The role of aryl hydrocarbon receptor in interleukin-23-dependent restoration of interleukin-22 following ethanol exposure and burn injury

Ann Surg. 2014 Mar;259(3):582-90. doi: 10.1097/SLA.0b013e3182a626f2.

Abstract

Objective: T-helper (Th)-17 lymphocytes play a crucial role in maintenance and regulation of gut immunity. Our laboratory has demonstrated that acute ethanol (EtOH) exposure before burn injury results in intestinal T cell suppression and enhanced bacterial translocation.

Background: To extend these studies, we examined the effects of EtOH exposure and burn injury on Th17 responses within intestinal lymphoid Peyer's patches (PP). We further investigated whether restitution of interleukin (IL)-23 enhances PP cell IL-17 and IL-22 after EtOH and burn injury.

Methods: Male mice, approximately 25 g, were gavaged with EtOH (2.9 mg/kg) before receiving an approximately 12.5% total body surface area full thickness burn. One day postinjury, PP mixed cells were cultured in the presence of plate-bound anti-CD3/soluble anti-CD28 in the presence or absence of IL-23 for 48 hours. Supernatants were harvested for IL-17 and IL-22 levels.

Results: When combined with EtOH intoxication, burn injury significantly decreased IL-17 and IL-22, as compared with sham injury. IL-23 treatment successfully increased levels of IL-22 but not IL-17. This restoration was prevented when PP cells were treated with CH-223191, an aryl hydrocarbon receptor inhibitor. To further delineate the mechanism of differential IL-17 and IL-22 suppression, PP cells were treated with phorbol 12-myristate 13-acetate (PMA) and ionomycin, which signal via protein kinase C (PKC) and calcium flux. Treatment with PMA and ionomycin significantly prevented the decrease in IL-17 but not IL-22 after EtOH exposure and burn injury.

Conclusions: These findings suggest that IL-23-mediated restoration of IL-22 is aryl hydrocarbon receptor dependent, whereas IL-17 requires activation of protein kinase C and intracellular calcium signaling.

Publication types

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

MeSH terms

  • Animals
  • Burns / immunology
  • Burns / metabolism*
  • Burns / pathology
  • Cells, Cultured
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Ethanol / pharmacology*
  • Flow Cytometry
  • Immunity, Cellular*
  • Interleukin-22
  • Interleukin-23 / drug effects
  • Interleukin-23 / immunology
  • Interleukin-23 / metabolism*
  • Interleukins / immunology
  • Interleukins / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Aryl Hydrocarbon / physiology*
  • Signal Transduction / drug effects
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Th17 Cells / pathology

Substances

  • Interleukin-23
  • Interleukins
  • Receptors, Aryl Hydrocarbon
  • Ethanol