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  • 1.
    Emami, S. Noushin
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Swedish University of Agricultural Sciences, Sweden.
    Lindberg, Bo G.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hua, Susanna
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hill, Sharon R.
    Mozuraitis, Raimondas
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Birgersson, Göran
    Borg-Karlson, Anna-Karin
    Ignell, Rickard
    Faye, Ingrid
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    A key malaria metabolite modulates vector blood seeking, feeding, and susceptibility to infection2017In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 355, no 6329Article in journal (Refereed)
    Abstract [en]

    Malaria infection renders humans more attractive to Anopheles gambiae sensu lato mosquitoes than uninfected people. The mechanisms remain unknown. We found that an isoprenoid precursor produced by Plasmodium falciparum, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), affects A. gambiae s. l. blood meal seeking and feeding behaviors as well as susceptibility to infection. HMBPP acts indirectly by triggering human red blood cells to increase the release of CO2, aldehydes, and monoterpenes, which together enhance vector attraction and stimulate vector feeding. When offered in a blood meal, HMBPP modulates neural, antimalarial, and oogenic gene transcription without affecting mosquito survival or fecundity; in a P. falciparum-infected blood meal, sporogony is increased.

  • 2. Kukutla, Phanidhar
    et al.
    Lindberg, Bo G.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Pei, Dong
    Rayl, Melanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Yu, Wanqin
    Steritz, Matthew
    Faye, Ingrid
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Xu, Jiannong
    Draft Genome Sequences of Elizabethkingia anophelis Strains R26T and Ag1 from the Midgut of the Malaria Mosquito Anopheles gambiae2013In: Genome Announcements, ISSN 2169-8287, Vol. 1, no 6, p. e01030-13-Article in journal (Refereed)
    Abstract [en]

    Elizabethkingia anophelis is a species in the family Flavobacteriaceae. It is a dominant resident in the mosquito gut and also a human pathogen. We present the draft genome sequences of two strains of E. anophelis, R26T and Ag1, which were isolated from the midgut of the malaria mosquito Anopheles gambiae.

  • 3. Kukutla, Phanidhar
    et al.
    Lindberg, Bo G.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Pei, Dong
    Rayl, Melanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Yu, Wanqin
    Steritz, Matthew
    Faye, Ingrid
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Xu, Jiannong
    Insights from the Genome Annotation of Elizabethkingia anophelis from the Malaria Vector Anopheles gambiae2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 5, p. e97715-Article in journal (Refereed)
    Abstract [en]

    Elizabethkingia anophelis is a dominant bacterial species in the gut ecosystem of the malaria vector mosquito Anopheles gambiae. We recently sequenced the genomes of two strains of E. anophelis, R26(T) and Ag1, isolated from different strains of A. gambiae. The two bacterial strains are identical with a few exceptions. Phylogenetically, Elizabethkingia is closer to Chryseobacterium and Riemerella than to Flavobacterium. In line with other Bacteroidetes known to utilize various polymers in their ecological niches, the E. anophelis genome contains numerous TonB dependent transporters with various substrate specificities. In addition, several genes belonging to the polysaccharide utilization system and the glycoside hydrolase family were identified that could potentially be of benefit for the mosquito carbohydrate metabolism. In agreement with previous reports of broad antibiotic resistance in E. anophelis, a large number of genes encoding efflux pumps and blactamases are present in the genome. The component genes of resistance-nodulation-division type efflux pumps were found to be syntenic and conserved in different taxa of Bacteroidetes. The bacterium also displays hemolytic activity and encodes several hemolysins that may participate in the digestion of erythrocytes in the mosquito gut. At the same time, the OxyR regulon and antioxidant genes could provide defense against the oxidative stress that is associated with blood digestion. The genome annotation and comparative genomic analysis revealed functional characteristics associated with the symbiotic relationship with the mosquito host.

