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Novel Omics Studies on Anisakid Nematodes

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (31 May 2020) | Viewed by 28112

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Prof. Dr. Stefano D'Amelio

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Department of Public Health and Infectious Diseases, Sapienza University of Rome, P.le Aldo Moro, 5 - 00185 Rome, Italy
Interests: zoonotic parasites; parasite systematics; host-parasite interactions
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Fabrizio Lombardo

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Guest Editor

Department of Public Health and Infectious Diseases, Sapienza University of Rome, 5, 00185 Rome, Italy
Interests: vector biology; molecular parasitology; mosquito; malaria; transcriptomics

Dr. Serena Cavallero

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Guest Editor

Department of Public Health and Infectious Diseases, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy
Interests: zoonotic helminths; STHs; host–parasite interactions; transcriptomics

Special Issue Information

Dear Colleagues,

Anisakids are cosmopolitan parasitic nematodes that depend on aquatic hosts to successfully complete their life-cycle. Definitive and intermediate hosts are marine mammals or fish-eating birds and crustaceans, respectively, while fish and squids can act as paratenic hosts. Anisakids are responsible for a relatively poorly known food-borne zoonosis, known as anisakidosis. This occurs as a consequence of accidental ingestion of L3s and is a mild to severe gastrointestinal and/or allergic disease.

Large attention has been given in the past to the taxonomy and phylogeny of anisakid nematodes, allowing to depict a clear picture of the wide diversity of existing sibling and morphospecies, as well as of the evolutionary relationships among species and genera. On the other hand, only few attempts have been made to describe the genomic, transcriptomic, and proteomic profiling of these nematodes.

The aim of the Special Issue will be to collect the most updated studies on:

- Advances in the genomics of Anisakid species;
- Implication of omics studies in food safety screening;
- Characterization of allergens and development of specific diagnostic tools;
- Gene expression at different stages and in different tissues and organs;
- Host–parasite interface;
- Genomic biodiversity;
- Proteomic profiling.

Prof. Stefano D'Amelio
Prof. Fabrizio Lombardo
Dr. Serena Cavallero
Guest Editors

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Keywords

Anisakid nematodes
Host–parasite interactions
Omics analyses
Allergens
Food borne zoonosis
Gastrointestinal parasites

Published Papers (10 papers)

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Editorial

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3 pages, 177 KiB

Open AccessEditorial

Novel Omics Studies on Anisakid Nematodes

by Serena Cavallero, Fabrizio Lombardo and Stefano D’Amelio

Genes 2021, 12(8), 1250; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12081250 - 16 Aug 2021

Viewed by 1184

Abstract

Parasitic nematodes infecting humans and animals are widely distributed in marine and terrestrial environments, causing considerable morbidity and mortality globally [...] Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

Research

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22 pages, 3066 KiB

Open AccessArticle

Quantitative Proteomics Comparison of Total Expressed Proteomes of Anisakis simplex Sensu Stricto, A. pegreffii, and Their Hybrid Genotype

by Susana C. Arcos, Lee Robertson, Sergio Ciordia, Isabel Sánchez-Alonso, Mercedes Careche, Noelia Carballeda-Sanguiao, Miguel Gonzalez-Muñoz and Alfonso Navas

Genes 2020, 11(8), 913; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11080913 - 10 Aug 2020

Cited by 2 | Viewed by 1982

Abstract

The total proteomes of Anisakis simplex s.s., A. pegreffii and their hybrid genotype have been compared by quantitative proteomics (iTRAQ approach), which considers the level of expressed proteins. Comparison was made by means of two independent experiments considering four biological replicates of A. simplex and two each for A. pegreffii and hybrid between both species. A total of 1811 and 1976 proteins have been respectively identified in the experiments using public databases. One hundred ninety-six proteins were found significantly differentially expressed, and their relationships with the nematodes’ biological replicates were estimated by a multidimensional statistical approach. Results of pairwise Log₂ ratio comparisons among them were statistically treated and supported in order to convert them into discrete character states. Principal component analysis (PCA) confirms the validity of the method. This comparison selected thirty seven proteins as discriminant taxonomic biomarkers among A. simplex, A. pegreffii and their hybrid genotype; 19 of these biomarkers, encoded by ten loci, are specific allergens of Anisakis (Ani s7, Ani s8, Ani s12, and Ani s14) and other (Ancylostoma secreted) is a common nematodes venom allergen. The rest of the markers comprise four unknown or non-characterized proteins; five different proteins (leucine) related to innate immunity, four proteolytic proteins (metalloendopeptidases), a lipase, a mitochondrial translocase protein, a neurotransmitter, a thyroxine transporter, and a structural collagen protein. The proposed methodology (proteomics and statistical) solidly characterize a set of proteins that are susceptible to take advantage of the new targeted proteomics. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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16 pages, 9382 KiB

