Essential Role of Neutrophils in the Protective Immune Response Induced by a Live Attenuated Leishmania Vaccine

J Immunol. 2020 Dec 15;205(12):3333-3347. doi: 10.4049/jimmunol.2000829. Epub 2020 Nov 11.

Abstract

No licensed vaccine exists against visceral leishmaniasis (VL), a disease caused by the Leishmania donovani parasite. We have previously reported both macrophages and dendritic cells play important role in the protection induced by a live attenuated centrin gene-deleted L. donovani (LdCen-/- ) parasite vaccine. The role of neutrophils in orchestrating the initial innate response to pathogens is widely recognized. To investigate the early interaction of LdCen-/- with neutrophils, we immunized mice intradermally in the ear pinna with LdCen-/- Compared with LdWT infection, LdCen-/- parasites induced higher recruitment of neutrophils to the ear dermis and ear draining lymph nodes (dLN) as early as 6-18 h after immunization, which were predominantly proinflammatory in nature. Neutrophils from ear dLN of LdCen-/- -immunized mice exhibited heightened expression of costimulatory molecules and attenuated expression of coinhibitory molecules necessary for higher T cell activation. Further phenotypic characterization revealed heterogeneous neutrophil populations containing Nα and Nβ subtypes in the ear dLN. Of the two, the parasitized Nα subset from LdCen-/- -immunized mice exhibited much stronger Ag-specific CD4+ T cell proliferation ex vivo. Adoptive transfer of neutrophils bearing LdCen-/- parasites induced an increased Th1 response in naive mice. Importantly, neutrophil depletion significantly abrogated Ag-specific CD4+ T cell proliferation in LdCen-/- -immunized mice and impaired protection against virulent challenge. Conversely, replenishing of neutrophils significantly restored the LdCen-/- -induced host-protective response. These results suggest that neutrophils are indispensable for protective immunity induced by LdCen-/- parasite vaccine.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Female
  • Leishmania donovani / genetics
  • Leishmania donovani / immunology*
  • Leishmaniasis Vaccines / genetics
  • Leishmaniasis Vaccines / immunology*
  • Leishmaniasis, Visceral / genetics
  • Leishmaniasis, Visceral / immunology
  • Leishmaniasis, Visceral / prevention & control*
  • Lymphocyte Activation*
  • Mice
  • Neutrophil Infiltration*
  • Neutrophils / immunology*
  • Th1 Cells / immunology*
  • Vaccines, Attenuated / genetics
  • Vaccines, Attenuated / immunology

Substances

  • Leishmaniasis Vaccines
  • Vaccines, Attenuated