Genetic background alters the severity and onset of neuromuscular disease caused by the loss of ubiquitin-specific protease 14 (usp14)
In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14...
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Published in | PloS one Vol. 8; no. 12; p. e84042 |
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Language | English |
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16.12.2013
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Abstract | In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14 in ataxia (ax (J)) mice results in reduced ubiquitin levels, motor endplate disease, Purkinje cell axonal dystrophy and decreased hippocampal paired pulse facilitation (PPF) during the first 4-6 weeks of life, and early postnatal lethality by two months of age. Although the loss of USP14 is comparable between the nmf375 and ax (J) mice, the nmf375 mice did not exhibit these ax (J) developmental abnormalities. However, by 12 weeks of age the nmf375 mutants present with ubiquitin depletion and motor endplate disease, indicating a continual role for USP14-mediated regulation of ubiquitin pools and neuromuscular junction (NMJ) structure in adult mice. The observation that motor endplate disease was only seen after ubiquitin depletion suggests that the preservation of NMJ structure requires the stable maintenance of synaptic ubiquitin pools. Differences in genetic background were shown to affect ubiquitin expression and dramatically alter the phenotypes caused by USP14 deficiency. |
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AbstractList | In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14 in ataxia (axJ) mice results in reduced ubiquitin levels, motor endplate disease, Purkinje cell axonal dystrophy and decreased hippocampal paired pulse facilitation (PPF) during the first 4-6 weeks of life, and early postnatal lethality by two months of age. Although the loss of USP14 is comparable between the nmf375 and axJ mice, the nmf375 mice did not exhibit these axJ developmental abnormalities. However, by 12 weeks of age the nmf375 mutants present with ubiquitin depletion and motor endplate disease, indicating a continual role for USP14-mediated regulation of ubiquitin pools and neuromuscular junction (NMJ) structure in adult mice. The observation that motor endplate disease was only seen after ubiquitin depletion suggests that the preservation of NMJ structure requires the stable maintenance of synaptic ubiquitin pools. Differences in genetic background were shown to affect ubiquitin expression and dramatically alter the phenotypes caused by USP14 deficiency. In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14 in ataxia (ax (J)) mice results in reduced ubiquitin levels, motor endplate disease, Purkinje cell axonal dystrophy and decreased hippocampal paired pulse facilitation (PPF) during the first 4-6 weeks of life, and early postnatal lethality by two months of age. Although the loss of USP14 is comparable between the nmf375 and ax (J) mice, the nmf375 mice did not exhibit these ax (J) developmental abnormalities. However, by 12 weeks of age the nmf375 mutants present with ubiquitin depletion and motor endplate disease, indicating a continual role for USP14-mediated regulation of ubiquitin pools and neuromuscular junction (NMJ) structure in adult mice. The observation that motor endplate disease was only seen after ubiquitin depletion suggests that the preservation of NMJ structure requires the stable maintenance of synaptic ubiquitin pools. Differences in genetic background were shown to affect ubiquitin expression and dramatically alter the phenotypes caused by USP14 deficiency. In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14 in ataxia (ax.sup.J) mice results in reduced ubiquitin levels, motor endplate disease, Purkinje cell axonal dystrophy and decreased hippocampal paired pulse facilitation (PPF) during the first 4-6 weeks of life, and early postnatal lethality by two months of age. Although the loss of USP14 is comparable between the nmf375 and ax.sup.J mice, the nmf375 mice did not exhibit these ax.sup.J developmental abnormalities. However, by 12 weeks of age the nmf375 mutants present with ubiquitin depletion and motor endplate disease, indicating a continual role for USP14-mediated regulation of ubiquitin pools and neuromuscular junction (NMJ) structure in adult mice. The observation that motor endplate disease was only seen after ubiquitin depletion suggests that the preservation of NMJ structure requires the stable maintenance of synaptic ubiquitin pools. Differences in genetic background were shown to affect ubiquitin expression and dramatically alter the phenotypes caused by USP14 deficiency. In this study, we identified and characterized an N -ethyl- N -nitrosourea (ENU) induced mutation in Usp14 ( nmf375 ) that leads to adult-onset neurological disease. The nmf375 mutation causes aberrant splicing of Usp14 mRNA, resulting in a 95% reduction in USP14. We previously showed that loss of USP14 in ataxia ( ax J ) mice results in reduced ubiquitin levels, motor endplate disease, Purkinje cell axonal dystrophy and decreased hippocampal paired pulse facilitation (PPF) during the first 4-6 weeks of life, and early postnatal lethality by two months of age. Although the loss of USP14 is comparable between the nmf375 and ax J mice, the nmf375 mice did not exhibit these ax J developmental abnormalities. However, by 12 weeks of age the nmf375 mutants present with ubiquitin depletion and motor endplate disease, indicating a continual role for USP14-mediated regulation of ubiquitin pools and neuromuscular junction (NMJ) structure in adult mice. The observation that motor endplate disease was only seen after ubiquitin depletion suggests that the preservation of NMJ structure requires the stable maintenance of synaptic ubiquitin pools. Differences in genetic background were shown to affect ubiquitin expression and dramatically alter the phenotypes caused by USP14 deficiency. |
Audience | Academic |
Author | Marshall, Andrea G Watson, Jennifer A Phillips, Scott E Walters, Brandon J Wilson, Scott M Wilson, Julie A Dobrunz, Lynn E Francillon, Ludwig Hallengren, Jada J |
AuthorAffiliation | Columbia University, United States of America Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America |
AuthorAffiliation_xml | – name: Columbia University, United States of America – name: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America |
Author_xml | – sequence: 1 givenname: Andrea G surname: Marshall fullname: Marshall, Andrea G organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 2 givenname: Jennifer A surname: Watson fullname: Watson, Jennifer A organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 3 givenname: Jada J surname: Hallengren fullname: Hallengren, Jada J organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 4 givenname: Brandon J surname: Walters fullname: Walters, Brandon J organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 5 givenname: Lynn E surname: Dobrunz fullname: Dobrunz, Lynn E organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 6 givenname: Ludwig surname: Francillon fullname: Francillon, Ludwig organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 7 givenname: Julie A surname: Wilson fullname: Wilson, Julie A organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 8 givenname: Scott E surname: Phillips fullname: Phillips, Scott E organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – sequence: 9 givenname: Scott M surname: Wilson fullname: Wilson, Scott M organization: Department of Neurobiology, Evelyn F. McKnight Brain Institute, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24358326$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Developmental Biology, St. Jude Children’s Research Hospital, Memphis, Tennessee, United States of America Competing Interests: 1- I am a paid consultant for Progenra Incorperated. 2- I have received an honorarium from Proteostasis and Elan Pharmaceuticals for seminars that I presented at their companies. This does not alter our adherence to all of the PLOS ONE policies on sharing data and materials. Conceived and designed the experiments: AGM SEP J. Watson SMW LED LF. Performed the experiments: AGM J. Wilson JJH BJW LF. Analyzed the data: AGW J. Watson JJH BJW. Contributed reagents/materials/analysis tools: LED. Wrote the manuscript: AGM J. Watson SEP SMW. |
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Snippet | In this study, we identified and characterized an N-ethyl-N-nitrosourea (ENU) induced mutation in Usp14 (nmf375) that leads to adult-onset neurological... In this study, we identified and characterized an N -ethyl- N -nitrosourea (ENU) induced mutation in Usp14 ( nmf375 ) that leads to adult-onset neurological... |
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SubjectTerms | Aberration Abnormalities Alternative Splicing Amyotrophic lateral sclerosis Animals Ataxia Axons - pathology Base Sequence Brain research Chromosome Mapping Depletion Disease Models, Animal Dystrophy Enzymes Ethyl nitrosourea Gene Expression Genetic aspects Hippocampus Hippocampus - metabolism Homeostasis - genetics Humans Kinases Laboratory animals Lethality Mice Motor Endplate - metabolism Motor Endplate - pathology mRNA Muscle Fibers, Skeletal - metabolism Muscle Fibers, Skeletal - pathology Mutants Mutation Nervous system Nervous system diseases Neurobiology Neuromuscular Diseases - enzymology Neuromuscular Diseases - genetics Neuromuscular Diseases - mortality Neuromuscular Junction - metabolism Neuromuscular Junction - pathology Neuromuscular junctions Neuronal Plasticity Neurophysiology Neurosciences Phenotype Pools Preservation Proteases Protein Subunits - genetics Proteins Purkinje Cells - cytology Purkinje Cells - metabolism Receptors, Cholinergic - chemistry Receptors, Cholinergic - genetics RNA RNA, Messenger - chemistry RNA, Messenger - genetics Severity of Illness Index Splicing Synapses - metabolism Ubiquitin Ubiquitin - genetics Ubiquitin - metabolism Ubiquitin Thiolesterase - deficiency Ubiquitin Thiolesterase - genetics Ubiquitin-specific proteinase |
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Title | Genetic background alters the severity and onset of neuromuscular disease caused by the loss of ubiquitin-specific protease 14 (usp14) |
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