Melatonin directly binds and inhibits death‐associated protein kinase 1 function in Alzheimer’s disease

Death‐associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD...

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Vydané v:Journal of pineal research Ročník 69; číslo 2; s. e12665 - n/a
Hlavní autori: Chen, Dongmei, Mei, Yingxue, Kim, Nami, Lan, Guihua, Gan, Chen‐Ling, Fan, Fei, Zhang, Tao, Xia, Yongfang, Wang, Long, Lin, Chun, Ke, Fang, Zhou, Xiao Zhen, Lu, Kun Ping, Lee, Tae Ho
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: England 01.09.2020
Predmet:
Alzheimer's disease
death‐associated protein kinase 1 (DAPK1)
melatonin
Pin1
tau
Pin1
tau
death-associated protein kinase 1 (DAPK1)
melatonin
Alzheimer's disease
ISSN:0742-3098, 1600-079X, 1600-079X
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Abstract Death‐associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD. Here, we identified melatonin as a critical regulator of DAPK1 levels and function. Melatonin significantly decreases DAPK1 expression in a post‐transcriptional manner in neuronal cell lines and mouse primary cortical neurons. Moreover, melatonin directly binds to DAPK1 and promotes its ubiquitination, resulting in increased DAPK1 protein degradation through a proteasome‐dependent pathway. Furthermore, in tau‐overexpressing mouse brain slices, melatonin treatment and the inhibition of DAPK1 kinase activity synergistically decrease tau phosphorylation at multiple sites related to AD. In addition, melatonin and DAPK1 inhibitor dramatically accelerate neurite outgrowth and increase the assembly of microtubules. Mechanistically, melatonin‐mediated DAPK1 degradation increases the activity of Pin1, a prolyl isomerase known to play a protective role against tau hyperphosphorylation and tau‐related pathologies. Finally, elevated DAPK1 expression shows a strong correlation with the decrease in melatonin levels in human AD brains. Combined, these results suggest that DAPK1 regulation by melatonin is a novel mechanism that controls tau phosphorylation and function and offers new therapeutic options for treating human AD.
AbstractList Death‐associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD. Here, we identified melatonin as a critical regulator of DAPK1 levels and function. Melatonin significantly decreases DAPK1 expression in a post‐transcriptional manner in neuronal cell lines and mouse primary cortical neurons. Moreover, melatonin directly binds to DAPK1 and promotes its ubiquitination, resulting in increased DAPK1 protein degradation through a proteasome‐dependent pathway. Furthermore, in tau‐overexpressing mouse brain slices, melatonin treatment and the inhibition of DAPK1 kinase activity synergistically decrease tau phosphorylation at multiple sites related to AD. In addition, melatonin and DAPK1 inhibitor dramatically accelerate neurite outgrowth and increase the assembly of microtubules. Mechanistically, melatonin‐mediated DAPK1 degradation increases the activity of Pin1, a prolyl isomerase known to play a protective role against tau hyperphosphorylation and tau‐related pathologies. Finally, elevated DAPK1 expression shows a strong correlation with the decrease in melatonin levels in human AD brains. Combined, these results suggest that DAPK1 regulation by melatonin is a novel mechanism that controls tau phosphorylation and function and offers new therapeutic options for treating human AD.
Death-associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD. Here, we identified melatonin as a critical regulator of DAPK1 levels and function. Melatonin significantly decreases DAPK1 expression in a post-transcriptional manner in neuronal cell lines and mouse primary cortical neurons. Moreover, melatonin directly binds to DAPK1 and promotes its ubiquitination, resulting in increased DAPK1 protein degradation through a proteasome-dependent pathway. Furthermore, in tau-overexpressing mouse brain slices, melatonin treatment and the inhibition of DAPK1 kinase activity synergistically decrease tau phosphorylation at multiple sites related to AD. In addition, melatonin and DAPK1 inhibitor dramatically accelerate neurite outgrowth and increase the assembly of microtubules. Mechanistically, melatonin-mediated DAPK1 degradation increases the activity of Pin1, a prolyl isomerase known to play a protective role against tau hyperphosphorylation and tau-related pathologies. Finally, elevated DAPK1 expression shows a strong correlation with the decrease in melatonin levels in human AD brains. Combined, these results suggest that DAPK1 regulation by melatonin is a novel mechanism that controls tau phosphorylation and function and offers new therapeutic options for treating human AD.
