Angiogenic patterning by STEEL, an endothelial-enriched long noncoding RNA

Endothelial cell (EC)-enriched protein coding genes, such as endothelial nitric oxide synthase (eNOS), define quintessential EC-specific physiologic functions. It is not clear whether long noncoding RNAs (lncRNAs) also define cardiovascular cell type-specific phenotypes, especially in the vascular e...

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Vydáno v:	Proceedings of the National Academy of Sciences - PNAS Ročník 115; číslo 10; s. 2401
Hlavní autoři:	Man, H S Jeffrey, Sukumar, Aravin N, Lam, Gabrielle C, Turgeon, Paul J, Yan, Matthew S, Ku, Kyung Ha, Dubinsky, Michelle K, Ho, J J David, Wang, Jenny Jing, Das, Sunit, Mitchell, Nora, Oettgen, Peter, Sefton, Michael V, Marsden, Philip A
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States 06.03.2018
Témata:	Animals Cells, Cultured Chromatin - metabolism Endothelial Cells - cytology Endothelial Cells - metabolism Endothelium, Vascular - cytology Hemodynamics Human Umbilical Vein Endothelial Cells Humans Mice Mice, SCID Neovascularization, Physiologic - genetics Neovascularization, Physiologic - physiology RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism long noncoding RNA endothelium chromatin angiogenesis hemodynamics
ISSN:	1091-6490, 1091-6490
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Abstract	Endothelial cell (EC)-enriched protein coding genes, such as endothelial nitric oxide synthase (eNOS), define quintessential EC-specific physiologic functions. It is not clear whether long noncoding RNAs (lncRNAs) also define cardiovascular cell type-specific phenotypes, especially in the vascular endothelium. Here, we report the existence of a set of EC-enriched lncRNAs and define a role for pliced- ranscript ndothelial- nriched lncRNA (STEEL) in angiogenic potential, macrovascular/microvascular identity, and shear stress responsiveness. STEEL is expressed from the terminus of the HOXD locus and is transcribed antisense to HOXD transcription factors. STEEL RNA increases the number and integrity of de novo perfused microvessels in an in vivo model and augments angiogenesis in vitro. The STEEL RNA is polyadenylated, nuclear enriched, and has microvascular predominance. Functionally, STEEL regulates a number of genes in diverse ECs. Of interest, STEEL up-regulates both eNOS and the transcription factor Kruppel-like factor 2 (KLF2), and is subject to feedback inhibition by both eNOS and shear-augmented KLF2. Mechanistically, STEEL up-regulation of eNOS and KLF2 is transcriptionally mediated, in part, via interaction of chromatin-associated STEEL with the poly-ADP ribosylase, PARP1. For instance, STEEL recruits PARP1 to the KLF2 promoter. This work identifies a role for EC-enriched lncRNAs in the phenotypic adaptation of ECs to both body position and hemodynamic forces and establishes a newer role for lncRNAs in the transcriptional regulation of EC identity.
AbstractList	Endothelial cell (EC)-enriched protein coding genes, such as endothelial nitric oxide synthase (eNOS), define quintessential EC-specific physiologic functions. It is not clear whether long noncoding RNAs (lncRNAs) also define cardiovascular cell type-specific phenotypes, especially in the vascular endothelium. Here, we report the existence of a set of EC-enriched lncRNAs and define a role for spliced-transcript endothelial-enriched lncRNA (STEEL) in angiogenic potential, macrovascular/microvascular identity, and shear stress responsiveness. STEEL is expressed from the terminus of the HOXD locus and is transcribed antisense to HOXD transcription factors. STEEL RNA increases the number and integrity of de novo perfused microvessels in an in vivo model and augments angiogenesis in vitro. The STEEL RNA is polyadenylated, nuclear enriched, and has microvascular predominance. Functionally, STEEL regulates a number of genes in diverse ECs. Of interest, STEEL up-regulates both eNOS and the transcription factor Kruppel-like factor 2 (KLF2), and is subject to feedback inhibition by both eNOS and shear-augmented KLF2. Mechanistically, STEEL up-regulation of eNOS and KLF2 is transcriptionally mediated, in part, via interaction of chromatin-associated STEEL with the poly-ADP ribosylase, PARP1. For instance, STEEL recruits PARP1 to the KLF2 promoter. This work identifies a role for EC-enriched lncRNAs in the phenotypic adaptation of ECs to both body position and hemodynamic forces and establishes a newer role for lncRNAs in the transcriptional regulation of EC identity.Endothelial cell (EC)-enriched protein coding genes, such as endothelial nitric oxide synthase (eNOS), define quintessential EC-specific physiologic functions. It is not clear whether long noncoding RNAs (lncRNAs) also define cardiovascular cell type-specific phenotypes, especially in the vascular endothelium. Here, we report the existence of a set of EC-enriched lncRNAs and define a role for spliced-transcript endothelial-enriched lncRNA (STEEL) in angiogenic potential, macrovascular/microvascular identity, and shear stress responsiveness. STEEL is expressed from the terminus of the HOXD locus and is transcribed antisense to HOXD transcription factors. STEEL RNA increases the number and integrity of de novo perfused microvessels in an in vivo model and augments angiogenesis in vitro. The STEEL RNA is polyadenylated, nuclear enriched, and has microvascular predominance. Functionally, STEEL regulates a number of genes in diverse ECs. Of interest, STEEL up-regulates both eNOS and the transcription factor Kruppel-like factor 2 (KLF2), and is subject to feedback inhibition by both eNOS and shear-augmented KLF2. Mechanistically, STEEL up-regulation of eNOS and KLF2 is transcriptionally mediated, in part, via interaction of chromatin-associated STEEL with the poly-ADP ribosylase, PARP1. For instance, STEEL recruits PARP1 to the KLF2 promoter. This work identifies a role for EC-enriched lncRNAs in the phenotypic adaptation of ECs to both body position and hemodynamic forces and establishes a newer role for lncRNAs in the transcriptional regulation of EC identity. Endothelial cell (EC)-enriched protein coding genes, such as endothelial nitric oxide synthase (eNOS), define quintessential EC-specific physiologic functions. It is not clear whether long noncoding RNAs (lncRNAs) also define cardiovascular cell type-specific phenotypes, especially in the vascular endothelium. Here, we report the existence of a set of EC-enriched lncRNAs and define a role for pliced- ranscript ndothelial- nriched lncRNA (STEEL) in angiogenic potential, macrovascular/microvascular identity, and shear stress responsiveness. STEEL is expressed from the terminus of the HOXD locus and is transcribed antisense to HOXD transcription factors. STEEL RNA increases the number and integrity of de novo perfused microvessels in an in vivo model and augments angiogenesis in vitro. The STEEL RNA is polyadenylated, nuclear enriched, and has microvascular predominance. Functionally, STEEL regulates a number of genes in diverse ECs. Of interest, STEEL up-regulates both eNOS and the transcription factor Kruppel-like factor 2 (KLF2), and is subject to feedback inhibition by both eNOS and shear-augmented KLF2. Mechanistically, STEEL up-regulation of eNOS and KLF2 is transcriptionally mediated, in part, via interaction of chromatin-associated STEEL with the poly-ADP ribosylase, PARP1. For instance, STEEL recruits PARP1 to the KLF2 promoter. This work identifies a role for EC-enriched lncRNAs in the phenotypic adaptation of ECs to both body position and hemodynamic forces and establishes a newer role for lncRNAs in the transcriptional regulation of EC identity.
Author	Turgeon, Paul J Das, Sunit Sukumar, Aravin N Lam, Gabrielle C Dubinsky, Michelle K Oettgen, Peter Man, H S Jeffrey Sefton, Michael V Marsden, Philip A Ho, J J David Wang, Jenny Jing Yan, Matthew S Ku, Kyung Ha Mitchell, Nora
Author_xml	– sequence: 1 givenname: H S Jeffrey surname: Man fullname: Man, H S Jeffrey organization: Keenan Research Centre for Biomedical Science in the Li Ka Shing Knowledge Institute, St. Michael's Hospital, University of Toronto, Toronto, ON M5B 1T8, Canada – sequence: 2 givenname: Aravin N surname: Sukumar fullname: Sukumar, Aravin N organization: Keenan Research Centre for Biomedical Science in the Li Ka Shing Knowledge Institute, St. Michael's Hospital, University of Toronto, Toronto, ON M5B 1T8, Canada – sequence: 3 givenname: Gabrielle C surname: Lam fullname: Lam, Gabrielle C organization: Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, ON M5S 3G9, Canada – sequence: 4 givenname: Paul J surname: Turgeon fullname: Turgeon, Paul J organization: Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON M5S 1A8, Canada – sequence: 5 givenname: Matthew S surname: Yan fullname: Yan, Matthew S organization: Department of Medical Biophysics, University of Toronto, Toronto, ON M5G 1L7, Canada – sequence: 6 givenname: Kyung Ha surname: Ku fullname: Ku, Kyung Ha organization: Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON M5S 1A8, Canada – sequence: 7 givenname: Michelle K surname: Dubinsky fullname: Dubinsky, Michelle K organization: Keenan Research Centre for Biomedical Science in the Li Ka Shing Knowledge Institute, St. Michael's Hospital, University of Toronto, Toronto, ON M5B 1T8, Canada – sequence: 8 givenname: J J David surname: Ho fullname: Ho, J J David organization: Department of Medical Biophysics, University of Toronto, Toronto, ON M5G 1L7, Canada – sequence: 9 givenname: Jenny Jing surname: Wang fullname: Wang, Jenny Jing organization: Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON M5S 1A8, Canada – sequence: 10 givenname: Sunit surname: Das fullname: Das, Sunit organization: Division of Neurosurgery and Keenan Research Centre for Biomedical Science, St. Michael's Hospital, University of Toronto, Toronto, ON M5B 1W8, Canada – sequence: 11 givenname: Nora surname: Mitchell fullname: Mitchell, Nora organization: Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115 – sequence: 12 givenname: Peter surname: Oettgen fullname: Oettgen, Peter organization: Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115 – sequence: 13 givenname: Michael V surname: Sefton fullname: Sefton, Michael V organization: Department of Chemical Engineering and Applied Chemistry, University of Toronto, Toronto, ON M5S 3E5, Canada – sequence: 14 givenname: Philip A surname: Marsden fullname: Marsden, Philip A email: p.marsden@utoronto.ca organization: Department of Medical Biophysics, University of Toronto, Toronto, ON M5G 1L7, Canada
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SubjectTerms	Animals Cells, Cultured Chromatin - metabolism Endothelial Cells - cytology Endothelial Cells - metabolism Endothelium, Vascular - cytology Hemodynamics Human Umbilical Vein Endothelial Cells Humans Mice Mice, SCID Neovascularization, Physiologic - genetics Neovascularization, Physiologic - physiology RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism
Title	Angiogenic patterning by STEEL, an endothelial-enriched long noncoding RNA
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