Salivary gland hypofunction induced by activation of innate immunity is dependent on type I interferon signaling

J Oral Pathol Med. 2013 Jan;42(1):66-72. doi: 10.1111/j.1600-0714.2012.01181.x. Epub 2012 Jun 5.

Abstract

Background: Activation of innate immunity through polyinosinic:polycytidylic acid [poly(I:C)] causes acute salivary gland hypofunction. As a major consequence of poly(I:C) treatment is type I interferon (IFN) production, this study was undertaken to investigate their role in salivary gland dysfunction.

Methods: Different strains of mice deficient in either interferon alpha receptor (IFNAR1(-/-)) or IL-6(-/-), or IL-10(-/-), or EBI3(-/-) were treated with poly(I:C). Salivary gland function was determined by measuring pilocarpine-induced saliva volume. Gene expression levels were measured by real-time PCR. Ca(2+) mobilization studies were performed using ex-vivo acinar cells.

Results: A single injection of poly(I:C) rapidly induced salivary gland hypofunction in wild-type B6 mice (41% drop in saliva volumes compared to PBS-treated mice). In contrast, the loss of function in poly(I:C)-treated IFNAR(-/-) mice was only 9.6%. Gene expression analysis showed reduced levels of Il-6, Il-10, and Il-27 in submandibular glands of poly(I:C)-treated IFNAR(-/-) mice. While salivary gland dysfunction in poly(I:C)-treated IL-10(-/-) and EBI3(-/-) mice was comparable to wild-type mice, the IL-6(-/-) mice were more resistant, with only a 21% drop in function. Pilocarpine-induced Ca(2+) flux was significantly suppressed in acinar cells obtained from poly(I:C)-treated wild-type mice.

Conclusions: Our data demonstrate that a combined action of type I IFNs and IL-6 contributes toward salivary gland hypofunction. This happens through interference with Ca(2+) mobilization within acinar cells. Thus, in acute viral infections and diseases like Sjögren's syndrome, elevated levels of type I IFNs and IL-6 can directly affect glandular function.

Publication types

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

MeSH terms

  • Animals
  • Calcium Signaling / physiology*
  • Female
  • Immunity, Innate*
  • Injections, Intraperitoneal
  • Interferon Type I / biosynthesis
  • Interferon Type I / physiology*
  • Interleukin-10 / biosynthesis
  • Interleukin-10 / physiology
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / physiology
  • Interleukin-6 / biosynthesis
  • Interleukin-6 / physiology*
  • Mice
  • Mice, Mutant Strains
  • Poly I-C / pharmacology
  • Receptor, Interferon alpha-beta / deficiency
  • Receptor, Interferon alpha-beta / immunology
  • Saliva / metabolism
  • Submandibular Gland / drug effects*
  • Submandibular Gland / metabolism
  • Xerostomia / chemically induced
  • Xerostomia / immunology*

Substances

  • Ifnar1 protein, mouse
  • Interferon Type I
  • Interleukin-17
  • Interleukin-6
  • Interleukin-10
  • Receptor, Interferon alpha-beta
  • Poly I-C