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1.  Hijacking of Host Cellular Functions by an Intracellular Parasite, the Microsporidian Anncaliia algerae 
PLoS ONE  2014;9(6):e100791.
Intracellular pathogens including bacteria, viruses and protozoa hijack host cell functions to access nutrients and to bypass cellular defenses and immune responses. These strategies have been acquired through selective pressure and allowed pathogens to reach an appropriate cellular niche for their survival and growth. To get new insights on how parasites hijack host cellular functions, we developed a SILAC (Stable Isotope Labeling by Amino Acids in Cell culture) quantitative proteomics workflow. Our study focused on deciphering the cross-talk in a host-parasite association, involving human foreskin fibroblasts (HFF) and the microsporidia Anncaliia algerae, a fungus related parasite with an obligate intracellular lifestyle and a strong host dependency. The host-parasite cross-talk was analyzed at five post-infection times 1, 6, 12 and 24 hours post-infection (hpi) and 8 days post-infection (dpi). A significant up-regulation of four interferon-induced proteins with tetratricopeptide repeats IFIT1, IFIT2, IFIT3 and MX1 was observed at 8 dpi suggesting a type 1 interferon (IFN) host response. Quantitative alteration of host proteins involved in biological functions such as signaling (STAT1, Ras) and reduction of the translation activity (EIF3) confirmed a host type 1 IFN response. Interestingly, the SILAC approach also allowed the detection of 148 A. algerae proteins during the kinetics of infection. Among these proteins many are involved in parasite proliferation, and an over-representation of putative secreted effectors proteins was observed. Finally our survey also suggests that A. algerae could use a transposable element as a lure strategy to escape the host innate immune system.
doi:10.1371/journal.pone.0100791
PMCID: PMC4072689  PMID: 24967735
3.  Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee 
Scientific Reports  2012;2:326.
In ecosystems, a variety of biological, chemical and physical stressors may act in combination to induce illness in populations of living organisms. While recent surveys reported that parasite-insecticide interactions can synergistically and negatively affect honeybee survival, the importance of sequence in exposure to stressors has hardly received any attention. In this work, Western honeybees (Apis mellifera) were sequentially or simultaneously infected by the microsporidian parasite Nosema ceranae and chronically exposed to a sublethal dose of the insecticide fipronil, respectively chosen as biological and chemical stressors. Interestingly, every combination tested led to a synergistic effect on honeybee survival, with the most significant impacts when stressors were applied at the emergence of honeybees. Our study presents significant outcomes on beekeeping management but also points out the potential risks incurred by any living organism frequently exposed to both pathogens and insecticides in their habitat.
doi:10.1038/srep00326
PMCID: PMC3310228  PMID: 22442753
4.  Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae 
PLoS ONE  2011;6(6):e21550.
Background
The honeybee, Apis mellifera, is undergoing a worldwide decline whose origin is still in debate. Studies performed for twenty years suggest that this decline may involve both infectious diseases and exposure to pesticides. Joint action of pathogens and chemicals are known to threaten several organisms but the combined effects of these stressors were poorly investigated in honeybees. Our study was designed to explore the effect of Nosema ceranae infection on honeybee sensitivity to sublethal doses of the insecticides fipronil and thiacloprid.
Methodology/Finding
Five days after their emergence, honeybees were divided in 6 experimental groups: (i) uninfected controls, (ii) infected with N. ceranae, (iii) uninfected and exposed to fipronil, (iv) uninfected and exposed to thiacloprid, (v) infected with N. ceranae and exposed 10 days post-infection (p.i.) to fipronil, and (vi) infected with N. ceranae and exposed 10 days p.i. to thiacloprid. Honeybee mortality and insecticide consumption were analyzed daily and the intestinal spore content was evaluated 20 days after infection. A significant increase in honeybee mortality was observed when N. ceranae-infected honeybees were exposed to sublethal doses of insecticides. Surprisingly, exposures to fipronil and thiacloprid had opposite effects on microsporidian spore production. Analysis of the honeybee detoxification system 10 days p.i. showed that N. ceranae infection induced an increase in glutathione-S-transferase activity in midgut and fat body but not in 7-ethoxycoumarin-O-deethylase activity.
Conclusions/Significance
After exposure to sublethal doses of fipronil or thiacloprid a higher mortality was observed in N. ceranae-infected honeybees than in uninfected ones. The synergistic effect of N. ceranae and insecticide on honeybee mortality, however, did not appear strongly linked to a decrease of the insect detoxification system. These data support the hypothesis that the combination of the increasing prevalence of N. ceranae with high pesticide content in beehives may contribute to colony depopulation.
doi:10.1371/journal.pone.0021550
PMCID: PMC3125288  PMID: 21738706
5.  Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation 
Behavioral Ecology  2011;22(2):392-400.
One of the most fascinating examples of parasite-induced host manipulation is that of hairworms, first, because they induce a spectacular “suicide” water-seeking behavior in their terrestrial insect hosts and, second, because the emergence of the parasite is not lethal per se for the host that can live several months following parasite release. The mechanisms hairworms use to increase the encounter rate between their host and water remain, however, poorly understood. Considering the selective landscape in which nematomorph manipulation has evolved as well as previously obtained proteomics data, we predicted that crickets harboring mature hairworms would display a modified behavioral response to light. Since following parasite emergence in water, the cricket host and parasitic worm do not interact physiologically anymore, we also predicted that the host would recover from the modified behaviors. We examined the effect of hairworm infection on different behavioral responses of the host when stimulated by light to record responses from uninfected, infected, and ex-infected crickets. We showed that hairworm infection fundamentally modifies cricket behavior by inducing directed responses to light, a condition from which they mostly recover once the parasite is released. This study supports the idea that host manipulation by parasites is subtle, complex, and multidimensional.
doi:10.1093/beheco/arq215
PMCID: PMC3071748  PMID: 22476265
behavior; insects; nematomorph; parasite manipulation; parasitism; phototaxis
6.  Virulence and resistance in a mosquito–microsporidium interaction 
Evolutionary Applications  2008;1(1):49-56.
Abstract
We review the results of a series of experiments involving Aedes aegypti and its microsporidian parasite Vavraia culicis to illustrate how intra-specific competition and parasitism shape life history traits. More specifically these experiments showed that some major components of virulence are host condition-dependent in this system, while others are not. We also briefly discuss the ways through which V. culicis modifies the physiological functioning of its host. We discuss the implications of these results for studies of host – parasite interactions in general and propose ways through which our studies could contribute to vector control and management programs.
doi:10.1111/j.1752-4571.2007.00004.x
PMCID: PMC3352405
Aedes; mosquitoes; microsporidia; resistance; Vavraia; virulence

Results 1-6 (6)