Obesity-Induced Cellular Senescence Drives Anxiety and Impairs Neurogenesis

Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role...

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Published in:	Cell metabolism Vol. 29; no. 5; pp. 1061 - 1077.e8
Main Authors:	Ogrodnik, Mikolaj, Zhu, Yi, Langhi, Larissa G.P., Tchkonia, Tamar, Krüger, Patrick, Fielder, Edward, Victorelli, Stella, Ruswhandi, Rifqha A., Giorgadze, Nino, Pirtskhalava, Tamar, Podgorni, Oleg, Enikolopov, Grigori, Johnson, Kurt O., Xu, Ming, Inman, Christine, Palmer, Allyson K., Schafer, Marissa, Weigl, Moritz, Ikeno, Yuji, Burns, Terry C., Passos, João F., von Zglinicki, Thomas, Kirkland, James L., Jurk, Diana
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 07-05-2019 Cell Press
Subjects:	aging Animals anxiety Anxiety - drug therapy Anxiety - etiology anxiety-like behavior Astrocytes - metabolism Behavior, Animal - drug effects brain Brain - cytology Brain - embryology Cells, Cultured Cellular Senescence - drug effects Cyclin-Dependent Kinase Inhibitor p16 - genetics Dasatinib - pharmacology Diet, High-Fat - adverse effects Disease Models, Animal Female Fibroblasts - metabolism high-fat diet Lipid Droplets Male Mice Mice, Inbred C57BL Mice, Transgenic Neurogenesis obesity Obesity - complications Obesity - etiology Quercetin - pharmacology senescence stem cells Tacrolimus - analogs & derivatives Tacrolimus - pharmacology Tacrolimus - therapeutic use senescence anxiety stem cells high-fat diet neurogenesis aging anxiety-like behavior brain lipid droplets obesity
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Abstract	Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16Ink4a-expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed “accumulation of lipids in senescence.” Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. [Display omitted] •Obesity drives senescence in glial cells in the LV of mouse brains•Obesity-induced senescence drives fat deposits in PV areas of the brain•Senescent cell clearance in obesity restores neurogenesis in the SVZ•Senescent cell clearance alleviates obesity-induced anxiety-like behavior Obesity, a growing health problem in western societies, is associated with increased senescent cells and neuropsychiatric disorders, including anxiety and depression. Ogrodnik and colleagues found that clearance of senescent cells in obese mice alleviates anxiety. Our study provides proof-of-concept evidence that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders.
AbstractList	Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16 -expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed "accumulation of lipids in senescence." Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16Ink4a-expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed “accumulation of lipids in senescence.” Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. [Display omitted] •Obesity drives senescence in glial cells in the LV of mouse brains•Obesity-induced senescence drives fat deposits in PV areas of the brain•Senescent cell clearance in obesity restores neurogenesis in the SVZ•Senescent cell clearance alleviates obesity-induced anxiety-like behavior Obesity, a growing health problem in western societies, is associated with increased senescent cells and neuropsychiatric disorders, including anxiety and depression. Ogrodnik and colleagues found that clearance of senescent cells in obese mice alleviates anxiety. Our study provides proof-of-concept evidence that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16Ink4a-expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed "accumulation of lipids in senescence." Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders.Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16Ink4a-expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed "accumulation of lipids in senescence." Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16 Ink4a -expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed “accumulation of lipids in senescence.” Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders. • Obesity drives senescence in glial cells in the LV of mouse brains • Obesity-induced senescence drives fat deposits in PV areas of the brain • Senescent cell clearance in obesity restores neurogenesis in the SVZ • Senescent cell clearance alleviates obesity-induced anxiety-like behavior Obesity, a growing health problem in western societies, is associated with increased senescent cells and neuropsychiatric disorders, including anxiety and depression. Ogrodnik and colleagues found that clearance of senescent cells in obese mice alleviates anxiety. Our study provides proof-of-concept evidence that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders.
Author	Tchkonia, Tamar Johnson, Kurt O. Ruswhandi, Rifqha A. Fielder, Edward Zhu, Yi Krüger, Patrick von Zglinicki, Thomas Victorelli, Stella Ogrodnik, Mikolaj Kirkland, James L. Giorgadze, Nino Passos, João F. Ikeno, Yuji Weigl, Moritz Podgorni, Oleg Pirtskhalava, Tamar Jurk, Diana Langhi, Larissa G.P. Schafer, Marissa Enikolopov, Grigori Xu, Ming Inman, Christine Palmer, Allyson K. Burns, Terry C.
