Unfolded protein response IRE1/XBP1 signaling is required for healthy mammalian brain aging

Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) str...

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Published inThe EMBO journal Vol. 41; no. 22; pp. e111952 - n/a
Main Authors Cabral‐Miranda, Felipe, Tamburini, Giovanni, Martinez, Gabriela, Ardiles, Alvaro O, Medinas, Danilo B, Gerakis, Yannis, Hung, Mei‐Li Diaz, Vidal, René, Fuentealba, Matias, Miedema, Tim, Duran‐Aniotz, Claudia, Diaz, Javier, Ibaceta‐Gonzalez, Cristobal, Sabusap, Carleen M, Bermedo‐Garcia, Francisca, Mujica, Paula, Adamson, Stuart, Vitangcol, Kaitlyn, Huerta, Hernan, Zhang, Xu, Nakamura, Tomohiro, Sardi, Sergio Pablo, Lipton, Stuart A, Kennedy, Brian K, Henriquez, Juan Pablo, Cárdenas, J Cesar, Plate, Lars, Palacios, Adrian G, Hetz, Claudio
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 17.11.2022
Springer Nature B.V
John Wiley and Sons Inc
Subjects
Ablation
Age
Aging
Aging (natural)
Aging - genetics
aging brain
Animal models
Animals
Brain
Brain - metabolism
Cognitive ability
EMBO24
EMBO27
EMBO32
Endoplasmic reticulum
Endoplasmic Reticulum Stress - genetics
ER stress
Gene transfer
Hippocampus
Mammals
Mice
Neurodegeneration
Neurodegenerative diseases
Phenotypes
Physiology
Protein folding
Protein Serine-Threonine Kinases - genetics
Proteins
Proteomics
proteostasis
Risk analysis
Risk factors
Senescence
Signal transduction
Signal Transduction - physiology
Signaling
Synapses
Unfolded Protein Response
UPR
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
XBP1s
ER stress
aging brain
proteostasis
UPR
XBP1s
Online AccessGet full text
ISSN0261-4189
1460-2075
1460-2075
DOI10.15252/embj.2022111952

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Abstract Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age‐related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging. Synopsis The UPR pathway sustains brain function, delaying the natural appearance of age‐associated phenotypes in mammals. IRE1/XBP1 signaling improves neuronal physiology, possibly by regulation of synaptic protein expression. Impairment of UPR signaling begins by middle age in the mouse brain. Ablation of IRE1 expression in the brain accelerates and exacerbates age‐associated cognitive decline. Overexpression of XBP1s, the active form of XBP1, in the brain improves age‐associated phenotypes in mice. XBP1s gene delivery to aged mice can revert brain dysfunction at the morphological, electrophysiological, molecular, and behavioral level. Proteomic profiling of aged animals overexpressing XBP1s highlights the modification of pathways related to synapse physiology and neurodegeneration. Graphical Abstract The unfolded protein response signaling components IRE1 and XBP1 are shown to play a role in age‐associated cognitive function and brain health in mice.
AbstractList Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age‐related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging. The unfolded protein response signaling components IRE1 and XBP1 are shown to play a role in age‐associated cognitive function and brain health in mice.
Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age‐related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging. Synopsis The UPR pathway sustains brain function, delaying the natural appearance of age‐associated phenotypes in mammals. IRE1/XBP1 signaling improves neuronal physiology, possibly by regulation of synaptic protein expression. Impairment of UPR signaling begins by middle age in the mouse brain. Ablation of IRE1 expression in the brain accelerates and exacerbates age‐associated cognitive decline. Overexpression of XBP1s, the active form of XBP1, in the brain improves age‐associated phenotypes in mice. XBP1s gene delivery to aged mice can revert brain dysfunction at the morphological, electrophysiological, molecular, and behavioral level. Proteomic profiling of aged animals overexpressing XBP1s highlights the modification of pathways related to synapse physiology and neurodegeneration. Graphical Abstract The unfolded protein response signaling components IRE1 and XBP1 are shown to play a role in age‐associated cognitive function and brain health in mice.
Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age-related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging.Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age-related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging.
Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age‐related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging. image The UPR pathway sustains brain function, delaying the natural appearance of age‐associated phenotypes in mammals. IRE1/XBP1 signaling improves neuronal physiology, possibly by regulation of synaptic protein expression. Impairment of UPR signaling begins by middle age in the mouse brain. Ablation of IRE1 expression in the brain accelerates and exacerbates age‐associated cognitive decline. Overexpression of XBP1s, the active form of XBP1, in the brain improves age‐associated phenotypes in mice. XBP1s gene delivery to aged mice can revert brain dysfunction at the morphological, electrophysiological, molecular, and behavioral level. Proteomic profiling of aged animals overexpressing XBP1s highlights the modification of pathways related to synapse physiology and neurodegeneration.
Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age-related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging.
Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We investigated the significance of the unfolded protein response (UPR), a major signaling pathway activated to cope with endoplasmic reticulum (ER) stress, in the functional deterioration of the mammalian brain during aging. We report that genetic disruption of the ER stress sensor IRE1 accelerated age‐related cognitive decline. In mouse models, overexpressing an active form of the UPR transcription factor XBP1 restored synaptic and cognitive function, in addition to reducing cell senescence. Proteomic profiling of hippocampal tissue showed that XBP1 expression significantly restore changes associated with aging, including factors involved in synaptic function and pathways linked to neurodegenerative diseases. The genes modified by XBP1 in the aged hippocampus where also altered. Collectively, our results demonstrate that strategies to manipulate the UPR in mammals may help sustain healthy brain aging. Synopsis The UPR pathway sustains brain function, delaying the natural appearance of age‐associated phenotypes in mammals. IRE1/XBP1 signaling improves neuronal physiology, possibly by regulation of synaptic protein expression. Impairment of UPR signaling begins by middle age in the mouse brain. Ablation of IRE1 expression in the brain accelerates and exacerbates age‐associated cognitive decline. Overexpression of XBP1s, the active form of XBP1, in the brain improves age‐associated phenotypes in mice. XBP1s gene delivery to aged mice can revert brain dysfunction at the morphological, electrophysiological, molecular, and behavioral level. Proteomic profiling of aged animals overexpressing XBP1s highlights the modification of pathways related to synapse physiology and neurodegeneration. The unfolded protein response signaling components IRE1 and XBP1 are shown to play a role in age‐associated cognitive function and brain health in mice.
Author Henriquez, Juan Pablo
Huerta, Hernan
Ibaceta‐Gonzalez, Cristobal
Cabral‐Miranda, Felipe
Fuentealba, Matias
Sardi, Sergio Pablo
Duran‐Aniotz, Claudia
Lipton, Stuart A
Gerakis, Yannis
Adamson, Stuart
Hung, Mei‐Li Diaz
Miedema, Tim
Kennedy, Brian K
Martinez, Gabriela
Nakamura, Tomohiro
Tamburini, Giovanni
Sabusap, Carleen M
Hetz, Claudio
Vitangcol, Kaitlyn
Ardiles, Alvaro O
Medinas, Danilo B
Zhang, Xu
Cárdenas, J Cesar
Diaz, Javier
Mujica, Paula
Plate, Lars
Vidal, René
Bermedo‐Garcia, Francisca
Palacios, Adrian G
AuthorAffiliation 14 Healthy Longevity Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore; Centre for Healthy Longevity, National University Health System; Departments of Biochemistry and Physiology, Yong Loo Lin School of Medicine, National University of Singapore Singapore Singapore
4 Instituto de Ciências Biomédicas Universidade Federal do Rio de Janeiro Rio de Janeiro Brazil
6 Centro de Neurología Traslacional, Escuela de Medicina Universidad de Valparaíso Valparaiso Chile
7 Center for Integrative Biology Universidad Mayor Santiago Chile
8 Departments of Chemistry and Biological Sciences Vanderbilt University Nashville TN USA
1 Center for Geroscience Brain Health and Metabolism Santiago Chile
5 Centro Interdisciplinario de Neurociencia de Valparaíso Universidad de Valparaiso Valparaiso Chile
2 Biomedical Neuroscience Institute, Faculty of Medicine University of Chile Santiago Chile
10 Buck Institute for Research on Aging Novato CA USA
11 Department of Molecula
AuthorAffiliation_xml – name: 8 Departments of Chemistry and Biological Sciences Vanderbilt University Nashville TN USA
– name: 4 Instituto de Ciências Biomédicas Universidade Federal do Rio de Janeiro Rio de Janeiro Brazil
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– name: 3 Program of Cellular and Molecular Biology, Institute of Biomedical Sciences, Faculty of Medicine University of Chile Santiago Chile
– name: 7 Center for Integrative Biology Universidad Mayor Santiago Chile
– name: 9 Department of Cell Biology, Center for Advanced Microscopy (CMA BioBio) Universidad de Concepción Concepción Chile
– name: 12 Rare and Neurological Diseases Therapeutic Area Sanofi Framingham MA USA
– name: 1 Center for Geroscience Brain Health and Metabolism Santiago Chile
– name: 10 Buck Institute for Research on Aging Novato CA USA
– name: 11 Department of Molecular Medicine and Neurodegeneration New Medicines Center The Scripps Research Institute La Jolla CA USA
– name: 14 Healthy Longevity Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore; Centre for Healthy Longevity, National University Health System; Departments of Biochemistry and Physiology, Yong Loo Lin School of Medicine, National University of Singapore Singapore Singapore
– name: 2 Biomedical Neuroscience Institute, Faculty of Medicine University of Chile Santiago Chile
– name: 5 Centro Interdisciplinario de Neurociencia de Valparaíso Universidad de Valparaiso Valparaiso Chile
