Infection-Induced Intestinal Oxidative Stress Triggers Organ-to-Organ Immunological Communication in Drosophila

Wu, Shih-Cheng; Liao, Chu‐Bin; Pan, Rong-Long; Juang, Jyh‐Lyh

doi:10.1016/j.chom.2012.03.004

Cited by 95 publications

(94 citation statements)

References 28 publications

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“…The present study using Drosophila third instar larvae supports the scenario that Toll signaling is a key mechanism in the host defense system that responds to endogenous inflammatory factors, consistent with the dedicated role of Toll-like receptors in vertebrate "danger" sensing (1,47,48). A number of previous studies that focused on nonmicrobial signal-activated host defense in Drosophila showed that the Imd/Relish cascade is activated by endogenous inflammatory agents, such as undigested DNA (49,50) and the neuro-peptide bursicon (51), as well as undefined humoral factors released from the intestine after tissue damage (52). The observation of different signaling pathways that are activated in response to various forms of stress, and in the dronc mutant, indicate that specific detection mechanisms are used to discriminate among various forms of threat.…”

Section: Discussionsupporting

confidence: 52%

Persephone/Spätzle Pathogen Sensors Mediate the Activation of Toll Receptor Signaling in Response to Endogenous Danger Signals in Apoptosis-deficient Drosophila

Ming

Obata

Kuranaga

et al. 2014

Journal of Biological Chemistry

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Section: Discussionsupporting

confidence: 52%

Persephone/Spätzle Pathogen Sensors Mediate the Activation of Toll Receptor Signaling in Response to Endogenous Danger Signals in Apoptosis-deficient Drosophila

Ming

Obata

Kuranaga

et al. 2014

Journal of Biological Chemistry

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“…The induction of gut immune-signaling pathways likely results from recognition of parasite-associated molecular patterns by the gut epithelia. Immune molecules produced by the gut epithelia, such as reactive oxygen species (19) or cardia-produced inducible nitric oxide (iNOS) (20), may further lead to systemic immune induction in other organs (21). Our previous study that investigated fat body responses in adult flies noted strong induction of the Imd pathway and one of its effector products (antimicrobial peptide Attacin-A) 72 h after exposure to trypanosomes (14).…”

Section: Resultsmentioning

confidence: 99%

Mammalian African trypanosome VSG coat enhances tsetse’s vector competence

Aksoy

Vigneron

Bing

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Tsetse flies are biological vectors of African trypanosomes, the protozoan parasites responsible for causing human and animal trypanosomiases across sub-Saharan Africa. Currently, no vaccines are available for disease prevention due to antigenic variation of the Variant Surface Glycoproteins (VSG) that coat parasites while they reside within mammalian hosts. As a result, interference with parasite development in the tsetse vector is being explored to reduce disease transmission. A major bottleneck to infection occurs as parasites attempt to colonize tsetse's midgut. One critical factor influencing this bottleneck is the fly's peritrophic matrix (PM), a semipermeable, chitinous barrier that lines the midgut. The mechanisms that enable trypanosomes to cross this barrier are currently unknown. Here, we determined that as parasites enter the tsetse's gut, VSG molecules released from trypanosomes are internalized by cells of the cardiathe tissue responsible for producing the PM. VSG internalization results in decreased expression of a tsetse microRNA (mir-275) and interferes with the Wnt-signaling pathway and the Iroquois/IRX transcription factor family. This interference reduces the function of the PM barrier and promotes parasite colonization of the gut early in the infection process. Manipulation of the insect midgut homeostasis by the mammalian parasite coat proteins is a novel function and indicates that VSG serves a dual role in trypanosome biology-that of facilitating transmission through its mammalian host and insect vector. We detail critical steps in the course of trypanosome infection establishment that can serve as novel targets to reduce the tsetse's vector competence and disease transmission.tsetse | trypanosome | VSG | peritrophic matrix | vector competence

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“…Furthermore, by analogy to Drosophila, other cellular and humoral responses that may also involve the fat body are likely to influence oocyst survival. In Drosophila, hemocytes are key intermediate components required for interorgan communication between the midgut and fat body and are required for activation of humoral immunity and pathogen elimination (36,37).…”

Section: Discussionmentioning

confidence: 99%

Hemocyte differentiation mediates the mosquito late-phase immune response against Plasmodium in Anopheles gambiae

Smith

Barillas‐Mury

Jacobs-Lorena

2015

Proc. Natl. Acad. Sci. U.S.A.

