Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae)

Insect Biochem Mol Biol. 2003 Nov;33(11):1155-64. doi: 10.1016/j.ibmb.2003.07.001.

Abstract

Fat body and hemocytes play a central role in cellular and humoral responses for systemic infections in invertebrates, similar to the mammalian liver and blood cells. Epithelial surfaces, in particular the midgut, participate in the initial local immune responses in order to aid in the generation of the terminal cytotoxic molecules that mediate non-self recognition. Here, we describe for the first time the immune responses of a cluster of cells at the foregut/midgut junction--known as proventriculus (cardia) in the medically and agriculturally important insect, tsetse fly (Diptera: Glossinidae). We provide evidence for the transcriptional induction of the antimicrobial peptides attacin and defensin as well as for the reactive nitrogen intermediate (RNI) nitric oxide synthase (NOS) upon microbial challenge by either microinjection or feeding. Proventriculus from immune challenged flies also has higher NOS and nitric oxide (NO) activities as well as increased levels of the reactive oxygen intermediate (ROI), hydrogen peroxide (H2O2). In several vector pathogen systems, including tsetse flies and African trypanosomes, stimulation of systemic responses prior to pathogen acquisition has been shown to reduce disease transmission. Furthermore, the induction of systemic immune responses has been documented while pathogens are still differentiating within the midgut environment. While evidence for a close molecular communication between the local and systemic responses is accumulating, the molecular signals that mediate these interactions are at present unknown. Reactive intermediates such as NO or H2O2 may function as immunological signals for mediating the molecular communication between the different insect compartments. We discuss the putative role of the proventriculus in invertebrate immunity and specifically speculate on its significance for trypanosome transmission in tsetse.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Northern
  • Defensins / biosynthesis
  • Defensins / genetics
  • Digestive System / cytology
  • Digestive System / immunology*
  • Escherichia coli / immunology
  • Fat Body / metabolism
  • Hydrogen Peroxide / metabolism
  • Immunity, Cellular / immunology
  • Insect Proteins / biosynthesis
  • Insect Proteins / genetics
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / metabolism
  • Reactive Nitrogen Species / metabolism
  • Reactive Oxygen Species / metabolism
  • Transcription, Genetic / immunology
  • Trypanosoma brucei brucei / immunology
  • Tsetse Flies / immunology*
  • Tsetse Flies / microbiology

Substances

  • Defensins
  • Insect Proteins
  • Reactive Nitrogen Species
  • Reactive Oxygen Species
  • attacin antibacterial protein, insect
  • Nitric Oxide
  • Hydrogen Peroxide
  • Nitric Oxide Synthase