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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Biology".

Deadline for manuscript submissions: closed (29 November 2023) | Viewed by 19573

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Prof. Dr. Michael Stear

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Guest Editor

Department of Animal, Plant and Soil Sciences, La Trobe University, Bundoora 3086, Australia
Interests: genetic variation in immunity to nematodes; selective breeding for disease resistance; host–parasite interactions; immunomodulation
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Dr. Katarzyna Donskow-Lysoniewska

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Guest Editor

Department of Experimental Immunotherapy, Faculty of Medicine, Lazarski University, 02-662 Warsaw, Poland
Interests: nematodes; Heligmosomoides polygyrus bakeri infection model; immunomodulation; regulatory T cells; immunomodulatory proteins; autoimmune disorders
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

We are pleased to announce the launch of a new Special Issue of IJMS on “Parasite Biology and Host–Parasite Interactions”.

Protozoan and metazoan parasites are a major cause of disease and death in humans and in domestic animals, including livestock and wildlife. Host–parasite interaction is complex, with the host immune response recognizing hundreds of parasite molecules and parasites using multiple mechanisms and producing multiple molecules to manipulate the immune system. Nonetheless, there has been steady progress in understanding and controlling parasite infections.

This Special Issue will bring together original research articles and reviews to examine our knowledge of parasite biology, observe the interactions between hosts and parasites, describe progress in parasite control, and highlight approaches that are proving to be productive. The focus is on molecular interactions, but clinical submissions with biomolecular experiments are welcomed.

Prof. Dr. Michael Stear
Dr. Katarzyna Donskow-Lysoniewska
Guest Editors

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

parasite
immunity
immunomodulation
helper T cells
IgA
IgE
eosinophils
mast cells
regulatory T cells
galectin

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Published Papers (10 papers)

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Research

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12 pages, 4566 KiB

Open AccessArticle

Trichinella spiralis-Secreted Products Promote Collagen Capsule Formation through TGF-β1/Smad3 Pathway

by Ge Cheng, Zifang Zhang, Yixuan Wang, Youjiao Zao, Ruoqi Wang, Mengying Gao, Miaomiao Feng, Xi Zhang and Peng Jiang

Int. J. Mol. Sci. 2023, 24(19), 15003; https://doi.org/10.3390/ijms241915003 - 9 Oct 2023

Cited by 1 | Viewed by 1568

Abstract

Trichinella spiralis (T. spiralis) muscle larvae colonize in the host’s skeletal muscle cells, which are surrounded by collagen capsules. The mechanism underlying muscle stage larva-induced collagen capsule formation remains unknown. To clarify the mechanism, a T. spiralis muscular-infected mouse model was established by a single lateral tail vein injection with 20,000 T. spiralis newborn larvae (NBL). The infected mice were treated with or without SB525334 (TGF-β1 receptor type I inhibitor). Diaphragms were obtained post-infection, and the expression levels of the TGF-β1/Smad3 pathway-related genes and collagen genes (type IV and VI) were observed during the process of collagen capsule formation. The changes in myoblasts under stimulation of the excretory–secretory (ES) products of NBL with or without SB525334 were further investigated. Results showed that the expression levels of type IV collagen gene, type VI collagen gene, Tgfb1, and Smad3 were significantly increased in infected mice muscle cells. The expression levels of all the above genes were enhanced by the products of NBL in myoblast cells. These changes were reversed by co-treatment with SB525334 in vivo and in vitro. In conclusion, the TGF-β1/Smad3 pathway can be activated by T. spiralis infection in muscle cells. The activated TGF-β1/Smad3 pathway can stimulate the secretion of collagens by myocytes and plays a promoting role in the process of collagen capsule formation. The research has the limitation that the protein identification of the products of NBL has yet to be performed. Therefore, the specific components in the T. spiralis ES products that induce collagen synthesis should be further investigated. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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14 pages, 3280 KiB

Open AccessArticle

The Impact of Intestinal Inflammation on Nematode’s Excretory–Secretory Proteome

by Marta Maruszewska-Cheruiyot, Ludmiła Szewczak, Katarzyna Krawczak-Wójcik, Magdalena Kierasińska, Michael Stear and Katarzyna Donskow-Łysoniewska

