Altered Levels of Proteins and Phosphoproteins, in the Absence of Early Causative Transcriptional Changes, Shape the Molecular Pathogenesis in the Brain of Young Presymptomatic Ki91 SCA3/MJD Mouse
Spinocerebellar ataxia type 3 (SCA3/MJD) is a polyQ neurodegenerative disease where the presymptomatic phase of pathogenesis is unknown. Therefore, we investigated the molecular network of transcriptomic and proteomic triggers in young presymptomatic SCA3/MJD brain from Ki91 knock-in mouse. We found...
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Published in | Molecular neurobiology Vol. 56; no. 12; pp. 8168 - 8202 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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New York
Springer US
01.12.2019
Springer Nature B.V |
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Abstract | Spinocerebellar ataxia type 3 (SCA3/MJD) is a polyQ neurodegenerative disease where the presymptomatic phase of pathogenesis is unknown. Therefore, we investigated the molecular network of transcriptomic and proteomic triggers in young presymptomatic SCA3/MJD brain from Ki91 knock-in mouse. We found that transcriptional dysregulations resulting from mutant ataxin-3 are not occurring in young Ki91 mice, while old Ki91 mice and also postmitotic patient SCA3 neurons demonstrate the late transcriptomic changes. Unlike the lack of early mRNA changes, we have identified numerous early changes of total proteins and phosphoproteins in 2-month-old Ki91 mouse cortex and cerebellum. We discovered the network of processes in presymptomatic SCA3 with three main groups of disturbed processes comprising altered proteins: (I) modulation of protein levels and DNA damage (Pabpc1, Ddb1, Nedd8), (II) formation of neuronal cellular structures (Tubb3, Nefh, p-Tau), and (III) neuronal function affected by processes following perturbed cytoskeletal formation (Mt-Co3, Stx1b, p-Syn1). Phosphoproteins downregulate in the young Ki91 mouse brain and their phosphosites are associated with kinases that interact with ATXN3 such as casein kinase, Camk2, and kinases controlled by another Atxn3 interactor p21 such as Gsk3, Pka, and Cdk kinases. We conclude that the onset of SCA3 pathology occurs without altered transcript level and is characterized by changed levels of proteins responsible for termination of translation, DNA damage, spliceosome, and protein phosphorylation. This disturbs global cellular processes such as cytoskeleton and transport of vesicles and mitochondria along axons causing energy deficit and neurodegeneration also manifesting in an altered level of transcripts at later ages. |
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AbstractList | Spinocerebellar ataxia type 3 (SCA3/MJD) is a polyQ neurodegenerative disease where the presymptomatic phase of pathogenesis is unknown. Therefore, we investigated the molecular network of transcriptomic and proteomic triggers in young presymptomatic SCA3/MJD brain from Ki91 knock-in mouse. We found that transcriptional dysregulations resulting from mutant ataxin-3 are not occurring in young Ki91 mice, while old Ki91 mice and also postmitotic patient SCA3 neurons demonstrate the late transcriptomic changes. Unlike the lack of early mRNA changes, we have identified numerous early changes of total proteins and phosphoproteins in 2-month-old Ki91 mouse cortex and cerebellum. We discovered the network of processes in presymptomatic SCA3 with three main groups of disturbed processes comprising altered proteins: (I) modulation of protein levels and DNA damage (Pabpc1, Ddb1, Nedd8), (II) formation of neuronal cellular structures (Tubb3, Nefh, p-Tau), and (III) neuronal function affected by processes following perturbed cytoskeletal formation (Mt-Co3, Stx1b, p-Syn1). Phosphoproteins downregulate in the young Ki91 mouse brain and their phosphosites are associated with kinases that interact with ATXN3 such as casein kinase, Camk2, and kinases controlled by another Atxn3 interactor p21 such as Gsk3, Pka, and Cdk kinases. We conclude that the onset of SCA3 pathology occurs without altered transcript level and is characterized by changed levels of proteins responsible for termination of translation, DNA damage, spliceosome, and protein phosphorylation. This disturbs global cellular processes such as cytoskeleton and transport of vesicles and mitochondria along axons causing energy deficit and neurodegeneration also manifesting in an altered level of transcripts at later ages. |
