Blockade of TNF-α rapidly inhibits pain responses in the central nervous system

  1. Georg Schettb,2
  1. aInstitute of Experimental and Clinical Pharmacology and Toxicology,
  2. bDepartment of Internal Medicine 3, and
  3. cDivision of Neuroradiology, University of Erlangen-Nuremberg, 91054 Erlangen, Germany;
  4. dInstitute of Immunology, Alexander Fleming Biomedical Sciences Research Center, 16672 Vari, Greece;
  5. eDepartment of Internal Medicine I, University of Regensburg, 93053 Regensburg, Germany; and
  6. fDepartment of Psychological and Brain Sciences, Programs in Neuroscience and Cognitive Science, Indiana University, Bloomington, IN 47405
  1. Edited* by Charles A. Dinarello, University of Colorado Denver, Aurora, CO, and approved December 29, 2010 (received for review August 19, 2010)

  • 1A.H., R.A., and J.R. contributed equally to this work.

  • 2To whom correspondence should be addressed. E-mail: georg.schett{at}uk-erlangen.de.

Abstract

There has been a consistent gap in understanding how TNF-α neutralization affects the disease state of arthritis patients so rapidly, considering that joint inflammation in rheumatoid arthritis is a chronic condition with structural changes. We thus hypothesized that neutralization of TNF-α acts through the CNS before directly affecting joint inflammation. Through use of functional MRI (fMRI), we demonstrate that within 24 h after neutralization of TNF-α, nociceptive CNS activity in the thalamus and somatosensoric cortex, but also the activation of the limbic system, is blocked. Brain areas showing blood-oxygen level-dependent signals, a validated method to assess neuronal activity elicited by pain, were significantly reduced as early as 24 h after an infusion of a monoclonal antibody to TNF-α. In contrast, clinical and laboratory markers of inflammation, such as joint swelling and acute phase reactants, were not affected by anti-TNF-α at these early time points. Moreover, arthritic mice overexpressing human TNF-α showed an altered pain behavior and a more intensive, widespread, and prolonged brain activity upon nociceptive stimuli compared with wild-type mice. Similar to humans, these changes, as well as the rewiring of CNS activity resulting in tight clustering in the thalamus, were rapidly reversed after neutralization of TNF-α. These results suggest that neutralization of TNF-α affects nociceptive brain activity in the context of arthritis, long before it achieves anti-inflammatory effects in the joints.

Footnotes

  • Author contributions: K.B. and G.S. designed research; A.H., R.A., J.R., S.F., C.H., S.K., M. Sergeeva, M.G., and G.S. performed research; A.H., G.K., and G.S. contributed new reagents/analytic tools; A.H., R.A., J.R., M. Saake, R.H.S., O.S., A.D., K.B., and G.S. analyzed data; and A.H. and G.S. wrote the paper.

  • The authors declare no conflict of interest.

  • *This Direct Submission article had a prearranged editor.

  • See Commentary on page 3461.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1011774108/-/DCSupplemental.

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