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Pathogens
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Proteomics of Host-Helminth Interactions
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Proteomics of Host-Helminth Interactions

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Parasitic Pathogens".

Deadline for manuscript submissions: closed (30 June 2021) | Viewed by 36197

Special Issue Editors

Dr. Mark Robinson

E-Mail Website
Guest Editor
Institute for Global Food Security, School of Biological Sciences, Queens University Belfast, Belfast BT9 5DL, UK
Interests: molecular biology of trematode parasites and their host interactions
Dr. Krystyna Cwiklinski

E-Mail Website
Guest Editor
School of Natural Sciences, Centre for One Health and Ryan Institute, National University of Ireland Galway, H91 TK33 Galway, Ireland
Interests: interrogation of omics datasets to investigate drug resistance, parasite development and host-parasite interaction to discover novel targets for vaccines and diagnostics

Special Issue Information

Dear Colleagues,

Helminth parasites remain a significant global human and animal health concern. The continued spread of drug resistance means that many parasite populations are difficult to manage and this has hastened the search for novel vaccine candidates and targets for improved diagnostic tests. Proteins secreted by helminths, or displayed on their outer surface, perform key roles in the host-parasite interaction and are thus leading candidates for these applications. In the past, profiling these was a major challenge due to the relative intractability of most species to conventional culture techniques and because of the low abundance/transient expression of the molecules themselves. However, the application and development of mass-spectrometry-based proteomics techniques has revolutionized our ability to identify helminth proteins, to study their modifications, and to profile changes in their expression during parasite growth and development. More recently, proteomics tools have been effectively used to investigate the interaction of helminth-derived molecules with host cells and to examine their effects on the host’s proteome. 

In this Special Issue, we aim to highlight recent advances in the field, covering the interaction of helminth parasites with their hosts from both perspectives.  By doing so, we hope to consolidate these developments and stimulate further discussion on the use of proteomics as a tool for investigating helminth-host interactions in the future.

Both original research and review articles are welcome.

Dr. Mark Robinson
Dr. Krystyna Cwiklinski
Guest Editors

Manuscript Submission Information

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Keywords

  • helminth
  • proteomics
  • host-parasite interactions
  • secretome
  • interactome

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Published Papers (10 papers)

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Editorial

Jump to: Research, Review, Other

3 pages, 186 KiB  
Editorial
Proteomics of Host-Helminth Interactions
by Mark W. Robinson and Krystyna Cwiklinski
Pathogens 2021, 10(10), 1317; https://doi.org/10.3390/pathogens10101317 - 13 Oct 2021
Cited by 2 | Viewed by 1804
Abstract
Helminth infections in people contribute to the 1 [...] Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)