Int. J. Mol. Sci. 2023, 24(18), 14127; https://doi.org/10.3390/ijms241814127 - 15 Sep 2023

Cited by 1 | Viewed by 1592

Abstract

Parasitic nematodes and their products are promising candidates for therapeutics against inflammatory bowel diseases (IBD). Two species of nematodes, the hookworm Necator americanus and the whipworm Trichuis suis, are being used in clinical treatment trials of IBD referred to as “helminth therapy”. Heligmosomoides polygyrus is a well-known model for human hookworm infections. Excretory–secretory (ES) products of H. polygyrus L4 stage that developed during colitis show a different immunomodulatory effect compared to the ES of H. polgyrus from healthy mice. The aim of the study was to evaluate excretory–secretory proteins produced by H. polygyrus L4 stage males and females that developed in the colitic milieu. Mass spectrometry was used to identify proteins. Blast2GO was used to investigate the functions of the discovered proteins. A total of 387 proteins were identified in the ES of H. polygyrus L4 males (HpC males), and 330 proteins were identified in the ES of L4 females that developed in the colitic milieu (HpC females). In contrast, only 200 proteins were identified in the ES of L4 males (Hp males) and 218 in the ES of L4 females (Hp females) that developed in control conditions. Most of the proteins (123) were detected in all groups. Unique proteins identified in the ES of HpC females included annexin, lysozyme-2, apyrase, and galectin. Venom allergen/Ancylostoma-secreted protein-like, transthyretin-like family proteins, and galectins were found in the secretome of HpC males but not in the secretome of control males. These molecules may be responsible for the therapeutic effects of nematodes in DSS-induced colitis. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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25 pages, 4152 KiB

Open AccessArticle

Modulation of LPS-Induced Neurodegeneration by Intestinal Helminth Infection in Ageing Mice

by Natalia Jermakow, Weronika Skarżyńska, Katarzyna Lewandowska, Ewelina Kiernozek, Katarzyna Goździk, Anna Mietelska-Porowska, Nadzieja Drela, Urszula Wojda and Maria Doligalska

Int. J. Mol. Sci. 2023, 24(18), 13994; https://doi.org/10.3390/ijms241813994 - 12 Sep 2023

Viewed by 1258

Abstract

Parasitic helminths induce a transient, short-term inflammation at the beginning of infection, but in persistent infection may suppress the systemic immune response by enhancing the activity of regulatory M2 macrophages. The aim of the study was to determine how nematode infection affects age-related neuroinflammation, especially macrophages in the nervous tissue. Here, intraperitoneal LPS-induced systemic inflammation resulting in brain neurodegeneration was enhanced by prolonged Heligmosomoides polygyrus infection in C57BL/6 mice. The changes in the brain coincided with the increase in M1 macrophages, reduced survivin level, enhanced APP and GFAP expression, chitin-like chains deposition in the brain and deterioration behaviour manifestations. These changes were also observed in transgenic C57BL/6 mice predisposed to develop neurodegeneration typical for Alzheimer’s disease in response to pathogenic stimuli. Interestingly, in mice infected with the nematode only, the greater M2 macrophage population resulted in better results in the forced swim test. Given the growing burden of neurodegenerative diseases, understanding such interactive associations can have significant implications for ageing health strategies and disease monitoring. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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10 pages, 1548 KiB

Open AccessArticle

Characterization of the Tongue Worm, Linguatula serrata (Pentastomida), Identified from Hares (Lepus europaeus) in Romania

by Beatrice Ana-Maria Jitea, Mirela Imre, Tiana Florea, Cătălin Bogdan Sîrbu, Iasmina Luca, Adrian Stancu, Alexandru Călin Cireșan and Gheorghe Dărăbuș

Int. J. Mol. Sci. 2023, 24(16), 12927; https://doi.org/10.3390/ijms241612927 - 18 Aug 2023

