Microglia senescence occurs in both substantia nigra and ventral tegmental area
During aging humans lose midbrain dopamine neurons, but not all dopamine regions exhibit vulnerability to neurodegeneration. Microglia maintain tissue homeostasis and neuronal support, but microglia become senescent and likely lose some of their functional abilities. Since aging is the greatest risk...
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| Veröffentlicht in: | Glia 2020-11, Vol.68 (11), p.2228-2245 |
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| creator | Shaerzadeh, Fatemeh Phan, Leah Miller, Douglas Dacquel, Maxwell Hachmeister, William Hansen, Carissa Bechtle, Alexandra Tu, Duan Martcheva, Maia Foster, Thomas C. Kumar, Ashok Streit, Wolfgang J. Khoshbouei, Habibeh |
| description | During aging humans lose midbrain dopamine neurons, but not all dopamine regions exhibit vulnerability to neurodegeneration. Microglia maintain tissue homeostasis and neuronal support, but microglia become senescent and likely lose some of their functional abilities. Since aging is the greatest risk factor for Parkinson's disease, we hypothesized that aging‐related changes in microglia and neurons occur in the vulnerable substantia nigra pars compacta (SNc) but not the ventral tegmental area (VTA). We conducted stereological analyses to enumerate microglia and dopaminergic neurons in the SNc and VTA of 1‐, 6‐, 9‐, 18‐, and 24‐month‐old C57BL/J6 mice using sections double‐stained with tyrosine hydroxylase (TH) and Iba1. Both brain regions show an increase in microglia with aging, whereas numbers of TH+ cells show no significant change after 9 months of age in SNc and 6 months in VTA. Morphometric analyses reveal reduced microglial complexity and projection area while cell body size increases with aging. Contact sites between microglia and dopaminergic neurons in both regions increase with aging, suggesting increased microglial support/surveillance of dopamine neurons. To assess neurotrophin expression in dopaminergic neurons, BDNF and TH mRNA were quantified. Results show that the ratio of BDNF to TH decreases in the SNc, but not the VTA. Gait analysis indicates subtle, aging‐dependent changes in gait indices. In conclusion, increases in microglial cell number, ratio of microglia to dopamine neurons, and contact sites suggest that innate biological mechanisms compensate for the aging‐dependent decline in microglia morphological complexity (senescence) to ensure continued neuronal support in the SNc and VTA.
Main Points
Microglia in SNc and VTA do not exhibit regionally specialized morphology.
There is an age‐dependent increase in microglia with reduced structural complexity (senescence).
Interactions between microglia and dopamine neurons are intensified with aging. |
| doi_str_mv | 10.1002/glia.23834 |
| format | Article |
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Main Points
Microglia in SNc and VTA do not exhibit regionally specialized morphology.
There is an age‐dependent increase in microglia with reduced structural complexity (senescence).
Interactions between microglia and dopamine neurons are intensified with aging.</description><identifier>ISSN: 0894-1491</identifier><identifier>EISSN: 1098-1136</identifier><identifier>DOI: 10.1002/glia.23834</identifier><identifier>PMID: 32275335</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Aging ; aging‐dependent neurodegeneration ; Body size ; Brain-derived neurotrophic factor ; Cell body ; Cell number ; Cell size ; Complexity ; Dopamine ; dopamine neurons ; Dopamine receptors ; Gait ; Health risks ; Homeostasis ; Hydroxylase ; Mesencephalon ; Microglia ; microglia complexity ; Movement disorders ; mRNA ; Neurodegeneration ; Neurodegenerative diseases ; Neurons ; Parkinson's disease ; Risk analysis ; Risk factors ; Senescence ; stereological analyses ; Substantia nigra ; Tyrosine ; Tyrosine 3-monooxygenase ; tyrosine hydroxylase; microglia senescence ; Ventral tegmentum</subject><ispartof>Glia, 2020-11, Vol.68 (11), p.2228-2245</ispartof><rights>2020 Wiley Periodicals, Inc.</rights><rights>2020 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4484-18b94e87e436b943df732cabe2214f6316e4f0be56cf96c0083a60d98df5f9513</citedby><cites>FETCH-LOGICAL-c4484-18b94e87e436b943df732cabe2214f6316e4f0be56cf96c0083a60d98df5f9513</cites><orcidid>0000-0002-1533-8771 ; 0000-0003-4973-9052</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fglia.23834$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fglia.23834$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32275335$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shaerzadeh, Fatemeh</creatorcontrib><creatorcontrib>Phan, Leah</creatorcontrib><creatorcontrib>Miller, Douglas</creatorcontrib><creatorcontrib>Dacquel, Maxwell</creatorcontrib><creatorcontrib>Hachmeister, William</creatorcontrib><creatorcontrib>Hansen, Carissa</creatorcontrib><creatorcontrib>Bechtle, Alexandra</creatorcontrib><creatorcontrib>Tu, Duan</creatorcontrib><creatorcontrib>Martcheva, Maia</creatorcontrib><creatorcontrib>Foster, Thomas C.