Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease
Introduction The inositol polyphosphate‐5‐phosphatase D (INPP5D) gene encodes a dual‐specificity phosphatase that can dephosphorylate both phospholipids and phosphoproteins. Single nucleotide polymorphisms in INPP5D impact risk for developing late onset sporadic Alzheimer's disease (LOAD). Meth...
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| Veröffentlicht in: | Alzheimer's & dementia 2023-06, Vol.19 (6), p.2239-2252 |
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| creator | Castranio, Emilie L. Hasel, Philip Haure‐Mirande, Jean‐Vianney Ramirez Jimenez, Angie V. Hamilton, B. Wade Kim, Rachel D. Glabe, Charles G. Wang, Minghui Zhang, Bin Gandy, Sam Liddelow, Shane A. Ehrlich, Michelle E. |
| description | Introduction
The inositol polyphosphate‐5‐phosphatase D (INPP5D) gene encodes a dual‐specificity phosphatase that can dephosphorylate both phospholipids and phosphoproteins. Single nucleotide polymorphisms in INPP5D impact risk for developing late onset sporadic Alzheimer's disease (LOAD).
Methods
To assess the consequences of inducible Inpp5d knockdown in microglia of APPKM670/671NL/PSEN1Δexon9 (PSAPP) mice, we injected 3‐month‐old Inpp5dfl/fl/Cx3cr1CreER/+ and PSAPP/Inpp5dfl/fl/Cx3cr1CreER/+ mice with either tamoxifen (TAM) or corn oil (CO) to induce recombination.
Results
At age 6 months, we found that the percent area of 6E10+ deposits and plaque‐associated microglia in Inpp5d knockdown mice were increased compared to controls. Spatial transcriptomics identified a plaque‐specific expression profile that was extensively altered by Inpp5d knockdown.
Discussion
These results demonstrate that conditional Inpp5d downregulation in the PSAPP mouse increases plaque burden and recruitment of microglia to plaques. Spatial transcriptomics highlighted an extended gene expression signature associated with plaques and identified CST7 (cystatin F) as a novel marker of plaques.
Highlights
Inpp5d knockdown increases plaque burden and plaque‐associated microglia number.
Spatial transcriptomics identifies an expanded plaque‐specific gene expression profile.
Plaque‐induced gene expression is altered by Inpp5d knockdown in microglia.
Our plaque‐associated gene signature overlaps with human Alzheimer's disease gene networks. |
| doi_str_mv | 10.1002/alz.12821 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10481344</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2743508002</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4161-44acac7bc2e4c3a5e4ebc52b67b5591bb284f84437740814a9f899753981868a3</originalsourceid><addsrcrecordid>eNp1kc1O3DAURq0KVGDaRV-g8q6wGLAdO3FW1YjyJw1tpLabbqwbzw3jykkGO0M1PD2GwKgs2NiWfHTs-32EfOLsmDMmTsDfH3OhBX9H9rlSYqpEUe5szznbIwcx_mVMMs3Ve7KX5VLqXBT7pLt2NvQ33oGnV9-rSn2j3rVuiHTl4XaNtOlDC4PrOwrdgo5gQLCDu3PDhrqODkuk1c9ZVdG2X0dM6wI97Rs68_dLdC2GL5EuXESI-IHsNuAjfnzeJ-T3-dmv08vp_MfF1elsPrWS53wqJViwRW0FSpuBQom1VaLOi1qpkte10LLRUmZF8TiShLLRZVmorNRc5xqyCfk6elfrusWFxW4I4M0quBbCxvTgzOubzi3NTX9nOJOaZ8k8IYfPhtCnHOJgWhcteg8dpjGNKGSmmE7xJ_RoRFOSMQZstu9wZh4LMqkg81RQYj___7Et-dJIAk5G4J_zuHnbZGbzP6PyAUNsmso</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2743508002</pqid></control><display><type>article</type><title>Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Castranio, Emilie L. ; Hasel, Philip ; Haure‐Mirande, Jean‐Vianney ; Ramirez Jimenez, Angie V. ; Hamilton, B. Wade ; Kim, Rachel D. ; Glabe, Charles G. ; Wang, Minghui ; Zhang, Bin ; Gandy, Sam ; Liddelow, Shane A. ; Ehrlich, Michelle E.</creator><creatorcontrib>Castranio, Emilie L. ; Hasel, Philip ; Haure‐Mirande, Jean‐Vianney ; Ramirez Jimenez, Angie V. ; Hamilton, B. Wade ; Kim, Rachel D. ; Glabe, Charles G. ; Wang, Minghui ; Zhang, Bin ; Gandy, Sam ; Liddelow, Shane A. ; Ehrlich, Michelle E.</creatorcontrib><description>Introduction
The inositol polyphosphate‐5‐phosphatase D (INPP5D) gene encodes a dual‐specificity phosphatase that can dephosphorylate both phospholipids and phosphoproteins. Single nucleotide polymorphisms in INPP5D impact risk for developing late onset sporadic Alzheimer's disease (LOAD).
