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Chronic sympathetic driven hypertension promotes atherosclerosis by enhancing hematopoiesis
Annas Al-Sharea, Man K. S. Lee, Alexandra Whillas, Danielle Michell, Waled Shihata, Alyce J Nicholls, Olivia D Cooney, Michael J Kraakman, Camilla Bertuzzo Veiga, Ann-Maree Jefferis, Kristy Jackson, Prabhakara R Nagareddy, Gavin Lambert, Connie H. Y Wong, Karen L Andrews, Geoff A Head, Jaye Chin-Dusting, Andrew J Murphy
Haematologica October 2018 : haematol.2018.192898; doi:10.3324/haematol.2018.192898
Annas Al-Sharea
Baker Heart and Diabetes Institute;
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Man K. S. Lee
Baker Heart and Diabetes Institute;
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Alexandra Whillas
Baker Heart and Diabetes Institute;
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Danielle Michell
Department of Medicine, Vanderbilt University School of Medicine, Nashville;
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Waled Shihata
Baker Heart and Diabetes Institute;
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Alyce J Nicholls
Monash University;
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Olivia D Cooney
Baker Heart and Diabetes Institute;
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Michael J Kraakman
Naomi Berrie Diabetes Center and Department of Medicine, Columbia University, New York;
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Camilla Bertuzzo Veiga
Baker Heart and Diabetes Institute;
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Ann-Maree Jefferis
Monash University;
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Kristy Jackson
Baker Heart and Diabetes Institute;
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Prabhakara R Nagareddy
Department of Nutrition Sciences, University of Alabama at Birmingham, Birmingham, Alabama;
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Gavin Lambert
Iverson Health Innovation Research Institute, Swinburne University of Technology, Hawthorn
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Connie H. Y Wong
Monash University;
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Karen L Andrews
Monash University;
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Geoff A Head
Baker Heart and Diabetes Institute;
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Jaye Chin-Dusting
Monash University;
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Andrew J Murphy
Baker Heart and Diabetes Institute;
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Author Affiliations

  1. Annas Al-Sharea1,*,
  2. Man K. S. Lee1,
  3. Alexandra Whillas1,
  4. Danielle Michell2,
  5. Waled Shihata1,
  6. Alyce J Nicholls3,
  7. Olivia D Cooney1,
  8. Michael J Kraakman4,
  9. Camilla Bertuzzo Veiga1,
  10. Ann-Maree Jefferis3,
  11. Kristy Jackson1,
  12. Prabhakara R Nagareddy5,
  13. Gavin Lambert6,
  14. Connie H. Y Wong3,
  15. Karen L Andrews3,
  16. Geoff A Head1,
  17. Jaye Chin-Dusting3 and
  18. Andrew J Murphy1
  1. 1 Baker Heart and Diabetes Institute;
  2. 2 Department of Medicine, Vanderbilt University School of Medicine, Nashville;
  3. 3 Monash University;
  4. 4 Naomi Berrie Diabetes Center and Department of Medicine, Columbia University, New York;
  5. 5 Department of Nutrition Sciences, University of Alabama at Birmingham, Birmingham, Alabama;
  6. 6 Iverson Health Innovation Research Institute, Swinburne University of Technology, Hawthorn
  1. ↵* Corresponding author; email: annas.al-sharea{at}baker.edu.au
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Abstract

Hypertension is a major, independent risk factor for atherosclerotic cardiovascular disease. However, this pathology can arise through multiple pathways, which could influence vascular disease through distinct mechanisms. An overactive sympathetic nervous system is a dominant pathway that can precipitate in elevated blood pressure. We aimed to determine how the sympathetic nervous system directly promotes atherosclerosis in the setting of hypertension. We used a mouse model of sympathetic nervous system-driven hypertension on the atherosclerotic-prone apolipoprotein E deficient background. When mice were placed on a western type diet for 16 weeks we showed the evolution of unstable atherosclerotic lesions. Fortuitously, the changes in lesion composition were independent of endothelial dysfunction, allowing for the discovery of alternative mechanisms. With the use of flow cytometry and bone marrow imaging, we found that sympathetic activation caused deterioration of the hematopoietic stem and progenitor cell niche in the bone marrow, promoting the liberation of these cells into the circulation and extramedullary hematopoiesis in the spleen. Specifically, sympathetic activation reduced the abundance of key hematopoietic stem and progenitor cell niche cells, sinusoidal endothelial cells and osteoblasts. Additionally, sympathetic bone marrow activity prompted neutrophils to secrete proteases to cleave the hematopoietic stem and progenitor cell surface receptor CXCR4. All these effects could be reversed using the β-blocker propranolol during the feeding period. These findings suggest that elevated blood pressure driven by the sympathetic nervous system can influence mechanisms that modulate the hematopoietic system to promote atherosclerosis and contribute to cardiovascular events.

  • Received March 7, 2018.
  • Accepted October 22, 2018.
  • Copyright © 2018, Ferrata Storti Foundation
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Keywords

hematopoietic stem cell
Hematopoiesis
Bone Marrow Microenvironment
Granulocytes, Monocytes, Macrophages
Atherosclerosis

Vol 104 Issue 2

Haematologica: 104 (2)
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Chronic sympathetic driven hypertension promotes atherosclerosis by enhancing hematopoiesis
Annas Al-Sharea, Man K. S. Lee, Alexandra Whillas, Danielle Michell, Waled Shihata, Alyce J Nicholls, Olivia D Cooney, Michael J Kraakman, Camilla Bertuzzo Veiga, Ann-Maree Jefferis, Kristy Jackson, Prabhakara R Nagareddy, Gavin Lambert, Connie H. Y Wong, Karen L Andrews, Geoff A Head, Jaye Chin-Dusting, Andrew J Murphy
Haematologica Oct 2018, haematol.2018.192898; DOI: 10.3324/haematol.2018.192898

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Annas Al-Sharea, Man K. S. Lee, Alexandra Whillas, Danielle Michell, Waled Shihata, Alyce J Nicholls, Olivia D Cooney, Michael J Kraakman, Camilla Bertuzzo Veiga, Ann-Maree Jefferis, Kristy Jackson, Prabhakara R Nagareddy, Gavin Lambert, Connie H. Y Wong, Karen L Andrews, Geoff A Head, Jaye Chin-Dusting, Andrew J Murphy
Haematologica Oct 2018, haematol.2018.192898; DOI: 10.3324/haematol.2018.192898
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