</creatorcontrib><creatorcontrib>Kumar, Ashok</creatorcontrib><creatorcontrib>Streit, Wolfgang J.</creatorcontrib><creatorcontrib>Khoshbouei, Habibeh</creatorcontrib><title>Microglia senescence occurs in both substantia nigra and ventral tegmental area</title><title>Glia</title><addtitle>Glia</addtitle><description>During aging humans lose midbrain dopamine neurons, but not all dopamine regions exhibit vulnerability to neurodegeneration. Microglia maintain tissue homeostasis and neuronal support, but microglia become senescent and likely lose some of their functional abilities. Since aging is the greatest risk factor for Parkinson's disease, we hypothesized that aging‐related changes in microglia and neurons occur in the vulnerable substantia nigra pars compacta (SNc) but not the ventral tegmental area (VTA). We conducted stereological analyses to enumerate microglia and dopaminergic neurons in the SNc and VTA of 1‐, 6‐, 9‐, 18‐, and 24‐month‐old C57BL/J6 mice using sections double‐stained with tyrosine hydroxylase (TH) and Iba1. Both brain regions show an increase in microglia with aging, whereas numbers of TH+ cells show no significant change after 9 months of age in SNc and 6 months in VTA. Morphometric analyses reveal reduced microglial complexity and projection area while cell body size increases with aging. Contact sites between microglia and dopaminergic neurons in both regions increase with aging, suggesting increased microglial support/surveillance of dopamine neurons. To assess neurotrophin expression in dopaminergic neurons, BDNF and TH mRNA were quantified. Results show that the ratio of BDNF to TH decreases in the SNc, but not the VTA. Gait analysis indicates subtle, aging‐dependent changes in gait indices. In conclusion, increases in microglial cell number, ratio of microglia to dopamine neurons, and contact sites suggest that innate biological mechanisms compensate for the aging‐dependent decline in microglia morphological complexity (senescence) to ensure continued neuronal support in the SNc and VTA.
Main Points
Microglia in SNc and VTA do not exhibit regionally specialized morphology.
There is an age‐dependent increase in microglia with reduced structural complexity (senescence).
Interactions between microglia and dopamine neurons are intensified with aging.</description><subject>Aging</subject><subject>aging‐dependent neurodegeneration</subject><subject>Body size</subject><subject>Brain-derived neurotrophic factor</subject><subject>Cell body</subject><subject>Cell number</subject><subject>Cell size</subject><subject>Complexity</subject><subject>Dopamine</subject><subject>dopamine neurons</subject><subject>Dopamine receptors</subject><subject>Gait</subject><subject>Health risks</subject><subject>Homeostasis</subject><subject>Hydroxylase</subject><subject>Mesencephalon</subject><subject>Microglia</subject><subject>microglia complexity</subject><subject>Movement disorders</subject><subject>mRNA</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative diseases</subject><subject>Neurons</subject><subject>Parkinson's disease</subject><subject>Risk analysis</subject><subject>Risk factors</subject><subject>Senescence</subject><subject>stereological analyses</subject><subject>Substantia nigra</subject><subject>Tyrosine</subject><subject>Tyrosine 3-monooxygenase</subject><subject>tyrosine hydroxylase; microglia senescence</subject><subject>Ventral tegmentum</subject><issn>0894-1491</issn><issn>1098-1136</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9kctKAzEUhoMoWi8bH0AG3IjQmtukmY1QipdCxY2uQyZzpo1MMzWZUXx7M04t6sJVTsjHx5__IHRK8IhgTK8WldUjyiTjO2hAcCaHhDCxiwZYZnxIeEYO0GEILxiTeBnvowNG6ThlLB2gxwdrfN0ZkgAOggFnIKmNaX1IrEvyulkmoc1Do10TIWcXXifaFckbuMbrKmlgsYpjnLQHfYz2Sl0FONmcR-j59uZpej-cP97NppP50HAuYyiZZxzkGDgTcWJFOWbU6BwoJbwUjAjgJc4hFabMhMFYMi1wkcmiTMssJewIXffedZuvoDB9GLX2dqX9h6q1Vb9fnF2qRf2mJEsFxZ3gYiPw9WsLoVErG39fVdpB3QYV-5SSSEFYRM__oC916138nqKcYx7LlJ3wsqdinyF4KLdhCFbdnlTXsvraU4TPfsbfot-LiQDpgXdbwcc_KnU3n0166SdoH536</recordid><startdate>202011</startdate><enddate>202011</enddate><creator>Shaerzadeh, Fatemeh</creator><creator>Phan, Leah</creator><creator>Miller, Douglas</creator><creator>Dacquel, Maxwell</creator><creator>Hachmeister, William</creator><creator>Hansen, Carissa</creator><creator>Bechtle, Alexandra</creator><creator>Tu, Duan</creator><creator>Martcheva, Maia</creator><creator>Foster, Thomas C.