In Vivo Assessment of Astrocyte Reactivity in Patients with Progressive Supranuclear Palsy
Objective Although astrocytic pathology is a pathological hallmark of progressive supranuclear palsy (PSP), its pathophysiological role remains unclear. This study aimed to assess astrocyte reactivity in vivo in patients with PSP. Furthermore, we investigated alterations in brain lactate levels and...
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| Veröffentlicht in: | Annals of neurology 2024-08, Vol.96 (2), p.247-261 |
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| creator | Hirata, Kosei Matsuoka, Kiwamu Tagai, Kenji Endo, Hironobu Tatebe, Harutsugu Ono, Maiko Kokubo, Naomi Kataoka, Yuko Oyama, Asaka Shinotoh, Hitoshi Takahata, Keisuke Obata, Takayuki Dehghani, Masoumeh Near, Jamie Kawamura, Kazunori Zhang, Ming‐Rong Shimada, Hitoshi Shimizu, Hiroshi Kakita, Akiyoshi Yokota, Takanori Tokuda, Takahiko Higuchi, Makoto Takado, Yuhei |
| description | Objective
Although astrocytic pathology is a pathological hallmark of progressive supranuclear palsy (PSP), its pathophysiological role remains unclear. This study aimed to assess astrocyte reactivity in vivo in patients with PSP. Furthermore, we investigated alterations in brain lactate levels and their relationship with astrocyte reactivity.
Methods
We included 30 patients with PSP‐Richardson syndrome and 30 healthy controls; in patients, tau deposition was confirmed through 18F‐florzolotau positron emission tomography. Myo‐inositol, an astroglial marker, and lactate were quantified in the anterior cingulate cortex through magnetic resonance spectroscopy. We measured plasma biomarkers, including glial fibrillary acidic protein as another astrocytic marker. The anterior cingulate cortex was histologically assessed in postmortem samples of another 3 patients with PSP with comparable disease durations.
Results
The levels of myo‐inositol and plasma glial fibrillary acidic protein were significantly higher in patients than those in healthy controls (p |
| doi_str_mv | 10.1002/ana.26962 |
| format | Article |
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Although astrocytic pathology is a pathological hallmark of progressive supranuclear palsy (PSP), its pathophysiological role remains unclear. This study aimed to assess astrocyte reactivity in vivo in patients with PSP. Furthermore, we investigated alterations in brain lactate levels and their relationship with astrocyte reactivity.
Methods
We included 30 patients with PSP‐Richardson syndrome and 30 healthy controls; in patients, tau deposition was confirmed through 18F‐florzolotau positron emission tomography. Myo‐inositol, an astroglial marker, and lactate were quantified in the anterior cingulate cortex through magnetic resonance spectroscopy. We measured plasma biomarkers, including glial fibrillary acidic protein as another astrocytic marker. The anterior cingulate cortex was histologically assessed in postmortem samples of another 3 patients with PSP with comparable disease durations.
Results
The levels of myo‐inositol and plasma glial fibrillary acidic protein were significantly higher in patients than those in healthy controls (p < 0.05); these increases were significantly associated with PSP rating scale and cognitive function scores (p < 0.05). The lactate level was high in patients, and correlated significantly with high myo‐inositol levels. Histological analysis of the anterior cingulate cortex in patients revealed reactive astrocytes, despite mild tau deposition, and no marked synaptic loss.
