Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS

Alpha-internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins (NF-L, NF-M, and NF-H) but has an unknown function. The earlier peak expression of alpha-internexin than the triplet during brain development and...

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Published inThe Journal of neuroscience Vol. 26; no. 39; pp. 10006 - 10019
Main Authors Yuan, Aidong, Rao, Mala V, Sasaki, Takahiro, Chen, Yuanxin, Kumar, Asok, Veeranna, Liem, Ronald K H, Eyer, Joel, Peterson, Alan C, Julien, Jean-Pierre, Nixon, Ralph A
Format Journal Article
LanguageEnglish
Published United States Society for Neuroscience 27.09.2006
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Abstract Alpha-internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins (NF-L, NF-M, and NF-H) but has an unknown function. The earlier peak expression of alpha-internexin than the triplet during brain development and its ability to form homopolymers, unlike the triplet, which are obligate heteropolymers, have supported a widely held view that alpha-internexin and neurofilament triplet form separate filament systems. Here, we demonstrate, however, that despite a postnatal decline in expression, alpha-internexin is as abundant as the triplet in the adult CNS and exists in a relatively fixed stoichiometry with these subunits. Alpha-internexin exhibits transport and turnover rates identical to those of triplet proteins in optic axons and colocalizes with NF-M on single neurofilaments by immunogold electron microscopy. Alpha-internexin also coassembles with all three neurofilament proteins into a single network of filaments in quadruple-transfected SW13vim(-) cells. Genetically deleting NF-M alone or together with NF-H in mice dramatically reduces alpha-internexin transport and content in axons throughout the CNS. Moreover, deleting alpha-internexin potentiates the effects of NF-M deletion on NF-H and NF-L transport. Finally, overexpressing a NF-H-LacZ fusion protein in mice induces alpha-internexin and neurofilament triplet to aggregate in neuronal perikarya and greatly reduces their transport and content selectively in axons. Our data show that alpha-internexin and the neurofilament proteins are functionally interdependent. The results strongly support the view that alpha-internexin is a fourth subunit of neurofilaments in the adult CNS, providing a basis for its close relationship with neurofilaments in CNS diseases associated with neurofilament accumulation.
AbstractList α-Internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins (NF-L, NF-M, and NF-H) but has an unknown function. The earlier peak expression of α-internexin than the triplet during brain development and its ability to form homopolymers, unlike the triplet, which are obligate heteropolymers, have supported a widely held view that α-internexin and neurofilament triplet form separate filament systems. Here, we demonstrate, however, that despite a postnatal decline in expression, α-internexin is as abundant as the triplet in the adult CNS and exists in a relatively fixed stoichiometry with these subunits. α-Internexin exhibits transport and turnover rates identical to those of triplet proteins in optic axons and colocalizes with NF-M on single neurofilaments by immunogold electron microscopy. α-Internexin also coassembles with all three neurofilament proteins into a single network of filaments in quadruple-transfected SW13vim(−) cells. Genetically deleting NF-M alone or together with NF-H in mice dramatically reduces α-internexin transport and content in axons throughout the CNS. Moreover, deleting α-internexin potentiates the effects of NF-M deletion on NF-H and NF-L transport. Finally, overexpressing a NF-H–LacZ fusion protein in mice induces α-internexin and neurofilament triplet to aggregate in neuronal perikarya and greatly reduces their transport and content selectively in axons. Our data show that α-internexin and the neurofilament proteins are functionally interdependent. The results strongly support the view that α-internexin is a fourth subunit of neurofilaments in the adult CNS, providing a basis for its close relationship with neurofilaments in CNS diseases associated with neurofilament accumulation.
