Neutrophil-derived S100 calcium-binding proteins A8/A9 promote reticulated thrombocytosis and atherogenesis in diabetes
Platelets play a critical role in atherogenesis and thrombosis-mediated myocardial ischemia, processes that are accelerated in diabetes. Whether hyperglycemia promotes platelet production and whether enhanced platelet production contributes to enhanced atherothrombosis remains unknown. Here we found...
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| Published in | The Journal of clinical investigation Vol. 127; no. 6; pp. 2133 - 2147 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Clinical Investigation
01.06.2017
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Platelets play a critical role in atherogenesis and thrombosis-mediated myocardial ischemia, processes that are accelerated in diabetes. Whether hyperglycemia promotes platelet production and whether enhanced platelet production contributes to enhanced atherothrombosis remains unknown. Here we found that in response to hyperglycemia, neutrophil-derived S100 calcium-binding proteins A8/A9 (S100A8/A9) interact with the receptor for advanced glycation end products (RAGE) on hepatic Kupffer cells, resulting in increased production of IL-6, a pleiotropic cytokine that is implicated in inflammatory thrombocytosis. IL-6 acts on hepatocytes to enhance the production of thrombopoietin, which in turn interacts with its cognate receptor c-MPL on megakaryocytes and bone marrow progenitor cells to promote their expansion and proliferation, resulting in reticulated thrombocytosis. Lowering blood glucose using a sodium-glucose cotransporter 2 inhibitor (dapagliflozin), depleting neutrophils or Kupffer cells, or inhibiting S100A8/A9 binding to RAGE (using paquinimod), all reduced diabetes-induced thrombocytosis. Inhibiting S100A8/A9 also decreased atherogenesis in diabetic mice. Finally, we found that patients with type 2 diabetes have reticulated thrombocytosis that correlates with glycated hemoglobin as well as increased plasma S100A8/A9 levels. These studies provide insights into the mechanisms that regulate platelet production and may aid in the development of strategies to improve on current antiplatelet therapies and to reduce cardiovascular disease risk in diabetes. |
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| AbstractList | Platelets play a critical role In atherogenesis and thrombosis-mediated myocardial Ischemia, processes that are accelerated In diabetes. Whether hyperglycemia promotes platelet production and whether enhanced platelet production contributes to enhanced atherothrombosis remains unknown. Here we found that in response to hyperglycemia, neutrophil-derived S100 calcium-binding proteins A8/A9 (S100A8/A9) interact with the receptor for advanced glycation end products (RAGE) on hepatic Kupffer cells, resulting in increased production of IL-6, a pleiotropic cytokine that is implicated in inflammatory thrombocytosis. IL-6 acts on hepatocytes to enhance the production of thrombopoietin, which in turn interacts with its cognate receptor c-MPL on megakaryocytes and bone marrow progenitor cells to promote their expansion and proliferation, resulting in reticulated thrombocytosis. Lowering blood glucose using a sodium -glucose cotransporter 2 inhibitor (dapagliflozin), depleting neutrophils or Kupffer cells, or inhibiting S100A8/A9 binding to RAGE (using paquinimod), all reduced diabetes-induced thrombocytosis. Inhibiting S100A8/A9 also decreased atherogenesis in diabetic mice. Finally, we found that patients with type 2 diabetes have reticulated thrombocytosis that correlates with glycated hemoglobin as well as increased plasma S100A8/A9 levels. These studies provide insights into the mechanisms that regulate platelet production and may aid in the development of strategies to improve on current antiplatelet therapies and to reduce cardiovascular disease risk in diabetes. Platelets play a critical role in atherogenesis and thrombosis-mediated myocardial ischemia, processes that are accelerated in diabetes. Whether hyperglycemia promotes platelet production and whether enhanced platelet production contributes to enhanced atherothrombosis remains unknown. Here we found that in response to hyperglycemia, neutrophil-derived S100 calcium-binding proteins A8/A9 (S100A8/A9) interact with the receptor for advanced glycation end products (RAGE) on hepatic Kupffer cells, resulting in increased production of IL-6, a pleiotropic cytokine that is implicated in inflammatory thrombocytosis. IL-6 acts on hepatocytes to enhance the production of thrombopoietin, which in turn interacts with its cognate receptor c-MPL on megakaryocytes and bone marrow progenitor cells to promote their expansion and proliferation, resulting