Disease activity accounts for long-term efficacy of IL-1 blockers in pyogenic sterile arthritis pyoderma gangrenosum and severe acne syndrome

Rheumatology (Oxford). 2016 Jul;55(7):1325-35. doi: 10.1093/rheumatology/kew031. Epub 2016 Mar 17.

Abstract

Objective: To provide a rationale for anti-IL-1 treatment in pyogenic sterile arthritis, pyoderma gangrenosum and acne (PAPA) by defining whether IL-1β secretion is enhanced; requires NLRP3; and correlates with proline-serine-threonine phosphatase-interacting protein 1 mutations, disease activity and/or the clinical picture in PAPA.

Methods: Monocytes were isolated from 13 patients and 35 healthy donors and studied at baseline and following activation. Secretion pattern of IL-1β, IL-1α, IL-1Ra, IL-6, IL-18 and TNF-α was assessed in supernatants by ELISA. The NLRP3 requirement for IL-1β secretion was investigated by silencing technique in PAPA and healthy donor monocytes. Long-term follow-up (mean 26 months, range 4-38) was performed in five patients enrolled in an anti-IL-1 regimen.

Results: IL-1β secretion in PAPA is increased, requires NLRP3 and correlates with disease activity. Patients with a history of osteoarticular flares release more IL-1β, IL-6 and TNF-α compared with those with predominant cutaneous recurrences. Monocytes from patients in anti-IL-1 treatment dramatically reduced IL-1β secretion after ex vivo activation, and long-term follow-up demonstrated decreased frequency of flares and normalization of acute phase reactants in all the patients. A straightforward correlation between genotype and IL-1β signalling was not observed suggesting that factors other than mutation itself may play a role in regulating IL-1β secretion and response to treatment in PAPA.

Conclusion: PAPA patients with active lesions display increased NLRP3-mediated IL-1β secretion, and long-term efficacy of IL-1 blockade was demonstrated. Even if other mechanisms related to the complex proline-serine-threonine phosphatase-interacting protein 1 protein networking might play additional roles, this study further supports the potential of IL-1 blockade as an effective therapeutic strategy in PAPA syndrome.

Keywords: IL-1; IL-1 receptor antagonist; NLRP3 inflammasome; PAPA syndrome; PSTPIP1; anti-IL-1 monoclonal antibody.

MeSH terms

  • Acne Vulgaris / blood
  • Acne Vulgaris / drug therapy*
  • Acne Vulgaris / pathology
  • Adolescent
  • Adult
  • Arthritis, Infectious / blood
  • Arthritis, Infectious / drug therapy*
  • Arthritis, Infectious / pathology
  • Case-Control Studies
  • Child
  • Child, Preschool
  • Disease Progression
  • Female
  • Follow-Up Studies
  • Humans
  • Immunologic Factors / antagonists & inhibitors*
  • Immunologic Factors / pharmacology
  • Interleukin-1 / antagonists & inhibitors*
  • Interleukin-1 / pharmacology
  • Interleukin-1beta / metabolism
  • Interleukin-6 / metabolism
  • Male
  • Middle Aged
  • Monocytes / drug effects*
  • Monocytes / physiology
  • NLR Family, Pyrin Domain-Containing 3 Protein / physiology
  • Pyoderma Gangrenosum / blood
  • Pyoderma Gangrenosum / drug therapy*
  • Pyoderma Gangrenosum / pathology
  • Signal Transduction / drug effects
  • Treatment Outcome
  • Tumor Necrosis Factor-alpha / metabolism
  • Young Adult

Substances

  • Immunologic Factors
  • Interleukin-1
  • Interleukin-1beta
  • Interleukin-6
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Tumor Necrosis Factor-alpha

Supplementary concepts

  • Pyogenic arthritis, pyoderma gangrenosum, and acne