Liquid crystalline ordering of antimicrobial peptide-RNA complexes controls TLR3 activation

Abstract

Double-stranded RNA (dsRNA) can induce potent production of pro-inflammatory cytokines in normal human epidermal keratinocytes (NHEK) by binding to endosomal Toll-like receptor-3 (TLR3). It is also known that the cationic human antimicrobial peptide LL37 forms electrostatic immune complexes with self-dsRNA to hyperactivate TLR3 in psoriatic keratinocytes. Here, we combine X-ray scattering experiments and computer simulations with measurements of NHEK cytokine production to elucidate a selection rule for cationic molecules that electrostatically condense dsRNA and activate TLR3. TLR3 activation intimately depends on the inter-RNA spacing and repeat number of parallel dsRNA molecules in the liquid-crystalline self-assembled complexes. Complexes that present dsRNA at the optimal spacing can engage multiple TLR3 receptors simultaneously, driving receptor clustering, super-selective receptor binding, and downstream immune amplification. We not only demonstrate the structural basis for LL37-mediated hyperactivation of NHEK in psoriasis, but also illustrate how to deterministically modulate immune responses in the skin by controlling the inter-RNA spacing within self-assembled polycation-dsRNA complexes.

Publication
In Journal of Investigative Dermatology 137(5): S12
Date