1-deoxysphingolipids bind to COUP-TF to modulate lymphatic and cardiac cell development
Identification of physiological modulators of nuclear hormone receptor (NHR) activity is paramount for understanding the link between metabolism and transcriptional networks that orchestrate development and cellular physiology. Using libraries of metabolic enzymes alongside their substrates and prod...
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Published in | Developmental cell Vol. 56; no. 22; pp. 3128 - 3145.e15 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
22.11.2021
Elsevier |
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Abstract | Identification of physiological modulators of nuclear hormone receptor (NHR) activity is paramount for understanding the link between metabolism and transcriptional networks that orchestrate development and cellular physiology. Using libraries of metabolic enzymes alongside their substrates and products, we identify 1-deoxysphingosines as modulators of the activity of NR2F1 and 2 (COUP-TFs), which are orphan NHRs that are critical for development of the nervous system, heart, veins, and lymphatic vessels. We show that these non-canonical alanine-based sphingolipids bind to the NR2F1/2 ligand-binding domains (LBDs) and modulate their transcriptional activity in cell-based assays at physiological concentrations. Furthermore, inhibition of sphingolipid biosynthesis phenocopies NR2F1/2 deficiency in endothelium and cardiomyocytes, and increases in 1-deoxysphingosine levels activate NR2F1/2-dependent differentiation programs. Our findings suggest that 1-deoxysphingosines are physiological regulators of NR2F1/2-mediated transcription.
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•1-deoxyphingosines bind and modulate NR2F1 and NR2F2 transcriptional activity•Genetic deletion of Sptlc2 phenocopies Nr2f2 deficiency in lymphatic development•Inhibition of sphingolipid synthesis impairs human cardiomyocyte differentiation•1-deoxysphingosine supplementation promotes human cardiomyocyte maturation
Wang et al. identify 1-deoxysphingosines as modulators of COUP-TF activity. Inhibition of sphingolipid biosynthesis mimics COUP-TF knockout phenotypes in lymphatic development and in human ESC-derived cardiomyocytes, whereas elevated levels of 1-deoxysphingosines enhance cardiomyocyte differentiation. Thus, sphingolipids could be physiological ligands for COUP-TFs and could play a critical role in development. |
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AbstractList | Identification of physiological modulators of nuclear hormone receptor (NHR) activity is paramount for understanding the link between metabolism and transcriptional networks that orchestrate development and cellular physiology. Using libraries of metabolic enzymes alongside their substrates and products, we identify 1-deoxysphingosines as modulators of the activity of NR2F1 and 2 (COUP-TFs), which are orphan NHRs that are critical for development of the nervous system, heart, veins, and lymphatic vessels. We show that these non-canonical alanine-based sphingolipids bind to the NR2F1/2 ligand-binding domains (LBDs) and modulate their transcriptional activity in cell-based assays at physiological concentrations. Furthermore, inhibition of sphingolipid biosynthesis phenocopies NR2F1/2 deficiency in endothelium and cardiomyocytes, and increases in 1-deoxysphingosine levels activate NR2F1/2-dependent differentiation programs. Our findings suggest that 1-deoxysphingosines are physiological regulators of NR2F1/2-mediated transcription.
[Display omitted]
•1-deoxyphingosines bind and modulate NR2F1 and NR2F2 transcriptional activity•Genetic deletion of Sptlc2 phenocopies Nr2f2 deficiency in lymphatic development•Inhibition of sphingolipid synthesis impairs human cardiomyocyte differentiation•1-deoxysphingosine supplementation promotes human cardiomyocyte maturation
Wang et al. identify 1-deoxysphingosines as modulators of COUP-TF activity. Inhibition of sphingolipid biosynthesis mimics COUP-TF knockout phenotypes in lymphatic development and in human ESC-derived cardiomyocytes, whereas elevated levels of 1-deoxysphingosines enhance cardiomyocyte differentiation. Thus, sphingolipids could be physiological ligands for COUP-TFs and could play a critical role in development. Identification of physiological modulators of nuclear hormone receptor (NHR) activity is paramount for understanding the link between metabolism and transcriptional networks that orchestrate development and cellular physiology. Using libraries of metabolic enzymes alongside their substrates and products, we identify 1-deoxysphingosines as modulators of the activity of NR2F1 and 2 (COUP-TFs), which are orphan NHRs that are critical for development of the nervous system, heart, veins, and lymphatic vessels. We show that these non-canonical alanine-based sphingolipids bind to the NR2F1/2 ligand-binding domains (LBDs) and modulate their transcriptional activity in cell-based assays at physiological concentrations. Furthermore, inhibition of sphingolipid biosynthesis phenocopies NR2F1/2 