Interleukin-6-signal transducer and activator of transcription-3 signaling mediates aortic dissections induced by angiotensin II via the T-helper lymphocyte 17-interleukin 17 axis in C57BL/6 mice

Arterioscler Thromb Vasc Biol. 2013 Jul;33(7):1612-21. doi: 10.1161/ATVBAHA.112.301049. Epub 2013 May 16.

Abstract

Objective: Dysregulated angiotensin II (Ang II) signaling induces local vascular interleukin-6 (IL-6) secretion, producing leukocyte infiltration and life-threatening aortic dissections. Precise mechanisms by which IL-6 signaling induces leukocyte recruitment remain unknown. T-helper 17 lymphocytes (Th17) have been implicated in vascular pathology, but their role in the development of aortic dissections is poorly understood. Here, we tested the relationship of IL-6-signal transducer and activator of transcription-3 signaling with Th17-induced inflammation in the formation of Ang II-induced dissections in C57BL/6 mice.

Approach and results: Ang II infusion induced aortic dissections and CD4(+)-interleukin 17A (IL-17A)-expressing Th17 cell accumulation in C57BL/6 mice. A blunted local Th17 activation, macrophage recruitment, and reduced incidence of aortic dissections were seen in IL-6(-/-) mice. To determine the pathological roles of Th17 lymphocytes, we treated Ang II-infused mice with IL-17A-neutralizing antibody or infused Ang II in genetically deficient IL-17A mice and found decreased aortic chemokine monocytic chemotactic protein-1 production and macrophage recruitment, leading to a reduction in aortic dissections. This effect was independent of blood pressure in IL-17A-neutralizing antibody experiment. Application of a cell-permeable signal transducer and activator of transcription-3 inhibitor to downregulate the IL-6 pathway decreased aortic dilation and Th17 cell recruitment. We also observed increased aortic Th17 infiltration and IL-17 mRNA expression in patients with thoracic aortic dissections. Finally, we found that Ang II-mediated aortic dissections occurred independent of blood pressure changes.

Conclusions: Our results indicate that the IL-6-signal transducer and activator of transcription-3 signaling pathway converges on Th17 recruitment and IL-17A signaling upstream of macrophage recruitment, mediating aortic dissections.

Keywords: T-lymphocytes, helper; angiotensin II; aortic dissection, familial; inflammation; interleukin-6; vascular inflammation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II*
  • Animals
  • Antibodies, Neutralizing / administration & dosage
  • Aorta / immunology*
  • Aorta / pathology
  • Aortic Aneurysm / chemically induced
  • Aortic Aneurysm / genetics
  • Aortic Aneurysm / immunology*
  • Aortic Aneurysm / pathology
  • Aortic Aneurysm / physiopathology
  • Aortic Aneurysm / prevention & control
  • Aortic Dissection / chemically induced
  • Aortic Dissection / genetics
  • Aortic Dissection / immunology*
  • Aortic Dissection / pathology
  • Aortic Dissection / physiopathology
  • Aortic Dissection / prevention & control
  • Blood Pressure
  • Chemokine CCL2 / metabolism
  • Disease Models, Animal
  • Gene Expression Regulation
  • Humans
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / metabolism*
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / deficiency
  • Interleukin-17 / genetics
  • Interleukin-17 / metabolism*
  • Interleukin-6 / deficiency
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism*
  • Lymphocyte Activation
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • RNA, Messenger / metabolism
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction*
  • Th17 Cells / immunology*
  • Tissue Culture Techniques

Substances

  • Antibodies, Neutralizing
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Il17a protein, mouse
  • Inflammation Mediators
  • Interleukin-17
  • Interleukin-6
  • RNA, Messenger
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Angiotensin II