Methods
To assess the consequences of inducible Inpp5d knockdown in microglia of APPKM670/671NL/PSEN1Δexon9 (PSAPP) mice, we injected 3‐month‐old Inpp5dfl/fl/Cx3cr1CreER/+ and PSAPP/Inpp5dfl/fl/Cx3cr1CreER/+ mice with either tamoxifen (TAM) or corn oil (CO) to induce recombination.
Results
At age 6 months, we found that the percent area of 6E10+ deposits and plaque‐associated microglia in Inpp5d knockdown mice were increased compared to controls. Spatial transcriptomics identified a plaque‐specific expression profile that was extensively altered by Inpp5d knockdown.
Discussion
These results demonstrate that conditional Inpp5d downregulation in the PSAPP mouse increases plaque burden and recruitment of microglia to plaques. Spatial transcriptomics highlighted an extended gene expression signature associated with plaques and identified CST7 (cystatin F) as a novel marker of plaques.
Highlights
Inpp5d knockdown increases plaque burden and plaque‐associated microglia number.
Spatial transcriptomics identifies an expanded plaque‐specific gene expression profile.
Plaque‐induced gene expression is altered by Inpp5d knockdown in microglia.
Our plaque‐associated gene signature overlaps with human Alzheimer's disease gene networks.</description><identifier>ISSN: 1552-5260</identifier><identifier>EISSN: 1552-5279</identifier><identifier>DOI: 10.1002/alz.12821</identifier><identifier>PMID: 36448627</identifier><language>eng</language><publisher>United States</publisher><subject>Alzheimer Disease - genetics ; Alzheimer Disease - metabolism ; Alzheimer's disease ; Amyloid beta-Peptides - metabolism ; Animals ; cystatin F ; Disease Models, Animal ; Humans ; Infant ; Inpp5d ; Mice ; Mice, Transgenic ; microglia ; Microglia - metabolism ; oligomer ; Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - genetics ; Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - metabolism ; Plaque, Amyloid - metabolism ; SHIP1 ; spatial transcriptomics</subject><ispartof>Alzheimer's & dementia, 2023-06, Vol.19 (6), p.2239-2252</ispartof><rights>2022 The Authors. published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><rights>2022 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4161-44acac7bc2e4c3a5e4ebc52b67b5591bb284f84437740814a9f899753981868a3</citedby><cites>FETCH-LOGICAL-c4161-44acac7bc2e4c3a5e4ebc52b67b5591bb284f84437740814a9f899753981868a3</cites><orcidid>0000-0001-9510-5611 ; 0000-0003-0774-5091 ; 0000-0002-9549-5653 ; 0000-0001-6455-4721 ; 0000-0001-9397-686X ; 0000-0003-4378-3685 ; 0000-0002-0840-1437 ; 0000-0002-5748-9666 ; 0000-0001-6817-7388</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%2Falz.12821$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Falz.12821$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36448627$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Castranio, Emilie L.</creatorcontrib><creatorcontrib>Hasel, Philip</creatorcontrib><creatorcontrib>Haure‐Mirande, Jean‐Vianney</creatorcontrib><creatorcontrib>Ramirez Jimenez, Angie V.</creatorcontrib><creatorcontrib>Hamilton, B. Wade</creatorcontrib><creatorcontrib>Kim, Rachel D.</creatorcontrib><creatorcontrib>Glabe, Charles G.</creatorcontrib><creatorcontrib>Wang, Minghui</creatorcontrib><creatorcontrib>Zhang, Bin</creatorcontrib><creatorcontrib>Gandy, Sam</creatorcontrib><creatorcontrib>Liddelow, Shane A.</creatorcontrib><creatorcontrib>Ehrlich, Michelle E.</creatorcontrib><title>Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease</title><title>Alzheimer's & dementia</title><addtitle>Alzheimers Dement</addtitle><description>Introduction
The inositol polyphosphate‐5‐phosphatase D (INPP5D) gene encodes a dual‐specificity phosphatase that can dephosphorylate both phospholipids and phosphoproteins. Single nucleotide polymorphisms in INPP5D impact risk for developing late onset sporadic Alzheimer's disease (LOAD).
Methods
To assess the consequences of inducible Inpp5d knockdown in microglia of APPKM670/671NL/PSEN1Δexon9 (PSAPP) mice, we injected 3‐month‐old Inpp5dfl/fl/Cx3cr1CreER/+ and PSAPP/Inpp5dfl/fl/Cx3cr1CreER/+ mice with either tamoxifen (TAM) or corn oil (CO) to induce recombination.
