A Complex Proteomic Response of the Parasitic Nematode Anisakis simplex s.s. to Escherichia coli Lipopolysaccharide

Mierzejewski, Karol; Stryiński, Robert; Łopieńska–Biernat, Elżbieta; Mateos, Jesús; Bogacka, Iwona; Carrera, Mónica

doi:10.1016/j.mcpro.2021.100166

Cited by 3 publications

(5 citation statements)

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“…Finally, in vitro experiments might represent a starting point for the study of helminth immunity. Anisakis simplex stimulated in vitro with E. coli LPS failed to activate pathways homologous to those of C. elegans immunity, nor did it express HDP, but rather proteins that engage in interactions with host immunity [39]. Despite the nematode's inability to recognize LPS through PAMPs, we speculate that as this is a conserved Gram-negative bacterial cell wall motif, it is nonetheless perceived through some other anisakid mechanism(s).…”

Section: Helminth Innate Immunitymentioning

confidence: 80%

Helminthic host defense peptides: using the parasite to defend the host

Mladineo¹,

Rončević²,

Gerdol³

et al. 2023

Trends in Parasitology

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Section: Helminth Innate Immunitymentioning

confidence: 80%

Helminthic host defense peptides: using the parasite to defend the host

Mladineo¹,

Rončević²,

Gerdol³

et al. 2023

Trends in Parasitology

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“…For example, OGDH interacts with 11 other proteins. Such connections in the case of gene silencing or direct blocking of the activity of a particular protein offer the chance of promising results, as they affect many metabolic pathways simultaneously, which has been discussed previously [41][42][43]. In addition, for the first time for A. simplex s. s., the tissue-specific host-pathogen interactions were investigated (see Figure 7, File S7).…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, in this study, we described for the first time the proteomic analysis of 2 tissues of the L4 developmental stage of A. simplex s. s. In the L4 stage, tissues, such as the cuticle and intestine, are fully developed and functional [27][28][29]. In addition, previous proteomic studies of A. simplex did not focus on comparative analysis of nematode tissues [41][42][43][44][45][46][47][48][49][50][51]. This work provides new insights into the tissue-specific proteome of A. simplex s. s., which was not previously possible.…”

Section: Discussionmentioning

confidence: 99%

“…The TMT-labeled peptide concentration was measured using a Pierce Quantitative Colorimetric Peptide Assay (Thermo Fisher Scientific, Waltham, MA, USA) according to the manufacturer's instructions. To increase the number of peptide identifications, eliminate the interference from co-isolated ions, and achieve results comparable to the MS3-based methods [42,116], the combined sample was fractionated using a Pierce High-pH Reversed-Phase Peptide Fractionation Kit (Thermo Fisher Scientific, Waltham, MA, USA) following the manufacturer's instructions. The peptide concentration in each fraction was determined by colorimetric analysis using the Quantitative Colorimetric Peptide Assay (Thermo Fisher Scientific, Waltham, MA, USA) following the manufacturer's instructions.…”

Section: Tmt Labeling and Reversed-phase Fractionationmentioning

confidence: 99%

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Tandem Mass Tagging (TMT) Reveals Tissue-Specific Proteome of L4 Larvae of Anisakis simplex s. s.: Enzymes of Energy and/or Carbohydrate Metabolism as Potential Drug Targets in Anisakiasis

Stryiński

Mateos

Carrera

et al. 2022

IJMS

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Anisakis simplex s. s. is a parasitic nematode of marine mammals and causative agent of anisakiasis in humans. The cuticle and intestine of the larvae are the tissues most responsible for direct and indirect contact, respectively, of the parasite with the host. At the L4 larval stage, tissues, such as the cuticle and intestine, are fully developed and functional, in contrast to the L3 stage. As such, this work provides for the first time the tissue-specific proteome of A. simplex s. s. larvae in the L4 stage. Statistical analysis (FC ≥ 2; p-value ≤ 0.01) showed that 107 proteins were differentially regulated (DRPs) between the cuticle and the rest of the larval body. In the comparison between the intestine and the rest of the larval body at the L4 stage, 123 proteins were identified as DRPs. Comparison of the individual tissues examined revealed a total of 272 DRPs, with 133 proteins more abundant in the cuticle and 139 proteins more abundant in the intestine. Detailed functional analysis of the identified proteins was performed using bioinformatics tools. Glycolysis and the tricarboxylic acid cycle were the most enriched metabolic pathways by cuticular and intestinal proteins, respectively, in the L4 stage of A. simplex s. s. The presence of two proteins, folliculin (FLCN) and oxoglutarate dehydrogenase (OGDH), was confirmed by Western blot, and their tertiary structure was predicted and compared with other species. In addition, host–pathogen interactions were identified, and potential new allergens were predicted. The result of this manuscript shows the largest number of protein identifications to our knowledge using proteomics tools for different tissues of L4 larvae of A. simplex s. s. The identified tissue-specific proteins could serve as targets for new drugs against anisakiasis.

