Use of zebrafish to study <i>Shigella</i> infection

Duggan, Gina; Mostowy, Serge

doi:10.1242/dmm.032151

Cited by 41 publications

(49 citation statements)

References 124 publications

(171 reference statements)

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“…Several reviews have focused on zebrafish as a model for infectious disease (Duggan & Mostowy, 2018;Sullivan et al, 2017;Tobin, May, & Wheeler, 2012), but all were focused on systemic disease models or localised infections of the swim bladder or hindbrain; none discussed infections of the gastrointestinal (GI) tract. Several reviews have focused on zebrafish as a model for infectious disease (Duggan & Mostowy, 2018;Sullivan et al, 2017;Tobin, May, & Wheeler, 2012), but all were focused on systemic disease models or localised infections of the swim bladder or hindbrain; none discussed infections of the gastrointestinal (GI) tract.…”

Section: Introductionmentioning

confidence: 99%

“…Due to its fecundity, genetic tractability, small size, rapid development, and optical transparency during early development, the zebrafish (Danio rerio) has emerged as one of the most well-used vertebrate model organisms in cellular microbiology. Several reviews have focused on zebrafish as a model for infectious disease (Duggan & Mostowy, 2018;Sullivan et al, 2017;Tobin, May, & Wheeler, 2012), but all were focused on systemic disease models or localised infections of the swim bladder or hindbrain; none discussed infections of the gastrointestinal (GI) tract. Over the last few years however, literature in this area has grown considerably, as has literature focusing on the microbiota, and characterisation of the transcriptional profiles and cell types of the zebrafish GI tract, allowing us to draw comparisons to the mammalian GI tract.…”

Section: Introductionmentioning

confidence: 99%

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The zebrafish as a model for gastrointestinal tract–microbe interactions

Flores

Nguyen

Odem

et al. 2020

Cellular Microbiology

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The zebrafish (Danio rerio) has become a widely used vertebrate model for bacterial, fungal, viral, and protozoan infections. Due to its genetic tractability, large clutch sizes, ease of manipulation, and optical transparency during early life stages, it is a particularly useful model to address questions about the cellular microbiology of host-microbe interactions. Although its use as a model for systemic infections, as well as infections localised to the hindbrain and swimbladder having been thoroughly reviewed, studies focusing on host-microbe interactions in the zebrafish gastrointestinal tract have been neglected. Here, we summarise recent findings regarding the developmental and immune biology of the gastrointestinal tract, drawing parallels to mammalian systems. We discuss the use of adult and larval zebrafish as models for gastrointestinal infections, and more generally, for studies of host-microbe interactions in the gut. K E Y W O R D S Danio rerio, gastrointestinal tract, host-pathogen interactions, infection model, microbiome, microbiota, zebrafish

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The zebrafish as a model for gastrointestinal tract–microbe interactions

Flores

Nguyen

Odem

et al. 2020

Cellular Microbiology

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“…The zebrafish model is increasingly being used to study human bacterial pathogens in vivo , including S. flexneri [18, 19]. The major pathogenic events that lead to shigellosis in humans (i.e., macrophage cell death, invasion and multiplication within epithelial cells, cell-to-cell spread, inflammatory destruction of the host epithelium) are recapitulated in a zebrafish model of S. flexneri infection [20]. Exploiting the optical accessibility of zebrafish larvae, it is possible to spatio-temporally examine the development, coordination and resolution of the innate immune response to S. flexneri in vivo .…”

Section: Introductionmentioning

confidence: 99%

Shigella sonneiinfection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence

Torraca

Kaforou

Watson

et al. 2019

Preprint

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42 Shigella flexneri is historically regarded as the primary agent of bacillary dysentery, yet the 43 closely-related Shigella sonnei is replacing S. flexneri, especially in developing countries. The 44 underlying reasons for this dramatic shift are mostly unknown. Using a zebrafish (Danio rerio) 45 model of Shigella infection, we discover that S. sonnei is more virulent than S. flexneri in vivo. 46 Whole animal dual-RNAseq and testing of bacterial mutants suggest that S. sonnei virulence 47 depends on its O-antigen oligosaccharide (which is unique among Shigella species). We show 48 in vivo using zebrafish and ex vivo using human neutrophils that S. sonnei O-antigen can 49 mediate neutrophil tolerance. Consistent with this, we demonstrate that O-antigen enables S. 50 sonnei to resist phagolysosome acidification and promotes neutrophil cell death. Chemical 51 inhibition or promotion of phagolysosome maturation respectively decreases and increases 52 neutrophil control of S. sonnei and zebrafish survival. Strikingly, larvae primed with a sublethal 3 53 dose of S. sonnei are protected against a secondary lethal dose of S. sonnei in an O-antigen-54 dependent manner, indicating that exposure to O-antigen can train the innate immune system 55 against S. sonnei. Collectively, these findings reveal O-antigen as an important therapeutic 56 target against bacillary dysentery, and may explain the rapidly increasing S. sonnei burden in 57 developing countries. 58 59 60 Author Summary 61 Shigella sonnei is predominantly responsible for dysentery in developed countries, and is 62 replacing Shigella flexneri in areas undergoing economic development and improvements in 63 water quality. Using Shigella infection of zebrafish (in vivo) and human neutrophils (in vitro), 64 we discover that S. sonnei is more virulent than S. flexneri because of neutrophil tolerance 65 mediated by its O-antigen oligosaccharide acquired from the environmental bacteria 66 Plesiomonas shigelloides. To inspire new approaches for S. sonnei control, we show that 67 increased phagolysosomal acidification or innate immune training can promote S. sonnei 68 clearance by neutrophils in vivo. These findings have major implications for our evolutionary 69 understanding of Shigella, and may explain why exposure to P. shigelloides in low and middle-70 income countries (LMICs) can protect against dysentery incidence. 71 72 73 4 80 has been a valuable discovery tool in the field of innate immunity, helping to illuminate the role 81 of neutrophil extracellular traps (NETs) [5], nucleotide-binding oligomerisation domain (NOD)-82 like receptors (NLRs) [6], bacterial autophagy [7], interferon-inducible guanylate-binding 83 proteins (GBPs) [8,9] and septin-mediated cell-autonomous immunity [10,11] in host 84 defence. 85 86 The genus Shigella comprises four different species (S. flexneri, S. sonnei, S. boydii, S. 87 dysenteriae), although DNA sequencing suggests they evolved from convergent evolution of 88 different founders [12]. The most recent strains of S. flexne...

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“…One of the limiting factors of the zebrafish model is the difference in temperature between zebrafish and the majority of the human virulent pathogens. In fact, zebrafish requires a temperature of 28°C, while human pathogens require a temperature of 37°C at which the development as well as the stress and immune response of zebrafish are significantly altered from those at 28°C (Duggan and Mostowy, 2018;Long et al, 2012).…”

Section: The C Elegans Model For Neuroimmune Interactions In Sensorymentioning

confidence: 99%