Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1

Summary: The protein α-synuclein, encoded by SNCA, accumulates in Parkinson’s disease (PD) and other synucleinopathies for reasons that remain unclear. Here, we investigated whether SNCA is regulated in vivo by the RNA-binding protein PUM1. We establish that PUM1 binds to SNCA’s 3′ UTR in mouse and...

Full description

Saved in:
Bibliographic Details
Main Authors: Maximilian Cabaj, Pietro G. Mazzara, Zachary A. Gaertner, Ruizhi Wang, Michaela M. Pauers, Lisa K. Randolph, Cláudio Gouveia Roque, Sean Feeney, Serena Raimo, Nicola de Prisco, Alexei Chemiakine, Xinyuan Wang, Ravi K. Singh, Swetha Rajasekaran, Hari K. Yalamanchili, Wayne Miles, Kristin Baldwin, Chaolin Zhang, Matthew B. Harms, Vikram Khurana, Vicky Brandt, Ulrich Hengst, Rajeshwar Awatramani, Vincenzo A. Gennarino
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725009167
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849762430458003456
author Maximilian Cabaj
Pietro G. Mazzara
Zachary A. Gaertner
Ruizhi Wang
Michaela M. Pauers
Lisa K. Randolph
Cláudio Gouveia Roque
Sean Feeney
Serena Raimo
Nicola de Prisco
Alexei Chemiakine
Xinyuan Wang
Ravi K. Singh
Swetha Rajasekaran
Hari K. Yalamanchili
Wayne Miles
Kristin Baldwin
Chaolin Zhang
Matthew B. Harms
Vikram Khurana
Vicky Brandt
Ulrich Hengst
Rajeshwar Awatramani
Vincenzo A. Gennarino
author_facet Maximilian Cabaj
Pietro G. Mazzara
Zachary A. Gaertner
Ruizhi Wang
Michaela M. Pauers
Lisa K. Randolph
Cláudio Gouveia Roque
Sean Feeney
Serena Raimo
Nicola de Prisco
Alexei Chemiakine
Xinyuan Wang
Ravi K. Singh
Swetha Rajasekaran
Hari K. Yalamanchili
Wayne Miles
Kristin Baldwin
Chaolin Zhang
Matthew B. Harms
Vikram Khurana
Vicky Brandt
Ulrich Hengst
Rajeshwar Awatramani
Vincenzo A. Gennarino
author_sort Maximilian Cabaj
collection DOAJ
description Summary: The protein α-synuclein, encoded by SNCA, accumulates in Parkinson’s disease (PD) and other synucleinopathies for reasons that remain unclear. Here, we investigated whether SNCA is regulated in vivo by the RNA-binding protein PUM1. We establish that PUM1 binds to SNCA’s 3′ UTR in mouse and human cells. In induced neurons from patients with SNCA locus triplication, PUM1 mRNA levels are lower than in healthy controls, but increasing PUM1 normalizes both SNCA mRNA and α-synuclein protein levels, largely by suppressing the long 3′ UTR SNCA isoform. In microfluidic chamber experiments, silencing PUM1 causes a redistribution of SNCA between the soma and axons. We also show that the previously described miR-7 regulation of SNCA mRNA requires PUM1. Lastly, we report finding several individuals with PD in clinical databases bearing variants in PUM1 that affect its RNA-binding ability. Understanding how RNA-binding proteins regulate α-synuclein could lead to viable new therapies for synucleinopathies.
format Article
id doaj-art-90bd31d64482437dbca10f3ee4f1aa29
institution DOAJ
issn 2211-1247
language English
publishDate 2025-08-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj-art-90bd31d64482437dbca10f3ee4f1aa292025-08-20T03:05:44ZengElsevierCell Reports2211-12472025-08-0144811614510.1016/j.celrep.2025.116145Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1Maximilian Cabaj0Pietro G. Mazzara1Zachary A. Gaertner2Ruizhi Wang3Michaela M. Pauers4Lisa K. Randolph5Cláudio Gouveia Roque6Sean Feeney7Serena Raimo8Nicola de Prisco9Alexei Chemiakine10Xinyuan Wang11Ravi K. Singh12Swetha Rajasekaran13Hari K. Yalamanchili14Wayne Miles15Kristin Baldwin16Chaolin Zhang17Matthew B. Harms18Vikram Khurana19Vicky Brandt20Ulrich Hengst21Rajeshwar Awatramani22Vincenzo A. Gennarino23Department of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Neurology, Northwestern University, Chicago, IL, USADepartment of Pathology and Cell Biology, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA; Department of Neurology, Columbia University Irving Medical Center, New York, NY, USADepartment of Pathology and Cell Biology, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USADoctoral Program in Neurobiology and Behavior, Columbia University, New York, NY, USATaub Institute for Research on Alzheimer’s Disease and the Aging Brain, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USADoctoral Program in Neurobiology and Behavior, Columbia University, New York, NY, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADivision of Movement Disorders, American Parkinson Disease Association (APDA) Center for Advanced Research and MSA Center of Excellence, Department of Neurology, Brigham and Women’s Hospital, Boston, MA, USA; Harvard Stem Cell Institute, Cambridge, MA, USADepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy University of Houston, Houston, TX, USADepartment of Cancer Biology and Genetics, The Ohio State University, 460 West 12th Avenue, Columbus, OH 43210, USA; The Ohio State University Comprehensive Cancer Center, The Ohio State University, 460 West 12th Avenue, Columbus, OH 43210, USAJan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital, Houston, TX, USA; USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX, USADepartment of Cancer Biology and Genetics, The Ohio State University, 460 West 12th Avenue, Columbus, OH 43210, USA; The Ohio State University Comprehensive Cancer Center, The Ohio State University, 460 West 12th Avenue, Columbus, OH 