Interpretation
We discovered high levels of astrocyte biomarkers in patients with PSP, suggesting astrocyte reactivity. The association between myo‐inositol and lactate levels suggests a link between reactive astrocytes and brain energy metabolism changes. Our results indicate that astrocyte reactivity in the anterior cingulate cortex precedes pronounced tau pathology and neurodegenerative processes in that region, and affects brain function in PSP. ANN NEUROL 2024;96:247–261</description><identifier>ISSN: 0364-5134</identifier><identifier>ISSN: 1531-8249</identifier><identifier>EISSN: 1531-8249</identifier><identifier>DOI: 10.1002/ana.26962</identifier><identifier>PMID: 38771066</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Astrocytes ; Biomarkers ; Brain ; Cognitive ability ; Cortex (cingulate) ; Deposition ; Disease control ; Energy metabolism ; Glial fibrillary acidic protein ; In vivo methods and tests ; Inositol ; Inositols ; Lactic acid ; Magnetic resonance spectroscopy ; Pathology ; Positron emission ; Positron emission tomography ; Progressive supranuclear palsy ; Proteins ; Tau protein</subject><ispartof>Annals of neurology, 2024-08, Vol.96 (2), p.247-261</ispartof><rights>2024 The Authors. published by Wiley Periodicals LLC on behalf of American Neurological Association.</rights><rights>2024 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3482-101f60420dea95e3094e5e3ea5ed4db304b0e5f1ac5f8e9f18ef693c546346303</cites><orcidid>0009-0007-9027-9277 ; 0000-0001-7484-8424 ; 0000-0002-5131-1533</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%2Fana.26962$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fana.26962$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>315,781,785,1418,27928,27929,45578,45579</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38771066$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hirata, Kosei</creatorcontrib><creatorcontrib>Matsuoka, Kiwamu</creatorcontrib><creatorcontrib>Tagai, Kenji</creatorcontrib><creatorcontrib>Endo, Hironobu</creatorcontrib><creatorcontrib>Tatebe, Harutsugu</creatorcontrib><creatorcontrib>Ono, Maiko</creatorcontrib><creatorcontrib>Kokubo, Naomi</creatorcontrib><creatorcontrib>Kataoka, Yuko</creatorcontrib><creatorcontrib>Oyama, Asaka</creatorcontrib><creatorcontrib>Shinotoh, Hitoshi</creatorcontrib><creatorcontrib>Takahata, Keisuke</creatorcontrib><creatorcontrib>Obata, Takayuki</creatorcontrib><creatorcontrib>Dehghani, Masoumeh</creatorcontrib><creatorcontrib>Near, Jamie</creatorcontrib><creatorcontrib>Kawamura, Kazunori</creatorcontrib><creatorcontrib>Zhang, Ming‐Rong</creatorcontrib><creatorcontrib>Shimada, Hitoshi</creatorcontrib><creatorcontrib>Shimizu, Hiroshi</creatorcontrib><creatorcontrib>Kakita, Akiyoshi</creatorcontrib><creatorcontrib>Yokota, Takanori</creatorcontrib><creatorcontrib>Tokuda, Takahiko</creatorcontrib><creatorcontrib>Higuchi, Makoto</creatorcontrib><creatorcontrib>Takado, Yuhei</creatorcontrib><title>In Vivo Assessment of Astrocyte Reactivity in Patients with Progressive Supranuclear Palsy</title><title>Annals of neurology</title><addtitle>Ann Neurol</addtitle><description>Objective
Although astrocytic pathology is a pathological hallmark of progressive supranuclear palsy (PSP), its pathophysiological role remains unclear. This study aimed to assess astrocyte reactivity in vivo in patients with PSP. Furthermore, we investigated alterations in brain lactate levels and their relationship with astrocyte reactivity.
Methods
We included 30 patients with PSP‐Richardson syndrome and 30 healthy controls; in patients, tau deposition was confirmed through 18F‐florzolotau positron emission tomography. Myo‐inositol, an astroglial marker, and lactate were quantified in the anterior cingulate cortex through magnetic resonance spectroscopy. We measured plasma biomarkers, including glial fibrillary acidic protein as another astrocytic marker. The anterior cingulate cortex was histologically assessed in postmortem samples of another 3 patients with PSP with comparable disease durations.
Results
The levels of myo‐inositol and plasma glial fibrillary acidic protein were significantly higher in patients than those in healthy controls (p < 0.05); these increases were significantly associated with PSP rating scale and cognitive function scores (p < 0.05). The lactate level was high in patients, and correlated significantly with high myo‐inositol levels. Histological analysis of the anterior cingulate cortex in patients revealed reactive astrocytes, despite mild tau deposition, and no marked synaptic loss.
