Interaction of Alpha-Synuclein With Lipids: Mitochondrial Cardiolipin as a Critical Player in the Pathogenesis of Parkinson’s Disease

Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson’s disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully un...

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Veröffentlicht in:Frontiers in neuroscience Jg. 14; S. 578993
Hauptverfasser: Gilmozzi, Valentina, Gentile, Giovanna, Castelo Rueda, Maria Paulina, Hicks, Andrew A., Pramstaller, Peter P., Zanon, Alessandra, Lévesque, Martin, Pichler, Irene
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Sprache:Englisch
Veröffentlicht: Lausanne Frontiers Research Foundation 06.10.2020
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ISSN:1662-453X, 1662-4548, 1662-453X
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Abstract Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson’s disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully understood. It is, however, widely regarded to be associated with the misfolding and accumulation of toxic intracellular aggregates. In fact, α-Syn is the most abundant protein component of Lewy bodies and Lewy neurites, which are also characterized by a high lipid content. Lipids, the main constituents of cellular membranes, have been implicated in many aspects of PD-related processes. α-Syn interacts with membrane phospholipids and free fatty acids via its N-terminal domain, and altered lipid-protein complexes might enhance both its binding to synaptic and mitochondrial membranes and its oligomerization. Several studies have highlighted a specific interaction of α-Syn with the phospholipid cardiolipin, a major constituent of mitochondrial membranes. By interacting with cardiolipin, α-Syn is able to disrupt mitochondrial membrane integrity, leading to mitochondrial dysfunction. Additionally, externalized cardiolipin is able to facilitate the refolding of toxic α-Syn species at the outer mitochondrial membrane. In this review, we discuss how α-Syn/lipid interactions, in particular the α-Syn/cardiolipin interaction at the mitochondrial membrane, may affect α-Syn aggregation and mitochondrial dysfunction and may thus represent an important mechanism in the pathogenesis of PD.
AbstractList Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson’s disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully understood. It is, however, widely regarded to be associated with the misfolding and accumulation of toxic intracellular aggregates. In fact, α-Syn is the most abundant protein component of Lewy bodies and Lewy neurites, which are also characterized by a high lipid content. Lipids, the main constituents of cellular membranes, have been implicated in many aspects of PD-related processes. α-Syn interacts with membrane phospholipids and free fatty acids via its N-terminal domain, and altered lipid-protein complexes might enhance both its binding to synaptic and mitochondrial membranes and its oligomerization. Several studies have highlighted a specific interaction of α-Syn with the phospholipid cardiolipin (CL), a major constituent of mitochondrial membranes. By interacting with CL, α-Syn is able to disrupt mitochondrial membrane integrity, leading to mitochondrial dysfunction. Additionally, externalized CL is able to facilitate the refolding of toxic α-Syn species at the outer mitochondrial membrane. In this review, we discuss how α-Syn/lipid interactions, in particular the α-Syn/CL interaction at the mitochondrial membrane, may affect α-Syn aggregation and mitochondrial dysfunction and may thus represent an important mechanism in the pathogenesis of PD.
Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson's disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully understood. It is, however, widely regarded to be associated with the misfolding and accumulation of toxic intracellular aggregates. In fact, α-Syn is the most abundant protein component of Lewy bodies and Lewy neurites, which are also characterized by a high lipid content. Lipids, the main constituents of cellular membranes, have been implicated in many aspects of PD-related processes. α-Syn interacts with membrane phospholipids and free fatty acids via its N-terminal domain, and altered lipid-protein complexes might enhance both its binding to synaptic and mitochondrial membranes and its oligomerization. Several studies have highlighted a specific interaction of α-Syn with the phospholipid cardiolipin (CL), a major constituent of mitochondrial membranes. By interacting with CL, α-Syn is able to disrupt mitochondrial membrane integrity, leading to mitochondrial dysfunction. Additionally, externalized CL is able to facilitate the refolding of toxic α-Syn species at the outer mitochondrial membrane. In this review, we discuss how α-Syn/lipid interactions, in particular the α-Syn/CL interaction at the mitochondrial membrane, may affect α-Syn aggregation and mitochondrial dysfunction and may thus represent an important mechanism in the pathogenesis of PD.Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson's disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully understood. It is, however, widely regarded to be associated with the misfolding and accumulation of toxic intracellular aggregates. In fact, α-Syn is the most abundant protein component of Lewy bodies and Lewy neurites, which are also characterized by a high lipid content. Lipids, the main constituents of cellular membranes, have been implicated in many aspects of PD-related processes. α-Syn interacts with membrane phospholipids and free fatty acids via its N-terminal domain, and altered lipid-protein complexes might enhance both its binding to synaptic and mitochondrial membranes and its oligomerization. Several studies have highlighted a specific interaction of α-Syn with the phospholipid cardiolipin (CL), a major constituent of mitochondrial membranes. By interacting with CL, α-Syn is able to disrupt mitochondrial membrane integrity, leading to mitochondrial dysfunction. Additionally, externalized CL is able to facilitate the refolding of toxic α-Syn species at the outer mitochondrial membrane. In this review, we discuss how α-Syn/lipid interactions, in particular the α-Syn/CL interaction at the mitochondrial membrane, may affect α-Syn aggregation and mitochondrial dysfunction and may thus represent an important mechanism in the pathogenesis of PD.
Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson’s disease (PD). Although its role in neurotransmission is well established, the precise role of this protein in disease pathogenesis is still not fully understood. It is, however, widely regarded to be associated with the misfolding and accumulation of toxic intracellular aggregates. In fact, α-Syn is the most abundant protein component of Lewy bodies and Lewy neurites, which are also characterized by a high lipid content. Lipids, the main constituents of cellular membranes, have been implicated in many aspects of PD-related processes. α-Syn interacts with membrane phospholipids and free fatty acids via its N-terminal domain, and altered lipid-protein complexes might enhance both its binding to synaptic and mitochondrial membranes and its oligomerization. Several studies have highlighted a specific interaction of α-Syn with the phospholipid cardiolipin, a major constituent of mitochondrial membranes. By interacting with cardiolipin, α-Syn is able to disrupt mitochondrial membrane integrity, leading to mitochondrial dysfunction. Additionally, externalized cardiolipin is able to facilitate the refolding of toxic α-Syn species at the outer mitochondrial membrane. In this review, we discuss how α-Syn/lipid interactions, in particular the α-Syn/cardiolipin interaction at the mitochondrial membrane, may affect α-Syn aggregation and mitochondrial dysfunction and may thus represent an important mechanism in the pathogenesis of PD.
Author Lévesque, Martin
Gentile, Giovanna
Hicks, Andrew A.
Pramstaller, Peter P.
Pichler, Irene
Castelo Rueda, Maria Paulina
Gilmozzi, Valentina
Zanon, Alessandra
AuthorAffiliation 1 Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck , Bolzano , Italy
2 Department of Neurology, University of Lübeck , Lübeck , Germany
3 Department of Psychiatry and Neurosciences, Cervo Brain Research Centre, Université Laval , Quebec, QC, Canada
AuthorAffiliation_xml – name: 1 Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of Lübeck , Bolzano , Italy
– name: 3 Department of Psychiatry and Neurosciences, Cervo Brain Research Centre, Université Laval , Quebec, QC, Canada
– name: 2 Department of Neurology, University of Lübeck , Lübeck , Germany
Author_xml – sequence: 1
  givenname: Valentina
  surname: Gilmozzi
  fullname: Gilmozzi, Valentina
– sequence: 2
  givenname: Giovanna
  surname: Gentile
  fullname: Gentile, Giovanna
– sequence: 3
  givenname: Maria Paulina
  surname: Castelo Rueda
  fullname: Castelo Rueda, Maria Paulina
– sequence: 4
  givenname: Andrew A.
  surname: Hicks
  fullname: Hicks, Andrew A.
– sequence: 5
  givenname: Peter P.
  surname: Pramstaller
  fullname: Pramstaller, Peter P.
– sequence: 6
  givenname: Alessandra
  surname: Zanon
  fullname: Zanon, Alessandra
– sequence: 7
  givenname: Martin
  surname: Lévesque
  fullname: Lévesque, Martin
– sequence: 8
  givenname: Irene
  surname: Pichler
  fullname: Pichler, Irene
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Copyright © 2020 Gilmozzi, Gentile, Castelo Rueda, Hicks, Pramstaller, Zanon, Lévesque and Pichler.
Copyright © 2020 Gilmozzi, Gentile, Castelo Rueda, Hicks, Pramstaller, Zanon, Lévesque and Pichler. 2020 Gilmozzi, Gentile, Castelo Rueda, Hicks, Pramstaller, Zanon, Lévesque and Pichler
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Edited by: Cong Liu, University of Chinese Academy of Sciences, China
This article was submitted to Neurodegeneration, a section of the journal Frontiers in Neuroscience
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Reviewed by: Yoshitaka Nagai, Osaka University, Japan; Ulf Dettmer, Harvard Medical School, United States
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Snippet Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson’s disease...
Alpha-Synuclein (α-Syn) is a central protein in the pathogenesis of synucleinopathies, a group of neurodegenerative disorders including Parkinson's disease...
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SubjectTerms aggregation
alpha-synuclein
Amino acids
Axons
Cardiolipin
Cell membranes
Disease
Fatty acids
Lewy bodies
Lipids
Membranes
Mitochondria
Movement disorders
Mutation
Neurodegeneration
Neurodegenerative diseases
Neurons
Neuroscience
Neurotransmission
Oligomerization
Parkinson's disease
Pathogenesis
Phospholipids
Physiology
Proteins
Synuclein
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