Research

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15 pages, 1938 KiB  
Article
Identification of Toxocara canis Antigen-Interacting Partners by Yeast Two-Hybrid Assay and a Putative Mechanism of These Host–Parasite Interactions
by Ewa Długosz, Małgorzata Milewska and Piotr Bąska
Pathogens 2021, 10(8), 949; https://doi.org/10.3390/pathogens10080949 - 28 Jul 2021
Cited by 5 | Viewed by 3110
Abstract
Toxocara canis is a zoonotic roundworm that infects humans and dogs all over the world. Upon infection, larvae migrate to various tissues leading to different clinical syndromes. The host–parasite interactions underlying the process of infection remain poorly understood. Here, we describe the application [...] Read more.
Toxocara canis is a zoonotic roundworm that infects humans and dogs all over the world. Upon infection, larvae migrate to various tissues leading to different clinical syndromes. The host–parasite interactions underlying the process of infection remain poorly understood. Here, we describe the application of a yeast two-hybrid assay to screen a human cDNA library and analyse the interactome of T. canis larval molecules. Our data identifies 16 human proteins that putatively interact with the parasite. These molecules were associated with major biological processes, such as protein processing, transport, cellular component organisation, immune response and cell signalling. Some of these identified interactions are associated with the development of a Th2 response, neutrophil activity and signalling in immune cells. Other interactions may be linked to neurodegenerative processes observed during neurotoxocariasis, and some are associated with lung pathology found in infected hosts. Our results should open new areas of research and provide further data to enable a better understanding of this complex and underestimated disease. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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30 pages, 2788 KiB  
Article
Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata
by Boontarikaan Wititkornkul, Benjamin J. Hulme, John J. Tomes, Nathan R. Allen, Chelsea N. Davis, Sarah D. Davey, Alan R. Cookson, Helen C. Phillips, Matthew J. Hegarty, Martin T. Swain, Peter M. Brophy, Ruth E. Wonfor and Russell M. Morphew
Pathogens 2021, 10(7), 912; https://doi.org/10.3390/pathogens10070912 - 20 Jul 2021
Cited by 9 | Viewed by 4611
Abstract
Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome [...] Read more.
Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome as free proteins or components of extracellular vesicles (EVs). Therefore, adult RNA was sequenced and de novo assembled to generate the first A. perfoliata transcriptome. In addition, excretory secretory products (ESP) from adult A. perfoliata were collected and EVs isolated using size exclusion chromatography, prior to proteomic analysis of the EVs, the EV surface and EV depleted ESP. Transcriptome analysis revealed 454 sequences homologous to known helminth immune modulators including two novel Sigma class GSTs, five α-HSP90s, and three α-enolases with isoforms of all three observed within the proteomic analysis of the secretome. Furthermore, secretome proteomics identified common helminth proteins across each sample with known EV markers, such as annexins and tetraspanins, observed in EV fractions. Importantly, 49 of the 454 putative immune modulators were identified across the secretome proteomics contained within and on the surface of EVs in addition to those identified in free ESP. This work provides the molecular tools for A. perfoliata to reveal key players in the host–parasite interaction within the horse host. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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11 pages, 2147 KiB  
Article
Proteomic Analysis of Fasciola hepatica Excretory and Secretory Products Co-Immunoprecipitated Using Time Course Infection Sera
by Zhuo Lan, Xiao-Lei Liu, Qing-Bo Lv, Min-Hao Zeng, Jun-Feng Gao, Qiao-Cheng Chang, Yuan-Yuan Chen and Chun-Ren Wang
Pathogens 2021, 10(6), 749; https://doi.org/10.3390/pathogens10060749 - 13 Jun 2021
Cited by 6 | Viewed by 3074
Abstract
Fasciola hepatica is a widespread pathogen that is known for its harmful effects on the health and productivity of ruminant animals. To identify the proteins present in all periods of infection with F. hepatica but not in those with Fasciola gigantica by shotgun [...] Read more.
Fasciola hepatica is a widespread pathogen that is known for its harmful effects on the health and productivity of ruminant animals. To identify the proteins present in all periods of infection with F. hepatica but not in those with Fasciola gigantica by shotgun liquid chromatography–tandem mass spectrometry (LC–MS/MS), we collected the ESPs and sera of F. hepatica and F. gigantica. In this study, the sheep were artificially infected with F. hepatica and the sera were collected at five different periods: 3 days post-infection (dpi), 7 dpi, 21 dpi, 63 dpi, and 112 dpi. The interacting proteins were pulled down from the sheep sera of all five periods and the sera with F. gigantica by co-immunoprecipitation (Co-IP) assay, before being identified by LC–MS/MS analysis. Thirty, twenty-two, twenty-three, twenty-seven, and twenty-two proteins were pulled down by the infected sera at 3 dpi, 7 dpi, 21 dpi, 63 dpi, and 112 dpi, respectively. Among them, 12 proteins existed in all periods, while six proteins could be detected in all periods in F. hepatica but not in F. gigantica. Protein relative pathway analysis revealed that these proteins mainly refer to the metabolism, regulation of genetic activity, and signal transduction of F. hepatica. In conclusion, this study provides meaningful data for the diagnosis of fasciolosis and to understand the interactions between F. hepatica and the host. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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Review

