A block of autophagy in lysosomal storage disorders

Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the underlying biochemical defects were identified, the mechanisms from enzyme deficiency to cell death are poorly understood. Here we show that ly...

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Published in:Human molecular genetics Vol. 17; no. 1; p. 119
Main Authors: Settembre, Carmine, Fraldi, Alessandro, Jahreiss, Luca, Spampanato, Carmine, Venturi, Consuelo, Medina, Diego, de Pablo, Raquel, Tacchetti, Carlo, Rubinsztein, David C, Ballabio, Andrea
Format: Journal Article
Language:English
Published: England 01.01.2008
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ISSN:0964-6906
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Abstract Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the underlying biochemical defects were identified, the mechanisms from enzyme deficiency to cell death are poorly understood. Here we show that lysosomal storage impairs autophagic delivery of bulk cytosolic contents to lysosomes. By studying the mouse models of two LSDs associated with severe neurodegeneration, multiple sulfatase deficiency (MSD) and mucopolysaccharidosis type IIIA (MPSIIIA), we observed an accumulation of autophagosomes resulting from defective autophagosome-lysosome fusion. An impairment of the autophagic pathway was demonstrated by the inefficient degradation of exogenous aggregate-prone proteins (i.e. expanded huntingtin and mutated alpha-synuclein) in cells from LSD mice. This impairment resulted in massive accumulation of polyubiquitinated proteins and of dysfunctional mitochondria which are the putative mediators of cell death. These data identify LSDs as 'autophagy disorders' and suggest the presence of common mechanisms in the pathogenesis of these and other neurodegenerative diseases.
AbstractList Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the underlying biochemical defects were identified, the mechanisms from enzyme deficiency to cell death are poorly understood. Here we show that lysosomal storage impairs autophagic delivery of bulk cytosolic contents to lysosomes. By studying the mouse models of two LSDs associated with severe neurodegeneration, multiple sulfatase deficiency (MSD) and mucopolysaccharidosis type IIIA (MPSIIIA), we observed an accumulation of autophagosomes resulting from defective autophagosome-lysosome fusion. An impairment of the autophagic pathway was demonstrated by the inefficient degradation of exogenous aggregate-prone proteins (i.e. expanded huntingtin and mutated alpha-synuclein) in cells from LSD mice. This impairment resulted in massive accumulation of polyubiquitinated proteins and of dysfunctional mitochondria which are the putative mediators of cell death. These data identify LSDs as 'autophagy disorders' and suggest the presence of common mechanisms in the pathogenesis of these and other neurodegenerative diseases.Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the underlying biochemical defects were identified, the mechanisms from enzyme deficiency to cell death are poorly understood. Here we show that lysosomal storage impairs autophagic delivery of bulk cytosolic contents to lysosomes. By studying the mouse models of two LSDs associated with severe neurodegeneration, multiple sulfatase deficiency (MSD) and mucopolysaccharidosis type IIIA (MPSIIIA), we observed an accumulation of autophagosomes resulting from defective autophagosome-lysosome fusion. An impairment of the autophagic pathway was demonstrated by the inefficient degradation of exogenous aggregate-prone proteins (i.e. expanded huntingtin and mutated alpha-synuclein) in cells from LSD mice. This impairment resulted in massive accumulation of polyubiquitinated proteins and of dysfunctional mitochondria which are the putative mediators of cell death. These data identify LSDs as 'autophagy disorders' and suggest the presence of common mechanisms in the pathogenesis of these and other neurodegenerative diseases.
Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the underlying biochemical defects were identified, the mechanisms from enzyme deficiency to cell death are poorly understood. Here we show that lysosomal storage impairs autophagic delivery of bulk cytosolic contents to lysosomes. By studying the mouse models of two LSDs associated with severe neurodegeneration, multiple sulfatase deficiency (MSD) and mucopolysaccharidosis type IIIA (MPSIIIA), we observed an accumulation of autophagosomes resulting from defective autophagosome-lysosome fusion. An impairment of the autophagic pathway was demonstrated by the inefficient degradation of exogenous aggregate-prone proteins (i.e. expanded huntingtin and mutated alpha-synuclein) in cells from LSD mice. This impairment resulted in massive accumulation of polyubiquitinated proteins and of dysfunctional mitochondria which are the putative mediators of cell death. These data identify LSDs as 'autophagy disorders' and suggest the presence of common mechanisms in the pathogenesis of these and other neurodegenerative diseases.
Author Venturi, Consuelo
Ballabio, Andrea
Tacchetti, Carlo
Rubinsztein, David C
Settembre, Carmine
Fraldi, Alessandro
Spampanato, Carmine
de Pablo, Raquel
Medina, Diego
Jahreiss, Luca
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  surname: Settembre
  fullname: Settembre, Carmine
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– sequence: 2
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  surname: Spampanato
  fullname: Spampanato, Carmine
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  surname: Rubinsztein
  fullname: Rubinsztein, David C
– sequence: 10
  givenname: Andrea
  surname: Ballabio
  fullname: Ballabio, Andrea
BackLink https://www.ncbi.nlm.nih.gov/pubmed/17913701$$D View this record in MEDLINE/PubMed
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Snippet Most lysosomal storage disorders (LSDs) are caused by deficiencies of lysosomal hydrolases. While LSDs were among the first inherited diseases for which the...
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StartPage 119
SubjectTerms Animals
Autophagy - genetics
Autophagy - physiology
Base Sequence
Cells, Cultured
DNA Primers - genetics
Humans
Lysosomal Storage Diseases - genetics
Lysosomal Storage Diseases - pathology
Lysosomal Storage Diseases - physiopathology
Lysosomal Storage Diseases, Nervous System - genetics
Lysosomal Storage Diseases, Nervous System - pathology
Lysosomal Storage Diseases, Nervous System - physiopathology
Lysosomes - pathology
Membrane Fusion
Mice
Microtubule-Associated Proteins - genetics
Microtubule-Associated Proteins - metabolism
Mitochondria - pathology
Mucopolysaccharidosis III - genetics
Mucopolysaccharidosis III - pathology
Mucopolysaccharidosis III - physiopathology
Multiple Sulfatase Deficiency Disease - genetics
Multiple Sulfatase Deficiency Disease - pathology
Multiple Sulfatase Deficiency Disease - physiopathology
Nerve Degeneration - genetics
Nerve Degeneration - pathology
Nerve Degeneration - physiopathology
Phagosomes - pathology
Transfection
Ubiquitination
Title A block of autophagy in lysosomal storage disorders
URI https://www.ncbi.nlm.nih.gov/pubmed/17913701
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