Open AccessArticle

Comparative Proteomics Analysis of Anisakis simplex s.s.—Evaluation of the Response of Invasive Larvae to Ivermectin

by Iwona Polak, Elżbieta Łopieńska-Biernat, Robert Stryiński, Jesús Mateos and Mónica Carrera

Genes 2020, 11(6), 710; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060710 - 26 Jun 2020

Cited by 13 | Viewed by 3717

Abstract

Ivermectin (IVM), an antiparasitic drug, has a positive effect against Anisakis simplex s.s. infection and has been used for the treatment and prevention of anisakiasis in humans. However, the molecular mechanism of action of IVM on A. simplex s.s. remains unknown. Herein, tandem mass tag (TMT) labeling and extensive liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) analysis were used to identify the effect of IVM on the proteome of A. simplex s.s. in vitro. During the study, 3433 proteins, of which 1247 had at least two protein unique peptides, were identified. Comparative proteomics analysis revealed that 59 proteins were differentially regulated (DRPs) in IVM-treated larvae, of which 14 proteins were upregulated and 38 were downregulated after 12 h of culture, but after 24 h, 12 proteins were upregulated and 22 were downregulated. The transcription level of five randomly selected DRPs was determined by real-time PCR as a supplement to the proteomic data. The functional enrichment analysis showed that most of the DRPs were involved in oxidoreductase activity, immunogenicity, protein degradation, and other biological processes. This study has, for the first time, provided comprehensive proteomics data on A. simplex s.s. response to IVM and might deliver new insight into the molecular mechanism by which IVM acts on invasive larvae of A. simplex s.s. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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18 pages, 6392 KiB

Open AccessArticle

Mass Spectrometry Based-Proteomic Analysis of Anisakis spp.: A Preliminary Study towards a New Diagnostic Tool

by Valeria Marzano, Stefania Pane, Gianluca Foglietta, Stefano Levi Mortera, Pamela Vernocchi, Andrea Onetti Muda and Lorenza Putignani

Genes 2020, 11(6), 693; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060693 - 24 Jun 2020

Cited by 20 | Viewed by 3161

Abstract

Anisakiasis is nowadays a well-known infection, mainly caused by the accidental ingestion of Anisakis larvae, following the consumption of raw or undercooked fishes and cephalopods. Due to the similarity of symptoms with those of common gastrointestinal disorders, this infection is often underestimated, and the need for new specific diagnostic tools is becoming crucial. Given the remarkable impact that MALDI–TOF MS biotyping had in the last decade in clinical routine practice for the recognition of bacterial and fungi strains, a similar scenario could be foreseen for the identification of parasites, such as nematodes. In this work, a MALDI–TOF MS profiling of Anisakis proteome was pursued with a view to constructing a first spectral library for the diagnosis of Anisakis infections. At the same time, a shotgun proteomics approach by LC–ESI–MS/MS was performed on the two main fractions obtained from protein extraction, to evaluate the protein species enriched by the protocol. A set of MALDI–TOF MS signals associated with proteins originating in the ribosomal fraction of the nematode extract was selected as a potential diagnostic tool for the identification of Anisakis spp. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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10 pages, 4841 KiB

Open AccessArticle

Leukocyte Nucleolus and Anisakis pegreffii—When Falling Apart Means Falling in Place

by Ivona Mladineo and Jerko Hrabar

Genes 2020, 11(6), 688; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060688 - 23 Jun 2020

Cited by 1 | Viewed by 2306

Abstract

The view of the nucleolus as a mere ribosomal factory has been recently expanded, highlighting its essential role in immune and stress-related signalling and orchestrating. It has been shown that the nucleolus structure, formed around nucleolus organiser regions (NORs) and attributed Cajal bodies, is prone to disassembly and reassembly correlated to various physiological and pathological stimuli. To evaluate the effect of parasite stimulus on the structure of the leukocyte nucleolus, we exposed rat peripheral blood mononuclear cells (PBMC) to the crude extract of the nematode A. pegreffii (Anisakidae), and compared the observed changes to the effect of control (RPMI-1640 media), immunosuppressive (MPA) and immunostimulant treatment (bacterial lipopolysaccharide (LPS) and viral analogue polyinosinic:polycytidylic acid (poly I:C)) by confocal microscopy. Poly I:C triggered the most accentuated changes such as nucleolar fragmentation and structural unravelling, LPS induced nucleolus thickening reminiscent of cell activation, while MPA induced disassembly of dense fibrillar and granular components. A. pegreffii crude extract triggered nucleolar segregation, expectedly more enhanced in treatment with a higher dose. This is the first evidence that leukocyte nucleoli already undergo structural changes 12 h post-parasitic stimuli, although these are likely to subside after successful cell activation. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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17 pages, 2330 KiB

