Loss of protein tyrosine phosphatase nonreceptor type 22 regulates interferon-γ-induced signaling in human monocytes

Gastroenterology. 2013 May;144(5):978-988.e10. doi: 10.1053/j.gastro.2013.01.048. Epub 2013 Feb 1.

Abstract

Background & aims: A gain-of-function variation within the locus that encodes protein tyrosine phosphatase nonreceptor type (PTPN)22 is associated with a reduced risk for Crohn's disease (CD), whereas a loss-of-function variant seems to promote autoimmune disorders. We investigated how loss of PTPN22 could contribute to chronic inflammation of the intestine.

Methods: Intestinal tissue samples from patients with or without inflammatory bowel disease (controls) were analyzed for levels of PTPN22 messenger RNA (mRNA) and protein. In human THP-1 monocytes, protein levels were analyzed by immunoblotting, mRNA levels by real-time polymerase chain reaction, and cytokine release by enzyme-linked immunosorbent assay.

Results: Intestinal tissue samples from patients with CD had reduced levels of PTPN22 mRNA and protein, compared with samples from controls. In human THP-1 monocytes, interferon-γ (IFN-γ) induced expression and activity of PTPN22. Loss of PTPN22 increased levels of p38-mitogen-activated protein kinase, but reduced phosphorylation of nuclear factor-κB subunits. Increased activity of suppressor of cytokine signaling-1 was accompanied by reduced phosphorylation of signal-transducer and activator of transcription protein 1 and signal-transducer and activator of transcription protein 3 in PTPN22-deficient cells incubated with cytokines. PTPN22 knockdown increased secretion of the inflammatory cytokines interleukin (IL)-6 and IL-17, but reduced expression or secretion of T-bet, intercellular adhesion molecule-1, nucleotide-binding oligomerization domain containing-2, monocyte chemoattractant protein-1, IL-2, and IL-12p40 in response to IFN-γ.

Conclusions: PTPN22 expression is reduced in intestinal tissues of patients with active CD. PTPN22 regulates intracellular signaling events and is induced by IFN-γ in human monocytes. Knockdown of PTPN22 alters activation of inflammatory signal transducers, increasing secretion of T-helper 17-related inflammatory mediators. Genetic variants that reduce PTPN22 activity might contribute to the pathogenesis of CD by these mechanisms.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Cell Communication
  • Crohn Disease / genetics*
  • Crohn Disease / metabolism
  • Crohn Disease / pathology
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Gene Expression Regulation*
  • Humans
  • Immunoblotting
  • Interferon-gamma / pharmacology*
  • Intestine, Small / drug effects
  • Intestine, Small / metabolism*
  • Intestine, Small / pathology
  • Male
  • Middle Aged
  • Monocytes / drug effects
  • Monocytes / metabolism*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 22 / genetics*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 22 / metabolism
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics*
  • Real-Time Polymerase Chain Reaction
  • Recombinant Proteins / pharmacology
  • Signal Transduction / genetics
  • Young Adult

Substances

  • RNA, Messenger
  • Recombinant Proteins
  • interferon gamma-1b
  • Interferon-gamma
  • PTPN22 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 22