Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts

Mitophagy stimulation has been shown to have a therapeutic effect on various neurodegenerative diseases. However, nontoxic mitophagy inducers are still very limited. In this study, we found that the natural alkaloid berberine exhibited mitophagy stimulation activity in various human cells. Berberine...

Full description

Saved in:
Bibliographic Details
Published in:International journal of molecular sciences 2023-12, Vol.25 (1), p.219
Main Authors: Um, Jee-Hyun, Lee, Kang-Min, Kim, Young-Yeon, Lee, Da-Ye, Kim, Eunmi, Kim, Dong-Hyun, Yun, Jeanho
Format: Article
Language:English
Subjects:
Adenosine
Adenylic acid
AMP-Activated Protein Kinases
Animals
B cells
Berberine - pharmacology
Biosynthesis
Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology
Cell death
Fibroblasts
Health aspects
Humans
Kinases
Mice
Mice, Knockout
Microscopy
Mitochondria
Mitochondrial Diseases
Mitophagy
Nervous system diseases
Parkinson Disease
Parkinson's disease
Phosphorylation
Protein kinases
Proteins
Scientific equipment and supplies industry
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3
cites cdi_FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3
container_end_page
container_issue 1
container_start_page 219
container_title International journal of molecular sciences
container_volume 25
creator Um, Jee-Hyun
Lee, Kang-Min
Kim, Young-Yeon
Lee, Da-Ye
Kim, Eunmi
Kim, Dong-Hyun
Yun, Jeanho
description Mitophagy stimulation has been shown to have a therapeutic effect on various neurodegenerative diseases. However, nontoxic mitophagy inducers are still very limited. In this study, we found that the natural alkaloid berberine exhibited mitophagy stimulation activity in various human cells. Berberine did not interfere with mitochondrial function, unlike the well-known mitophagy inducer carbonyl cyanide m-chlorophenyl hydrazone (CCCP), and subsequently induced mitochondrial biogenesis. Berberine treatment induced the activation of adenosine monophosphate-activated protein kinase (AMPK), and the AMPK inhibitor compound C abolished berberine-induced mitophagy, suggesting that AMPK activation is essential for berberine-induced mitophagy. Notably, berberine treatment reversed mitochondrial dysfunction in PINK1 knockout mouse embryonic fibroblasts. Our results suggest that berberine is a mitophagy-specific inducer and can be used as a therapeutic treatment for neurodegenerative diseases, including Parkinson's disease, and that natural alkaloids are potential sources of mitophagy inducers.
doi_str_mv 10.3390/ijms25010219
format article
fullrecord <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10779002</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A779212712</galeid><sourcerecordid>A779212712</sourcerecordid><originalsourceid>FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3</originalsourceid><addsrcrecordid>eNptkk9v1DAQxSMEomXhxhlZ4sKBFP9JNvEJhdLCalvoAc6W7Yw3XhJ7sZNK-534kDjaUrYI-WDL7zfvaUaTZS8JPmOM43d2O0RaYoIp4Y-yU1JQmmO8rB4fvU-yZzFuMaaMlvxpdsJqihmr-Wn26wMEBcE6QCvXThoiuraj33Vys0djF_y06VDTgvNxZq69S5qPSR8hb_Rob9OjRTfBj2AdWlsnIyDpWtQM0Fsfknyw1J13bbCyRx_30Uwu1XqHUs3N6suaoLXz-oefxhQxJYeLQYW9d1ajS6uCV72MY3yePTGyj_Di7l5k3y8vvp1_zq--flqdN1e5Lmo85lwZY2pOcAnEMEnqotYVBlKWChS0SlUlN1oDa5kyJWUEAzdyWVVay3bJDFtk7w--u0kN0GpwY5C92AU7yLAXXlrxUHG2Ext_KwiuKj6PeZG9uXMI_ucEcRSDjRr6XjpI_QnKCSuKmjCS0Nf_oFs_BZf6mylak2VdLv9SG9mDsM74FKxnU9GkTEpoRebYs_9Q6bQwWO0dGJv-HxS8PRTo4GMMYO6bJFjM6yWO1yvhr44Hcw__2Sf2G4U6z3s</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2912816856</pqid></control><display><type>article</type><title>Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts</title><source>Publicly Available Content Database</source><source>PubMed Central</source><creator>Um, Jee-Hyun ; Lee, Kang-Min ; Kim, Young-Yeon ; Lee, Da-Ye ; Kim, Eunmi ; Kim, Dong-Hyun ; Yun, Jeanho</creator><creatorcontrib>Um, Jee-Hyun ; Lee, Kang-Min ; Kim, Young-Yeon ; Lee, Da-Ye ; Kim, Eunmi ; Kim, Dong-Hyun ; Yun, Jeanho</creatorcontrib><description>Mitophagy stimulation has been shown to have a therapeutic effect on various neurodegenerative diseases. However, nontoxic mitophagy inducers are still very limited. In this study, we found that the natural alkaloid berberine exhibited mitophagy stimulation activity in various human cells. Berberine did not interfere with mitochondrial function, unlike the well-known mitophagy inducer carbonyl cyanide m-chlorophenyl hydrazone (CCCP), and subsequently induced mitochondrial biogenesis. Berberine treatment induced the activation of adenosine monophosphate-activated protein kinase (AMPK), and the AMPK inhibitor compound C abolished berberine-induced mitophagy, suggesting that AMPK activation is essential for berberine-induced mitophagy. Notably, berberine treatment reversed mitochondrial dysfunction in PINK1 knockout mouse embryonic fibroblasts. Our results suggest that berberine is a mitophagy-specific inducer and can be used as a therapeutic treatment for neurodegenerative diseases, including Parkinson's disease, and that natural alkaloids are potential sources of mitophagy inducers.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms25010219</identifier><identifier>PMID: 38203389</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Adenosine ; Adenylic acid ; AMP-Activated Protein Kinases ; Animals ; B cells ; Berberine - pharmacology ; Biosynthesis ; Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology ; Cell death ; Fibroblasts ; Health aspects ; Humans ; Kinases ; Mice ; Mice, Knockout ; Microscopy ; Mitochondria ; Mitochondrial Diseases ; Mitophagy ; Nervous system diseases ; Parkinson Disease ; Parkinson's disease ; Phosphorylation ; Protein kinases ; Proteins ; Scientific equipment and supplies industry</subject><ispartof>International journal of molecular sciences, 2023-12, Vol.25 (1), p.219</ispartof><rights>COPYRIGHT 2023 MDPI AG</rights><rights>2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 by the authors. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3</citedby><cites>FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3</cites><orcidid>0000-0001-7700-5123 ; 0000-0002-0546-8273</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2912816856/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2912816856?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,75096</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38203389$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Um, Jee-Hyun</creatorcontrib><creatorcontrib>Lee, Kang-Min</creatorcontrib><creatorcontrib>Kim, Young-Yeon</creatorcontrib><creatorcontrib>Lee, Da-Ye</creatorcontrib><creatorcontrib>Kim, Eunmi</creatorcontrib><creatorcontrib>Kim, Dong-Hyun</creatorcontrib><creatorcontrib>Yun, Jeanho</creatorcontrib><title>Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Mitophagy stimulation has been shown to have a therapeutic effect on various neurodegenerative diseases. However, nontoxic mitophagy inducers are still very limited. In this study, we found that the natural alkaloid berberine exhibited mitophagy stimulation activity in various human cells. Berberine did not interfere with mitochondrial function, unlike the well-known mitophagy inducer carbonyl cyanide m-chlorophenyl hydrazone (CCCP), and subsequently induced mitochondrial biogenesis. Berberine treatment induced the activation of adenosine monophosphate-activated protein kinase (AMPK), and the AMPK inhibitor compound C abolished berberine-induced mitophagy, suggesting that AMPK activation is essential for berberine-induced mitophagy. Notably, berberine treatment reversed mitochondrial dysfunction in PINK1 knockout mouse embryonic fibroblasts. Our results suggest that berberine is a mitophagy-specific inducer and can be used as a therapeutic treatment for neurodegenerative diseases, including Parkinson's disease, and that natural alkaloids are potential sources of mitophagy inducers.