Cited by 3 | Viewed by 1965

Abstract

Linguatula serrata (Frölich, 1789) is a widespread parasite known as the tongue worm belonging to the family Linguatulidae. The adult form of the parasite is usually located in the upper respiratory tract of domestic and wild carnivores while the larval forms are located in the visceral organs of intermediate hosts (various herbivorous mammals). Twenty-four European brown hares (Lepus europaeus) were examined in this study, of which two were positive with L. serrata nymphs. The collected nymphs were examined morphologically using electron-microscopic analysis and molecularly by amplification of 18S rRNA and COX1 genes. Lung tissue samples were also collected and histopathological examination was performed. Histopathological examination revealed the following lesions: generalized inflammatory oedema, granulomas with necrosis, calcification and fibrosis in the bronchial tree. The results of molecular sequencing for L. serrata specimens collected from the European brown hares are deposited in GenBank. This study presents the first report on Linguatula serrata nymphs collected from L. europaeus in Romania, using molecular and morphological characterization simultaneously. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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19 pages, 2847 KiB

Open AccessArticle

Honey Bee Larval Hemolymph as a Source of Key Nutrients and Proteins Offers a Promising Medium for Varroa destructor Artificial Rearing

by Vincent Piou, Caroline Vilarem, Solène Blanchard, Jean-Marc Strub, Fabrice Bertile, Michel Bocquet, Karim Arafah, Philippe Bulet and Angélique Vétillard

Int. J. Mol. Sci. 2023, 24(15), 12443; https://doi.org/10.3390/ijms241512443 - 4 Aug 2023

Cited by 5 | Viewed by 2035

Abstract

Varroa destructor, a major ectoparasite of the Western honey bee Apis mellifera, is a widespread pest that damages colonies in the Northern Hemisphere. Throughout their lifecycle, V. destructor females feed on almost every developmental stage of their host, from the last larval instar to the adult. The parasite is thought to feed on hemolymph and fat body, although its exact diet and nutritional requirements are poorly known. Using artificial Parafilm™ dummies, we explored the nutrition of V. destructor females and assessed their survival when fed on hemolymph from bee larvae, pupae, or adults. We compared the results with mites fed on synthetic solutions or filtered larval hemolymph. The results showed that the parasites could survive for several days or weeks on different diets. Bee larval hemolymph yielded the highest survival rates, and filtered larval plasma was sufficient to maintain the mites for 14 days or more. This cell-free solution therefore theoretically contains all the necessary nutrients for mite survival. Because some bee proteins are known to be hijacked without being digested by the parasite, we decided to run a proteomic analysis of larval honey bee plasma to highlight the most common proteins in our samples. A list of 54 proteins was compiled, including several energy metabolism proteins such as Vitellogenin, Hexamerin, or Transferrins. These molecules represent key nutrient candidates that could be crucial for V. destructor survival. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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18 pages, 1186 KiB

Open AccessArticle

Genome-Wide Analysis of Haemonchus contortus Proteases and Protease Inhibitors Using Advanced Informatics Provides Insights into Parasite Biology and Host–Parasite Interactions

by Yuanting Zheng, Neil D. Young, Jiangning Song and Robin B. Gasser

Int. J. Mol. Sci. 2023, 24(15), 12320; https://doi.org/10.3390/ijms241512320 - 1 Aug 2023

