Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway

Parkinson's Disease (PD) is characterized by midbrain dopaminergic (mDA) neuron degeneration in the ventral midbrain, contributing to debilitating motor symptoms. This study investigated whether Protein Tyrosine Phosphatase Receptor Sigma (PTPRS), a known inhibitor of axonal growth through chon...

Full description

Saved in:
Bibliographic Details
Main Authors: Joshua Peter, Kaejaren C.N. Caldwell, Lucas McClain, Jason Tchieu, Ashley E. Ross, Yu Luo
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Neurobiology of Disease
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0969996125002396
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850077869943816192
author Joshua Peter
Kaejaren C.N. Caldwell
Lucas McClain
Jason Tchieu
Ashley E. Ross
Yu Luo
author_facet Joshua Peter
Kaejaren C.N. Caldwell
Lucas McClain
Jason Tchieu
Ashley E. Ross
Yu Luo
author_sort Joshua Peter
collection DOAJ
description Parkinson's Disease (PD) is characterized by midbrain dopaminergic (mDA) neuron degeneration in the ventral midbrain, contributing to debilitating motor symptoms. This study investigated whether Protein Tyrosine Phosphatase Receptor Sigma (PTPRS), a known inhibitor of axonal growth through chondroitin sulfate proteoglycan (CSPG) interaction, plays a role in mDA neuron survival, function, and regeneration in PD. Our data show that inhibition of PTPRS using intracellular sigma peptide (ISP) enhances human mDA neuron neurite outgrowth in vitro, suggesting an inhibitory role of this receptor in the differentiation of human embryonic stem cell (hESC)-derived mDA neurons in vitro. However, genetic deletion and pharmacological inhibition of PTPRS does not affect mDA neuron survival, axon density, or motor behavior in 6-OHDA unilateral partially lesioned mice. Similarly, mDA-specific deletion of Ptprs does not affect the basal behavioral measurement in cKO mice, including general locomotion and motor learning. Interestingly, however, Ptprs deletion led to a reduced response in the behavior sensitization to repeated methamphetamine (METH) exposure in cKO mice, suggesting a dampened response in synaptic function in cKO mice under these conditions. Ex vivo voltammetry recording in the striatum indeed shows altered parameters of dopamine (DA) release upon stimulation. These findings indicate that the inhibition of PTPRS function in human mDA neuron progenitors might be a promising strategy for enhancing neurite outgrowth or incorporation in host tissues in transplantation therapies. Finally, our data support that inhibition of PTPRS function in mDA neurons in adult mice in vivo could inhibit METH induced plasticity and behavioral sensitization.
format Article
id doaj-art-ab781b83ec274effb85d64cf34b8fca9
institution DOAJ
issn 1095-953X
language English
publishDate 2025-09-01
publisher Elsevier
record_format Article
series Neurobiology of Disease
spelling doaj-art-ab781b83ec274effb85d64cf34b8fca92025-08-20T02:45:42ZengElsevierNeurobiology of Disease1095-953X2025-09-0121310702310.1016/j.nbd.2025.107023Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathwayJoshua Peter0Kaejaren C.N. Caldwell1Lucas McClain2Jason Tchieu3Ashley E. Ross4Yu Luo5Department of Molecular and Cellular Biosciences, University of Cincinnati, Cincinnati, OH 45229, USANeuroscience Graduate Program, University of Cincinnati, Cincinnati, OH 45229, USADepartment of Molecular and Cellular Biosciences, University of Cincinnati, Cincinnati, OH 45229, USADivision of Developmental Biology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH 45229, USADepartment of Chemistry, University of Cincinnati, Cincinnati, OH 45221, USADepartment of Molecular and Cellular Biosciences, University of Cincinnati, Cincinnati, OH 45229, USA; Neuroscience Graduate Program, University of Cincinnati, Cincinnati, OH 45229, USA; Division of Immunobiology, Cincinnati Children's Hospital Medical Center and the University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA; Corresponding author at: Department of Molecular and Cellular Biosciences, University of Cincinnati, Cincinnati, OH 45229, USA.Parkinson's Disease (PD) is characterized by midbrain dopaminergic (mDA) neuron degeneration in the ventral midbrain, contributing to debilitating motor symptoms. This study investigated whether Protein Tyrosine Phosphatase Receptor Sigma (PTPRS), a known inhibitor of axonal growth through chondroitin sulfate proteoglycan (CSPG) interaction, plays a role in mDA neuron survival, function, and regeneration in PD. Our data show that inhibition of PTPRS using intracellular sigma peptide (ISP) enhances human mDA neuron neurite outgrowth in vitro, suggesting an inhibitory role of this receptor in the differentiation of human embryonic stem cell (hESC)-derived mDA neurons in vitro. However, genetic deletion and pharmacological inhibition of PTPRS does not affect mDA neuron survival, axon density, or motor behavior in 6-OHDA unilateral partially lesioned mice. Similarly, mDA-specific deletion of Ptprs does not affect the basal behavioral measurement in cKO mice, including general locomotion and motor learning. Interestingly, however, Ptprs deletion led to a reduced response in the behavior sensitization to repeated methamphetamine (METH) exposure in cKO mice, suggesting a dampened response in synaptic function in cKO mice under these conditions. Ex vivo voltammetry recording in the striatum indeed shows altered parameters of dopamine (DA) release upon stimulation. These findings indicate that the inhibition of PTPRS function in human mDA neuron progenitors might be a promising strategy for enhancing neurite outgrowth or incorporation in host tissues in transplantation therapies. Finally, our data support that inhibition of PTPRS function in mDA neurons in adult mice in vivo could inhibit METH induced plasticity and behavioral sensitization.http://www.sciencedirect.com/science/article/pii/S0969996125002396PTPRSDopaminergic neuronsSynapsesParkinson's disease
spellingShingle Joshua Peter
Kaejaren C.N. Caldwell
Lucas McClain
Jason Tchieu
Ashley E. Ross
Yu Luo
Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
Neurobiology of Disease
PTPRS
Dopaminergic neurons
Synapses
Parkinson's disease
title Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
title_full Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
title_fullStr Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
title_full_unstemmed Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
title_short Inhibition of PTPRS function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
title_sort inhibition of ptprs function does not affect the survival or regeneration of dopaminergic neurons but alters synaptic function in the nigrostriatal pathway
topic PTPRS
Dopaminergic neurons
Synapses
Parkinson's disease
url http://www.sciencedirect.com/science/article/pii/S0969996125002396
work_keys_str_mv AT joshuapeter inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway
AT kaejarencncaldwell inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway
AT lucasmcclain inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway
AT jasontchieu inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway
AT ashleyeross inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway
AT yuluo inhibitionofptprsfunctiondoesnotaffectthesurvivalorregenerationofdopaminergicneuronsbutalterssynapticfunctioninthenigrostriatalpathway