</creator><creator>Kumar, Ashok</creator><creator>Streit, Wolfgang J.</creator><creator>Khoshbouei, Habibeh</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1533-8771</orcidid><orcidid>https://orcid.org/0000-0003-4973-9052</orcidid></search><sort><creationdate>202011</creationdate><title>Microglia senescence occurs in both substantia nigra and ventral tegmental area</title><author>Shaerzadeh, Fatemeh ; Phan, Leah ; Miller, Douglas ; Dacquel, Maxwell ; Hachmeister, William ; Hansen, Carissa ; Bechtle, Alexandra ; Tu, Duan ; Martcheva, Maia ; Foster, Thomas C. ; Kumar, Ashok ; Streit, Wolfgang J. ; Khoshbouei, Habibeh</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4484-18b94e87e436b943df732cabe2214f6316e4f0be56cf96c0083a60d98df5f9513</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aging</topic><topic>aging‐dependent neurodegeneration</topic><topic>Body size</topic><topic>Brain-derived neurotrophic factor</topic><topic>Cell body</topic><topic>Cell number</topic><topic>Cell size</topic><topic>Complexity</topic><topic>Dopamine</topic><topic>dopamine neurons</topic><topic>Dopamine receptors</topic><topic>Gait</topic><topic>Health risks</topic><topic>Homeostasis</topic><topic>Hydroxylase</topic><topic>Mesencephalon</topic><topic>Microglia</topic><topic>microglia complexity</topic><topic>Movement disorders</topic><topic>mRNA</topic><topic>Neurodegeneration</topic><topic>Neurodegenerative diseases</topic><topic>Neurons</topic><topic>Parkinson's disease</topic><topic>Risk analysis</topic><topic>Risk factors</topic><topic>Senescence</topic><topic>stereological analyses</topic><topic>Substantia nigra</topic><topic>Tyrosine</topic><topic>Tyrosine 3-monooxygenase</topic><topic>tyrosine hydroxylase; 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Microglia maintain tissue homeostasis and neuronal support, but microglia become senescent and likely lose some of their functional abilities. Since aging is the greatest risk factor for Parkinson's disease, we hypothesized that aging‐related changes in microglia and neurons occur in the vulnerable substantia nigra pars compacta (SNc) but not the ventral tegmental area (VTA). We conducted stereological analyses to enumerate microglia and dopaminergic neurons in the SNc and VTA of 1‐, 6‐, 9‐, 18‐, and 24‐month‐old C57BL/J6 mice using sections double‐stained with tyrosine hydroxylase (TH) and Iba1. Both brain regions show an increase in microglia with aging, whereas numbers of TH+ cells show no significant change after 9 months of age in SNc and 6 months in VTA. Morphometric analyses reveal reduced microglial complexity and projection area while cell body size increases with aging. Contact sites between microglia and dopaminergic neurons in both regions increase with aging, suggesting increased microglial support/surveillance of dopamine neurons. To assess neurotrophin expression in dopaminergic neurons, BDNF and TH mRNA were quantified. Results show that the ratio of BDNF to TH decreases in the SNc, but not the VTA. Gait analysis indicates subtle, aging‐dependent changes in gait indices. In conclusion, increases in microglial cell number, ratio of microglia to dopamine neurons, and contact sites suggest that innate biological mechanisms compensate for the aging‐dependent decline in microglia morphological complexity (senescence) to ensure continued neuronal support in the SNc and VTA.
Main Points
Microglia in SNc and VTA do not exhibit regionally specialized morphology.
There is an age‐dependent increase in microglia with reduced structural complexity (senescence).
Interactions between microglia and dopamine neurons are intensified with aging.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32275335</pmid><doi>10.1002/glia.23834</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-1533-8771</orcidid><orcidid>https://orcid.org/0000-0003-4973-9052</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | Aging aging‐dependent neurodegeneration Body size Brain-derived neurotrophic factor Cell body Cell number Cell size Complexity Dopamine dopamine neurons Dopamine receptors Gait Health risks Homeostasis Hydroxylase Mesencephalon Microglia microglia complexity Movement disorders mRNA Neurodegeneration Neurodegenerative diseases Neurons Parkinson's disease Risk analysis Risk factors Senescence stereological analyses Substantia nigra Tyrosine Tyrosine 3-monooxygenase tyrosine hydroxylase microglia senescence Ventral tegmentum |
| title | Microglia senescence occurs in both substantia nigra and ventral tegmental area |
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