AuthorAffiliation	9 Near East University, Arts and Sciences Faculty, Molecular Biology and Genetics, Nicosia, North Cyprus POB 99138 Mersin 10, Turkey 3 Department of Anesthesiology, Stony Brook School of Medicine, 101 Nicolls Road, Stony Brook, New York, NY 11794, USA 6 Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY, USA 2 Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA 8 Departments of Neurologic Surgery and Neuroscience, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA 5 Department of Nano-, Bio-, Information Technology and Cognitive Science, Moscow Institute of Physics and Technology, Moscow, Russia 7 The Barshop Institute for Longevity and Aging Studies, San Antonio, Department of Pathology, The University of Texas Health Science Center at San Antonio, Research Service, Audie L. Murphy VA Hospital (STVHCS), San Antonio, TX 78229, USA 1 Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Camp
AuthorAffiliation_xml	– name: 7 The Barshop Institute for Longevity and Aging Studies, San Antonio, Department of Pathology, The University of Texas Health Science Center at San Antonio, Research Service, Audie L. Murphy VA Hospital (STVHCS), San Antonio, TX 78229, USA – name: 9 Near East University, Arts and Sciences Faculty, Molecular Biology and Genetics, Nicosia, North Cyprus POB 99138 Mersin 10, Turkey – name: 5 Department of Nano-, Bio-, Information Technology and Cognitive Science, Moscow Institute of Physics and Technology, Moscow, Russia – name: 10 Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN 55905, USA – name: 2 Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – name: 8 Departments of Neurologic Surgery and Neuroscience, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – name: 1 Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – name: 4 Center for Developmental Genetics, Stony Brook University, 100 Nicolls Road, Stony Brook, New York, NY 11794, USA – name: 3 Department of Anesthesiology, Stony Brook School of Medicine, 101 Nicolls Road, Stony Brook, New York, NY 11794, USA – name: 6 Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY, USA
Author_xml	– sequence: 1 givenname: Mikolaj surname: Ogrodnik fullname: Ogrodnik, Mikolaj organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 2 givenname: Yi surname: Zhu fullname: Zhu, Yi organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 3 givenname: Larissa G.P. surname: Langhi fullname: Langhi, Larissa G.P. organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 4 givenname: Tamar surname: Tchkonia fullname: Tchkonia, Tamar organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 5 givenname: Patrick surname: Krüger fullname: Krüger, Patrick organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 6 givenname: Edward surname: Fielder fullname: Fielder, Edward organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 7 givenname: Stella surname: Victorelli fullname: Victorelli, Stella organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 8 givenname: Rifqha A. surname: Ruswhandi fullname: Ruswhandi, Rifqha A. organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 9 givenname: Nino surname: Giorgadze fullname: Giorgadze, Nino organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 10 givenname: Tamar surname: Pirtskhalava fullname: Pirtskhalava, Tamar organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 11 givenname: Oleg surname: Podgorni fullname: Podgorni, Oleg organization: Department of Anesthesiology, Stony Brook School of Medicine, 101 Nicolls Road, Stony Brook, New York, NY 11794, USA – sequence: 12 givenname: Grigori surname: Enikolopov fullname: Enikolopov, Grigori organization: Department of Anesthesiology, Stony Brook School of Medicine, 101 Nicolls Road, Stony Brook, New York, NY 11794, USA – sequence: 13 givenname: Kurt O. surname: Johnson fullname: Johnson, Kurt O. organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 14 givenname: Ming surname: Xu fullname: Xu, Ming organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 15 givenname: Christine surname: Inman fullname: Inman, Christine organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 16 givenname: Allyson K. surname: Palmer fullname: Palmer, Allyson K. organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 17 givenname: Marissa surname: Schafer fullname: Schafer, Marissa organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 18 givenname: Moritz surname: Weigl fullname: Weigl, Moritz organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 19 givenname: Yuji surname: Ikeno fullname: Ikeno, Yuji organization: The Barshop Institute for Longevity and Aging Studies, San Antonio, Department of Pathology, The University of Texas Health Science Center at San Antonio, Research Service, Audie L. Murphy VA Hospital (STVHCS), San Antonio, TX 78229, USA – sequence: 20 givenname: Terry C. surname: Burns fullname: Burns, Terry C. organization: Departments of Neurologic Surgery and Neuroscience, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 21 givenname: João F. surname: Passos fullname: Passos, João F. organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 22 givenname: Thomas surname: von Zglinicki fullname: von Zglinicki, Thomas organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK – sequence: 23 givenname: James L. surname: Kirkland fullname: Kirkland, James L. email: kirkland.james@mayo.edu organization: Robert and Arlene Kogod Center on Aging, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA – sequence: 24 givenname: Diana orcidid: 0000-0003-4486-0857 surname: Jurk fullname: Jurk, Diana email: diana.jurk1@ncl.ac.uk organization: Institute for Cell and Molecular Biosciences, Newcastle University Institute for Ageing, Campus for Ageing and Vitality, Newcastle upon Tyne NE4 5PL, UK
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/30612898$$D View this record in MEDLINE/PubMed
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Snippet	Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity...
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SubjectTerms	aging Animals anxiety Anxiety - drug therapy Anxiety - etiology anxiety-like behavior Astrocytes - metabolism Behavior, Animal - drug effects brain Brain - cytology Brain - embryology Cells, Cultured Cellular Senescence - drug effects Cyclin-Dependent Kinase Inhibitor p16 - genetics Dasatinib - pharmacology Diet, High-Fat - adverse effects Disease Models, Animal Female Fibroblasts - metabolism high-fat diet Lipid Droplets Male Mice Mice, Inbred C57BL Mice, Transgenic Neurogenesis obesity Obesity - complications Obesity - etiology Quercetin - pharmacology senescence stem cells Tacrolimus - analogs & derivatives Tacrolimus - pharmacology Tacrolimus - therapeutic use
Title	Obesity-Induced Cellular Senescence Drives Anxiety and Impairs Neurogenesis
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