alpha -Internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins (NF-L, NF-M, and NF-H) but has an unknown function. The earlier peak expression of alpha -internexin than the triplet during brain development and its ability to form homopolymers, unlike the triplet, which are obligate heteropolymers, have supported a widely held view that alpha -internexin and neurofilament triplet form separate filament systems. Here, we demonstrate, however, that despite a postnatal decline in expression, alpha -internexin is as abundant as the triplet in the adult CNS and exists in a relatively fixed stoichiometry with these subunits. alpha -Internexin exhibits transport and turnover rates identical to those of triplet proteins in optic axons and colocalizes with NF-M on single neurofilaments by immunogold electron microscopy. alpha -Internexin also coassembles with all three neurofilament proteins into a single network of filaments in quadruple-transfected SW13vim(-) cells. Genetically deleting NF-M alone or together with NF-H in mice dramatically reduces alpha -internexin transport and content in axons throughout the CNS. Moreover, deleting alpha -internexin potentiates the effects of NF-M deletion on NF-H and NF-L transport. Finally, overexpressing a NF-H-LacZ fusion protein in mice induces alpha -internexin and neurofilament triplet to aggregate in neuronal perikarya and greatly reduces their transport and content selectively in axons. Our data show that alpha -internexin and the neurofilament proteins are functionally interdependent. The results strongly support the view that alpha -internexin is a fourth subunit of neurofilaments in the adult CNS, providing a basis for its close relationship with neurofilaments in CNS diseases associated with neurofilament accumulation.
Author Julien, Jean-Pierre
Peterson, Alan C
Sasaki, Takahiro
Kumar, Asok
Veeranna
Nixon, Ralph A
Liem, Ronald K H
Chen, Yuanxin
Yuan, Aidong
Rao, Mala V
Eyer, Joel
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  surname: Yuan
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  organization: Center for Dementia Research, Nathan Kline Institute, Orangeburg, New York 10962, USA. yuan@nki.rfmh.org
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  givenname: Mala V
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  surname: Chen
  fullname: Chen, Yuanxin
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  surname: Kumar
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  surname: Nixon
  fullname: Nixon, Ralph A
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PublicationTitle The Journal of neuroscience
PublicationTitleAlternate J Neurosci
PublicationYear 2006
Publisher Society for Neuroscience
Publisher_xml – name: Society for Neuroscience
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SSID ssj0007017
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Snippet Alpha-internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins...
α-Internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins (NF-L,...
alpha -Internexin, a neuronal intermediate filament protein implicated in neurodegenerative disease, coexists with the neurofilament (NF) triplet proteins...
SourceID pubmedcentral
proquest
crossref
pubmed
SourceType Open Access Repository
Aggregation Database
Index Database
StartPage 10006
SubjectTerms Animals
Axons - chemistry
Axons - ultrastructure
Crosses, Genetic
Female
Intermediate Filament Proteins - analysis
Intermediate Filament Proteins - deficiency
Intermediate Filament Proteins - genetics
Intermediate Filament Proteins - physiology
Intermediate Filament Proteins - ultrastructure
Intermediate Filaments - chemistry
Intermediate Filaments - ultrastructure
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Microscopy, Confocal
Microscopy, Fluorescence
Microscopy, Immunoelectron
Multiprotein Complexes
Nerve Degeneration - metabolism
Nerve Degeneration - pathology
Neurofilament Proteins - analysis
Neurofilament Proteins - deficiency
Neurofilament Proteins - genetics
Neurofilament Proteins - physiology
Neurofilament Proteins - ultrastructure
Protein Interaction Mapping
Protein Transport
Rats
Recombinant Fusion Proteins - analysis
Recombinant Fusion Proteins - physiology
Retinal Ganglion Cells - chemistry
Retinal Ganglion Cells - ultrastructure
Spinal Cord - chemistry
Spinal Cord - ultrastructure
Structure-Activity Relationship
Transfection
Title Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS
URI https://www.ncbi.nlm.nih.gov/pubmed/17005864
https://search.proquest.com/docview/19362299
https://search.proquest.com/docview/68900976
https://pubmed.ncbi.nlm.nih.gov/PMC6674481
Volume 26
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