  • 4.
    Lindberg, Bo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Insights from the genome annotation of Elizabethkingia anophelis from the malaria vector Anopheles gambiaeManuscript (preprint) (Other academic)
  • 5.
    Lindberg, Bo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Medium from γ-irradiated Escherichia coli Bacteria Stimulates a Unique Immune Response in Drosophila CellsManuscript (preprint) (Other academic)
  • 6.
    Lindberg, Bo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Novel Modes of Immune Activation in Anopheles gambiae and Drosophila melanogaster2014Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Malaria is a disease of poverty and continues to plague a great part of the world’s population. An increased understanding of the interactions between the vector mosquito, the malaria parasite, and also the mosquito gut microbiota are pivotal for the development of novel measures against the disease. The first aim of this thesis was to gain a deeper knowledge of the microbial compounds that elicit immune responses in the main malaria vector Anopheles gambiae and also using the model organism Drosophila melanogaster. The second aim was to analyse the genome characteristics in silico of a bacterial symbiont from the mosquito midgut. In Paper I, we investigated the immunogenic effects of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate in Anopheles. This compound is the primary activator of human Vγ9Vδ2 T cells and is only produced by organisms that use the non-mevalonate pathway for isoprenoid synthesis, such as Plasmodium and most eubacteria but not animals. We show that the parasite releases compounds of this nature and that provision of HMBPP in the bloodmeal induces an immune response in the mosquito. In Paper II, we investigated whether bacteria inactivated by gamma-irradiation could still stimulate potent immune responses in Drosophila cells. We show that E. coli retains the capacity to synthesize and release peptidoglycan de novo for several days after the irradiation event. When cells were stimulated with supernatants from irradiated bacteria, however, a unique response was observed. In Paper III, we presented the draft genome sequence of Elizabethkingia anophelis, a predominant gut symbiont of An. gambiae recently described in our lab and subsequently found in another laboratory strain of the mosquito. The genome data were then annotated in Paper IV to gain insights into the symbiotic characteristics of the bacterium, as well as the genetic background for its strong antibiotic resistance. In conclusion, this thesis work has shed light on novel modes for stimulating immune responses in insects and also led to the characterization of a predominant bacteria in the mosquito gut that may be used in future malaria intervention strategies. 

  • 7.
    Lindberg, Bo G.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Merritt, Eleanor A.
    Rayl, Melanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Liu, Chenxiao
    Parmryd, Ingela
    Olofsson, Berit
    Stockholm University, Faculty of Science, Department of Organic Chemistry.
    Faye, Ingrid
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Immunogenic and Antioxidant Effects of a Pathogen-Associated Prenyl Pyrophosphate in Anopheles gambiae2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 8, p. e73868-Article in journal (Refereed)
    Abstract [en]

    Despite efficient vector transmission, Plasmodium parasites suffer great bottlenecks during their developmental stages within Anopheles mosquitoes. The outcome depends on a complex three-way interaction between host, parasite and gut bacteria. Although considerable progress has been made recently in deciphering Anopheles effector responses, little is currently known regarding the underlying microbial immune elicitors. An interesting candidate in this sense is the pathogen-derived prenyl pyrophosphate and designated phosphoantigen (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), found in Plasmodium and most eubacteria but not in higher eukaryotes. HMBPP is the most potent stimulant known of human V gamma 9V delta 2 T cells, a unique lymphocyte subset that expands during several infections including malaria. In this study, we show that V(Y)9V delta 2 T cells proliferate when stimulated with supernatants from intraerythrocytic stages of Plasmodium falciparum cultures, suggesting that biologically relevant doses of phosphoantigens are excreted by the parasite. Next, we used Anopheles gambiae to investigate the immune-and redox-stimulating effects of HMBPP. We demonstrate a potent activation in vitro of all but one of the signaling pathways earlier implicated in the human V(Y)9V delta 2 T cell response, as p38, JNK and PI3K/Akt but not ERK were activated in the A. gambiae 4a3B cell line. Additionally, both HMBPP and the downstream endogenous metabolite isopentenyl pyrophosphate displayed antioxidant effects by promoting cellular tolerance to hydrogen peroxide challenge. When provided in the mosquito blood meal, HMBPP induced temporal changes in the expression of several immune genes. In contrast to meso-diaminopimelic acid containing peptidoglycan, HMBPP induced expression of dual oxidase and nitric oxide synthase, two key determinants of Plasmodium infection. Furthermore, temporal fluctuations in midgut bacterial numbers were observed. The multifaceted effects observed in this study indicates that HMBPP is an important elicitor in common for both Plasmodium and gut bacteria in the mosquito.

