Stereochemistry and innate immune recognition: (+)-norbinaltorphimine targets myeloid differentiation protein 2 and inhibits toll-like receptor 4 signaling

FASEB J. 2019 Aug;33(8):9577-9587. doi: 10.1096/fj.201900173RRR. Epub 2019 Jun 4.

Abstract

Deregulation of innate immune TLR4 signaling contributes to various diseases including neuropathic pain and drug addiction. Naltrexone is one of the rare TLR4 antagonists with good blood-brain barrier permeability and showing no stereoselectivity for TLR4. By linking 2 naltrexone units through a rigid pyrrole spacer, the bivalent ligand norbinaltorphimine was formed. Interestingly, (+)-norbinaltorphimine [(+)-1] showed ∼25 times better TLR4 antagonist activity than naltrexone in microglial BV-2 cell line, whereas (-)-norbinaltorphimine [(-)-1] lost TLR4 activity. The enantioselectivity of norbinaltorphimine was further confirmed in primary microglia, astrocytes, and macrophages. The activities of meso isomer of norbinaltorphimine and the molecular dynamic simulation results demonstrate that the stereochemistry of (+)-1 is derived from the (+)-naltrexone pharmacophore. Moreover, (+)-1 significantly increased and prolonged morphine analgesia in vivo. The efficacy of (+)-1 is long lasting. This is the first report showing enantioselective modulation of the innate immune TLR signaling.-Zhang, X., Peng, Y., Grace, P. M., Metcalf, M. D., Kwilasz, A. J., Wang, Y., Zhang, T., Wu, S., Selfridge, B. R., Portoghese, P. S., Rice, K. C., Watkins, L. R., Hutchinson, M. R., Wang, X. Stereochemistry and innate immune recognition: (+)-norbinaltorphimine targets myeloid differentiation protein 2 and inhibits toll-like receptor 4 signaling.

Keywords: MD-2; TLR4; enantioselective modulation; morphine analgesia; norbinaltorphimine.

Publication types

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

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Cell Differentiation / drug effects
  • Cell Line
  • Cells, Cultured
  • Interleukin-1beta / metabolism
  • Lymphocyte Antigen 96 / metabolism*
  • Male
  • Mice
  • Microglia / drug effects
  • Microglia / metabolism
  • Naltrexone / analogs & derivatives*
  • Naltrexone / chemistry
  • Naltrexone / pharmacology
  • Protein Structure, Secondary
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects
  • Stereoisomerism
  • Structure-Activity Relationship
  • Toll-Like Receptor 4 / antagonists & inhibitors
  • Toll-Like Receptor 4 / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-1beta
  • Ly96 protein, mouse
  • Lymphocyte Antigen 96
  • Toll-Like Receptor 4
  • Tumor Necrosis Factor-alpha
  • norbinaltorphimine
  • Naltrexone