deficiency in endothelium and cardiomyocytes, and increases in 1-deoxysphingosine levels activate NR2F1/2-dependent differentiation programs. Our findings suggest that 1-deoxysphingosines are physiological regulators of NR2F1/2-mediated transcription. Identification of physiological modulators of nuclear hormone receptor (NHR) activity is paramount for understanding the link between metabolism and transcriptional networks that orchestrate development and cellular physiology. Using libraries of metabolic enzymes alongside their substrates and products, we identify 1-deoxysphingosines as modulators of NR2F1/2 (COUP-TFs) activity, which are orphan NHRs critical for development of the nervous system, heart, veins, and lymphatic vessels. We show that these non-canonical alanine-based sphingolipids bind to the NR2F1/2 ligand binding domains (LBDs) and modulate their transcriptional activity in cell-based assays at physiological concentrations. Furthermore, inhibition of sphingolipid biosynthesis phenocopies NR2F1/2 deficiency in endothelium and cardiomyocytes, while increases in 1-deoxysphingosine levels activate NR2F1/2-dependent differentiation programs. Our findings suggest that 1-deoxysphingosines are found in tissues at concentrations high enough to have a physiological function as regulators of NR2F1/2-mediated transcription. 1-deoxysphingosines are physiological modulators of COUP-TFs. Wang et al identify 1-deoxysphingosines as modulator of COUP-TF activity. Inhibition of sphingolipid biosynthesis mimics COUP-TF knockout phenotypes in lymphatic development and in human ESC-derived cardiomyocytes whereas elevated levels of 1-deoxysphingosines enhance cardiomyocyte differentiation. Thus, sphingolipids could be physiological ligands for COUP-TFs with a critical role in development. |
Author | Wang, Ting Alecu, Irina Tao, Jinglian Arenz, Christoph Wang, Zheng Kaech, Susan M. Seo, Dong Eun Lee, Ho-Joon Jackson, Benjamin Parker, Mikhail Zhou, Ting Ivanova, Natalia B. de Fabritus, Lauriane Burkhardt, Daniel Gleinich, Anne S. Krishnaswamy, Smita Hornemann, Thorsten Ramazanov, Bulat R. Wang, Zhirui van de Pavert, Serge A. Santori, Fabio R. Saied, Essa M. Xu, Shihao Azadi, Parastoo |
AuthorAffiliation | 7 Institut für Chemie, Humboldt Universität zu Berlin, Berlin 12489, Germany 11 Department of Cell Biology, Yale University, New Haven, CT 06520, USA 3 Department of Genetics and Cell Biology, Basic Medical College, Qingdao University, Qingdao, Shandong 266071, China 15 Institute of Clinical Chemistry, University and University Hospital of Zurich, Zurich, CH-8091, Switzerland 6 Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA 2 Department of Hematology, Tianjin Medical University General Hospital, Tianjin 300052, China 5 Aix-Marseille University, CNRS, INSERM, Centre d’Immunologie de Marseille-Luminy, 13288 Marseille Cedex 9, France 4 Department of Reproductive Medicine, the Affiliated Hospital of Qingdao University, Qingdao, Shandong 266000, China 8 Chemistry Department, Faculty of Science, Suez Canal University, Ismailia 41522, Egypt 10 Center for Genome Analysis, Yale University, New Haven, CT 06510, USA 1 Department of Immunobiology, Yale Un |
AuthorAffiliation_xml | – name: 6 Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA – name: 7 Institut für Chemie, Humboldt Universität zu Berlin, Berlin 12489, Germany – name: 12 Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA – name: 3 Department of Genetics and Cell Biology, Basic Medical College, Qingdao University, Qingdao, Shandong 266071, China – name: 2 Department of Hematology, Tianjin Medical University General Hospital, Tianjin 300052, China – name: 4 Department of Reproductive Medicine, the Affiliated Hospital of Qingdao University, Qingdao, Shandong 266000, China – name: 11 Department of Cell Biology, Yale University, New Haven, CT 06520, USA – name: 16 Lead contact – name: 5 Aix-Marseille University, CNRS, INSERM, Centre d’Immunologie de Marseille-Luminy, 13288 Marseille Cedex 9, France – name: 1 Department of Immunobiology, Yale University, New Haven, CT 06520, USA – name: 9 Department of Genetics, Yale University, New Haven, CT 06520, USA – name: 13 NOMIS Center for Immunobiology and Microbial Pathogenesis, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA – name: 15 Institute of Clinical Chemistry, University and University Hospital of Zurich, Zurich, CH-8091, Switzerland – name: 8 Chemistry Department, Faculty of Science, Suez Canal University, Ismailia 41522, Egypt – name: 10 Center for Genome Analysis, Yale University, New Haven, CT 06510, USA – name: 14 Neural Regeneration Laboratory, Department of Biochemistry, Microbiology, and Immunology, University of Ottawa, Ottawa, K1H 8M5, Canada |