  • 8.
    Lindberg, Bo G.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Oldenvi, Sandra
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Steiner, Håkan
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Medium from gamma-irradiated Escherichia coli bacteria stimulates a unique immune response in Drosophila cells2014In: Developmental and Comparative Immunology, ISSN 0145-305X, E-ISSN 1879-0089, Vol. 46, no 2, p. 392-400Article in journal (Refereed)
    Abstract [en]

    It is well known that gamma-irradiated, non-dividing bacteria can elicit potent immune responses in mammals. Compared to traditional heat or chemical inactivation of microbes, gamma -irradiation likely preserves metabolic activity and antigenic features to a larger extent. We have previously shown that antimicrobial peptides are induced in Drosophila by peptidoglycan fragments secreted into the medium of exponentially growing bacterial cultures. In this study, we gamma-irradiated Escherichia coil cells at a dose that halted cell division. The temporal synthesis and release of peptidoglycan fragments were followed as well as the potential of bacterial supernatants to induce immune responses in Drosophila S2 cells. We demonstrate that peptidoglycan synthesis continues for several days post irradiation and that monomeric peptidoglycan is shed into the medium. Whole transcriptome analysis revealed a strong immune response against the bacterial medium. The response to medium taken directly post irradiation shows a large overlap to that of peptidoglycan. Medium from prolonged bacterial incubation does, however, stimulate a selective set of immune genes. A shift towards a stress response was instead observed with a striking induction of several heat shock proteins. Our findings suggest that gamma-irradiated bacteria release elicitors that stimulate a novel response in Drosophila.

  • 9.
    Lindberg, Bo G.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Tang, Xiongzhuo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Dantoft, Widad
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Gohel, Priya
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Seyedoleslami Esfahani, Shiva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Lindvall, Jessica M.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Engström, Ylva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Nubbin isoform antagonism governs Drosophila intestinal immune homeostasis2018In: PLoS Pathogens, ISSN 1553-7366, E-ISSN 1553-7374, Vol. 14, no 3, article id e1006936Article in journal (Refereed)
    Abstract [en]

    Gut immunity is regulated by intricate and dynamic mechanisms to ensure homeostasis despite a constantly changing microbial environment. Several regulatory factors have been described to participate in feedback responses to prevent aberrant immune activity. Little is, however, known about how transcriptional programs are directly tuned to efficiently adapt host gut tissues to the current microbiome. Here we show that the POU/Oct gene nubbin (nub) encodes two transcription factor isoforms, Nub-PB and Nub-PD, which antagonistically regulate immune gene expression in Drosophila. Global transcriptional profiling of adult flies overexpressing Nub-PB in immunocompetent tissues revealed that this form is a strong transcriptional activator of a large set of immune genes. Further genetic analyses showed that Nub-PB is sufficient to drive expression both independently and in conjunction with nuclear factor kappa B (NF-κB), JNK and JAK/STAT pathways. Similar overexpression of Nub-PD did, conversely, repress expression of the same targets. Strikingly, isoform co-overexpression normalized immune gene transcription, suggesting antagonistic activities. RNAi-mediated knockdown of individual nub transcripts in enterocytes confirmed antagonistic regulation by the two isoforms and that both are necessary for normal immune gene transcription in the midgut. Furthermore, enterocyte-specific Nub-PB expression levels had a strong impact on gut bacterial load as well as host lifespan. Overexpression of Nub-PB enhanced bacterial clearance of ingested Erwinia carotovora carotovora 15. Nevertheless, flies quickly succumbed to the infection, suggesting a deleterious immune response. In line with this, prolonged overexpression promoted a proinflammatory signature in the gut with induction of JNK and JAK/STAT pathways, increased apoptosis and stem cell proliferation. These findings highlight a novel regulatory mechanism of host-microbe interactions mediated by antagonistic transcription factor isoforms.

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