Neurokinin-1 receptor agonists bias therapeutic dendritic cells to induce type 1 immunity by licensing host dendritic cells to produce IL-12

Blood. 2013 Apr 11;121(15):2923-33. doi: 10.1182/blood-2012-07-446054. Epub 2013 Jan 30.

Abstract

Substance-P and hemokinin-1 are proinflammatory neuropeptides with potential to promote type 1 immunity through agonistic binding to neurokinin-1 receptor (NK1R). Dendritic cells (DCs) are professional antigen-presenting cells that initiate and regulate the outcome of innate and adaptive immune responses. Immunostimulatory DCs are highly desired for the development of positive immunization techniques. DCs express functional NK1R; however, regardless of their potential DC-stimulatory function, the ability of NK1R agonists to promote immunostimulatory DCs remains unexplored. Here, we demonstrate that NK1R signaling activates therapeutic DCs capable of biasing type 1 immunity by inhibition of interleukin-10 (IL-10) synthesis and secretion, without affecting their low levels of IL-12 production. The potent type 1 effector immune response observed following cutaneous administration of NK1R-signaled DCs required their homing in skin-draining lymph nodes (sDLNs) where they induced inflammation and licensed endogenous-conventional sDLN-resident and -recruited inflammatory DCs to secrete IL-12. Our data demonstrate that NK1R signaling promotes immunostimulatory DCs, and provide relevant insight into the mechanisms used by neuromediators to regulate innate and adaptive immune responses.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Cells, Cultured
  • Cyclic AMP Response Element-Binding Protein / immunology
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Dendritic Cells / transplantation
  • Flow Cytometry
  • Immunity, Cellular / immunology*
  • Immunization / methods
  • Immunophenotyping
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Interleukin-12 / genetics
  • Interleukin-12 / immunology*
  • Interleukin-12 / metabolism
  • Mechanistic Target of Rapamycin Complex 2
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Multiprotein Complexes / immunology
  • Multiprotein Complexes / metabolism
  • Receptors, Neurokinin-1 / agonists
  • Receptors, Neurokinin-1 / immunology*
  • Receptors, Neurokinin-1 / metabolism
  • Signal Transduction / immunology
  • TOR Serine-Threonine Kinases / immunology
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Multiprotein Complexes
  • Receptors, Neurokinin-1
  • Interleukin-10
  • Interleukin-12
  • Mechanistic Target of Rapamycin Complex 2
  • TOR Serine-Threonine Kinases