Death-associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD. Here, we identified melatonin as a critical regulator of DAPK1 levels and function. Melatonin significantly decreases DAPK1 expression in a post-transcriptional manner in neuronal cell lines and mouse primary cortical neurons. Moreover, melatonin directly binds to DAPK1 and promotes its ubiquitination, resulting in increased DAPK1 protein degradation through a proteasome-dependent pathway. Furthermore, in tau-overexpressing mouse brain slices, melatonin treatment and the inhibition of DAPK1 kinase activity synergistically decrease tau phosphorylation at multiple sites related to AD. In addition, melatonin and DAPK1 inhibitor dramatically accelerate neurite outgrowth and increase the assembly of microtubules. Mechanistically, melatonin-mediated DAPK1 degradation increases the activity of Pin1, a prolyl isomerase known to play a protective role against tau hyperphosphorylation and tau-related pathologies. Finally, elevated DAPK1 expression shows a strong correlation with the decrease in melatonin levels in human AD brains. Combined, these results suggest that DAPK1 regulation by melatonin is a novel mechanism that controls tau phosphorylation and function and offers new therapeutic options for treating human AD.Death-associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant DAPK1 regulation is implicated in the development of AD. However, little is known about whether and how DAPK1 function is regulated in AD. Here, we identified melatonin as a critical regulator of DAPK1 levels and function. Melatonin significantly decreases DAPK1 expression in a post-transcriptional manner in neuronal cell lines and mouse primary cortical neurons. Moreover, melatonin directly binds to DAPK1 and promotes its ubiquitination, resulting in increased DAPK1 protein degradation through a proteasome-dependent pathway. Furthermore, in tau-overexpressing mouse brain slices, melatonin treatment and the inhibition of DAPK1 kinase activity synergistically decrease tau phosphorylation at multiple sites related to AD. In addition, melatonin and DAPK1 inhibitor dramatically accelerate neurite outgrowth and increase the assembly of microtubules. Mechanistically, melatonin-mediated DAPK1 degradation increases the activity of Pin1, a prolyl isomerase known to play a protective role against tau hyperphosphorylation and tau-related pathologies. Finally, elevated DAPK1 expression shows a strong correlation with the decrease in melatonin levels in human AD brains. Combined, these results suggest that DAPK1 regulation by melatonin is a novel mechanism that controls tau phosphorylation and function and offers new therapeutic options for treating human AD.
Author Lan, Guihua
Ke, Fang
Gan, Chen‐Ling
Xia, Yongfang
Wang, Long
Lin, Chun
Lu, Kun Ping
Lee, Tae Ho
Chen, Dongmei
Fan, Fei
Mei, Yingxue
Kim, Nami
Zhang, Tao
Zhou, Xiao Zhen
AuthorAffiliation 5 Fujian Health College, Fuzhou, Fujian, China
1 Fujian Key Laboratory for Translational Research in Cancer and Neurodegenerative Diseases, Institute for Translational Medicine, School of Basic Medical Sciences, Fujian Medical University, Fuzhou, Fujian, China
2 Division of Translational Therapeutics, Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
4 Fujian Provincial Key Laboratory of Neuroglia and Diseases, Laboratory of Pain Research, School of Basic Medical Sciences, Fujian Medical University, Fuzhou, Fujian, China
3 Fujian Provincial Key Laboratory of Natural Medicine Pharmacology, Institute of Materia Medica, School of Pharmacy, Fujian Medical University, Fuzhou, Fujian, China
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32358852$$D View this record in MEDLINE/PubMed
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ISSN 0742-3098
1600-079X
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Issue 2
Keywords Pin1
tau
death-associated protein kinase 1 (DAPK1)
melatonin
Alzheimer's disease
Language English
License 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
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Notes Dongmei Chen and Yingxue Mei contributed equally to this work.
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
DC designed the studies, analyzed the data, and wrote the manuscript. DC and YM performed most of experiments. NK performed qPCR and in vitro kinase assay, and edited the manuscript. GL performed immunohistochemical analysis and edited the manuscript. FF and CL helped with brain slice experiments and edited the manuscript. C.-LG and FK helped with biotin-melatonin experiments and edited the manuscript. TZ provided advice and edited the manuscript. YX and LW provided advice and technical assistance. XZZ and KPL provided human specimens and wrote the manuscript. THL conceived and supervised the project, designed the studies, and wrote the manuscript.
AUTHOR CONTRIBUTIONS
ORCID 0000-0001-5968-1478
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/7890046
PMID 32358852
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PublicationCentury 2000
PublicationDate September 2020
PublicationDateYYYYMMDD 2020-09-01
PublicationDate_xml – month: 09
  year: 2020
  text: September 2020
PublicationDecade 2020
PublicationPlace England
PublicationPlace_xml – name: England
PublicationTitle Journal of pineal research
PublicationTitleAlternate J Pineal Res
PublicationYear 2020
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Snippet Death‐associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant...
Death-associated protein kinase 1 (DAPK1) is upregulated in the brains of human Alzheimer's disease (AD) patients compared with normal subjects, and aberrant...
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StartPage e12665
SubjectTerms Alzheimer's disease
death‐associated protein kinase 1 (DAPK1)
melatonin
Pin1
tau
Title Melatonin directly binds and inhibits death‐associated protein kinase 1 function in Alzheimer’s disease
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjpi.12665
https://www.ncbi.nlm.nih.gov/pubmed/32358852
https://www.proquest.com/docview/2397668367
https://pubmed.ncbi.nlm.nih.gov/PMC7890046
Volume 69
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