Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.

The capacity of a cell to maintain proteostasis progressively declines during aging. Virtually all age-associated neurodegenerative disorders associated with aggregation of neurotoxic proteins are linked to defects in the cellular proteostasis network, including insufficient lysosomal hydrolysis. He...

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Main Authors: Lukas Habernig, Filomena Broeskamp, Andreas Aufschnaiter, Jutta Diessl, Carlotta Peselj, Elisabeth Urbauer, Tobias Eisenberg, Ana de Ory, Sabrina Büttner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-11-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009911&type=printable
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author Lukas Habernig
Filomena Broeskamp
Andreas Aufschnaiter
Jutta Diessl
Carlotta Peselj
Elisabeth Urbauer
Tobias Eisenberg
Ana de Ory
Sabrina Büttner
author_facet Lukas Habernig
Filomena Broeskamp
Andreas Aufschnaiter
Jutta Diessl
Carlotta Peselj
Elisabeth Urbauer
Tobias Eisenberg
Ana de Ory
Sabrina Büttner
author_sort Lukas Habernig
collection DOAJ
description The capacity of a cell to maintain proteostasis progressively declines during aging. Virtually all age-associated neurodegenerative disorders associated with aggregation of neurotoxic proteins are linked to defects in the cellular proteostasis network, including insufficient lysosomal hydrolysis. Here, we report that proteotoxicity in yeast and Drosophila models for Parkinson's disease can be prevented by increasing the bioavailability of Ca2+, which adjusts intracellular Ca2+ handling and boosts lysosomal proteolysis. Heterologous expression of human α-synuclein (αSyn), a protein critically linked to Parkinson's disease, selectively increases total cellular Ca2+ content, while the levels of manganese and iron remain unchanged. Disrupted Ca2+ homeostasis results in inhibition of the lysosomal protease cathepsin D and triggers premature cellular and organismal death. External administration of Ca2+ reduces αSyn oligomerization, stimulates cathepsin D activity and in consequence restores survival, which critically depends on the Ca2+/calmodulin-dependent phosphatase calcineurin. In flies, increasing the availability of Ca2+ discloses a neuroprotective role of αSyn upon manganese overload. In sum, we establish a molecular interplay between cathepsin D and calcineurin that can be activated by Ca2+ administration to counteract αSyn proteotoxicity.
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issn 1553-7390
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publishDate 2021-11-01
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spelling doaj-art-3275e960d02c424789ab4ab1a2d49e6a2025-08-20T02:31:41ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-11-011711e100991110.1371/journal.pgen.1009911Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.Lukas HabernigFilomena BroeskampAndreas AufschnaiterJutta DiesslCarlotta PeseljElisabeth UrbauerTobias EisenbergAna de OrySabrina BüttnerThe capacity of a cell to maintain proteostasis progressively declines during aging. Virtually all age-associated neurodegenerative disorders associated with aggregation of neurotoxic proteins are linked to defects in the cellular proteostasis network, including insufficient lysosomal hydrolysis. Here, we report that proteotoxicity in yeast and Drosophila models for Parkinson's disease can be prevented by increasing the bioavailability of Ca2+, which adjusts intracellular Ca2+ handling and boosts lysosomal proteolysis. Heterologous expression of human α-synuclein (αSyn), a protein critically linked to Parkinson's disease, selectively increases total cellular Ca2+ content, while the levels of manganese and iron remain unchanged. Disrupted Ca2+ homeostasis results in inhibition of the lysosomal protease cathepsin D and triggers premature cellular and organismal death. External administration of Ca2+ reduces αSyn oligomerization, stimulates cathepsin D activity and in consequence restores survival, which critically depends on the Ca2+/calmodulin-dependent phosphatase calcineurin. In flies, increasing the availability of Ca2+ discloses a neuroprotective role of αSyn upon manganese overload. In sum, we establish a molecular interplay between cathepsin D and calcineurin that can be activated by Ca2+ administration to counteract αSyn proteotoxicity.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009911&type=printable
spellingShingle Lukas Habernig
Filomena Broeskamp
Andreas Aufschnaiter
Jutta Diessl
Carlotta Peselj
Elisabeth Urbauer
Tobias Eisenberg
Ana de Ory
Sabrina Büttner
Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
PLoS Genetics
title Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
title_full Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
title_fullStr Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
title_full_unstemmed Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
title_short Ca2+ administration prevents α-synuclein proteotoxicity by stimulating calcineurin-dependent lysosomal proteolysis.
title_sort ca2 administration prevents α synuclein proteotoxicity by stimulating calcineurin dependent lysosomal proteolysis
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009911&type=printable
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