Interpretation
We discovered high levels of astrocyte biomarkers in patients with PSP, suggesting astrocyte reactivity. The association between myo‐inositol and lactate levels suggests a link between reactive astrocytes and brain energy metabolism changes. Our results indicate that astrocyte reactivity in the anterior cingulate cortex precedes pronounced tau pathology and neurodegenerative processes in that region, and affects brain function in PSP. ANN NEUROL 2024;96:247–261</description><subject>Astrocytes</subject><subject>Biomarkers</subject><subject>Brain</subject><subject>Cognitive ability</subject><subject>Cortex (cingulate)</subject><subject>Deposition</subject><subject>Disease control</subject><subject>Energy metabolism</subject><subject>Glial fibrillary acidic protein</subject><subject>In vivo methods and tests</subject><subject>Inositol</subject><subject>Inositols</subject><subject>Lactic acid</subject><subject>Magnetic resonance spectroscopy</subject><subject>Pathology</subject><subject>Positron emission</subject><subject>Positron emission tomography</subject><subject>Progressive supranuclear palsy</subject><subject>Proteins</subject><subject>Tau protein</subject><issn>0364-5134</issn><issn>1531-8249</issn><issn>1531-8249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><recordid>eNp10F1LwzAUBuAgipvTC_-ABLzRi24nTZq2l2P4MRg6_LrwpmTtqWZ07Uzajf57o51eCELgEHjOy-El5JTBkAH4I1WqoS9j6e-RPgs48yJfxPukD1wKL2Bc9MiRtUsAiCWDQ9LjURgykLJPXqclfdGbio6tRWtXWNa0yt2vNlXa1kgfUKW13ui6pbqkc1VrRyzd6vqdzk31ZtyW3iB9bNZGlU1aoDKOFbY9Jge5m3iymwPyfH31NLn1Zvc308l45qVcRL7HgOUShA8ZqjhADrFAN1AFmIlswUEsAIOcqTTII4xzFmEuY54GQnL3gA_IRZe7NtVHg7ZOVtqmWBSqxKqxCYcgdAuCc0fP_9Bl1ZjSXedU6DrxOYuduuxUaiprDebJ2uiVMm3CIPkqPHGFJ9-FO3u2S2wWK8x-5U_DDow6sNUFtv8nJeO7cRf5CRZpiXw</recordid><startdate>202408</startdate><enddate>202408</enddate><creator>Hirata, Kosei</creator><creator>Matsuoka, Kiwamu</creator><creator>Tagai, Kenji</creator><creator>Endo, Hironobu</creator><creator>Tatebe, Harutsugu</creator><creator>Ono, Maiko</creator><creator>Kokubo, Naomi</creator><creator>Kataoka, Yuko</creator><creator>Oyama, Asaka</creator><creator>Shinotoh, Hitoshi</creator><creator>Takahata, Keisuke</creator><creator>Obata, Takayuki</creator><creator>Dehghani, Masoumeh</creator><creator>Near, Jamie</creator><creator>Kawamura, Kazunori</creator><creator>Zhang, Ming‐Rong</creator><creator>Shimada, Hitoshi</creator><creator>Shimizu, Hiroshi</creator><creator>Kakita, Akiyoshi</creator><creator>Yokota, Takanori</creator><creator>Tokuda, Takahiko</creator><creator>Higuchi, Makoto</creator><creator>Takado, Yuhei</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0007-9027-9277</orcidid><orcidid>https://orcid.org/0000-0001-7484-8424</orcidid><orcidid>https://orcid.org/0000-0002-5131-1533</orcidid></search><sort><creationdate>202408</creationdate><title>In Vivo Assessment of Astrocyte Reactivity in Patients with Progressive Supranuclear Palsy</title><author>Hirata, Kosei ; Matsuoka, Kiwamu ; Tagai, Kenji ; Endo, Hironobu ; Tatebe, Harutsugu ; Ono, Maiko ; Kokubo, Naomi ; Kataoka, Yuko ; Oyama, Asaka ; Shinotoh, Hitoshi ; Takahata, Keisuke ; Obata, Takayuki ; Dehghani, Masoumeh ; Near, Jamie ; Kawamura, Kazunori ; Zhang, Ming‐Rong ; Shimada, Hitoshi ; Shimizu, Hiroshi ; Kakita, Akiyoshi ; Yokota, Takanori ; Tokuda, Takahiko ; Higuchi, Makoto ; Takado, Yuhei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3482-101f60420dea95e3094e5e3ea5ed4db304b0e5f1ac5f8e9f18ef693c546346303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Astrocytes</topic><topic>Biomarkers</topic><topic>Brain</topic><topic>Cognitive ability</topic><topic>Cortex (cingulate)</topic><topic>Deposition</topic><topic>Disease control</topic><topic>Energy metabolism</topic><topic>Glial fibrillary acidic protein</topic><topic>In vivo methods and tests</topic><topic>Inositol</topic><topic>Inositols</topic><topic>Lactic acid</topic><topic>Magnetic resonance spectroscopy</topic><topic>Pathology</topic><topic>Positron emission</topic><topic>Positron emission tomography</topic><topic>Progressive supranuclear palsy</topic><topic>Proteins</topic><topic>Tau