43210, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Systems Biology, Columbia University Irving Medical Center, New York, NY, USA; Department of Biochemistry and Molecular Biophysics, Columbia University Irving Medical Center, New York, NY, USADepartment of Neurology, Columbia University Irving Medical Center, New York, NY, USADivision of Movement Disorders, American Parkinson Disease Association (APDA) Center for Advanced Research and MSA Center of Excellence, Department of Neurology, Brigham and Women’s Hospital, Boston, MA, USA; Harvard Stem Cell Institute, Cambridge, MA, USA; Harvard Medical School, Boston, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USADepartment of Pathology and Cell Biology, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA; Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USADepartment of Neurology, Northwestern University, Chicago, IL, USADepartment of Genetics and Development, Columbia University Irving Medical Center, New York, NY, USA; Department of Neurology, Columbia University Irving Medical Center, New York, NY, USA; Department of Pediatrics, Columbia University Irving Medical Center, New York, NY, USA; Columbia Stem Cell Initiative, Columbia University Irving Medical Center, New York, NY, USA; Initiative for Columbia Ataxia and Tremor, Columbia University Irving Medical Center, New York, NY, USA; Corresponding authorSummary: The protein α-synuclein, encoded by SNCA, accumulates in Parkinson’s disease (PD) and other synucleinopathies for reasons that remain unclear. Here, we investigated whether SNCA is regulated in vivo by the RNA-binding protein PUM1. We establish that PUM1 binds to SNCA’s 3′ UTR in mouse and human cells. In induced neurons from patients with SNCA locus triplication, PUM1 mRNA levels are lower than in healthy controls, but increasing PUM1 normalizes both SNCA mRNA and α-synuclein protein levels, largely by suppressing the long 3′ UTR SNCA isoform. In microfluidic chamber experiments, silencing PUM1 causes a redistribution of SNCA between the soma and axons. We also show that the previously described miR-7 regulation of SNCA mRNA requires PUM1. Lastly, we report finding several individuals with PD in clinical databases bearing variants in PUM1 that affect its RNA-binding ability. Understanding how RNA-binding proteins regulate α-synuclein could lead to viable new therapies for synucleinopathies.http://www.sciencedirect.com/science/article/pii/S2211124725009167CP: NeuroscienceCP: Molecular biology
spellingShingle Maximilian Cabaj
Pietro G. Mazzara
Zachary A. Gaertner
Ruizhi Wang
Michaela M. Pauers
Lisa K. Randolph
Cláudio Gouveia Roque
Sean Feeney
Serena Raimo
Nicola de Prisco
Alexei Chemiakine
Xinyuan Wang
Ravi K. Singh
Swetha Rajasekaran
Hari K. Yalamanchili
Wayne Miles
Kristin Baldwin
Chaolin Zhang
Matthew B. Harms
Vikram Khurana
Vicky Brandt
Ulrich Hengst
Rajeshwar Awatramani
Vincenzo A. Gennarino
Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
Cell Reports
CP: Neuroscience
CP: Molecular biology
title Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
title_full Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
title_fullStr Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
title_full_unstemmed Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
title_short Alpha-synuclein abundance and localization are regulated by the RNA-binding protein PUMILIO1
title_sort alpha synuclein abundance and localization are regulated by the rna binding protein pumilio1
topic CP: Neuroscience
CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124725009167
work_keys_str_mv AT maximiliancabaj alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT pietrogmazzara alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT zacharyagaertner alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT ruizhiwang alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT michaelampauers alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT lisakrandolph alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT claudiogouveiaroque alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT seanfeeney alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT serenaraimo alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT nicoladeprisco alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT alexeichemiakine alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT xinyuanwang alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT raviksingh alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT swetharajasekaran alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT harikyalamanchili alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT waynemiles alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT kristinbaldwin alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT chaolinzhang alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT matthewbharms alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT vikramkhurana alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT vickybrandt alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT ulrichhengst alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT rajeshwarawatramani alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1
AT vincenzoagennarino alphasynucleinabundanceandlocalizationareregulatedbythernabindingproteinpumilio1