in reticulated thrombocytosis. Lowering blood glucose using a sodium-glucose cotransporter 2 inhibitor (dapagliflozin), depleting neutrophils or Kupffer cells, or inhibiting S100A8/A9 binding to RAGE (using paquinimod), all reduced diabetes-induced thrombocytosis. Inhibiting S100A8/A9 also decreased atherogenesis in diabetic mice. Finally, we found that patients with type 2 diabetes have reticulated thrombocytosis that correlates with glycated hemoglobin as well as increased plasma S100A8/A9 levels. These studies provide insights into the mechanisms that regulate platelet production and may aid in the development of strategies to improve on current antiplatelet therapies and to reduce cardiovascular disease risk in diabetes.Platelets play a critical role in atherogenesis and thrombosis-mediated myocardial ischemia, processes that are accelerated in diabetes. Whether hyperglycemia promotes platelet production and whether enhanced platelet production contributes to enhanced atherothrombosis remains unknown. Here we found that in response to hyperglycemia, neutrophil-derived S100 calcium-binding proteins A8/A9 (S100A8/A9) interact with the receptor for advanced glycation end products (RAGE) on hepatic Kupffer cells, resulting in increased production of IL-6, a pleiotropic cytokine that is implicated in inflammatory thrombocytosis. IL-6 acts on hepatocytes to enhance the production of thrombopoietin, which in turn interacts with its cognate receptor c-MPL on megakaryocytes and bone marrow progenitor cells to promote their expansion and proliferation, resulting in reticulated thrombocytosis. Lowering blood glucose using a sodium-glucose cotransporter 2 inhibitor (dapagliflozin), depleting neutrophils or Kupffer cells, or inhibiting S100A8/A9 binding to RAGE (using paquinimod), all reduced diabetes-induced thrombocytosis. Inhibiting S100A8/A9 also decreased atherogenesis in diabetic mice. Finally, we found that patients with type 2 diabetes have reticulated thrombocytosis that correlates with glycated hemoglobin as well as increased plasma S100A8/A9 levels. These studies provide insights into the mechanisms that regulate platelet production and may aid in the development of strategies to improve on current antiplatelet therapies and to reduce cardiovascular disease risk in diabetes. |
| Audience | Academic |
| Author | Dragoljevic, Dragana Febbraio, Mark A. Nagareddy, Prabhakara R. Murphy, Andrew J. Kammoun, Helene L. Al-Sharea, Annas Goldberg, Ira J. Basu, Debapriya Whillas, Alexandra Flynn, Michelle Barrett, Tessa J. Heywood, Sarah Lee, Man K.S. Hanssen, Nordin M.J. Kraakman, Michael J. Montenont, Emilie Cooper, Mark E. Fisher, Edward A. Berger, Jeffrey S. Westein, Erik Chin-Dusting, Jaye |
| AuthorAffiliation | 5 Department of Internal Medicine, Cardiovascular Research Institute Maastricht (CARIM), School of Cardiovascular Diseases, Maastricht University, Maastricht, Netherlands 6 Cellular and Molecular Metabolism Laboratory, Garvan Institute of Medical Research, Darlinghurst, New South Wales, Australia 10 Department of Nutrition Sciences, University of Alabama at Birmingham, Birmingham, Alabama, USA 11 Department of Immunology, Monash University, Melbourne, Victoria, Australia 4 Division of Endocrinology, Diabetes and Metabolism, New York University School of Medicine, New York, New York, USA 2 Division of Cardiology 1 Haematopoiesis and Leukocyte Biology, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia 9 Diabetic Complications, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia 3 Division of Hematology, and 7 Vascular Biomechanics, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia 8 Department of Pharmacology, Monash University, Clayton, Victoria, A |
| AuthorAffiliation_xml | – name: 4 Division of Endocrinology, Diabetes and Metabolism, New York University School of Medicine, New York, New York, USA – name: 8 Department of Pharmacology, Monash University, Clayton, Victoria, Australia – name: 11 Department of Immunology, Monash University, Melbourne, Victoria, Australia – name: 6 Cellular and Molecular Metabolism Laboratory, Garvan Institute of Medical Research, Darlinghurst, New South Wales, Australia – name: 9 Diabetic Complications, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia – name: 7 Vascular Biomechanics, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia – name: 1 Haematopoiesis and Leukocyte Biology, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia – name: 5 Department of Internal Medicine, Cardiovascular Research Institute Maastricht (CARIM), School of Cardiovascular Diseases, Maastricht University, Maastricht, Netherlands – name: 3 Division of Hematology, and – name: 10 Department of Nutrition Sciences, University of Alabama at Birmingham, Birmingham, Alabama, USA – name: 2 Division of Cardiology |
