A Specific Primed Immune Response in Drosophila Is Dependent on Phagocytes

Department of Microbiology and Immunology, Stanford University, Stanford, California, United States of America.
PLoS Pathogens (Impact Factor: 8.06). 04/2007; 3(3):e26. DOI: 10.1371/journal.ppat.0030026
Source: PubMed

ABSTRACT Author Summary

Due to the common practice of vaccination and prominence of AIDS, people are already aware of the distinction between adaptive and innate immunity without realizing it. All organisms have an innate immune response, but only vertebrates possess T cells and the ability to produce antibodies. It has been a long-standing assumption that invertebrate immune systems are not adaptive and respond identically to multiple challenges. In this study, we demonstrate that the fly innate immune response adapts to repeated challenges; flies preinoculated with dead Streptococcus pneumoniae are protected against a second, otherwise-lethal dose. Although the underlying mechanisms are likely to be very different, this primed response is reminiscent to vaccine-induced protection in that it exhibits coarse specificity (dead S. pneumoniae only protects against itself), persists for the life of the fly and is dependent on phagocytic cells. This result prompts the obvious question of whether the innate immune system of vertebrates shares a similar biology. Such a finding is of particular interest since immunocompromised individuals only possess an innate immune system.

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Available from: Marc S Dionne, Aug 21, 2015
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    • "In some animals, pathogen challenge increases resistance to subsequent infections (a pattern referred to as immune priming, see Pham et al. 2007; Lawniczak et al. 2007; Roth et al. 2009); but, in other animals, it enhances aspects of physiology, often to the detriment of their ability to fight off subsequent live infections (Leroy et al. 2012; Papp et al. 2012; Ermolaeva et al. 2013). Although it is unknown whether the physiological benefits of pathogen challenges fulfill the characteristic pattern of hormesis (an inverted " U " dose–response relationship with beneficial effects at low doses and toxic effects at high doses), the finding that life-history traits can be improved by a single dose of pathogen challenge suggests that hormesis can be induced by host responses to pathogen challenge (Leroy et al. 2012; Papp et al. 2012; Ermolaeva et al. 2013). "
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    ABSTRACT: Many have argued that we may be able to extend life and improve human health through hormesis, the beneficial effects of low-level toxins and other stressors. But, studies of hormesis in model systems have not yet established whether stress-induced benefits are cost-free, artefacts of inbreeding, or come with deleterious side-effects. Here we provide evidence that hormesis results in trade-offs with immunity. We find that a single topical dose of dead spores of the entomopathogenic fungus, Metarhizium robertsii, increases the longevity of the fruit fly, Drosophila melanogaster, without significant decreases in fecundity. We find that hormetic benefits of pathogen challenge are greater in lines which lack key components of anti-fungal immunity (Dif and Turandot M). And, in outbred fly lines, we find that topical pathogen challenge enhances both survival and fecundity, but reduces ability to fight off live infections. The results provide evidence that hormesis is manifested by stress-induced trade-offs with immunity, not cost-free benefits or artefacts of inbreeding. Our findings illuminate mechanisms underlying pathogen-induced life history trade-offs, and indicate that reduced immune function may be an ironic side-effect of the “elixirs of life.”This article is protected by copyright. All rights reserved.
    Evolution 05/2014; 68(8). DOI:10.1111/evo.12453 · 4.66 Impact Factor
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    • "As we used a B. bassiana strain isolated from our study site of F. selysi (Reber and Chapuisat 2012b), it is possible that the pathogen has co-evolved with its host and thus is able to evade the immune response in F. selysi, but not in L. niger (e.g., Schmid-Hempel 2009). Whatever the reason , immune priming is likely to depend on many factors such as host and pathogen species, host conditions, pathogen dose, and virulence (this study; Pham et al. 2007; Gonz alez-Tokman et al. 2010; Reber and Chapuisat 2012a "
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    ABSTRACT: Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life-history theory predicts that immune priming and large investment in immunity should be more frequent in long-lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up-regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.
    Ecology and Evolution 05/2014; 4(10). DOI:10.1002/ece3.1070 · 1.66 Impact Factor
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    • "Although there have been more and more research on the immune priming of invertebrate, most of the previous studies have concentrated on the reduced mortality to evaluate the enhanced immune protection . It was demonstrated in Drosophila melanogaster Meigen (Diptera: Drosophilidae) that the protective effect of immune priming to Streptococcus pneumoniae infection depended on the phagocytes and Toll pathway (Pham et al. 2007). Recently, Roth and Kurtz (2009) demonstrated that phagocytic activity of the woodlouse Porcellio scaber Latreille (Isopoda: Porcellionidae ) was increased in a pathogen-speciÞc manner after priming. "
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    ABSTRACT: The current study investigated the characteristics and mechanism of the invertebrate immune priming using Galleria mellonella (L.) (Lepidoptera: Pyralidae) larvae (host) and Photorhabdus luminescens TT01 (pathogen) as a model. The following parameters of the G. mellonella larvae primed by hemocoel injection of heat-killed cells of TT01 or Bacillus thuringiensis HD-1 were determined at designated times after priming and then compared and analyzed systematically: mortality of the primed larvae against TT01 infection (immune protection level), hemocyte density, phagocytosis and encapsulation abilities ofhemocyte, and antibacterial activity of cell free hemolymph (major innate parameters). The results showed that 1) immune priming increased survival of the larvae against a lethal infection of TT01 and the levels and periods of protection correlated positively to the priming dose; 2) the changes on the levels of protection and the major innate parameters of the larvae primed with either TT01 or HD-1 followed a similar pattern of the convex curve, although the levels and the timing of changes differed significantly among the four innate immune parameters and between two priming bacteria; and 3) the immune protection level at a time after priming was correlated to the overall level of four innate immune parameters of the primed larvae. The current study demonstrated that the immune priming phenomenon of G. mellonella larvae has low level of specificity, and it was achieved mainly by the regulation on the quantity and activity of major innate immune parameters, such as hemocytes, antimicrobial peptides, and enzymes.
    Journal of Economic Entomology 04/2014; 107(2):559-69. DOI:10.1603/EC13455 · 1.61 Impact Factor
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