Results
At age 6 months, we found that the percent area of 6E10+ deposits and plaque‐associated microglia in Inpp5d knockdown mice were increased compared to controls. Spatial transcriptomics identified a plaque‐specific expression profile that was extensively altered by Inpp5d knockdown.
Discussion
These results demonstrate that conditional Inpp5d downregulation in the PSAPP mouse increases plaque burden and recruitment of microglia to plaques. Spatial transcriptomics highlighted an extended gene expression signature associated with plaques and identified CST7 (cystatin F) as a novel marker of plaques.
Highlights
Inpp5d knockdown increases plaque burden and plaque‐associated microglia number.
Spatial transcriptomics identifies an expanded plaque‐specific gene expression profile.
Plaque‐induced gene expression is altered by Inpp5d knockdown in microglia.
Our plaque‐associated gene signature overlaps with human Alzheimer's disease gene networks.</description><subject>Alzheimer Disease - genetics</subject><subject>Alzheimer Disease - metabolism</subject><subject>Alzheimer's disease</subject><subject>Amyloid beta-Peptides - metabolism</subject><subject>Animals</subject><subject>cystatin F</subject><subject>Disease Models, Animal</subject><subject>Humans</subject><subject>Infant</subject><subject>Inpp5d</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>microglia</subject><subject>Microglia - metabolism</subject><subject>oligomer</subject><subject>Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - genetics</subject><subject>Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - metabolism</subject><subject>Plaque, Amyloid - metabolism</subject><subject>SHIP1</subject><subject>spatial transcriptomics</subject><issn>1552-5260</issn><issn>1552-5279</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc1O3DAURq0KVGDaRV-g8q6wGLAdO3FW1YjyJw1tpLabbqwbzw3jykkGO0M1PD2GwKgs2NiWfHTs-32EfOLsmDMmTsDfH3OhBX9H9rlSYqpEUe5szznbIwcx_mVMMs3Ve7KX5VLqXBT7pLt2NvQ33oGnV9-rSn2j3rVuiHTl4XaNtOlDC4PrOwrdgo5gQLCDu3PDhrqODkuk1c9ZVdG2X0dM6wI97Rs68_dLdC2GL5EuXESI-IHsNuAjfnzeJ-T3-dmv08vp_MfF1elsPrWS53wqJViwRW0FSpuBQom1VaLOi1qpkte10LLRUmZF8TiShLLRZVmorNRc5xqyCfk6elfrusWFxW4I4M0quBbCxvTgzOubzi3NTX9nOJOaZ8k8IYfPhtCnHOJgWhcteg8dpjGNKGSmmE7xJ_RoRFOSMQZstu9wZh4LMqkg81RQYj___7Et-dJIAk5G4J_zuHnbZGbzP6PyAUNsmso</recordid><startdate>202306</startdate><enddate>202306</enddate><creator>Castranio, Emilie L.</creator><creator>Hasel, Philip</creator><creator>Haure‐Mirande, Jean‐Vianney</creator><creator>Ramirez Jimenez, Angie V.</creator><creator>Hamilton, B. Wade</creator><creator>Kim, Rachel D.</creator><creator>Glabe, Charles G.</creator><creator>Wang, Minghui</creator><creator>Zhang, Bin</creator><creator>Gandy, Sam</creator><creator>Liddelow, Shane A.</creator><creator>Ehrlich, Michelle E.</creator><scope>24P</scope><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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9510-5611</orcidid><orcidid>https://orcid.org/0000-0003-0774-5091</orcidid><orcidid>https://orcid.org/0000-0002-9549-5653</orcidid><orcidid>https://orcid.org/0000-0001-6455-4721</orcidid><orcidid>https://orcid.org/0000-0001-9397-686X</orcidid><orcidid>https://orcid.org/0000-0003-4378-3685</orcidid><orcidid>https://orcid.org/0000-0002-0840-1437</orcidid><orcidid>https://orcid.org/0000-0002-5748-9666</orcidid><orcidid>https://orcid.org/0000-0001-6817-7388</orcidid></search><sort><creationdate>202306</creationdate><title>Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease</title><author>Castranio, Emilie L. ; Hasel, Philip ; Haure‐Mirande, Jean‐Vianney ; Ramirez Jimenez, Angie V. ; Hamilton, B. Wade ; Kim, Rachel D. ; Glabe, Charles G. ; Wang, Minghui ; Zhang, Bin ; Gandy, Sam ; Liddelow, Shane A. ; Ehrlich, Michelle E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4161-44acac7bc2e4c3a5e4ebc52b67b5591bb284f84437740814a9f899753981868a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Alzheimer Disease - genetics</topic><topic>Alzheimer Disease - metabolism</topic><topic>Alzheimer's disease</topic><topic>Amyloid beta-Peptides - metabolism</topic><topic>Animals</topic><topic>cystatin F</topic><topic>Disease Models, Animal</topic><topic>Humans</topic><topic>Infant</topic><topic>Inpp5d</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>microglia</topic><topic>Microglia - metabolism</topic><topic>oligomer</topic><topic>Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - genetics</topic><topic>Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - metabolism</topic><topic>Plaque, Amyloid - metabolism</topic><topic>SHIP1</topic><topic>spatial transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Castranio, Emilie L.