Open AccessArticle

Immunoreactive Proteins in the Esophageal Gland Cells of Anisakis Simplex Sensu Stricto Detected by MALDI-TOF/TOF Analysis

by Lee Robertson, Susana C. Arcos, Sergio Ciordia, Noelia Carballeda-Sanguiao, María del Carmen Mena, Isabel Sánchez-Alonso, Miguel Gonzalez-Muñoz, Mercedes Careche and Alfonso Navas

Genes 2020, 11(6), 683; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060683 - 22 Jun 2020

Cited by 7 | Viewed by 2390

Abstract

In plant and animal nematode parasites, proteins derived from esophageal gland cells have been shown to be important in the host-nematodes relationship but little is known about the allergenic potential of these proteins in the genus Anisakis. Taking into account the increase of anisakiasis and allergies related to these nematodes, immunoreactive properties of gland cell proteins were investigated. Two hundred ventricles were manually dissected from L3 stage larvae of Aniskakis simplex s.s. to allow direct protein analysis. Denaturing gel electrophoresis followed by monochromatic silver staining which revealed the presence of differential (enriched) proteins when compared to total nematode extracts. Such comparison was performed by means of 1D and 2D electrophoresis. Pooled antisera from Anisakis spp.-allergic patients were used in western blots revealing the presence of 13 immunoreactive bands in the ventricular extracts in 1D, with 82 spots revealed in 2D. The corresponding protein bands and spots were excised from the silver-stained gel and protein assignation was made by MALDI-TOF/TOF. A total of 13 (including proteoforms) were unambiguously identified. The majority of these proteins are known to be secreted by nematodes into the external environment, of which three are described as being major allergens in other organisms with different phylogenetic origin and one is an Anisakis simplex allergen. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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15 pages, 1137 KiB

Open AccessArticle

Differences in Gene Expression Profiles of Seven Target Proteins in Third-Stage Larvae of Anisakis simplex (Sensu Stricto) by Sites of Infection in Blue Whiting (Micromesistius poutassou)

by Marialetizia Palomba, Paolo Cipriani, Lucilla Giulietti, Arne Levsen, Giuseppe Nascetti and Simonetta Mattiucci

Genes 2020, 11(5), 559; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11050559 - 17 May 2020

Cited by 14 | Viewed by 3085

Abstract

The third-stage larvae of the parasitic nematode genus Anisakis tend to encapsulate in different tissues including the musculature of fish. Host tissue penetration and degradation involve both mechanic processes and the production of proteins encoded by an array of genes. Investigating larval gene profiles during the fish infection has relevance in understanding biological traits in the parasite’s adaptive ability to cope with the fish hosts’ defense responses. The present study aimed to investigate the gene expression levels of some proteins in L3 of A. simplex (s.s.) infecting different tissues of blue whiting Micromesistius poutassou, a common fish host of the parasite in the NE Atlantic. The following genes encoding for Anisakis spp. proteins were studied: Kunitz-type trypsin inhibitor (TI), hemoglobin (hb), glycoprotein (GP), trehalase (treh), zinc metallopeptidase 13 (nas 13), ubiquitin-protein ligase (hyd) and sideroflexin 2 (sfxn 2). Significant differences in gene transcripts (by quantitative real-time PCR, qPCR) were observed in larvae located in various tissues of the fish host, with respect to the control. ANOVA analysis showed that relative gene expression levels of the seven target genes in the larvae are linked to the infection site in the fish host. Genes encoding some of the target proteins seem to be involved in the host tissue migration and survival of the parasite in the hostile target tissues of the fish host. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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6 pages, 519 KiB

Open AccessCommunication

First Molecular Diagnosis of Clinical Cases of Gastric Anisakiosis in Spain

by Xavier Roca-Geronès, M. Magdalena Alcover, Carla Godínez-González, Olga González-Moreno, Miquel Masachs, Roser Fisa and Isabel Montoliu

