Trichinella-induced immunomodulation: Another tale of helminth success

Bruschi, Fabrizio; Ashour, Dalia S.; Othman, Ahmad A.

doi:10.1016/j.fawpar.2022.e00164

Cited by 18 publications

(17 citation statements)

References 200 publications

(266 reference statements)

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“…Many parasitic nematodes encyst within host tissue (e.g. Cooperia punctata [ 45 ] and Trichinella spiralis [ 46 ], which both invade the intestinal mucosa during their development), migrate through aerobic host tissues (e.g. Ascaris lumbricoides [ 47 ], Necator americanus [ 48 ], and Nippostrongylus brasiliensis [ 49 ], which all migrate through circulatory and pulmonary tissues), or actively seek host blood (e.g.…”

Section: Resultsmentioning

confidence: 99%

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematode Heligmosomoides bakeri

Pollo,

Leon-Coria,

Liu

et al. 2023

Parasites Vectors

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Background Heligmosomoides bakeri (often mistaken for Heligmosomoides polygyrus) is a promising model for parasitic nematodes with the key advantage of being amenable to study and manipulation within a controlled laboratory environment. While draft genome sequences are available for this worm, which allow for comparative genomic analyses between nematodes, there is a notable lack of information on its gene expression. Methods We generated biologically replicated RNA-seq datasets from samples taken throughout the parasitic life of H. bakeri. RNA from tissue-dwelling and lumen-dwelling worms, collected under a dissection microscope, was sequenced on an Illumina platform. Results We find extensive transcriptional sexual dimorphism throughout the fourth larval and adult stages of this parasite and identify alternative splicing, glycosylation, and ubiquitination as particularly important processes for establishing and/or maintaining sex-specific gene expression in this species. We find sex-linked differences in transcription related to aging and oxidative and osmotic stress responses. We observe a starvation-like signature among transcripts whose expression is consistently upregulated in males, which may reflect a higher energy expenditure by male worms. We detect evidence of increased importance for anaerobic respiration among the adult worms, which coincides with the parasite’s migration into the physiologically hypoxic environment of the intestinal lumen. Furthermore, we hypothesize that oxygen concentration may be an important driver of the worms encysting in the intestinal mucosa as larvae, which not only fully exposes the worms to their host’s immune system but also shapes many of the interactions between the host and parasite. We find stage- and sex-specific variation in the expression of immunomodulatory genes and in anthelmintic targets. Conclusions We examine how different the male and female worms are at the molecular level and describe major developmental events that occur in the worm, which extend our understanding of the interactions between this parasite and its host. In addition to generating new hypotheses for follow-up experiments into the worm’s behavior, physiology, and metabolism, our datasets enable future more in-depth comparisons between nematodes to better define the utility of H. bakeri as a model for parasitic nematodes in general. Graphical Abstract

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Section: Resultsmentioning

confidence: 99%

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematode Heligmosomoides bakeri

Pollo,

Leon-Coria,

Liu

et al. 2023

Parasites Vectors

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“…Many parasitic nematodes encyst within host tissue (ex. Cooperia punctata [37] and Trichinella spiralis [38], which both invade the intestinal mucosa during their development), migrate through aerobic host tissues (ex. Ascaris lumbricoides [39], Necator americanus [40], and Nippostrongylus brasiliensis [41], which all migrate through circulatory and pulmonary tissues), or actively seek host blood (ex.…”

Section: Resultsmentioning

confidence: 99%

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematodeHeligmosomoides bakeri