Author | Piasecki, Piotr Wojciechowski, Paweł Rydzanicz, Małgorzata Figlerowicz, Marek Jungverdorben, Johannes Marczak, Łukasz Kurkowiak, Małgorzata Brüstle, Oliver Figiel, Maciej Handschuh, Luiza Wiatr, Kalina Płoski, Rafał |
Author_xml | – sequence: 1 givenname: Kalina surname: Wiatr fullname: Wiatr, Kalina organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 2 givenname: Piotr surname: Piasecki fullname: Piasecki, Piotr organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 3 givenname: Łukasz surname: Marczak fullname: Marczak, Łukasz organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 4 givenname: Paweł surname: Wojciechowski fullname: Wojciechowski, Paweł organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences, Institute of Computing Science, Poznan University of Technology – sequence: 5 givenname: Małgorzata surname: Kurkowiak fullname: Kurkowiak, Małgorzata organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 6 givenname: Rafał surname: Płoski fullname: Płoski, Rafał organization: Department of Medical Genetics, Medical University of Warsaw – sequence: 7 givenname: Małgorzata surname: Rydzanicz fullname: Rydzanicz, Małgorzata organization: Department of Medical Genetics, Medical University of Warsaw – sequence: 8 givenname: Luiza surname: Handschuh fullname: Handschuh, Luiza organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 9 givenname: Johannes surname: Jungverdorben fullname: Jungverdorben, Johannes organization: Institute of Reconstructive Neurobiology, LIFE & BRAIN Center, University of Bonn School of Medicine & University Hospital Bonn – sequence: 10 givenname: Oliver surname: Brüstle fullname: Brüstle, Oliver organization: Institute of Reconstructive Neurobiology, LIFE & BRAIN Center, University of Bonn School of Medicine & University Hospital Bonn – sequence: 11 givenname: Marek surname: Figlerowicz fullname: Figlerowicz, Marek organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences – sequence: 12 givenname: Maciej orcidid: 0000-0003-3961-4635 surname: Figiel fullname: Figiel, Maciej email: mfigiel@ibch.poznan.pl organization: Institute of Bioorganic Chemistry, Polish Academy of Sciences |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31201651$$D View this record in MEDLINE/PubMed |
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Keywords | Spinocerebellar Presymptomatic Ataxin-3 Mouse SCA3 MJD CAG Ataxia Proteome Phosphoproteome Knock-in PolyQ |
Language | English |
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Snippet | Spinocerebellar ataxia type 3 (SCA3/MJD) is a polyQ neurodegenerative disease where the presymptomatic phase of pathogenesis is unknown. Therefore, we... |
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SubjectTerms | Age Factors Animals Ataxin Ataxin-3 - genetics Ataxin-3 - metabolism Axons Biomedical and Life Sciences Biomedicine Brain Brain - metabolism Brain - pathology Casein Cell Biology Cells, Cultured Cerebellum Cytoskeleton Deoxyribonucleic acid DNA DNA damage Humans Kinases Machado-Joseph disease Machado-Joseph Disease - genetics Machado-Joseph Disease - metabolism Mice Mice, 129 Strain Mice, Inbred C57BL Mice, Transgenic Mitochondria Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Neurobiology Neurodegeneration Neurodegenerative diseases Neurology Neurosciences Pathogenesis Phosphoproteins Phosphoproteins - genetics Phosphoproteins - metabolism Phosphorylation Polyglutamine diseases Protein kinase A Proteins Proteomics Tau protein Transcription Transcription, Genetic - physiology Translation termination Trinucleotide repeat diseases |
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Title | Altered Levels of Proteins and Phosphoproteins, in the Absence of Early Causative Transcriptional Changes, Shape the Molecular Pathogenesis in the Brain of Young Presymptomatic Ki91 SCA3/MJD Mouse |
URI | https://link.springer.com/article/10.1007/s12035-019-01643-4 https://www.ncbi.nlm.nih.gov/pubmed/31201651 https://www.proquest.com/docview/2239964427 https://search.proquest.com/docview/2312802922 https://pubmed.ncbi.nlm.nih.gov/PMC6834541 |
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