Genes 2020, 11(4), 452; https://doi.org/10.3390/genes11040452 - 22 Apr 2020

Cited by 10 | Viewed by 2488

Abstract

Anisakiosis is a fish-borne disease with gastrointestinal and/or allergic symptoms caused by the consumption of raw or undercooked fish parasitized with nematode larvae of the genus Anisakis. In Europe, Anisakis pegreffii has been detected as the causative agent, although the sibling species Anisakis simplex sensu stricto (s.s.) is also known to cause the disease in other parts of the world, and discrepancies exist regarding their respective pathogenic potential. In Spain a high number of cases has been recorded, with marinated anchovies being the main source of infection, although no specific diagnosis has been documented in humans. In this study, we analyzed three cases of anisakiosis in patients from Barcelona (Spain) who had consumed undercooked hake. All patients described epigastric pain and several larval nematodes were removed endoscopically from their stomachs. Larvae were morphologically characterized as third-stage larvae of Anisakis simplex sensu lato (s.l.) and molecularly identified as A. simplex (s.s.) by means of PCR RFLP of the ITS region of the rDNA and sequencing of the elongation factor1 alpha1 (EF1 α-1) nDNA gen. This study represents the first specific identification of Anisakis larvae in clinical cases of anisakiosis reported in Spain. Specific molecular diagnosis is of crucial importance for assessing the health risk of Anisakis sibling species. Hake consumption stands out as a risk factor for anisakiosis, since this fish species can be highly parasitized. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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15 pages, 1153 KiB

Open AccessArticle

Comparative Transcriptomics Reveals Clues for Differences in Pathogenicity between Hysterothylacium aduncum, Anisakis simplex sensu stricto and Anisakis pegreffii

by Serena Cavallero, Fabrizio Lombardo, Marco Salvemini, Antonella Pizzarelli, Cinzia Cantacessi and Stefano D’Amelio

Genes 2020, 11(3), 321; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11030321 - 18 Mar 2020

Cited by 22 | Viewed by 3400

Abstract

Ascaridoid nematodes are widespread in marine fishes. Despite their major socioeconomic importance, mechanisms associated to the fish-borne zoonotic disease anisakiasis are still obscure. RNA-Seq and de-novo assembly were herein applied to RNA extracted from larvae and dissected pharynx of Hysterothylacium aduncum (HA), a non-pathogenic nematode. Assembled transcripts in HA were annotated and compared to the transcriptomes of the zoonotic species Anisakis simplex sensu stricto (AS) and Anisakis pegreffii (AP). Approximately 60,000,000 single-end reads were generated for HA, AS and AP. Transcripts in HA encoded for 30,254 putative peptides while AS and AP encoded for 20,574 and 20,840 putative peptides, respectively. Differential gene expression analyses yielded 471, 612 and 526 transcripts up regulated in the pharynx of HA, AS and AP. The transcriptomes of larvae and pharynx of HA were enriched in transcripts encoding collagen, peptidases, ribosomal proteins and in heat-shock motifs. Transcripts encoding proteolytic enzymes, anesthetics, inhibitors of primary hemostasis and virulence factors, anticoagulants and immunomodulatory peptides were up-regulated in AS and AP pharynx. This study represents the first transcriptomic characterization of a marine parasitic nematode commonly recovered in fish and probably of negligible concern for public health. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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Review

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18 pages, 732 KiB

Open AccessReview

Advances in Omic Studies Drive Discoveries in the Biology of Anisakid Nematodes

by Stefano D’Amelio, Fabrizio Lombardo, Antonella Pizzarelli, Ilaria Bellini and Serena Cavallero

Genes 2020, 11(7), 801; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11070801 - 15 Jul 2020

Cited by 15 | Viewed by 3537

Abstract

Advancements in technologies employed in high-throughput next-generation sequencing (NGS) methods are supporting the spread of studies that, combined with advances in computational biology and bioinformatics, have greatly accelerated discoveries within basic and biomedical research for many parasitic diseases. Here, we review the most updated “omic” studies performed on anisakid nematodes, a family of marine parasites that are causative agents of the fish-borne zoonosis known as anisakiasis or anisakidosis. Few deposited data on Anisakis genomes are so far available, and this still hinders the deep and highly accurate characterization of biological aspects of interest, even as several transcriptomic and proteomic studies are becoming available. These have been aimed at discovering and characterizing molecules specific to peculiar developmental parasitic stages or tissues, as well as transcripts with pathogenic potential as toxins and allergens, with a broad relevance for a better understanding of host–pathogen relationships and for the development of reliable diagnostic tools. Full article

(This article belongs to the Special Issue Novel Omics Studies on Anisakid Nematodes)

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