A Novel Class of Small Molecule Agonists with Preference for Human over Mouse TLR4 Activation

PLoS One. 2016 Oct 13;11(10):e0164632. doi: 10.1371/journal.pone.0164632. eCollection 2016.

Abstract

The best-characterized Toll-like receptor 4 (TLR4) ligands are lipopolysaccharide (LPS) and its chemically modified and detoxified variant, monophosphoryl lipid A (MPL). Although both molecules are active for human TLR4, they demonstrate a potency preference for mouse TLR4 based on data from transfected cell lines and primary cells of both species. After a high throughput screening process of small molecule libraries, we have discovered a new class of TLR4 agonist with a species preference profile differing from MPL. Products of the 4-component Ugi synthesis reaction were demonstrated to potently trigger human TLR4-transfected HEK cells but not mouse TLR4, although inclusion of the human MD2 with mTLR4 was able to partially recover activity. Co-expression of CD14 was not required for optimal activity of Ugi compounds on transfected cells, as it is for LPS. The species preference profile for the panel of Ugi compounds was found to be strongly active for human and cynomolgus monkey primary cells, with reduced but still substantial activity for most Ugi compounds on guinea pig cells. Mouse, rat, rabbit, ferret, and cotton rat cells displayed little or no activity when exposed to Ugi compounds. However, engineering the human versions of TLR4 and MD2 to be expressed in mTLR4/MD2 deficient mice allowed for robust activity by Ugi compounds both in vitro and in vivo. These findings extend the range of compounds available for development as agonists of TLR4 and identify novel molecules which reverse the TLR4 triggering preference of MPL for mouse TLR4 over human TLR4. Such compounds may be amenable to formulation as more potent human-specific TLR4L-based adjuvants than typical MPL-based adjuvants.

MeSH terms

  • Amides / chemical synthesis
  • Amides / chemistry
  • Animals
  • Binding Sites
  • Bone Marrow Cells / cytology
  • Cells, Cultured
  • Chemokines / metabolism
  • Cytokines / metabolism
  • Dendritic Cells / cytology
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Genes, Reporter / genetics
  • Guinea Pigs
  • HEK293 Cells
  • Humans
  • Lipopolysaccharide Receptors / genetics
  • Lipopolysaccharides / toxicity
  • Lymphocyte Antigen 96 / deficiency
  • Lymphocyte Antigen 96 / genetics
  • Lymphocyte Antigen 96 / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Molecular Docking Simulation
  • Protein Binding
  • Protein Structure, Tertiary
  • Rabbits
  • Rats
  • Signal Transduction / drug effects
  • Small Molecule Libraries / chemical synthesis
  • Small Molecule Libraries / chemistry*
  • Small Molecule Libraries / pharmacology
  • Spleen / cytology
  • Spleen / drug effects
  • Spleen / metabolism
  • Toll-Like Receptor 4 / agonists
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism*

Substances

  • Amides
  • Chemokines
  • Cytokines
  • Lipopolysaccharide Receptors
  • Lipopolysaccharides
  • Lymphocyte Antigen 96
  • Small Molecule Libraries
  • Toll-Like Receptor 4

Grants and funding

This study was sponsored/funded by MedImmune, the global biologics R&D arm of AstraZeneca. The funder provided support in the form of salaries for authors JDM, DSH, ER, SKM, DH, CM, NF, AT, LY, NW, SK, MEC, and JCW, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.