Ablation of SGK1 Impairs Endothelial Cell Migration and Tube Formation Leading to Decreased Neo-Angiogenesis Following Myocardial Infarction
Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after my...
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| Published in | PloS one Vol. 8; no. 11; p. e80268 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
12.11.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0080268 |
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| Abstract | Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-κB signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro, and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo. |
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| AbstractList | Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-κB signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro , and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo. Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-[kappa]B signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro, and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo. Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-κB signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro , and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo. Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-κB signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro, and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo.Serum and glucocorticoid inducible kinase 1 (SGK1) plays a pivotal role in early angiogenesis during embryonic development. In this study, we sought to define the SGK1 downstream signalling pathways in the adult heart and to elucidate their role in cardiac neo-angiogenesis and wound healing after myocardial ischemia. To this end, we employed a viable SGK1 knockout mouse model generated in a 129/SvJ background. Ablation of SGK1 in these mice caused a significant decrease in phosphorylation of SGK1 target protein NDRG1, which correlated with alterations in NF-κB signalling and expression of its downstream target protein, VEGF-A. Disruption of these signalling pathways was accompanied by smaller heart and body size. Moreover, the lack of SGK1 led to defective endothelial cell (ECs) migration and tube formation in vitro, and increased scarring with decreased angiogenesis in vivo after myocardial infarct. This study underscores the importance of SGK1 signalling in cardiac neo-angiogenesis and wound healing after an ischemic insult in vivo. |
| Audience | Academic |
| Author | Lexow, Jonas Sarathchandra, Padmini Poggioli, Tommaso Monassier, Laurent Terracciano, Cesare Zhou, Jessica Q. Rosenzweig, Anthony Rosenthal, Nadia Lang, Florian Damilano, Federico Zarrinpashneh, Elham Santini, Maria Paola |
| AuthorAffiliation | 2 Laboratoire de Neurobiologie et Pharmacologie cardiovasculaire, Strasbourg, France 3 Physiologisches Institut der Universität Tübingen, Tübingen, Germany 4 Cardiovascular Division, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, United States of America University College London, United Kingdom 1 Heart Science Centre, National Heart and Lung Institute, Imperial College London, Harefield, United Kingdom 5 Australian Regenerative Medicine Institute, European Molecular Biology Laboratory Australia/Monash University, Melbourne, Australia |
| AuthorAffiliation_xml | – name: 3 Physiologisches Institut der Universität Tübingen, Tübingen, Germany – name: 5 Australian Regenerative Medicine Institute, European Molecular Biology Laboratory Australia/Monash University, Melbourne, Australia – name: University College London, United Kingdom – name: 2 Laboratoire de Neurobiologie et Pharmacologie cardiovasculaire, Strasbourg, France – name: 1 Heart Science Centre, National Heart and Lung Institute, Imperial College London, Harefield, United Kingdom – name: 4 Cardiovascular Division, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, United States of America |
| Author_xml | – sequence: 1 givenname: Elham surname: Zarrinpashneh fullname: Zarrinpashneh, Elham – sequence: 2 givenname: Tommaso surname: Poggioli fullname: Poggioli, Tommaso – sequence: 3 givenname: Padmini surname: Sarathchandra fullname: Sarathchandra, Padmini – sequence: 4 givenname: Jonas surname: Lexow fullname: Lexow, Jonas – sequence: 5 givenname: Laurent surname: Monassier fullname: Monassier, Laurent – sequence: 6 givenname: Cesare surname: Terracciano fullname: Terracciano, Cesare – sequence: 7 givenname: Florian surname: Lang fullname: Lang, Florian – sequence: 8 givenname: Federico surname: Damilano fullname: Damilano, Federico – sequence: 9 givenname: Jessica Q. surname: Zhou fullname: Zhou, Jessica Q. – sequence: 10 givenname: Anthony surname: Rosenzweig fullname: Rosenzweig, Anthony – sequence: 11 givenname: Nadia surname: Rosenthal fullname: Rosenthal, Nadia – sequence: 12 givenname: Maria Paola surname: Santini fullname: Santini, Maria Paola |
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| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Zarrinpashneh et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Distributed under a Creative Commons Attribution 4.0 International License 2013 Zarrinpashneh et al 2013 Zarrinpashneh et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: EZ MPS. Performed the experiments: EZ MPS TP JL LM PS JQZ. Analyzed the data: EZ MPS JL LM FL NR AR FD CT. Contributed reagents/materials/analysis tools: EZ MPS FL LM FD JQZ AR CT. Wrote the manuscript: EZ MPS NR. Competing Interests: The authors have declared that no competing interests exist. |
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| SubjectTerms | Ablation Analysis Angiogenesis Animals Body size Cancer Cardiology Cardiology and cardiovascular system Cell adhesion & migration Cell Cycle Proteins - metabolism Cell migration Cell Movement - genetics Cell Size Disease Models, Animal Downstream Embryogenesis Embryonic growth stage Endothelial cells Endothelial Cells - metabolism Endothelium Fibrosis Gene expression Glucocorticoids Heart Heart attack Heart diseases Human health and pathology Immediate-Early Proteins - genetics Immediate-Early Proteins - metabolism In vivo methods and tests Intracellular Signaling Peptides and Proteins - metabolism Ischemia Kinases Life Sciences Mice Mice, Knockout Myocardial infarction Myocardial Infarction - genetics Myocardial Infarction - metabolism Myocardial Infarction - pathology Myocardial ischemia Myocardial Ischemia - genetics Myocardial Ischemia - metabolism Myocardial Ischemia - pathology Myocytes, Cardiac - metabolism Myocytes, Cardiac - pathology Neovascularization, Pathologic - genetics Neovascularization, Pathologic - metabolism NF-kappa B - metabolism NF-κB protein Phenotype Phosphorylation Physiology Protein Serine-Threonine Kinases - genetics Protein Serine-Threonine Kinases - metabolism Proteins Proteomics Rodents Scars Science Signal Transduction Signaling Vascular endothelial growth factor Wound healing |
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| Title | Ablation of SGK1 Impairs Endothelial Cell Migration and Tube Formation Leading to Decreased Neo-Angiogenesis Following Myocardial Infarction |
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