α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1

doi:10.1111/acel.12922

Title: α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1

Authors:

Sampaio‐Marques, Belém ^[1]; Guedes, Ana ^[1]; Vasilevskiy, Igor ^[1]; Gonçalves, Susana ^[2]; Outeiro, Tiago F. ^[3]; Winderickx, Joris ^[4]; Burhans, William C. ^[5];

^[1]

School of Medicine, Life and Health Sciences Research Institute (ICVS) University of Minho Braga Portugal, ICVS/3B’s ‐ PT Government Associate Laboratory Guimarães Portugal
Faculdade de Ciências Médicas, CEDOC – Chronic Diseases Research Center Universidade Nova de Lisboa Lisboa Portugal
Faculdade de Ciências Médicas, CEDOC – Chronic Diseases Research Center Universidade Nova de Lisboa Lisboa Portugal, Department of Experimental Neurodegeneration, Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB) University Medical Center Göttingen Göttingen Germany, Center for Biostructural Imaging of Neurodegeneration Göttingen Germany, Max Planck Institute for Experimental Medicine Göttingen Germany
Functional Biology KU Leuven Heverlee Belgium
Department of Molecular and Cellular Biology Roswell Park Cancer Institute Buffalo New York

Publication Date:: 2019-04-11

Sponsoring Org.:: USDOE Office of Nuclear Energy (NE), Fuel Cycle Technologies (NE-5)

OSTI Identifier:: 1506720

Alternate Identifier(s):: OSTI ID: 1506721

Grant/Contract Number:: SFRH/BPD/90533/2012

Resource Type:: Published Article

Journal Name:: Aging Cell

Additional Journal Information:: Journal Name: Aging Cell Journal Volume: 18 Journal Issue: 4; Journal ID: ISSN 1474-9718

Publisher:: Wiley-Blackwell

Country of Publication:: United States

Language:: English

Citation Formats


                    Sampaio‐Marques, Belém, Guedes, Ana, Vasilevskiy, Igor, Gonçalves, Susana, Outeiro, Tiago F., Winderickx, Joris, Burhans, William C., and Ludovico, Paula. α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1.  United States: N. p., 2019. 
        Web.  doi:10.1111/acel.12922.

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                    Sampaio‐Marques, Belém, Guedes, Ana, Vasilevskiy, Igor, Gonçalves, Susana, Outeiro, Tiago F., Winderickx, Joris, Burhans, William C., & Ludovico, Paula. α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1.  United States.  doi:10.1111/acel.12922.

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                    Sampaio‐Marques, Belém, Guedes, Ana, Vasilevskiy, Igor, Gonçalves, Susana, Outeiro, Tiago F., Winderickx, Joris, Burhans, William C., and Ludovico, Paula. Thu .  
        "α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1".  United States.  doi:10.1111/acel.12922.

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@article{osti_1506720,

  title        = {α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1},

  author       = {Sampaio‐Marques, Belém and Guedes, Ana and Vasilevskiy, Igor and Gonçalves, Susana and Outeiro, Tiago F. and Winderickx, Joris and Burhans, William C. and Ludovico, Paula},

  abstractNote = {},

  doi          = {10.1111/acel.12922},

  journal      = {Aging Cell},

  number       = 4,

  volume       = 18,

  place        = {United States},

  year         = {2019},

  month        = {4}

}

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DOI: 10.1111/acel.12922

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Title: α‐Synuclein toxicity in yeast and human cells is caused by cell cycle re‐entry and autophagy degradation of ribonucleotide reductase 1

Citation Formats

Cell Cycle Analysis of Yeasts journal, July 2000

Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) journal, January 2016

DJ-1 interactions with α-synuclein attenuate aggregation and cellular toxicity in models of Parkinson’s disease journal, July 2014

Leveraging DNA Damage Response Signaling to Identify Yeast Genes Controlling Genome Stability journal, February 2015

Cell cycle aberrations by α-synuclein over-expression and cyclin B immunoreactivity in Lewy bodies journal, September 2003

Cyclin-Dependent Kinase Activity Is Required for Apoptotic Death But Not Inclusion Formation in Cortical Neurons after Proteasomal Inhibition journal, February 2003

Yeast models of Parkinson’s disease-associated molecular pathologies journal, June 2017

DNA replication stress-induced loss of reproductive capacity in S. cerevisiae and its inhibition by caloric restriction journal, April 2013

DNA Replication Stress Is a Determinant of Chronological Lifespan in Budding Yeast journal, August 2007

The mechanism of sirtuin 2–mediated exacerbation of alpha-synuclein toxicity in models of Parkinson disease journal, March 2017

Autophagy-Dependent Regulation of the DNA Damage Response Protein Ribonucleotide Reductase 1 journal, February 2011

Re-expression of cell cycle markers in aged neurons and muscles: Whether cells should divide or die? journal, January 2017

Sodium butyrate rescues dopaminergic cells from alpha-synuclein-induced transcriptional deregulation and DNA damage journal, March 2017

Sirtuins and Proteolytic Systems: Implications for Pathogenesis of Synucleinopathies journal, May 2015

MEC1-Dependent Redistribution of the Sir3 Silencing Protein from Telomeres to DNA Double-Strand Breaks journal, May 1999

Cyclin Cln3 Is Retained at the ER and Released by the J Chaperone Ydj1 in Late G1 to Trigger Cell Cycle Entry journal, June 2007

α-synuclein toxicity in neurodegeneration: mechanism and therapeutic strategies journal, February 2017

Diversity in the Regulation of Autophagy and Mitophagy: Lessons from Parkinson's Disease journal, January 2011

Glucose tolerance status and risk of dementia in the community: The Hisayama Study journal, September 2011

