TDP-43 mediates SREBF2-regulated gene expression required for oligodendrocyte myelination
Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol...
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| Published in | The Journal of cell biology Vol. 220; no. 9; p. 1 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Rockefeller University Press
06.09.2021
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| Abstract | Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol metabolism in oligodendrocytes. TDP-43 binds directly to mRNA of SREBF2, the master transcription regulator for cholesterol metabolism, and multiple mRNAs encoding proteins responsible for cholesterol biosynthesis and uptake, including HMGCR, HMGCS1, and LDLR. TDP-43 depletion leads to reduced SREBF2 and LDLR expression, and cholesterol levels in vitro and in vivo. TDP-43–mediated changes in cholesterol levels can be restored by reintroducing SREBF2 or LDLR. Additionally, cholesterol supplementation rescues demyelination caused by TDP-43 deletion. Furthermore, oligodendrocytes harboring TDP-43 pathology from FTD patients show reduced HMGCR and HMGCS1, and coaggregation of LDLR and TDP-43. Collectively, our results indicate that TDP-43 plays a role in cholesterol homeostasis in oligodendrocytes, and cholesterol dysmetabolism may be implicated in TDP-43 proteinopathies–related diseases. |
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| AbstractList | Ho et al. provide a novel insight on how loss of TDP-43 (a major disease protein) leads to SREBF2 (a key regulator)–dependent disruption of cholesterol metabolism, which in turn affects myelination. Their results further implicate that disturbance of cholesterol metabolism may be involved in ALS, FTD, and TDP-43 proteinopathies–related disease.
Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol metabolism in oligodendrocytes. TDP-43 binds directly to mRNA of SREBF2, the master transcription regulator for cholesterol metabolism, and multiple mRNAs encoding proteins responsible for cholesterol biosynthesis and uptake, including
HMGCR
,
HMGCS1
, and
LDLR
. TDP-43 depletion leads to reduced SREBF2 and LDLR expression, and cholesterol levels in vitro and in vivo. TDP-43–mediated changes in cholesterol levels can be restored by reintroducing SREBF2 or LDLR. Additionally, cholesterol supplementation rescues demyelination caused by TDP-43 deletion. Furthermore, oligodendrocytes harboring TDP-43 pathology from FTD patients show reduced HMGCR and HMGCS1, and coaggregation of LDLR and TDP-43. Collectively, our results indicate that TDP-43 plays a role in cholesterol homeostasis in oligodendrocytes, and cholesterol dysmetabolism may be implicated in TDP-43 proteinopathies–related diseases. Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol metabolism in oligodendrocytes. TDP-43 binds directly to mRNA of SREBF2, the master transcription regulator for cholesterol metabolism, and multiple mRNAs encoding proteins responsible for cholesterol biosynthesis and uptake, including HMGCR, HMGCS1, and LDLR. TDP-43 depletion leads to reduced SREBF2 and LDLR expression, and cholesterol levels in vitro and in vivo. TDP-43-mediated changes in cholesterol levels can be restored by reintroducing SREBF2 or LDLR. Additionally, cholesterol supplementation rescues demyelination caused by TDP-43 deletion. Furthermore, oligodendrocytes harboring TDP-43 pathology from FTD patients show reduced HMGCR and HMGCS1, and coaggregation of LDLR and TDP-43. Collectively, our results indicate that TDP-43 plays a role in cholesterol homeostasis in oligodendrocytes, and cholesterol dysmetabolism may be implicated in TDP-43 proteinopathies-related diseases. Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol metabolism in oligodendrocytes. TDP-43 binds directly to mRNA of SREBF2, the master transcription regulator for cholesterol metabolism, and multiple mRNAs encoding proteins responsible for cholesterol biosynthesis and uptake, including HMGCR, HMGCS1, and LDLR. TDP-43 depletion leads to reduced SREBF2 and LDLR expression, and cholesterol levels in vitro and in vivo. TDP-43-mediated changes in cholesterol levels can be restored by reintroducing SREBF2 or LDLR. Additionally, cholesterol supplementation rescues demyelination caused by TDP-43 deletion. Furthermore, oligodendrocytes harboring TDP-43 pathology from FTD patients show reduced HMGCR and HMGCS1, and coaggregation of LDLR and TDP-43. Collectively, our results indicate that TDP-43 plays a role in cholesterol homeostasis in oligodendrocytes, and cholesterol dysmetabolism may be implicated in TDP-43 proteinopathies-related diseases.Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that TDP-43, the pathological signature protein for amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), influences cholesterol metabolism in oligodendrocytes. TDP-43 binds directly to mRNA of SREBF2, the master transcription regulator for cholesterol metabolism, and multiple mRNAs encoding proteins responsible for cholesterol biosynthesis and uptake, including HMGCR, HMGCS1, and LDLR. TDP-43 depletion leads to reduced SREBF2 and LDLR expression, and cholesterol levels in vitro and in vivo. TDP-43-mediated changes in cholesterol levels can be restored by reintroducing SREBF2 or LDLR. Additionally, cholesterol supplementation rescues demyelination caused by TDP-43 deletion. Furthermore, oligodendrocytes harboring TDP-43 pathology from FTD patients show reduced HMGCR and HMGCS1, and coaggregation of LDLR and TDP-43. Collectively, our results indicate that TDP-43 plays a role in cholesterol homeostasis in oligodendrocytes, and cholesterol dysmetabolism may be implicated in TDP-43 proteinopathies-related diseases. |
| Author | Ong, Sarah J.M. Cazenave-Gassiot, Amaury Kim, Seung Hyun Agrawal, Ira Arogundade, Olubankole Aladesuyi Foo, Juat Chin Ravits, John Viera-Ortiz, Ashley Muralidharan, Sneha Tucker-Kellogg, Greg Ling, Shuo-Chien Ho, Wan Yun Hoon, Shawn Lee, Edward B. Nguyen, Aivi T. Rodriguez, Maria J. Wenk, Markus R. Hor, Jin Hui Lim, Kenneth Lim, Su Min Chang, Jer-Cherng Ng, Shi-Yan |
| AuthorAffiliation | 13 Program in Neuroscience and Behavior Disorders, Duke–National University of Singapore Medical School, Singapore 3 Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 7 Molecular Engineering Laboratory, ASTAR Research Entities, Singapore 1 Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 9 Department of Neurology, and Biomedical Research Institute, Hanyang University College of Medicine, Seoul, South Korea 5 Translational Neuropathology Research Laboratory, Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 2 Computational Biology Programme, Faculty of Science, National University of Singapore, Singapore 12 Healthy Longevity Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 8 Department of Neurosciences, University of California, San Diego, La Jolla, CA 10 Department of Neurology, Mass |
| AuthorAffiliation_xml | – name: 6 Institute of Molecular and Cell Biology, ASTAR Research Entities, Singapore – name: 1 Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore – name: 9 Department of Neurology, and Biomedical Research Institute, Hanyang University College of Medicine, Seoul, South Korea – name: 3 Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore – name: 5 Translational Neuropathology Research Laboratory, Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA – name: 2 Computational Biology Programme, Faculty of Science, National University of Singapore, Singapore – name: 10 Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA – name: 12 Healthy Longevity Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore, Singapore – name: 11 Department of Biological Sciences, National University of Singapore, Singapore – name: 4 Singapore Lipidomics Incubator, Life Sciences Institute, National University of Singapore, Singapore – name: 7 Molecular Engineering Laboratory, ASTAR Research Entities, Singapore – name: 8 Department of Neurosciences, University of California, San Diego, La Jolla, CA – name: 13 Program in Neuroscience and Behavior Disorders, Duke–National University of Singapore Medical School, Singapore |
