Deep sequencing of the innate immune transcriptomic response of zebrafish embryos to Salmonella infection

Ordas, Anita; Hegedűs, Zoltán; Henkel, Christiaan V.; Stockhammer, Oliver W.; Butler, Derek; Jansen, Hans J.; Rácz, Péter; Mink, Mátyás; Spaink, Herman P.; Meijer, Annemarie H.

doi:10.1016/j.fsi.2010.08.022

Cited by 69 publications

(64 citation statements)

References 28 publications

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“…2A, 2B). As observed in previous S. typhimurium infection studies, several negative regulators of immunity signaling are induced concomitantly with the induction of proinflammatory genes (38,53). Similar to the increased induction of proinflammatory genes, infected ptpn6 morphants also showed increased induction levels of several of these negative regulators, such as irak3, socs3a, and socs3b, and NF-kB inhibitor genes (nfkbiaa, nfkbiab, nfkbib, and nfkbiz).…”

Section: Glucocorticoid Treatment Enhances the Ptpn6 Morphant Phenotypesupporting

confidence: 80%

“…The advantage of this model for functional analysis of ptpn6 was that the response to S. typhimurium infection can be analyzed at 36 hpf (8 hpi) (38,53), thus avoiding that the microarray analysis is affected by secondary effects of the late inflammatory phenotype (observed at 4-6 dpf). RNA samples from infected and mock-injected ptpn6 MO1 morphants or control embryos from three replicate experiments were analyzed using a common reference approach (Fig.…”

Section: Glucocorticoid Treatment Enhances the Ptpn6 Morphant Phenotypementioning

confidence: 99%

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Deficiency in Hematopoietic Phosphatase Ptpn6/Shp1 Hyperactivates the Innate Immune System and Impairs Control of Bacterial Infections in Zebrafish Embryos

Kanwal

Zakrzewska

Hertog

et al. 2013

The Journal of Immunology

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Deficiency in Src homology region 2 domain-containing phosphatase 1/protein tyrosine phosphatase nonreceptor type 6 (SHP1/PTPN6) is linked with chronic inflammatory diseases and hematological malignancies in humans. In this study, we exploited the embryonic and larval stages of zebrafish (Danio rerio) as an animal model to study ptpn6 function in the sole context of innate immunity. We show that ptpn6 knockdown induces a spontaneous inflammation-associated phenotype at the late larval stage. Surprisingly, glucocorticoid treatment did not suppress inflammation under ptpn6 knockdown conditions but further enhanced leukocyte infiltration and proinflammatory gene expression. Experiments in a germ-free environment showed that the late larval phenotype was microbe independent. When ptpn6 knockdown embryos were challenged with Salmonella typhimurium or Mycobacterium marinum at earlier stages of development, the innate immune system was hyperactivated to a contraproductive level that impaired the control of these pathogenic bacteria. Transcriptome analysis demonstrated that Kyoto Encyclopedia of Genes and Genomes pathways related to pathogen recognition and cytokine signaling were significantly enriched under these conditions, suggesting that ptpn6 functions as a negative regulator that imposes a tight control over the level of innate immune response activation during infection. In contrast to the hyperinduction of proinflammatory cytokine genes under ptpn6 knockdown conditions, anti-inflammatory il10 expression was not hyperinduced. These results support that ptpn6 has a crucial regulatory function in preventing host-detrimental effects of inflammation and is essential for a successful defense mechanism against invading microbes.

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Section: Glucocorticoid Treatment Enhances the Ptpn6 Morphant Phenotypesupporting

confidence: 80%

Section: Glucocorticoid Treatment Enhances the Ptpn6 Morphant Phenotypementioning

confidence: 99%

Deficiency in Hematopoietic Phosphatase Ptpn6/Shp1 Hyperactivates the Innate Immune System and Impairs Control of Bacterial Infections in Zebrafish Embryos

Kanwal

Zakrzewska

Hertog

et al. 2013

The Journal of Immunology

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“…The innate host immune response to inflammatory bacterial infection was probed with zebrafish embryos infected with Salmonella typhimurium using both RNA-seq and tag-based sequencing (Ordas et al, 2011). In this study, two sequencing methods showed a strong correlation of sequence read counts per transcript and an overlap of 241 transcripts differentially expressed in response to infection.…”

Section: Quantifying Transcript Levelmentioning

confidence: 99%

RNA-Seq Technology and Its Application in Fish Transcriptomics

Qian

Ba²,

Zhuang³

et al. 2014

OMICS: A Journal of Integrative Biology

299

147

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High-throughput sequencing technologies, also known as next-generation sequencing (NGS) technologies, have revolutionized the way that genomic research is advancing. In addition to the static genome, these state-of-art technologies have been recently exploited to analyze the dynamic transcriptome, and the resulting technology is termed RNA sequencing (RNA-seq). RNA-seq is free from many limitations of other transcriptomic approaches, such as microarray and tag-based sequencing method. Although RNA-seq has only been available for a short time, studies using this method have completely changed our perspective of the breadth and depth of eukaryotic transcriptomes. In terms of the transcriptomics of teleost fishes, both model and non-model species have benefited from the RNA-seq approach and have undergone tremendous advances in the past several years. RNA-seq has helped not only in mapping and annotating fish transcriptome but also in our understanding of many biological processes in fish, such as development, adaptive evolution, host immune response, and stress response. In this review, we first provide an overview of each step of RNA-seq from library construction to the bioinformatic analysis of the data. We then summarize and discuss the recent biological insights obtained from the RNA-seq studies in a variety of fish species.

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“…The analysis is far from complete because the role of individual effectors has been studied only in a few cases. DNA microarrays or deep sequencing [157] are being used to compare the effect of wild-type and specific mutant strains of Salmonella. These methods could also be used to analyze the transcriptional profiles of cultured cells expressing or not a particular effector.…”

Section: Global Responsesmentioning

confidence: 99%

Impact ofSalmonella entericaType III Secretion System Effectors on the Eukaryotic Host Cell

Ramos‐Morales

2012

ISRN Cell Biology

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Type III secretion systems are molecular machines used by many Gram-negative bacterial pathogens to inject proteins, known as effectors, directly into eukaryotic host cells. These proteins manipulate host signal transduction pathways and cellular processes to the pathogen's advantage. Salmonella enterica possesses two virulence-related type III secretion systems that deliver more than forty effectors. This paper reviews our current knowledge about the functions, biochemical activities, host targets, and impact on host cells of these effectors. First, the concerted action of effectors at the cellular level in relevant aspects of the interaction between Salmonella and its hosts is analyzed. Then, particular issues that will drive research in the field in the near future are discussed. Finally, detailed information about each individual effector is provided.

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Deep sequencing of the innate immune transcriptomic response of zebrafish embryos to Salmonella infection

Cited by 69 publications

References 28 publications

Deficiency in Hematopoietic Phosphatase Ptpn6/Shp1 Hyperactivates the Innate Immune System and Impairs Control of Bacterial Infections in Zebrafish Embryos

Deficiency in Hematopoietic Phosphatase Ptpn6/Shp1 Hyperactivates the Innate Immune System and Impairs Control of Bacterial Infections in Zebrafish Embryos

RNA-Seq Technology and Its Application in Fish Transcriptomics

Impact ofSalmonella entericaType III Secretion System Effectors on the Eukaryotic Host Cell

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