| Author_xml | – sequence: 1 givenname: Michael J. surname: Kraakman fullname: Kraakman, Michael J. – sequence: 2 givenname: Man K.S. surname: Lee fullname: Lee, Man K.S. – sequence: 3 givenname: Annas surname: Al-Sharea fullname: Al-Sharea, Annas – sequence: 4 givenname: Dragana surname: Dragoljevic fullname: Dragoljevic, Dragana – sequence: 5 givenname: Tessa J. surname: Barrett fullname: Barrett, Tessa J. – sequence: 6 givenname: Emilie surname: Montenont fullname: Montenont, Emilie – sequence: 7 givenname: Debapriya surname: Basu fullname: Basu, Debapriya – sequence: 8 givenname: Sarah surname: Heywood fullname: Heywood, Sarah – sequence: 9 givenname: Helene L. surname: Kammoun fullname: Kammoun, Helene L. – sequence: 10 givenname: Michelle surname: Flynn fullname: Flynn, Michelle – sequence: 11 givenname: Alexandra surname: Whillas fullname: Whillas, Alexandra – sequence: 12 givenname: Nordin M.J. surname: Hanssen fullname: Hanssen, Nordin M.J. – sequence: 13 givenname: Mark A. surname: Febbraio fullname: Febbraio, Mark A. – sequence: 14 givenname: Erik surname: Westein fullname: Westein, Erik – sequence: 15 givenname: Edward A. orcidid: 0000-0001-9802-143X surname: Fisher fullname: Fisher, Edward A. – sequence: 16 givenname: Jaye surname: Chin-Dusting fullname: Chin-Dusting, Jaye – sequence: 17 givenname: Mark E. surname: Cooper fullname: Cooper, Mark E. – sequence: 18 givenname: Jeffrey S. surname: Berger fullname: Berger, Jeffrey S. – sequence: 19 givenname: Ira J. surname: Goldberg fullname: Goldberg, Ira J. – sequence: 20 givenname: Prabhakara R. surname: Nagareddy fullname: Nagareddy, Prabhakara R. – sequence: 21 givenname: Andrew J. surname: Murphy fullname: Murphy, Andrew J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28504650$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2017 American Society for Clinical Investigation Copyright American Society for Clinical Investigation Jun 2017 Copyright © 2017, American Society for Clinical Investigation 2017 American Society for Clinical Investigation |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Authorship note: M.J. Kraakman and M.K.S. Lee contributed equally to this work. P.R. Nagareddy and A.J. Murphy are co-senior authors. |
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| References | B20 B64 B21 B65 B22 B23 B67 B24 B68 B25 B69 B26 B27 Leiter (B63) 2005; 27 Shah (B74) 2013; 11 Node (B62) 2009; 8 Dindar (B60) 2013; 62 B70 B71 Wolber (B29) 2001; 86 B73 B30 B31 Daley (B72) 2008; 83 B75 B32 B33 Scott (B38) 2016; 7 B34 B35 Muscari (B17) 2008; 99 B36 B37 B39 Sungaran (B28) 1997; 89 B1 B2 B3 No authors listed (B12) 1994; 308 B4 B5 B6 B9 Bayraktar (B44) 1994; 22 B40 Aryangat (B66) 2010; 6 B42 B43 B46 Huo (B8) 2003; 9 Roy (B45) 1988; 29 B48 B49 Sokunbi (B7) 1994; 10 Nicolucci (B47) 2011; 34 Suppl 2 Björk (B41) 2009; 7 B50 B51 B52 B53 B10 B11 Gregory (B54) 1998; 160 B55 B56 B13 B57 B14 B58 B15 B59 B16 B18 B19 B61 28615358 - Sci Transl Med. 2017 Jun 14;9(394) |
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| Snippet | Platelets play a critical role in atherogenesis and thrombosis-mediated myocardial ischemia, processes that are accelerated in diabetes. Whether hyperglycemia... Platelets play a critical role In atherogenesis and thrombosis-mediated myocardial Ischemia, processes that are accelerated In diabetes. Whether hyperglycemia... |
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| SubjectTerms | Advanced glycosylation end products Animals Antiplatelet therapy Atherogenesis Atherosclerosis Atherosclerosis - immunology Atherosclerosis - metabolism Biomedical research Blood platelets Blood Platelets - physiology Bone marrow Calcium Calcium binding proteins Calgranulin A - physiology Calgranulin B - physiology Cardiovascular disease Cardiovascular diseases Cell proliferation Chemokines Complications and side effects Cytokines Development and progression Diabetes Diabetes mellitus Diabetes Mellitus, Experimental - complications Diabetes Mellitus, Experimental - immunology Diabetes Mellitus, Experimental - metabolism Glucose Glycosylation Health aspects Hemoglobin Hepatocytes Humans Hyperglycemia Inflammation Interleukin 6 Ischemia Kupffer cells Leukocytes (neutrophilic) Lupus Male Megakaryocytes Mice, Inbred C57BL Mice, Knockout Mice, Obese Mortality Myocardial ischemia Na+/glucose cotransporter Neutrophils Neutrophils - metabolism Osteoprogenitor cells Platelets Proteins Rodents Sodium Stem cells Thrombocytosis Thrombocytosis - immunology Thrombocytosis - metabolism Thrombosis |
| Title | Neutrophil-derived S100 calcium-binding proteins A8/A9 promote reticulated thrombocytosis and atherogenesis in diabetes |
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