</description><subject>Adenosine</subject><subject>Adenylic acid</subject><subject>AMP-Activated Protein Kinases</subject><subject>Animals</subject><subject>B cells</subject><subject>Berberine - pharmacology</subject><subject>Biosynthesis</subject><subject>Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology</subject><subject>Cell death</subject><subject>Fibroblasts</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Kinases</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Microscopy</subject><subject>Mitochondria</subject><subject>Mitochondrial Diseases</subject><subject>Mitophagy</subject><subject>Nervous system diseases</subject><subject>Parkinson Disease</subject><subject>Parkinson's disease</subject><subject>Phosphorylation</subject><subject>Protein kinases</subject><subject>Proteins</subject><subject>Scientific equipment and supplies industry</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNptkk9v1DAQxSMEomXhxhlZ4sKBFP9JNvEJhdLCalvoAc6W7Yw3XhJ7sZNK-534kDjaUrYI-WDL7zfvaUaTZS8JPmOM43d2O0RaYoIp4Y-yU1JQmmO8rB4fvU-yZzFuMaaMlvxpdsJqihmr-Wn26wMEBcE6QCvXThoiuraj33Vys0djF_y06VDTgvNxZq69S5qPSR8hb_Rob9OjRTfBj2AdWlsnIyDpWtQM0Fsfknyw1J13bbCyRx_30Uwu1XqHUs3N6suaoLXz-oefxhQxJYeLQYW9d1ajS6uCV72MY3yePTGyj_Di7l5k3y8vvp1_zq--flqdN1e5Lmo85lwZY2pOcAnEMEnqotYVBlKWChS0SlUlN1oDa5kyJWUEAzdyWVVay3bJDFtk7w--u0kN0GpwY5C92AU7yLAXXlrxUHG2Ext_KwiuKj6PeZG9uXMI_ucEcRSDjRr6XjpI_QnKCSuKmjCS0Nf_oFs_BZf6mylak2VdLv9SG9mDsM74FKxnU9GkTEpoRebYs_9Q6bQwWO0dGJv-HxS8PRTo4GMMYO6bJFjM6yWO1yvhr44Hcw__2Sf2G4U6z3s</recordid><startdate>20231222</startdate><enddate>20231222</enddate><creator>Um, Jee-Hyun</creator><creator>Lee, Kang-Min</creator><creator>Kim, Young-Yeon</creator><creator>Lee, Da-Ye</creator><creator>Kim, Eunmi</creator><creator>Kim, Dong-Hyun</creator><creator>Yun, Jeanho</creator><general>MDPI AG</general><general>MDPI</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7700-5123</orcidid><orcidid>https://orcid.org/0000-0002-0546-8273</orcidid></search><sort><creationdate>20231222</creationdate><title>Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts</title><author>Um, Jee-Hyun ; Lee, Kang-Min ; Kim, Young-Yeon ; Lee, Da-Ye ; Kim, Eunmi ; Kim, Dong-Hyun ; Yun, Jeanho</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Adenosine</topic><topic>Adenylic acid</topic><topic>AMP-Activated Protein Kinases</topic><topic>Animals</topic><topic>B cells</topic><topic>Berberine - pharmacology</topic><topic>Biosynthesis</topic><topic>Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology</topic><topic>Cell death</topic><topic>Fibroblasts</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Kinases</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Microscopy</topic><topic>Mitochondria</topic><topic>Mitochondrial Diseases</topic><topic>Mitophagy</topic><topic>Nervous system diseases</topic><topic>Parkinson Disease</topic><topic>Parkinson's disease</topic><topic>Phosphorylation</topic><topic>Protein kinases</topic><topic>Proteins</topic><topic>Scientific equipment and supplies industry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Um, Jee-Hyun</creatorcontrib><creatorcontrib>Lee, Kang-Min</creatorcontrib><creatorcontrib>Kim, Young-Yeon</creatorcontrib><creatorcontrib>Lee, Da-Ye</creatorcontrib><creatorcontrib>Kim, Eunmi</creatorcontrib><creatorcontrib>Kim, Dong-Hyun</creatorcontrib><creatorcontrib>Yun, Jeanho</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 Central (Corporate)</collection><collection>Health &amp; Medical Complete (ProQuest Database)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Proquest Research Library</collection><collection>Research Library (Corporate)</collection><collection>ProQuest Central (New)</collection><collection>ProQuest One Academic (New)</collection><collection>Publicly Available Content Database</collection><collection>ProQuest Health &amp; Medical Research Collection</collection><collection>ProQuest One Academic Middle East (New)</collection><collection>ProQuest One Health &amp; Nursing</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Um, Jee-Hyun</au><au>Lee, Kang-Min</au><au>Kim, Young-Yeon</au><au>Lee, Da-Ye</au><au>Kim, Eunmi</au><au>Kim, Dong-Hyun</au><au>Yun, Jeanho</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2023-12-22</date><risdate>2023</risdate><volume>25</volume><issue>1</issue><spage>219</spage><pages>219-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Mitophagy stimulation has been shown to have a therapeutic effect on various neurodegenerative diseases. However, nontoxic mitophagy inducers are still very limited. In this study, we found that the natural alkaloid berberine exhibited mitophagy stimulation activity in various human cells. Berberine did not interfere with mitochondrial function, unlike the well-known mitophagy inducer carbonyl cyanide m-chlorophenyl hydrazone (CCCP), and subsequently induced mitochondrial biogenesis. Berberine treatment induced the activation of adenosine monophosphate-activated protein kinase (AMPK), and the AMPK inhibitor compound C abolished berberine-induced mitophagy, suggesting that AMPK activation is essential for berberine-induced mitophagy. Notably, berberine treatment reversed mitochondrial dysfunction in PINK1 knockout mouse embryonic fibroblasts. Our results suggest that berberine is a mitophagy-specific inducer and can be used as a therapeutic treatment for neurodegenerative diseases, including Parkinson's disease, and that natural alkaloids are potential sources of mitophagy inducers.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>38203389</pmid><doi>10.3390/ijms25010219</doi><orcidid>https://orcid.org/0000-0001-7700-5123</orcidid><orcidid>https://orcid.org/0000-0002-0546-8273</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1422-0067
ispartof International journal of molecular sciences, 2023-12, Vol.25 (1), p.219
issn 1422-0067
1661-6596
1422-0067
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10779002
source Publicly Available Content Database; PubMed Central
subjects Adenosine
Adenylic acid
AMP-Activated Protein Kinases
Animals
B cells
Berberine - pharmacology
Biosynthesis
Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology
Cell death
Fibroblasts
Health aspects
Humans
Kinases
Mice
Mice, Knockout
Microscopy
Mitochondria
Mitochondrial Diseases
Mitophagy
Nervous system diseases
Parkinson Disease
Parkinson's disease
Phosphorylation
Protein kinases
Proteins
Scientific equipment and supplies industry
title Berberine Induces Mitophagy through Adenosine Monophosphate-Activated Protein Kinase and Ameliorates Mitochondrial Dysfunction in PINK1 Knockout Mouse Embryonic Fibroblasts
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-22T18%3A14%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Berberine%20Induces%20Mitophagy%20through%20Adenosine%20Monophosphate-Activated%20Protein%20Kinase%20and%20Ameliorates%20Mitochondrial%20Dysfunction%20in%20PINK1%20Knockout%20Mouse%20Embryonic%20Fibroblasts&rft.jtitle=International%20journal%20of%20molecular%20sciences&rft.au=Um,%20Jee-Hyun&rft.date=2023-12-22&rft.volume=25&rft.issue=1&rft.spage=219&rft.pages=219-&rft.issn=1422-0067&rft.eissn=1422-0067&rft_id=info:doi/10.3390/ijms25010219&rft_dat=%3Cgale_pubme%3EA779212712%3C/gale_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c480t-9bfff89105e1f3a1848c70e155bebedbb759fcce3d3bf52310e9fa677ccad63f3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2912816856&rft_id=info:pmid/38203389&rft_galeid=A779212712&rfr_iscdi=true