Cited by 4 | Viewed by 1828

Abstract

Biodiversity within the animal kingdom is associated with extensive molecular diversity. The expansion of genomic, transcriptomic and proteomic data sets for invertebrate groups and species with unique biological traits necessitates reliable in silico tools for the accurate identification and annotation of molecules and molecular groups. However, conventional tools are inadequate for lesser-known organismal groups, such as eukaryotic pathogens (parasites), so that improved approaches are urgently needed. Here, we established a combined sequence- and structure-based workflow system to harness well-curated publicly available data sets and resources to identify, classify and annotate proteases and protease inhibitors of a highly pathogenic parasitic roundworm (nematode) of global relevance, called Haemonchus contortus (barber’s pole worm). This workflow performed markedly better than conventional, sequence-based classification and annotation alone and allowed the first genome-wide characterisation of protease and protease inhibitor genes and gene products in this worm. In total, we identified 790 genes encoding 860 proteases and protease inhibitors representing 83 gene families. The proteins inferred included 280 metallo-, 145 cysteine, 142 serine, 121 aspartic and 81 “mixed” proteases as well as 91 protease inhibitors, all of which had marked physicochemical diversity and inferred involvements in >400 biological processes or pathways. A detailed investigation revealed a remarkable expansion of some protease or inhibitor gene families, which are likely linked to parasitism (e.g., host–parasite interactions, immunomodulation and blood-feeding) and exhibit stage- or sex-specific transcription profiles. This investigation provides a solid foundation for detailed explorations of the structures and functions of proteases and protease inhibitors of H. contortus and related nematodes, and it could assist in the discovery of new drug or vaccine targets against infections or diseases. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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18 pages, 3511 KiB

Open AccessArticle

The Proteome and Lipidome of Extracellular Vesicles from Haemonchus contortus to Underpin Explorations of Host–Parasite Cross–Talk

by Tao Wang, Tiana F. Koukoulis, Laura J. Vella, Huaqi Su, Adityas Purnianto, Shuai Nie, Ching-Seng Ang, Guangxu Ma, Pasi K. Korhonen, Aya C. Taki, Nicholas A. Williamson, Gavin E. Reid and Robin B. Gasser

Int. J. Mol. Sci. 2023, 24(13), 10955; https://doi.org/10.3390/ijms241310955 - 30 Jun 2023

Cited by 2 | Viewed by 1813

Abstract

Many parasitic worms have a major adverse impact on human and animal populations worldwide due to the chronicity of their infections. There is a growing body of evidence indicating that extracellular vesicles (EVs) are intimately involved in modulating (suppressing) inflammatory/immune host responses and parasitism. As one of the most pathogenic nematodes of livestock animals, Haemonchus contortus is an ideal model system for EV exploration. Here, employing a multi-step enrichment process (in vitro culture, followed by ultracentrifugation, size exclusion and filtration), we enriched EVs from H. contortus and undertook the first comprehensive (qualitative and quantitative) multi-omic investigation of EV proteins and lipids using advanced liquid chromatography–mass spectrometry and informatics methods. We identified and quantified 561 proteins and 446 lipids in EVs and compared these molecules with those of adult worms. We identified unique molecules in EVs, such as proteins linked to lipid transportation and lipid species (i.e., sphingolipids) associated with signalling, indicating the involvement of these molecules in parasite-host cross-talk. This work provides a solid starting point to explore the functional roles of EV-specific proteins and lipids in modulating parasite-host cross-talk, and the prospect of finding ways of disrupting or interrupting this relationship to suppress or eliminate parasite infection. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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19 pages, 6972 KiB

Open AccessArticle

Molecular Characterization of the Interplay between Fasciola hepatica Juveniles and Laminin as a Mechanism to Adhere to and Break through the Host Intestinal Wall

by Judit Serrat, María Torres-Valle, Marta López-García, David Becerro-Recio, Mar Siles-Lucas and Javier González-Miguel

Int. J. Mol. Sci. 2023, 24(9), 8165; https://doi.org/10.3390/ijms24098165 - 3 May 2023