protein</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hirata, Kosei</creatorcontrib><creatorcontrib>Matsuoka, Kiwamu</creatorcontrib><creatorcontrib>Tagai, Kenji</creatorcontrib><creatorcontrib>Endo, Hironobu</creatorcontrib><creatorcontrib>Tatebe, Harutsugu</creatorcontrib><creatorcontrib>Ono, Maiko</creatorcontrib><creatorcontrib>Kokubo, Naomi</creatorcontrib><creatorcontrib>Kataoka, Yuko</creatorcontrib><creatorcontrib>Oyama, Asaka</creatorcontrib><creatorcontrib>Shinotoh, Hitoshi</creatorcontrib><creatorcontrib>Takahata, Keisuke</creatorcontrib><creatorcontrib>Obata, Takayuki</creatorcontrib><creatorcontrib>Dehghani, Masoumeh</creatorcontrib><creatorcontrib>Near, Jamie</creatorcontrib><creatorcontrib>Kawamura, Kazunori</creatorcontrib><creatorcontrib>Zhang, Ming‐Rong</creatorcontrib><creatorcontrib>Shimada, Hitoshi</creatorcontrib><creatorcontrib>Shimizu, Hiroshi</creatorcontrib><creatorcontrib>Kakita, Akiyoshi</creatorcontrib><creatorcontrib>Yokota, Takanori</creatorcontrib><creatorcontrib>Tokuda, Takahiko</creatorcontrib><creatorcontrib>Higuchi, Makoto</creatorcontrib><creatorcontrib>Takado, Yuhei</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Annals of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hirata, Kosei</au><au>Matsuoka, Kiwamu</au><au>Tagai, Kenji</au><au>Endo, Hironobu</au><au>Tatebe, Harutsugu</au><au>Ono, Maiko</au><au>Kokubo, Naomi</au><au>Kataoka, Yuko</au><au>Oyama, Asaka</au><au>Shinotoh, Hitoshi</au><au>Takahata, Keisuke</au><au>Obata, Takayuki</au><au>Dehghani, Masoumeh</au><au>Near, Jamie</au><au>Kawamura, Kazunori</au><au>Zhang, Ming‐Rong</au><au>Shimada, Hitoshi</au><au>Shimizu, Hiroshi</au><au>Kakita, Akiyoshi</au><au>Yokota, Takanori</au><au>Tokuda, Takahiko</au><au>Higuchi, Makoto</au><au>Takado, Yuhei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>In Vivo Assessment of Astrocyte Reactivity in Patients with Progressive Supranuclear Palsy</atitle><jtitle>Annals of neurology</jtitle><addtitle>Ann Neurol</addtitle><date>2024-08</date><risdate>2024</risdate><volume>96</volume><issue>2</issue><spage>247</spage><epage>261</epage><pages>247-261</pages><issn>0364-5134</issn><issn>1531-8249</issn><eissn>1531-8249</eissn><abstract>Objective
Although astrocytic pathology is a pathological hallmark of progressive supranuclear palsy (PSP), its pathophysiological role remains unclear. This study aimed to assess astrocyte reactivity in vivo in patients with PSP. Furthermore, we investigated alterations in brain lactate levels and their relationship with astrocyte reactivity.
Methods
We included 30 patients with PSP‐Richardson syndrome and 30 healthy controls; in patients, tau deposition was confirmed through 18F‐florzolotau positron emission tomography. Myo‐inositol, an astroglial marker, and lactate were quantified in the anterior cingulate cortex through magnetic resonance spectroscopy. We measured plasma biomarkers, including glial fibrillary acidic protein as another astrocytic marker. The anterior cingulate cortex was histologically assessed in postmortem samples of another 3 patients with PSP with comparable disease durations.
Results
The levels of myo‐inositol and plasma glial fibrillary acidic protein were significantly higher in patients than those in healthy controls (p < 0.05); these increases were significantly associated with PSP rating scale and cognitive function scores (p < 0.05). The lactate level was high in patients, and correlated significantly with high myo‐inositol levels. Histological analysis of the anterior cingulate cortex in patients revealed reactive astrocytes, despite mild tau deposition, and no marked synaptic loss.
Interpretation
We discovered high levels of astrocyte biomarkers in patients with PSP, suggesting astrocyte reactivity. The association between myo‐inositol and lactate levels suggests a link between reactive astrocytes and brain energy metabolism changes. Our results indicate that astrocyte reactivity in the anterior cingulate cortex precedes pronounced tau pathology and neurodegenerative processes in that region, and affects brain function in PSP. ANN NEUROL 2024;96:247–261</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>38771066</pmid><doi>10.1002/ana.26962</doi><tpages>15</tpages><orcidid>https://orcid.org/0009-0007-9027-9277</orcidid><orcidid>https://orcid.org/0000-0001-7484-8424</orcidid><orcidid>https://orcid.org/0000-0002-5131-1533</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Astrocytes Biomarkers Brain Cognitive ability Cortex (cingulate) Deposition Disease control Energy metabolism Glial fibrillary acidic protein In vivo methods and tests Inositol Inositols Lactic acid Magnetic resonance spectroscopy Pathology Positron emission Positron emission tomography Progressive supranuclear palsy Proteins Tau protein |
| title | In Vivo Assessment of Astrocyte Reactivity in Patients with Progressive Supranuclear Palsy |
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