Lysozyme M-positive monocytes mediate angiotensin II-induced arterial hypertension and vascular dysfunction

Circulation. 2011 Sep 20;124(12):1370-81. doi: 10.1161/CIRCULATIONAHA.111.034470. Epub 2011 Aug 29.

Abstract

Background: Angiotensin II (ATII), a potent vasoconstrictor, causes hypertension, promotes infiltration of myelomonocytic cells into the vessel wall, and stimulates both vascular and inflammatory cell NADPH oxidases. The predominant source of reactive oxygen species, eg, vascular (endothelial, smooth muscle, adventitial) versus phagocytic NADPH oxidase, and the role of myelomonocytic cells in mediating arterial hypertension have not been defined yet.

Methods and results: Angiotensin II (1 mg · kg(-1) · d(-1) for 7 days) increased the number of both CD11b(+)Gr-1(low)F4/80(+) macrophages and CD11b(+)Gr-1(high)F4/80(-) neutrophils in mouse aorta (verified by flow cytometry). Selective ablation of lysozyme M-positive (LysM(+)) myelomonocytic cells by low-dose diphtheria toxin in mice with inducible expression of the diphtheria toxin receptor (LysM(iDTR) mice) reduced the number of monocytes in the circulation and limited ATII-induced infiltration of these cells into the vascular wall, whereas the number of neutrophils was not reduced. Depletion of LysM(+) cells attenuated ATII-induced blood pressure increase (measured by radiotelemetry) and vascular endothelial and smooth muscle dysfunction (assessed by aortic ring relaxation studies) and reduced vascular superoxide formation (measured by chemiluminescence, cytochrome c assay, and oxidative fluorescence microtopography) and the expression of NADPH oxidase subunits gp91(phox) and p67(phox) (assessed by Western blot and mRNA reverse-transcription polymerase chain reaction). Adoptive transfer of wild-type CD11b(+)Gr-1(+) monocytes into depleted LysM(iDTR) mice reestablished ATII-induced vascular dysfunction, oxidative stress, and arterial hypertension, whereas transfer of CD11b(+)Gr-1(+) neutrophils or monocytes from gp91(phox) or ATII receptor type 1 knockout mice did not. CONCLUSIONS- Infiltrating monocytes with a proinflammatory phenotype and macrophages rather than neutrophils appear to be essential for ATII-induced vascular dysfunction and arterial hypertension.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • CD11b Antigen / metabolism
  • Endothelium, Vascular / immunology
  • Endothelium, Vascular / metabolism
  • Gene Expression / immunology
  • Hypertension / chemically induced
  • Hypertension / immunology*
  • Hypertension / metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Monocytes / immunology
  • Monocytes / metabolism*
  • Muramidase / genetics
  • Muramidase / immunology*
  • Muramidase / metabolism*
  • Muscle, Smooth, Vascular / immunology
  • Muscle, Smooth, Vascular / metabolism
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Nitric Oxide / metabolism
  • Oxidative Stress / physiology
  • Reactive Oxygen Species / metabolism
  • Receptors, Chemokine / metabolism
  • Respiratory Burst / physiology
  • Vasculitis / chemically induced
  • Vasculitis / immunology*
  • Vasculitis / metabolism
  • Vasoconstrictor Agents / pharmacology

Substances

  • CD11b Antigen
  • Gr-1 protein, mouse
  • Reactive Oxygen Species
  • Receptors, Chemokine
  • Vasoconstrictor Agents
  • Angiotensin II
  • Nitric Oxide
  • Muramidase
  • lysozyme M, mouse