Pin1-Targeted Therapy for Systemic Lupus Erythematosus

Arthritis Rheumatol. 2016 Oct;68(10):2503-13. doi: 10.1002/art.39741.

Abstract

Objective: Systemic lupus erythematosus (SLE) is a debilitating autoimmune disease affecting multiple organs in the body, but therapeutic options are still very limited and often come with adverse effects. Increasing evidence has underlined an important role of the Toll-like receptor 7 (TLR-7)/TLR-9/interleukin-1 receptor-associated kinase 1 (IRAK-1)/interferon regulatory factor 7 (IRF-7) pathway in the development and progression of SLE. Notably, the prolyl isomerase Pin1 is an essential regulator of IRAK-1 in TLR-7/TLR-9 signaling, but its role in SLE is unknown. We undertook this study to determine whether Pin1 is activated and plays any role in the development and treatment of SLE.

Methods: Activation of Pin1 and TLR-7/TLR-9/IRAK-1/IRF-7 signaling was determined in various cell types among peripheral blood mononuclear cells from healthy controls and SLE patients. The effects of Pin1 and TLR signaling on SLE development were determined using validated Pin1 short hairpin RNA (shRNA), Pin1 genetic knockout, and the small-molecule Pin1 inhibitor all-trans-retinoic acid (ATRA) in immune cells and in several strains of lupus-prone mice.

Results: We found abnormal activation of Pin1 and its downstream targets IRAK-1 and IRF-7 in SLE patients. Furthermore, inhibition of Pin1 using either validated Pin1 shRNA or ATRA blocked TLR-7-induced activation of IRAK-1 and IRF-7 in SLE patient-derived immune cells. Moreover, in multiple lupus-prone animals, both Pin1 knockout and ATRA strikingly attenuated the expression of autoimmunity, including skin lesions, lymphadenopathy, splenomegaly, glomerulonephritis, proteinuria, and production of anti-double-stranded DNA antibodies and CD4-CD8- T cells, and also prolonged overall survival in MRL/lpr and B6.lpr mice.

Conclusion: Pin1 plays a critical role in the development of SLE, and Pin1-targeted therapy offers a promising new strategy for treating SLE.

Publication types

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

MeSH terms

  • Animals
  • Cell Culture Techniques
  • Cell Line
  • Flow Cytometry
  • Gene Knockdown Techniques
  • Humans
  • Immunoblotting
  • In Vitro Techniques
  • Interferon Regulatory Factor-7 / drug effects*
  • Interferon Regulatory Factor-7 / immunology
  • Interleukin-1 Receptor-Associated Kinases / drug effects*
  • Interleukin-1 Receptor-Associated Kinases / immunology
  • Leukocytes, Mononuclear / drug effects*
  • Leukocytes, Mononuclear / immunology
  • Lupus Erythematosus, Systemic / drug therapy*
  • Lupus Erythematosus, Systemic / immunology
  • Mice
  • Mice, Inbred MRL lpr
  • Mice, Knockout
  • Molecular Targeted Therapy
  • Monocytes / drug effects
  • Monocytes / immunology
  • NIMA-Interacting Peptidylprolyl Isomerase / antagonists & inhibitors*
  • NIMA-Interacting Peptidylprolyl Isomerase / genetics
  • NIMA-Interacting Peptidylprolyl Isomerase / immunology
  • RNA, Small Interfering / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • Th17 Cells / drug effects
  • Th17 Cells / immunology
  • Toll-Like Receptor 7 / drug effects*
  • Toll-Like Receptor 7 / immunology
  • Toll-Like Receptor 9 / drug effects*
  • Toll-Like Receptor 9 / immunology
  • Tretinoin / pharmacology*

Substances

  • Interferon Regulatory Factor-7
  • NIMA-Interacting Peptidylprolyl Isomerase
  • RNA, Small Interfering
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • Tretinoin
  • Interleukin-1 Receptor-Associated Kinases