143

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Plasmodium parasites must complete development in the mosquito vector for transmission to occur. The mosquito innate immune response is remarkably efficient in limiting parasite numbers. Previous work has identified a LPS-induced TNFα transcription factor (LITAF)-like transcription factor, LITAF-like 3 (LL3), which significantly influences parasite numbers. Here, we demonstrate that LL3 does not influence invasion of the mosquito midgut epithelium or ookinete-to-oocyst differentiation but mediates a late-phase immune response that decreases oocyst survival. LL3 expression in the midgut and hemocytes is activated by ookinete midgut invasion and is independent of the mosquito microbiota, suggesting that LL3 may be a component of a wound-healing response. LL3 silencing abrogates the ability of mosquito hemocytes to differentiate and respond to parasite infection, implicating hemocytes as critical modulators of the late-phase immune response.osquitoes of the genus Anopheles are the obligate vectors for the transmission of the malaria parasite. Despite much effort invested to understand the interactions between the mosquito immune system and the parasite, our knowledge of these processes remains incomplete. The mosquito innate immune response effectively reduces parasite numbers, resulting in a severe bottleneck at the oocyst stage (1). There is evidence to suggest that multiple pathways contribute to parasite killing during two separate stages, or phases, of parasite development (1). An "early phase" occurs ∼18-24 h after blood feeding, as Plasmodium ookinetes invade the midgut epithelium and emerge on the basal side facing the hemocoel. During invasion, ookinetes are marked by epithelial nitration in a response regulated by the Jun N-terminal kinase (JNK) pathway, to promote thioester-containing protein 1 (TEP1) binding to the ookinete surface (2, 3). Once bound, TEP1 is believed to initiate a complement-like cascade that ultimately leads to parasite lysis or melanization (4-7).Parasites that evade this early-phase complement-like recognition and elimination are thought to be subjected to a second, "latephase" immune response that further decreases parasite numbers. This model is supported by the observation that the number of mature oocysts is significantly less than the number of early oocysts (8). Silencing the transcription factors STAT-A and STAT-B significantly increases oocyst survival, thus implicating the STAT pathway in this response (8). Conversely, constitutive activation of the STAT pathway via silencing the repressor SOCS (suppressor of cytokine signaling) resulted in increased levels of nitric oxide synthase (NOS) production and enhanced oocyst killing (8). These observations are in agreement with other studies that implicate NOS and subsequent NO production as important determinants of malaria parasite survival (9-11).Previously, we have characterized a LITAF-like transcription factor, LPS-induced TNFα transcription factor (LITAF)-like 3 (LL3), in Anopheles gambiae that mediates a potent antiPlasmod...

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Infection-Induced Intestinal Oxidative Stress Triggers Organ-to-Organ Immunological Communication in Drosophila

Cited by 95 publications

References 28 publications

Persephone/Spätzle Pathogen Sensors Mediate the Activation of Toll Receptor Signaling in Response to Endogenous Danger Signals in Apoptosis-deficient Drosophila

Persephone/Spätzle Pathogen Sensors Mediate the Activation of Toll Receptor Signaling in Response to Endogenous Danger Signals in Apoptosis-deficient Drosophila

Mammalian African trypanosome VSG coat enhances tsetse’s vector competence

Hemocyte differentiation mediates the mosquito late-phase immune response against Plasmodium in Anopheles gambiae

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