Author_xml | – sequence: 1 givenname: Ting surname: Wang fullname: Wang, Ting organization: Department of Immunobiology, Yale University, New Haven, CT 06520, USA – sequence: 2 givenname: Zheng surname: Wang fullname: Wang, Zheng organization: Department of Genetics and Cell Biology, Basic Medical College, Qingdao University, Qingdao, Shandong 266071, China – sequence: 3 givenname: Lauriane surname: de Fabritus fullname: de Fabritus, Lauriane organization: Aix-Marseille Universite, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML), 13288 Marseille Cedex 9, France – sequence: 4 givenname: Jinglian surname: Tao fullname: Tao, Jinglian organization: Department of Hematology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 5 givenname: Essa M. surname: Saied fullname: Saied, Essa M. organization: Institut für Chemie, Humboldt Universität zu Berlin, Berlin 12489, Germany – sequence: 6 givenname: Ho-Joon surname: Lee fullname: Lee, Ho-Joon organization: Department of Genetics, Yale University, New Haven, CT 06520, USA – sequence: 7 givenname: Bulat R. surname: Ramazanov fullname: Ramazanov, Bulat R. organization: Department of Cell Biology, Yale University, New Haven, CT 06520, USA – sequence: 8 givenname: Benjamin surname: Jackson fullname: Jackson, Benjamin organization: Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA – sequence: 9 givenname: Daniel surname: Burkhardt fullname: Burkhardt, Daniel organization: Department of Genetics, Yale University, New Haven, CT 06520, USA – sequence: 10 givenname: Mikhail surname: Parker fullname: Parker, Mikhail organization: Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA – sequence: 11 givenname: Anne S. surname: Gleinich fullname: Gleinich, Anne S. organization: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA – sequence: 12 givenname: Zhirui surname: Wang fullname: Wang, Zhirui organization: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA – sequence: 13 givenname: Dong Eun surname: Seo fullname: Seo, Dong Eun organization: Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA – sequence: 14 givenname: Ting surname: Zhou fullname: Zhou, Ting organization: Department of Immunobiology, Yale University, New Haven, CT 06520, USA – sequence: 15 givenname: Shihao surname: Xu fullname: Xu, Shihao organization: NOMIS Center for Immunobiology and Microbial Pathogenesis, the Salk Institute for Biological Studies, La Jolla, CA 92037, USA – sequence: 16 givenname: Irina surname: Alecu fullname: Alecu, Irina organization: Neural Regeneration Laboratory, Department of Biochemistry, Microbiology, and Immunology, University of Ottawa, Ottawa K1H 8M5, Canada – sequence: 17 givenname: Parastoo surname: Azadi fullname: Azadi, Parastoo organization: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA – sequence: 18 givenname: Christoph surname: Arenz fullname: Arenz, Christoph organization: Institut für Chemie, Humboldt Universität zu Berlin, Berlin 12489, Germany – sequence: 19 givenname: Thorsten surname: Hornemann fullname: Hornemann, Thorsten organization: Institute of Clinical Chemistry, University and University Hospital of Zurich, Zurich 8091, Switzerland – sequence: 20 givenname: Smita surname: Krishnaswamy fullname: Krishnaswamy, Smita organization: Department of Genetics, Yale University, New Haven, CT 06520, USA – sequence: 21 givenname: Serge A. surname: van de Pavert fullname: van de Pavert, Serge A. organization: Aix-Marseille Universite, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy (CIML), 13288 Marseille Cedex 9, France – sequence: 22 givenname: Susan M. surname: Kaech fullname: Kaech, Susan M. email: skaech@salk.edu organization: NOMIS Center for Immunobiology and Microbial Pathogenesis, the Salk Institute for Biological Studies, La Jolla, CA 92037, USA – sequence: 23 givenname: Natalia B. surname: Ivanova fullname: Ivanova, Natalia B. email: natalia.ivanova@uga.edu organization: Center for Molecular Medicine, Department of Genetics, University of Georgia, Athens, GA 30602, USA – sequence: 24 givenname: Fabio R. surname: Santori fullname: Santori, Fabio R. email: fabio.santori@yale.edu organization: Department of Immunobiology, Yale University, New Haven, CT 06520, USA |
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Keywords | SPTLC2 sphingolipid cardiomyocyte NR2F1 metabolism NR2F2 COUP-TF 1-deoxysphingosine NR2F6 lymphatic |
Language | English |
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Notes | These authors contributed equally. Conceptualization, methodology, writing, review and editing: FRS, NBI. Supervision and project administration: FRS, NBI and SMK. Investigation and validation: TW, LF, ZW, JT, BRR, BJ, TZ, AG, ZhiW, PA, SX, MP, DES, TH, CA, EMS, IA, and SvP, NBI, FRS. Resources: ZW, JT, TH, CA, EMS and IA. Formal data analysis and curation: NBI, BRR, HJL, DB and SK. Author contributions |
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SubjectTerms | 1-deoxysphingosine Animals cardiomyocyte Cell Differentiation - drug effects Cell Differentiation - physiology COUP-TF Gene Expression Regulation - drug effects Gene Expression Regulation - physiology Humans Life Sciences lymphatic Lymphatic Vessels - drug effects metabolism Mice NR2F1 NR2F2 NR2F6 Organogenesis - drug effects Organogenesis - physiology Repressor Proteins - physiology sphingolipid Sphingolipids - pharmacology SPTLC2 |
Title | 1-deoxysphingolipids bind to COUP-TF to modulate lymphatic and cardiac cell development |
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