</creatorcontrib><creatorcontrib>Hasel, Philip</creatorcontrib><creatorcontrib>Haure‐Mirande, Jean‐Vianney</creatorcontrib><creatorcontrib>Ramirez Jimenez, Angie V.</creatorcontrib><creatorcontrib>Hamilton, B. Wade</creatorcontrib><creatorcontrib>Kim, Rachel D.</creatorcontrib><creatorcontrib>Glabe, Charles G.</creatorcontrib><creatorcontrib>Wang, Minghui</creatorcontrib><creatorcontrib>Zhang, Bin</creatorcontrib><creatorcontrib>Gandy, Sam</creatorcontrib><creatorcontrib>Liddelow, Shane A.</creatorcontrib><creatorcontrib>Ehrlich, Michelle E.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Alzheimer's & dementia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Castranio, Emilie L.</au><au>Hasel, Philip</au><au>Haure‐Mirande, Jean‐Vianney</au><au>Ramirez Jimenez, Angie V.</au><au>Hamilton, B. Wade</au><au>Kim, Rachel D.</au><au>Glabe, Charles G.</au><au>Wang, Minghui</au><au>Zhang, Bin</au><au>Gandy, Sam</au><au>Liddelow, Shane A.</au><au>Ehrlich, Michelle E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease</atitle><jtitle>Alzheimer's & dementia</jtitle><addtitle>Alzheimers Dement</addtitle><date>2023-06</date><risdate>2023</risdate><volume>19</volume><issue>6</issue><spage>2239</spage><epage>2252</epage><pages>2239-2252</pages><issn>1552-5260</issn><eissn>1552-5279</eissn><abstract>Introduction
The inositol polyphosphate‐5‐phosphatase D (INPP5D) gene encodes a dual‐specificity phosphatase that can dephosphorylate both phospholipids and phosphoproteins. Single nucleotide polymorphisms in INPP5D impact risk for developing late onset sporadic Alzheimer's disease (LOAD).
Methods
To assess the consequences of inducible Inpp5d knockdown in microglia of APPKM670/671NL/PSEN1Δexon9 (PSAPP) mice, we injected 3‐month‐old Inpp5dfl/fl/Cx3cr1CreER/+ and PSAPP/Inpp5dfl/fl/Cx3cr1CreER/+ mice with either tamoxifen (TAM) or corn oil (CO) to induce recombination.
Results
At age 6 months, we found that the percent area of 6E10+ deposits and plaque‐associated microglia in Inpp5d knockdown mice were increased compared to controls. Spatial transcriptomics identified a plaque‐specific expression profile that was extensively altered by Inpp5d knockdown.
Discussion
These results demonstrate that conditional Inpp5d downregulation in the PSAPP mouse increases plaque burden and recruitment of microglia to plaques. Spatial transcriptomics highlighted an extended gene expression signature associated with plaques and identified CST7 (cystatin F) as a novel marker of plaques.
Highlights
Inpp5d knockdown increases plaque burden and plaque‐associated microglia number.
Spatial transcriptomics identifies an expanded plaque‐specific gene expression profile.
Plaque‐induced gene expression is altered by Inpp5d knockdown in microglia.
Our plaque‐associated gene signature overlaps with human Alzheimer's disease gene networks.</abstract><cop>United States</cop><pmid>36448627</pmid><doi>10.1002/alz.12821</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-9510-5611</orcidid><orcidid>https://orcid.org/0000-0003-0774-5091</orcidid><orcidid>https://orcid.org/0000-0002-9549-5653</orcidid><orcidid>https://orcid.org/0000-0001-6455-4721</orcidid><orcidid>https://orcid.org/0000-0001-9397-686X</orcidid><orcidid>https://orcid.org/0000-0003-4378-3685</orcidid><orcidid>https://orcid.org/0000-0002-0840-1437</orcidid><orcidid>https://orcid.org/0000-0002-5748-9666</orcidid><orcidid>https://orcid.org/0000-0001-6817-7388</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Alzheimer Disease - genetics Alzheimer Disease - metabolism Alzheimer's disease Amyloid beta-Peptides - metabolism Animals cystatin F Disease Models, Animal Humans Infant Inpp5d Mice Mice, Transgenic microglia Microglia - metabolism oligomer Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - genetics Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases - metabolism Plaque, Amyloid - metabolism SHIP1 spatial transcriptomics |
| title | Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease |
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