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  • Review Article
  • Published:

Immunity in Drosophila melanogaster — from microbial recognition to whole-organism physiology

Nature Reviews Immunology volume 14, pages 796–810 (2014)Cite this article

Subjects

Key Points

  • The gut response to microorganisms comprises mechanisms of bacterial elimination — through the production of reactive oxygen species and antimicrobial peptides — that are coordinated with stress and repair mechanisms.

  • The gut microorganisms of Drosophila melanogaster alter the growth of larvae and the physiology of adults, modulating nutrition and intestinal homeostasis.

  • Hyperactivation of inflammatory signalling leads to metabolic shifts and altered growth.

  • Organism-wide metabolic changes influence immunity through changes in inflammatory signalling and antimicrobial peptide expression.

  • Systemic alterations in steroid hormones modulate multiple aspects of the immune response.

  • Immune signalling components are involved in newly discovered cell death and neurodegeneration pathways.

  • Classic Toll- and Imd-induced nuclear factor-κB pathways, along with phagocytosis, are central pillars of antimicrobial defence in D. melanogaster.

Abstract

Since the discovery of antimicrobial peptide responses 40 years ago, the fruit fly Drosophila melanogaster has proven to be a powerful model for the study of innate immunity. Early work focused on innate immune mechanisms of microbial recognition and subsequent nuclear factor-κB signal transduction. More recently, D. melanogaster has been used to understand how the immune response is regulated and coordinated at the level of the whole organism. For example, researchers have used this model in studies investigating interactions between the microbiota and the immune system at barrier epithelial surfaces that ensure proper nutritional and immune homeostasis both locally and systemically. In addition, studies in D. melanogaster have been pivotal in uncovering how the immune response is regulated by both endocrine and metabolic signalling systems, and how the immune response modifies these systems as part of a homeostatic circuit. In this Review, we briefly summarize microbial recognition and antiviral immunity in D. melanogaster, and we highlight recent studies that have explored the effects of organism-wide regulation of the immune response and, conversely, the effects of the immune response on organism physiology.

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Figure 1: Innate immunity in Drosophila melanogaster.
Figure 2: Immune recognition of microbial agents in Drosophila melanogaster.
Figure 3: Nucleic acid recognition and antiviral defences in Drosophila melanogaster.
Figure 4: Drosophila melanogaster intestinal immune response to infection.
Figure 5: Systemic regulation of Drosophila melanogaster immune responses.

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Acknowledgements

N.B. is supported by New York State Stem Cell Science (grant C029542) and the US National Science Foundation (grant 1354421). S.C is supported by Burroughs Wellcome Fund, and both S.C. and N.S. are supported by the US Department of Health and Human Services and National Institutes of Health, National Institute of Allergy and Infectious Diseases grants: R01 AI095500-01A1 and R01 AI074951-06A1 (to S.C.), and R01 AI060025, R01 AI099708 and P01 AG033561 (to N.S.).

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Authors and Affiliations

  1. Department of Entomology, Cornell University, Ithaca, 14853, New York, USA

    Nicolas Buchon

  2. Division of Infectious Diseases and Immunology, University of Massachusetts School of Medicine, Worcester, 01605, Massachusetts, USA

    Neal Silverman

  3. Department of Microbiology, Penn Genome Frontiers Institute, University of Pennsylvania, Philadelphia, 19104, Pennsylvania, USA

    Sara Cherry

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  1. Nicolas Buchon
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PowerPoint slides

Glossary

Selfish genetic elements

DNA sequences that enhance their own transmission relative to other elements in the genome, and that are thought to be either neutral or detrimental to the fitness of the organism. These elements, which include transposons, constitute a large proportion of eukaryotic genomes.

RNA interference

(RNAi). RNA-directed inhibition of gene expression that is typically achieved by causing the degradation of specific mRNA molecules.

Autophagy

An evolutionarily conserved process in which an acidic double-membrane-bound vesicle, known as an autophagosome, sequesters intracellular contents (such as damaged organelles and macromolecules, or pathogens) and targets them for degradation through fusion to lysosomes. This process is essential for the response to starvation because it facilitates the recycling of cellular components, and it can also be targeted to intracellular bacteria or viruses to restrict their growth.

Haemocytes

Cells found within the haemolymph of an insect that are equivalent to the blood cells in vertebrates. Different types of haemocyte are plasmatocytes, crystal cells and lamellocytes. These cells have important roles in immunity through the secretion of cytokines and phagocytic clearance of invaders.

Mitophagy

A specialized form of autophagy that selectively targets and degrades mitochondria.

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Buchon, N., Silverman, N. & Cherry, S. Immunity in Drosophila melanogaster — from microbial recognition to whole-organism physiology. Nat Rev Immunol 14, 796–810 (2014). https://doi.org/10.1038/nri3763

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