Loss of braking signals during inflammation: a factor affecting the development and disease course of multiple sclerosis

Arch Neurol. 2011 Jul;68(7):879-88. doi: 10.1001/archneurol.2011.32. Epub 2011 Mar 14.

Abstract

Background: In a recent genome-wide transcriptional analysis, we identified a gene signature for multiple sclerosis (MS), which reverted back to normal during pregnancy. Reversion was particularly evident for 7 genes: SOCS2, TNFAIP3, NR4A2, CXCR4, POLR2J, FAM49B, and STAG3L1, most of which encode negative regulators of inflammation.

Objectives: To corroborate dysregulation of genes, to evaluate the prognostic value of genes, and to study modulation of genes during different treatments.

Design: Comparison study.

Setting: Italian referral center for MS.

Patients: Quantitative polymerase chain reaction measurements were performed for 274 patients with MS and 60 healthy controls. Of the 274 patients with MS, 113 were treatment-naive patients in the initial stages of their disorder who were followed up in real-world clinical settings and categorized on the basis of disease course. The remaining 161 patients with MS received disease-modifying therapies (55 patients were treated with interferon beta, 52 with glatiramer acetate, and 54 with natalizumab) for a mean (SD) of 12 (2) months.

Main outcome measures: Gene expression levels, relapse rate, and change in Expanded Disability Status Scale.

Results: We found a dysregulated gene pathway (P ≤ .006), with a downregulation of genes encoding negative regulators. The SOCS2, NR4A2, and TNFAIP3 genes were inversely correlated with both relapse rate (P ≤ .002) and change in Expanded Disability Status Scale (P ≤ .005). SOCS2 was modulated by both interferon beta and glatiramer acetate, TNFAIP3 was modulated by glatiramer acetate, and NR4A2 was not altered at all. No changes were induced by natalizumab.

Conclusions: We demonstrate that there is a new molecular pathogenic mechanism that underlies the initiation and progression of MS. Defects in negative-feedback loops of inflammation lead to an overactivation of the immune system so as to predispose the brain to inflammation-sensitive MS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • DNA-Binding Proteins
  • Disability Evaluation
  • Disease Progression
  • Female
  • Gene Expression / drug effects
  • Gene Expression Profiling / methods
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology*
  • Humans
  • Immunologic Factors / therapeutic use
  • Intracellular Signaling Peptides and Proteins / genetics
  • Longitudinal Studies
  • Male
  • Middle Aged
  • Multiple Sclerosis / drug therapy
  • Multiple Sclerosis / genetics*
  • Multiple Sclerosis / physiopathology*
  • Nuclear Proteins / genetics
  • Nuclear Receptor Subfamily 4, Group A, Member 2 / genetics
  • Oligonucleotide Array Sequence Analysis / methods
  • Recurrence
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Young Adult

Substances

  • DNA-Binding Proteins
  • Immunologic Factors
  • Intracellular Signaling Peptides and Proteins
  • NR4A2 protein, human
  • Nuclear Proteins
  • Nuclear Receptor Subfamily 4, Group A, Member 2
  • SOCS2 protein, human
  • Suppressor of Cytokine Signaling Proteins
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3