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“…Combining a genetically defensible model organism such as C. elegans with the functional evaluation of metabolomics and/or lipidomics holds great promise for expanding our knowledge of metabolism and metabolic regulation ( Salzer and Witting, 2021 ). While there are numerous published studies on the genomes ( Mattiucci et al, 2016 ; Coghlan et al, 2019 ; Łopieńska-Biernat et al, 2019 ), transcriptomes ( Cavallero et al, 2018 ; Kim et al, 2018 ; Llorens et al, 2018 ; Łopieńska-Biernat et al, 2018 ; Cavallero et al, 2020 ), and proteomes ( Stryiński et al, 2019 ; Stryiński et al, 2022 ; Polak et al, 2020 ; Mierzejewski et al, 2021 ; Kochanowski et al, 2022 ) of A. simplex , less attention has been paid to its metabolome. Metabolic changes between L3 and L4 larval stages of A. simplex have been studied previously, however in a narrow range, e.g., of one metabolic pathway ( Łopieńska-Biernat et al, 2008 ; Łopieńska-Biernat et al, 2018 ; Łopieńska-Biernat et al, 2019 ), and almost nothing is known about the complement of an intermediate or end product of metabolism in Anisakis nematodes, especially in the stages found in humans (L3 and L4).…”

Section: Discussionmentioning

confidence: 99%

Metabolomic analysis reveals a differential adaptation process of the larval stages of Anisakis simplex to the host environment

Polak

Stryiński

Majewska

et al. 2023

Front. Mol. Biosci.

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Introduction:Anisakis simplex are parasitic nematodes that cause anisakiasis. The possibility of infection with this parasite is through consumption of raw or undercooked fish products. A. simplex infections are often misdiagnosed, especially in subclinical cases that do not present with typical symptoms such as urticaria, angioedema, and gastrointestinal allergy. The resulting allergic reactions range from rapid-onset and potentially fatal anaphylactic reactions to chronic, debilitating conditions. While there have been numerous published studies on the genomes and proteomes of A. simplex, less attention has been paid to the metabolomes. Metabolomics is concerned with the composition of metabolites in biological systems. Dynamic responses to endogenous and exogenous stimuli are particularly well suited for the study of holistic metabolic responses. In addition, metabolomics can be used to determine metabolic activity at different stages of development or during growth.Materials and methods: In this study, we reveal for the first time the metabolomes of infectious stages (L3 and L4) of A. simplex using untargeted metabolomics by ultra-performance liquid chromatography-mass spectrometry.Results: In the negative ionization mode (ESI-), we identified 172 different compounds, whereas in the positive ionization mode (ESI+), 186 metabolites were found. Statistical analysis showed that 60 metabolites were found in the ESI- mode with different concentration in each group, of which 21 were more enriched in the L3 larvae and 39 in the L4 stage of A. simplex. Comparison of the individual developmental stages in the ESI + mode also revealed a total of 60 differential metabolites, but 32 metabolites were more enriched in the L3 stage larvae, and 28 metabolites were more concentrated in the L4 stage.Discussion: The metabolomics study revealed that the developmental stages of A. simplex differed in a number of metabolic pathways, including nicotinate and nicotinamide metabolism. In addition, molecules responsible for successful migration within their host, such as pyridoxine and prostaglandins (E1, E2, F1a) were present in the L4 stage. In contrast, metabolic pathways for amino acids, starch, and sucrose were mainly activated in the L3 stage. Our results provide new insights into the comparative metabolome profiles of two different developmental stages of A. simplex.

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A Complex Proteomic Response of the Parasitic Nematode Anisakis simplex s.s. to Escherichia coli Lipopolysaccharide

Cited by 3 publications

References 105 publications

Helminthic host defense peptides: using the parasite to defend the host

Helminthic host defense peptides: using the parasite to defend the host

Tandem Mass Tagging (TMT) Reveals Tissue-Specific Proteome of L4 Larvae of Anisakis simplex s. s.: Enzymes of Energy and/or Carbohydrate Metabolism as Potential Drug Targets in Anisakiasis

Metabolomic analysis reveals a differential adaptation process of the larval stages of Anisakis simplex to the host environment

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