Cited by 3 | Viewed by 2076

Abstract

Fasciola hepatica is the main causative agent of fasciolosis, a zoonotic parasitic disease of growing public health concern. F. hepatica metacercariae are ingested by the host and excyst in the intestine, thereby releasing the newly excysted juveniles (FhNEJ), which traverse the gut wall and migrate towards the biliary ducts. Since blocking F. hepatica development is challenging after crossing of the intestinal wall, targeting this first step of migration might result in increased therapeutic success. The intestinal extracellular matrix (ECM) is constituted by a network of structural proteins, including laminin (LM) and fibronectin (FN), that provide mechanical support while acting as physical barrier against intestinal pathogens. Here, we employed ELISA and immunofluorescent assays to test for the presence of LM- and FN-binding proteins on a tegument-enriched antigenic fraction of FhNEJ, and further determined their identity by two-dimensional electrophoresis coupled to mass spectrometry. Additionally, we performed enzymatic assays that revealed for the first time the capability of the juvenile-specific cathepsin L3 to degrade LM, and that LM degradation by FhNEJ proteins is further potentiated in the presence of host plasminogen. Finally, a proteomic analysis showed that the interaction with LM triggers protein changes in FhNEJ that may be relevant for parasite growth and adaptation inside the mammalian host. Altogether, our study provides valuable insights into the molecular interplay between FhNEJ and the intestinal ECM, which may lead to the identification of targetable candidates for the development of more effective control strategies against fasciolosis. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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13 pages, 2107 KiB

Open AccessArticle

Variability in the Response against Teladorsagia circumcincta in Lambs of Two Canarian Sheep Breeds

by Tara Pérez-Hernández, Julia N. Hernández, Cynthia Machín, Tom N. McNeilly, Alasdair J. Nisbet, Jacqueline B. Matthews, Stewart T. G. Burgess and Jorge F. González

Int. J. Mol. Sci. 2023, 24(1), 29; https://doi.org/10.3390/ijms24010029 - 20 Dec 2022

Cited by 2 | Viewed by 2020

Abstract

The increasing resistance to anthelmintics has necessitated the exploration of alternative control strategies of gastrointestinal nematode (GIN) infections. A sustainable option is genetic selection based on differences in susceptibility to GIN infection between and within breeds of sheep. Here, three-month-old Canaria Hair breed (GIN-resistant) and Canaria Sheep breed (GIN-susceptible) showed no significant between-breed differences after trickle infection with Teladorsagia circumcincta, whereas considerable individual variability was found in both breeds. Next, data from lambs of both breeds were used to explore the relationships between parasitological variables and T. circumcincta-specific IgA levels, local immune cell populations, and abomasal lymph node gene expression to understand the possible mechanisms underlying resistance. Mucosal IgA levels as well as numbers of globular leukocytes and MHC-II⁺ cells were associated with protection. Analysis of lymph node gene expression revealed the associations between lower parasite numbers and cumulative fecal egg counts and several immune pathways, such as leukocyte cell adhesion, activation and differentiation of T cells, in particular CD4⁺ and IL-4 production. The data obtained here may inform on the relationship between phenotypic resistance variability and protective responses at the humoral, cellular, and transcriptomic levels, thus contributing to identifying immune responses in young lambs that could be used as markers for selection. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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Review

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21 pages, 2728 KiB

Open AccessReview

Metacyclogenesis as the Starting Point of Chagas Disease

by Alessandro Zanard Lopes Ferreira, Carla Nunes de Araújo, Isabela Cunha Costa Cardoso, Karen Stephanie de Souza Mangabeira, Amanda Pereira Rocha, Sébastien Charneau, Jaime Martins Santana, Flávia Nader Motta and Izabela Marques Dourado Bastos

Int. J. Mol. Sci. 2024, 25(1), 117; https://doi.org/10.3390/ijms25010117 - 21 Dec 2023

Cited by 1 | Viewed by 1631

Abstract

Chagas disease is a neglected infectious disease caused by the protozoan Trypanosoma cruzi, primarily transmitted by triatomine vectors, and it threatens approximately seventy-five million people worldwide. This parasite undergoes a complex life cycle, transitioning between hosts and shifting from extracellular to intracellular stages. To ensure its survival in these diverse environments, T. cruzi undergoes extreme morphological and molecular changes. The metacyclic trypomastigote (MT) form, which arises from the metacyclogenesis (MTG) process in the triatomine hindgut, serves as a crucial link between the insect and human hosts and can be considered the starting point of Chagas disease. This review provides an overview of the current knowledge regarding the parasite’s life cycle, molecular pathways, and mechanisms involved in metabolic and morphological adaptations during MTG, enabling the MT to evade the immune system and successfully infect human cells. Full article

(This article belongs to the Special Issue Parasite Biology and Host-Parasite Interactions)

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