Pollo

Coria

Finney

et al. 2022

Preprint

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Heligmosomoides polygyrus is a promising model for parasitic nematodes with the key advantage of being amenable to study and manipulation within a controlled laboratory environment. While draft genome sequences are available for this worm, which allow for comparative genomic analyses between nematodes, there is a notable lack of information on its gene expression. Here, we have generated biologically replicated RNA-seq datasets from samples taken throughout the parasitic life of H. polygyrus. We find extensive transcriptional sexual dimorphism throughout the fourth larval and adult stages of this parasite and identify alternative splicing, glycosylation, and ubiquitination as particularly important processes for establishing and/or maintaining sex-specific gene expression in this species. Further, we find sex-linked differences in transcription related to aging and oxidative and osmotic stress responses. Additionally, we observe a starvation-like signature among transcripts whose expression is consistently up-regulated in males, which may reflect a higher energy expenditure by male worms. We detect evidence of increased importance for anaerobic respiration among the adult worms, which coincides with the parasite’s migration into the physiologically hypoxic environment of the intestinal lumen. Further, we hypothesize that oxygen concentration may be an important driver of the worms encysting in the intestinal mucosa as larvae, which not only fully exposes the worms to their host’s immune system, but also shapes many of the interactions between the host and parasite. We find stage- and sex-specific variation in the expression of immunomodulatory genes and in anthelmintic targets. In addition to generating new hypotheses for follow-up experiments into the worm’s behaviour, physiology, and metabolism, our datasets enable future more in-depth comparisons between nematodes to better define the utility of H. polygyrus as a model for parasitic nematodes in general.Author SummaryParasitic nematodes (roundworms) that infect humans and livestock are a major health and economic burden but are challenging to study in a laboratory environment because of their required hosts. One strategy to get around this difficulty is to first study a rodent model to guide targeted experiments in the more difficult study system. Heligmosomoides polygyrus is closely related to the nematode parasites of humans and livestock and naturally parasitizes mice. We have generated information on the expression of all of the genes in this worm throughout the stages of its life when it is parasitic. This information allows us to examine how different the male and female worms are at the molecular level. We also describe major developmental events that occur in the worm, which extend our understanding of the interactions between this parasite and its host. We analyse the expression of genes known to be involved in interfering with host immune responses and others known to be targeted by drugs designed to kill worms. This new information will allow for better comparisons among nematodes to assess how well this rodent model system works for studying parasitic nematodes in general.

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“…T. spiralis was reported to delay and modulate Type 1 diabetes onset and progression by either T. spiralis infection or parasite products, which are useful in medical treatments for other illnesses [35]. Moreover, according to Bruschi, Ashour and Othman [20], T. spiralis has an inhibitory effect on neutrophil inflammatory function, experimental autoimmune encephalomyelitis and regulated human dendritic cell activation. Moreover, T. spiralis infection protected mice against colitis [36] and acute lung injury induced by bacterial lipopolysaccharide (LPS) [37], as well as their immunoprotective inference on house dust mites-induced allergic airway remodelling in mice [38].…”

Section: Genementioning

confidence: 99%

Trichinella spiralis Larval Extract as a Biological Anti‐Tumor Therapy in a Murine Model of Ehrlich Solid Carcinoma

Younis,

Salama,

Elmehy

et al. 2024

Parasite Immunology

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Trichinella spiralis (T. spiralis) is an immunomodulating parasite that can adversely affect tumor growth and extend host lifespan. The aim of this study was to elucidate the mechanisms by which T. spiralis larval antigens achieve this effect using Ehrlich solid carcinoma (ESC) murine model. Assessment was done by histopathological and immunohistochemical analysis of caspase‐3, TNF‐α, Ki‐67 and CD31. Additionally, Bcl2 and Bcl2‐associated protein X (Bax) relative gene expression was assessed by molecular analysis for studying the effect of T. spiralis crude larval extract (CLE) antigen on tumor necrosis, apoptosis, cell proliferation and angiogenesis. We found that both T. spiralis infection and CLE caused a decrease in the areas of necrosis in ESC. Moreover, they led to increased apoptosis through activation of caspase‐3, up‐regulation of pro‐apoptotic gene, Bax and down‐regulation of anti‐apoptotic gene, Bcl2. Also, T. spiralis infection and CLE diminished ESC proliferation, as evidenced by decreasing Ki‐67. T. spiralis infection and CLE were able to suppress the development of ESC by inhibiting tumor proliferation, inducing apoptosis and decreasing tumor necrosis, with subsequent decrease in tumor metastasis. T. spiralis CLE antigen may be considered as a promising complementary immunotherapeutic agent in the treatment of cancer.

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Trichinella-induced immunomodulation: Another tale of helminth success

Cited by 18 publications

References 200 publications

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematode Heligmosomoides bakeri

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematode Heligmosomoides bakeri

Transcriptional patterns of sexual dimorphism and in host developmental programs in the model parasitic nematodeHeligmosomoides bakeri

Trichinella spiralis Larval Extract as a Biological Anti‐Tumor Therapy in a Murine Model of Ehrlich Solid Carcinoma

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