>Molina, Anthony J A</creatorcontrib><creatorcontrib>Yadav, Hariom</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The journals of gerontology. 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Alzheimer’s disease (AD) is a progressive, age-related neurodegenerative disorder that affects a large proportion of the older population. It currently lacks effective treatments, placing a heavy burden on patients, families, health care systems, and society. This is mainly due to our limited comprehension of the pathophysiology of AD progression, as well as the lack of effective drug targets and intervention timing to address the underlying pathology. AD is a multifactorial condition, and emerging evidence suggests that abnormalities in the gut microbiota play a significant role as environmental and multifaceted contributors to AD, although the exact mechanisms are yet to be fully explored. Changes in the composition of microbiota influence host neuronal health through their metabolites. These metabolites regulate intestinal epithelia, blood-brain barrier permeability, and neuroinflammation by affecting mitochondrial function. The decline in the proportion of beneficial microbes and their essential metabolites during aging and AD is directly linked to poor mitochondrial function, although the specific mechanisms remain unclear. In this review, we discuss recent developments in understanding the impact of the microbiome and its metabolites on various cell types, their influence on the integrity of the gut and blood-brain barriers, systemic and brain inflammation, and cell-specific effects in AD pathology. This information is expected to pave the way for a new understanding of the interactions between microbiota and mitochondria in AD, providing a foundation for the development of novel treatments for AD.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>37738628</pmid><doi>10.1093/gerona/glad226</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-4504-1597</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aging Alzheimer Disease Alzheimer's disease Blood-brain barrier Brain Cognitive ability Cognitive Dysfunction Digestive system Gastrointestinal Microbiome Gastrointestinal tract Humans Inflammation Intestinal microflora Membrane permeability Metabolites Microbiomes Microbiota Mitochondria Nerve Degeneration Neurodegenerative diseases Pathology Pathophysiology THE JOURNAL OF GERONTOLOGY: Biological Sciences Therapeutic targets |
title | The Triple Alliance: Microbiome, Mitochondria, and Metabolites in the Context of Age-Related Cognitive Decline and Alzheimer’s Disease |
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