Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease

Huntington disease’s (HD) is a neurodegenerative disorder caused by the expansion of a polyglutamine region (PolyQ) within the huntingtin protein (HTT). Mutated huntingtin (mHTT) is cytotoxic, particularly for striatal medium spiny neurons (MSNs), whose degeneration is the hallmark of HD. Autophagy...

Full description

Saved in:
Bibliographic Details
Main Authors: Diego Luis-Ravelo, Felipe Fumagallo-Reading, Alejandro Febles-Casquero, Jonathan Lopez-Fernandez, Daniel J. Marcellino, Tomas Gonzalez-Hernandez
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/14/9/652
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850155731397902336
author Diego Luis-Ravelo
Felipe Fumagallo-Reading
Alejandro Febles-Casquero
Jonathan Lopez-Fernandez
Daniel J. Marcellino
Tomas Gonzalez-Hernandez
author_facet Diego Luis-Ravelo
Felipe Fumagallo-Reading
Alejandro Febles-Casquero
Jonathan Lopez-Fernandez
Daniel J. Marcellino
Tomas Gonzalez-Hernandez
author_sort Diego Luis-Ravelo
collection DOAJ
description Huntington disease’s (HD) is a neurodegenerative disorder caused by the expansion of a polyglutamine region (PolyQ) within the huntingtin protein (HTT). Mutated huntingtin (mHTT) is cytotoxic, particularly for striatal medium spiny neurons (MSNs), whose degeneration is the hallmark of HD. Autophagy inducers currently available promote the clearance of toxic proteins. However, due to their low selectivity and the possibility that prolonged autophagy hampers essential processes in unaffected cells, researchers have questioned their benefits in neurodegenerative diseases. Since MSNs express dopamine receptors D2 (DRD2) and D3 (DRD3) and DRD2/DRD3 agonists may activate autophagy, here, we explored how healthy and mHTT-challenged cells respond to prolonged DRD2/DRD3 agonist treatment. Autophagy activation and its effects on mHTT/polyQ clearance were studied in R6/1 mice (a genetic model of HD), their wild-type littermates, and <i>DRD2</i>- and <i>DRD3</i>-HEK cells expressing a pathogenic (Q74) and a non-pathogenic (Q23) polyQ fragment of mHTT treated with the DRD2/DRD3 agonist pramipexole. Two forms of DRD3-mediated autophagy were found: a transient mTORC1-dependent in WT mice and <i>Q23-DRD3</i>-HEK cells and a persistent AMPK-ULK1-activated in R6/1 mice and <i>Q74-DRD3</i>-HEK cells. This also promoted a robust clearance of soluble mHTT/polyQ and neuroprotection in striatal neurons and <i>DRD3</i>-HEK cells. The findings indicate that DRD3-induced autophagy may be a safe, disease-modifying intervention in HD patients.
format Article
id doaj-art-ce70a02a36614feb8655693381574b83
institution OA Journals
issn 2073-4409
language English
publishDate 2025-04-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj-art-ce70a02a36614feb8655693381574b832025-08-20T02:24:47ZengMDPI AGCells2073-44092025-04-0114965210.3390/cells14090652Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s DiseaseDiego Luis-Ravelo0Felipe Fumagallo-Reading1Alejandro Febles-Casquero2Jonathan Lopez-Fernandez3Daniel J. Marcellino4Tomas Gonzalez-Hernandez5Institute of Biomedical Technologies, University of La Laguna, 38200 Tenerife, SpainInstitute of Biomedical Technologies, University of La Laguna, 38200 Tenerife, SpainDepartment of Basic Medical Sciences, Faculty of Medicine, University of La Laguna, 38200 Tenerife, SpainInstitute of Biomedical Technologies, University of La Laguna, 38200 Tenerife, SpainDepartment of Medical and Translational Biology, Umeå University, 901 87 Umeå, SwedenInstitute of Biomedical Technologies, University of La Laguna, 38200 Tenerife, SpainHuntington disease’s (HD) is a neurodegenerative disorder caused by the expansion of a polyglutamine region (PolyQ) within the huntingtin protein (HTT). Mutated huntingtin (mHTT) is cytotoxic, particularly for striatal medium spiny neurons (MSNs), whose degeneration is the hallmark of HD. Autophagy inducers currently available promote the clearance of toxic proteins. However, due to their low selectivity and the possibility that prolonged autophagy hampers essential processes in unaffected cells, researchers have questioned their benefits in neurodegenerative diseases. Since MSNs express dopamine receptors D2 (DRD2) and D3 (DRD3) and DRD2/DRD3 agonists may activate autophagy, here, we explored how healthy and mHTT-challenged cells respond to prolonged DRD2/DRD3 agonist treatment. Autophagy activation and its effects on mHTT/polyQ clearance were studied in R6/1 mice (a genetic model of HD), their wild-type littermates, and <i>DRD2</i>- and <i>DRD3</i>-HEK cells expressing a pathogenic (Q74) and a non-pathogenic (Q23) polyQ fragment of mHTT treated with the DRD2/DRD3 agonist pramipexole. Two forms of DRD3-mediated autophagy were found: a transient mTORC1-dependent in WT mice and <i>Q23-DRD3</i>-HEK cells and a persistent AMPK-ULK1-activated in R6/1 mice and <i>Q74-DRD3</i>-HEK cells. This also promoted a robust clearance of soluble mHTT/polyQ and neuroprotection in striatal neurons and <i>DRD3</i>-HEK cells. The findings indicate that DRD3-induced autophagy may be a safe, disease-modifying intervention in HD patients.https://www.mdpi.com/2073-4409/14/9/652dopamine receptorsHuntington’s diseaseneuroprotectionULK1mTORC1AMPK
spellingShingle Diego Luis-Ravelo
Felipe Fumagallo-Reading
Alejandro Febles-Casquero
Jonathan Lopez-Fernandez
Daniel J. Marcellino
Tomas Gonzalez-Hernandez
Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
Cells
dopamine receptors
Huntington’s disease
neuroprotection
ULK1
mTORC1
AMPK
title Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
title_full Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
title_fullStr Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
title_full_unstemmed Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
title_short Dopamine Receptor D3 Induces Transient, mTORC1-Dependent Autophagy That Becomes Persistent, AMPK-Mediated, and Neuroprotective in Experimental Models of Huntington’s Disease
title_sort dopamine receptor d3 induces transient mtorc1 dependent autophagy that becomes persistent ampk mediated and neuroprotective in experimental models of huntington s disease
topic dopamine receptors
Huntington’s disease
neuroprotection
ULK1
mTORC1
AMPK
url https://www.mdpi.com/2073-4409/14/9/652
work_keys_str_mv AT diegoluisravelo dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease
AT felipefumagalloreading dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease
AT alejandrofeblescasquero dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease
AT jonathanlopezfernandez dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease
AT danieljmarcellino dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease
AT tomasgonzalezhernandez dopaminereceptord3inducestransientmtorc1dependentautophagythatbecomespersistentampkmediatedandneuroprotectiveinexperimentalmodelsofhuntingtonsdisease