| Author_xml | – sequence: 1 givenname: Wan Yun surname: Ho fullname: Ho, Wan Yun – sequence: 2 givenname: Jer-Cherng surname: Chang fullname: Chang, Jer-Cherng – sequence: 3 givenname: Kenneth surname: Lim fullname: Lim, Kenneth – sequence: 4 givenname: Amaury orcidid: 0000-0002-3050-634X surname: Cazenave-Gassiot fullname: Cazenave-Gassiot, Amaury – sequence: 5 givenname: Aivi T. orcidid: 0000-0003-1809-9451 surname: Nguyen fullname: Nguyen, Aivi T. – sequence: 6 givenname: Juat Chin surname: Foo fullname: Foo, Juat Chin – sequence: 7 givenname: Sneha orcidid: 0000-0001-6383-4289 surname: Muralidharan fullname: Muralidharan, Sneha – sequence: 8 givenname: Ashley orcidid: 0000-0003-4633-0622 surname: Viera-Ortiz fullname: Viera-Ortiz, Ashley – sequence: 9 givenname: Sarah J.M. surname: Ong fullname: Ong, Sarah J.M. – sequence: 10 givenname: Jin Hui surname: Hor fullname: Hor, Jin Hui – sequence: 11 givenname: Ira orcidid: 0000-0002-2195-6090 surname: Agrawal fullname: Agrawal, Ira – sequence: 12 givenname: Shawn surname: Hoon fullname: Hoon, Shawn – sequence: 13 givenname: Olubankole Aladesuyi surname: Arogundade fullname: Arogundade, Olubankole Aladesuyi – sequence: 14 givenname: Maria J. surname: Rodriguez fullname: Rodriguez, Maria J. – sequence: 15 givenname: Su Min orcidid: 0000-0002-5769-4854 surname: Lim fullname: Lim, Su Min – sequence: 16 givenname: Seung Hyun orcidid: 0000-0001-9644-9598 surname: Kim fullname: Kim, Seung Hyun – sequence: 17 givenname: John surname: Ravits fullname: Ravits, John – sequence: 18 givenname: Shi-Yan surname: Ng fullname: Ng, Shi-Yan – sequence: 19 givenname: Markus R. surname: Wenk fullname: Wenk, Markus R. – sequence: 20 givenname: Edward B. orcidid: 0000-0002-4589-1180 surname: Lee fullname: Lee, Edward B. – sequence: 21 givenname: Greg orcidid: 0000-0001-8407-9251 surname: Tucker-Kellogg fullname: Tucker-Kellogg, Greg – sequence: 22 givenname: Shuo-Chien orcidid: 0000-0002-0300-8812 surname: Ling fullname: Ling, Shuo-Chien |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34347016$$D View this record in MEDLINE/PubMed |
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| Snippet | Cholesterol metabolism operates autonomously within the central nervous system (CNS), where the majority of cholesterol resides in myelin. We demonstrate that... Ho et al. provide a novel insight on how loss of TDP-43 (a major disease protein) leads to SREBF2 (a key regulator)–dependent disruption of cholesterol... |
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| SubjectTerms | Amyotrophic lateral sclerosis Animals Biosynthesis Central nervous system Cholesterol Cholesterol - metabolism Dementia disorders Demyelination Depletion Disease Models, Animal DNA-Binding Proteins - deficiency DNA-Binding Proteins - genetics Female Frontal Lobe - metabolism Frontal Lobe - pathology Frontotemporal dementia Frontotemporal Dementia - genetics Frontotemporal Dementia - metabolism Frontotemporal Dementia - pathology Gene expression Gene Expression Profiling Gene Expression Regulation Homeostasis Humans Hydroxymethylglutaryl-CoA Synthase - genetics Hydroxymethylglutaryl-CoA Synthase - metabolism Lipid metabolism Lipid Metabolism - genetics Male Membrane and lipid biology Metabolism Mice Mice, Inbred C57BL Mice, Knockout Myelin Myelin Sheath - metabolism Myelin Sheath - pathology Myelination Neuroscience Oligodendrocytes Oligodendroglia - metabolism Oligodendroglia - pathology Organoids - metabolism Organoids - pathology Physiology Primary Cell Culture Proteins Receptors, LDL - genetics Receptors, LDL - metabolism RNA biology Signal Transduction Spinal Cord - metabolism Spinal Cord - pathology Sterol Regulatory Element Binding Protein 2 - genetics Sterol Regulatory Element Binding Protein 2 - metabolism Supplements Temporal Lobe - metabolism Temporal Lobe - pathology Transcription |
| Title | TDP-43 mediates SREBF2-regulated gene expression required for oligodendrocyte myelination |
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