Primary cilia control glucose homeostasis via islet paracrine interactions
Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remai...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 16; pp. 8912 - 8923 |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
21.04.2020
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.2001936117 |
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| Abstract | Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remain incompletely characterized. We generated mice specifically lacking β-cell primary cilia, a cellular organelle that has been implicated in regulating insulin secretion, and found that the β-cell cilia are required for glucose sensing, calcium influx, insulin secretion, and cross regulation of α- and δ-cells. Protein expression profiling in islets confirms perturbation in these cellular processes and reveals additional targets of cilia-dependent signaling. At the organism level, the deletion of β-cell cilia disrupts circulating hormone levels, impairs glucose homeostasis and fuel usage, and leads to the development of diabetes. Together, these findings demonstrate that primary cilia not only orchestrate β-cell–intrinsic activity but also mediate cross talk both within the islet and from islets to other metabolic tissues, thus providing a unique role of cilia in nutrient metabolism and insight into the pathophysiology of diabetes. |
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| AbstractList | Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remain incompletely characterized. We generated mice specifically lacking β-cell primary cilia, a cellular organelle that has been implicated in regulating insulin secretion, and found that the β-cell cilia are required for glucose sensing, calcium influx, insulin secretion, and cross regulation of α- and δ-cells. Protein expression profiling in islets confirms perturbation in these cellular processes and reveals additional targets of cilia-dependent signaling. At the organism level, the deletion of β-cell cilia disrupts circulating hormone levels, impairs glucose homeostasis and fuel usage, and leads to the development of diabetes. Together, these findings demonstrate that primary cilia not only orchestrate β-cell-intrinsic activity but also mediate cross talk both within the islet and from islets to other metabolic tissues, thus providing a unique role of cilia in nutrient metabolism and insight into the pathophysiology of diabetes.Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remain incompletely characterized. We generated mice specifically lacking β-cell primary cilia, a cellular organelle that has been implicated in regulating insulin secretion, and found that the β-cell cilia are required for glucose sensing, calcium influx, insulin secretion, and cross regulation of α- and δ-cells. Protein expression profiling in islets confirms perturbation in these cellular processes and reveals additional targets of cilia-dependent signaling. At the organism level, the deletion of β-cell cilia disrupts circulating hormone levels, impairs glucose homeostasis and fuel usage, and leads to the development of diabetes. Together, these findings demonstrate that primary cilia not only orchestrate β-cell-intrinsic activity but also mediate cross talk both within the islet and from islets to other metabolic tissues, thus providing a unique role of cilia in nutrient metabolism and insight into the pathophysiology of diabetes. Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remain incompletely characterized. We generated mice specifically lacking β-cell primary cilia, a cellular organelle that has been implicated in regulating insulin secretion, and found that the β-cell cilia are required for glucose sensing, calcium influx, insulin secretion, and cross regulation of α- and δ-cells. Protein expression profiling in islets confirms perturbation in these cellular processes and reveals additional targets of cilia-dependent signaling. At the organism level, the deletion of β-cell cilia disrupts circulating hormone levels, impairs glucose homeostasis and fuel usage, and leads to the development of diabetes. Together, these findings demonstrate that primary cilia not only orchestrate β-cell–intrinsic activity but also mediate cross talk both within the islet and from islets to other metabolic tissues, thus providing a unique role of cilia in nutrient metabolism and insight into the pathophysiology of diabetes. The primary cilium is a small subcompartment of the cell but has powerful influence on pancreatic islet function. In this study, we find a critical role for cilia in regulating β-cell function and energy metabolism. Importantly, the deletion of β-cell cilia disrupts intercellular communication and leads to islet dysfunction and diabetes, as seen in a number of human ciliopathy syndromes. These results should help elucidate pathophysiology of human ciliopathy and aid the development of pharmacologic agents targeting primary cilia that may lead to a more effective treatment for human diabetes. Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is the close approximation and communication among heterogeneous cell populations, but the structural mediators of islet cellular cross talk remain incompletely characterized. We generated mice specifically lacking β-cell primary cilia, a cellular organelle that has been implicated in regulating insulin secretion, and found that the β-cell cilia are required for glucose sensing, calcium influx, insulin secretion, and cross regulation of α- and δ-cells. Protein expression profiling in islets confirms perturbation in these cellular processes and reveals additional targets of cilia-dependent signaling. At the organism level, the deletion of β-cell cilia disrupts circulating hormone levels, impairs glucose homeostasis and fuel usage, and leads to the development of diabetes. Together, these findings demonstrate that primary cilia not only orchestrate β-cell–intrinsic activity but also mediate cross talk both within the islet and from islets to other metabolic tissues, thus providing a unique role of cilia in nutrient metabolism and insight into the pathophysiology of diabetes. |
| Author | Conway, Hannah E. Hughes, Jing W. Cho, Jung Hoon DiGruccio, Michael R. Ng, Xue Wen Urano, Fumihiko Abreu, Damien Piston, David W. Roseman, Henry F. |
| Author_xml | – sequence: 1 givenname: Jing W. surname: Hughes fullname: Hughes, Jing W. – sequence: 2 givenname: Jung Hoon surname: Cho fullname: Cho, Jung Hoon – sequence: 3 givenname: Hannah E. surname: Conway fullname: Conway, Hannah E. – sequence: 4 givenname: Michael R. surname: DiGruccio fullname: DiGruccio, Michael R. – sequence: 5 givenname: Xue Wen surname: Ng fullname: Ng, Xue Wen – sequence: 6 givenname: Henry F. surname: Roseman fullname: Roseman, Henry F. – sequence: 7 givenname: Damien surname: Abreu fullname: Abreu, Damien – sequence: 8 givenname: Fumihiko surname: Urano fullname: Urano, Fumihiko – sequence: 9 givenname: David W. surname: Piston fullname: Piston, David W. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32253320$$D View this record in MEDLINE/PubMed |
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| Snippet | Pancreatic islets regulate glucose homeostasis through coordinated actions of hormone-secreting cells. What underlies the function of the islet as a unit is... The primary cilium is a small subcompartment of the cell but has powerful influence on pancreatic islet function. In this study, we find a critical role for... |
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| SubjectTerms | Animals Beta cells Biological Sciences Calcium - metabolism Calcium influx Cell Communication - physiology Cellular structure Chemoreception Cilia Cilia - genetics Cilia - metabolism Cilia - pathology Clonal deletion Crosstalk Diabetes Diabetes mellitus Diabetes Mellitus - genetics Diabetes Mellitus - pathology Disease Models, Animal Energy Metabolism - physiology Female Glucagon-Secreting Cells - metabolism Glucose Glucose - metabolism Homeostasis Humans Insulin Insulin - metabolism Insulin Secretion Insulin-Secreting Cells - cytology Insulin-Secreting Cells - metabolism Insulin-Secreting Cells - pathology Male Mice Mice, Knockout Pancreas Paracrine signalling Perturbation Secretion Signal Transduction - physiology |
| Title | Primary cilia control glucose homeostasis via islet paracrine interactions |
| URI | https://www.jstor.org/stable/26929660 https://www.ncbi.nlm.nih.gov/pubmed/32253320 https://www.proquest.com/docview/2394268132 https://www.proquest.com/docview/2387255888 https://pubmed.ncbi.nlm.nih.gov/PMC7184063 |
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