Recent Developments in Yeast Aging journal, January 2007

Essential Function of Mec1, the Budding Yeast ATM/ATR Checkpoint-Response Kinase, in Protein Homeostasis journal, August 2018

SNCA (α-synuclein)-induced toxicity in yeast cells is dependent on Sir2-mediated mitophagy journal, October 2012

Caloric restriction alleviates alpha-synuclein toxicity in aged yeast cells by controlling the opposite roles of Tor1 and Sir2 on autophagy journal, January 2017

Alpha-synuclein functions in the nucleus to protect against hydroxyurea-induced replication stress in yeast journal, June 2011

Effect of chloroquine on proteolytic processes and energy metabolism in yeast journal, February 1984

α-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity journal, September 2006

Yeast Cells Provide Insight into Alpha-Synuclein Biology and Pathobiology journal, December 2003

Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease journal, October 2003

A pathway of targeted autophagy is induced by DNA damage in budding yeast journal, February 2017

Activation of ataxia telangiectasia muted under experimental models and human Parkinson’s disease journal, May 2010

The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease journal, February 2007

The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage journal, July 2001

Role of the Cell Cycle Re-Initiation in DNA Damage Response of Post-Mitotic Cells and Its Implication in the Pathogenesis of Neurodegenerative Diseases journal, April 2016

YGR198w ( YPP1 ) targets A30P α-synuclein to the vacuole for degradation journal, June 2007

Role of Cell Cycle Re-Entry in Neurons: A Common Apoptotic Mechanism of Neuronal Cell Death journal, October 2011

Alpha-synuclein and Protein Degradation Systems: a Reciprocal Relationship journal, September 2012

Heat Shock Prevents Alpha-synuclein-induced Apoptosis in a Yeast Model of Parkinson's Disease journal, September 2005

Cell Cycle Analysis of Yeasts
journal, July 2000

Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
journal, January 2016

DJ-1 interactions with α-synuclein attenuate aggregation and cellular toxicity in models of Parkinson’s disease
journal, July 2014

Leveraging DNA Damage Response Signaling to Identify Yeast Genes Controlling Genome Stability
journal, February 2015

Cell cycle aberrations by α-synuclein over-expression and cyclin B immunoreactivity in Lewy bodies
journal, September 2003

Cyclin-Dependent Kinase Activity Is Required for Apoptotic Death But Not Inclusion Formation in Cortical Neurons after Proteasomal Inhibition
journal, February 2003

Yeast models of Parkinson’s disease-associated molecular pathologies
journal, June 2017

DNA replication stress-induced loss of reproductive capacity in S. cerevisiae and its inhibition by caloric restriction
journal, April 2013

DNA Replication Stress Is a Determinant of Chronological Lifespan in Budding Yeast
journal, August 2007

The mechanism of sirtuin 2–mediated exacerbation of alpha-synuclein toxicity in models of Parkinson disease
journal, March 2017

Autophagy-Dependent Regulation of the DNA Damage Response Protein Ribonucleotide Reductase 1
journal, February 2011

Re-expression of cell cycle markers in aged neurons and muscles: Whether cells should divide or die?
journal, January 2017

Sodium butyrate rescues dopaminergic cells from alpha-synuclein-induced transcriptional deregulation and DNA damage
journal, March 2017

Sirtuins and Proteolytic Systems: Implications for Pathogenesis of Synucleinopathies
journal, May 2015

MEC1-Dependent Redistribution of the Sir3 Silencing Protein from Telomeres to DNA Double-Strand Breaks
journal, May 1999

Cyclin Cln3 Is Retained at the ER and Released by the J Chaperone Ydj1 in Late G1 to Trigger Cell Cycle Entry
journal, June 2007

α-synuclein toxicity in neurodegeneration: mechanism and therapeutic strategies
journal, February 2017

Diversity in the Regulation of Autophagy and Mitophagy: Lessons from Parkinson's Disease
journal, January 2011

Glucose tolerance status and risk of dementia in the community: The Hisayama Study
journal, September 2011

Recent Developments in Yeast Aging
journal, January 2007

Essential Function of Mec1, the Budding Yeast ATM/ATR Checkpoint-Response Kinase, in Protein Homeostasis
journal, August 2018

SNCA (α-synuclein)-induced toxicity in yeast cells is dependent on Sir2-mediated mitophagy
journal, October 2012

Caloric restriction alleviates alpha-synuclein toxicity in aged yeast cells by controlling the opposite roles of Tor1 and Sir2 on autophagy
journal, January 2017

Alpha-synuclein functions in the nucleus to protect against hydroxyurea-induced replication stress in yeast
journal, June 2011

Effect of chloroquine on proteolytic processes and energy metabolism in yeast
journal, February 1984

α-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity
journal, September 2006

Yeast Cells Provide Insight into Alpha-Synuclein Biology and Pathobiology
journal, December 2003

Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease
journal, October 2003

A pathway of targeted autophagy is induced by DNA damage in budding yeast
journal, February 2017

Activation of ataxia telangiectasia muted under experimental models and human Parkinson’s disease
journal, May 2010

The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease
journal, February 2007

The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage
journal, July 2001

Role of the Cell Cycle Re-Initiation in DNA Damage Response of Post-Mitotic Cells and Its Implication in the Pathogenesis of Neurodegenerative Diseases
journal, April 2016

YGR198w ( YPP1 ) targets A30P α-synuclein to the vacuole for degradation
journal, June 2007

Role of Cell Cycle Re-Entry in Neurons: A Common Apoptotic Mechanism of Neuronal Cell Death
journal, October 2011

Alpha-synuclein and Protein Degradation Systems: a Reciprocal Relationship
journal, September 2012

Heat Shock Prevents Alpha-synuclein-induced Apoptosis in a Yeast Model of Parkinson's Disease
journal, September 2005