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– sequence: 5
  givenname: Danilo B
  orcidid: 0000-0002-1822-1974
  surname: Medinas
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  organization: Center for Geroscience, Brain Health and Metabolism, Biomedical Neuroscience Institute, Faculty of Medicine, University of Chile, Program of Cellular and Molecular Biology, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile
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  givenname: Yannis
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  fullname: Gerakis, Yannis
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– sequence: 7
  givenname: Mei‐Li Diaz
  surname: Hung
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– sequence: 8
  givenname: René
  surname: Vidal
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– sequence: 9
  givenname: Matias
  surname: Fuentealba
  fullname: Fuentealba, Matias
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  organization: Department of Molecular Medicine and Neurodegeneration New Medicines Center, The Scripps Research Institute
– sequence: 21
  givenname: Tomohiro
  surname: Nakamura
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  surname: Sardi
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  organization: Department of Molecular Medicine and Neurodegeneration New Medicines Center, The Scripps Research Institute, Department of Neurosciences, School of Medicine, University of California, San Diego
– sequence: 24
  givenname: Brian K
  surname: Kennedy
  fullname: Kennedy, Brian K
  organization: Buck Institute for Research on Aging, Healthy Longevity Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore; Centre for Healthy Longevity, National University Health System; Departments of Biochemistry and Physiology, Yong Loo Lin School of Medicine, National University of Singapore
– sequence: 25
  givenname: Juan Pablo
  surname: Henriquez
  fullname: Henriquez, Juan Pablo
  organization: Department of Cell Biology, Center for Advanced Microscopy (CMA BioBio), Universidad de Concepción
– sequence: 26
  givenname: J Cesar
  surname: Cárdenas
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  organization: Center for Geroscience, Brain Health and Metabolism, Center for Integrative Biology, Universidad Mayor, Buck Institute for Research on Aging
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  orcidid: 0000-0003-4363-6116
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  givenname: Adrian G
  orcidid: 0000-0003-1532-7527
  surname: Palacios
  fullname: Palacios, Adrian G
  organization: Centro Interdisciplinario de Neurociencia de Valparaíso, Universidad de Valparaiso
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  surname: Hetz
  fullname: Hetz, Claudio
  email: chetz@uchile.cl, chetz@buckinstitute.org
  organization: Center for Geroscience, Brain Health and Metabolism, Biomedical Neuroscience Institute, Faculty of Medicine, University of Chile, Program of Cellular and Molecular Biology, Institute of Biomedical Sciences, Faculty of Medicine, University of Chile, Buck Institute for Research on Aging
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36314651$$D View this record in MEDLINE/PubMed
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  doi: 10.1016/0197-4580(87)90072-8
– ident: e_1_2_9_37_1
  doi: 10.1016/j.bbrc.2007.01.156
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Snippet Aging is a major risk factor to develop neurodegenerative diseases and is associated with decreased buffering capacity of the proteostasis network. We...
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pubmed
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springer
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StartPage e111952
SubjectTerms Ablation
Age
Aging
Aging (natural)
Aging - genetics
aging brain
Animal models
Animals
Brain
Brain - metabolism
Cognitive ability
EMBO24
EMBO27
EMBO32
Endoplasmic reticulum
Endoplasmic Reticulum Stress - genetics
ER stress
Gene transfer
Hippocampus
Mammals
Mice
Neurodegeneration
Neurodegenerative diseases
Phenotypes
Physiology
Protein folding
Protein Serine-Threonine Kinases - genetics
Proteins
Proteomics
proteostasis
Risk analysis
Risk factors
Senescence
Signal transduction
Signal Transduction - physiology
Signaling
Synapses
Unfolded Protein Response
UPR
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
XBP1s
Title Unfolded protein response IRE1/XBP1 signaling is required for healthy mammalian brain aging
URI https://link.springer.com/article/10.15252/embj.2022111952
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.2022111952
https://www.ncbi.nlm.nih.gov/pubmed/36314651
https://www.proquest.com/docview/2737031560
https://www.proquest.com/docview/2730647425
https://pubmed.ncbi.nlm.nih.gov/PMC9670206
Volume 41
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