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10 pages, 2613 KiB  
Review
Proteomics of Gnathostomiasis: A Way Forward for Diagnosis and Treatment Development
by Tipparat Thiangtrongjit, Kathyleen Nogrado, Thawatchai Ketboonlue, Preeyarat Malaitong, Poom Adisakwattana and Onrapak Reamtong
Pathogens 2021, 10(9), 1080; https://doi.org/10.3390/pathogens10091080 - 25 Aug 2021
Cited by 3 | Viewed by 4281
Abstract
Gnathostoma spinigerum is the most common cause of gnathostomiasis in humans. It has a complex life cycle, which requires two intermediate hosts and a definitive host, and poses a high risk for zoonosis. Definitive prognosis of gnathostomiasis relies mainly on the isolation of [...] Read more.
Gnathostoma spinigerum is the most common cause of gnathostomiasis in humans. It has a complex life cycle, which requires two intermediate hosts and a definitive host, and poses a high risk for zoonosis. Definitive prognosis of gnathostomiasis relies mainly on the isolation of advanced-stage larvae (aL3), which is very challenging especially if the aL3 is sequestered in difficult-to-reach organs. There is also a lack of a confirmatory diagnostic test for gnathostomiasis. With the ongoing advancement of proteomics, a potential diagnostic approach is underway using immunoproteomics and immunodiagnostics. In addition to this, the employment of mass spectrometry could further elucidate not only understanding the biology of the parasite but also determining potential targets of prospective drugs and vaccines. This article reports the past, present, and future application of proteomics in the study of gnathostomiasis. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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8 pages, 226 KiB  
Review
Modulation of the Host Immune Response by Schistosome Egg-Secreted Proteins Is a Critical Avenue of Host–Parasite Communication
by Jack P. Carson and Geoffrey N. Gobert
Pathogens 2021, 10(7), 863; https://doi.org/10.3390/pathogens10070863 - 8 Jul 2021
Cited by 13 | Viewed by 2760
Abstract
During a schistosome infection, the interactions that occur between the mammalian host and the parasite change rapidly once egg laying begins. Both juvenile and adult schistosomes adapt to indefinitely avoid the host immune system. In contrast, the survival of eggs relies on quickly [...] Read more.
During a schistosome infection, the interactions that occur between the mammalian host and the parasite change rapidly once egg laying begins. Both juvenile and adult schistosomes adapt to indefinitely avoid the host immune system. In contrast, the survival of eggs relies on quickly traversing from the host. Following the commencement of egg laying, the host immune response undergoes a shift from a type 1 helper (Th1) inflammatory response to a type 2 helper (Th2) granulomatous response. This change is driven by immunomodulatory proteins within the egg excretory/secretory products (ESPs), which interact with host cells and alter their behaviour to promote egg translocation. However, in parallel, these ESPs also provoke the development of chronic schistosomiasis pathology. Recent studies using high-throughput proteomics have begun to characterise the components of schistosome egg ESPs, particularly those of Schistosoma mansoni, S. japonicum and S. haematobium. Future application of this knowledge may lead to the identification of proteins with novel immunomodulatory activity or pathological importance. However, efforts in this area are limited by a lack of in situ or in vivo functional characterisation of these proteins. This review will highlight the current knowledge of the content and demonstrated functions of schistosome egg ESPs. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
13 pages, 294 KiB  
Review
Prospects of Using High-Throughput Proteomics to Underpin the Discovery of Animal Host–Nematode Interactions
by Tao Wang and Robin B. Gasser
Pathogens 2021, 10(7), 825; https://doi.org/10.3390/pathogens10070825 - 30 Jun 2021
Cited by 9 | Viewed by 2829
Abstract
Parasitic nematodes impose a significant public health burden, and cause major economic losses to agriculture worldwide. Due to the widespread of anthelmintic resistance and lack of effective vaccines for most nematode species, there is an urgent need to discover novel therapeutic and vaccine [...] Read more.
Parasitic nematodes impose a significant public health burden, and cause major economic losses to agriculture worldwide. Due to the widespread of anthelmintic resistance and lack of effective vaccines for most nematode species, there is an urgent need to discover novel therapeutic and vaccine targets, informed through an understanding of host–parasite interactions. Proteomics, underpinned by genomics, enables the global characterisation proteins expressed in a particular cell type, tissue and organism, and provides a key to insights at the host–parasite interface using advanced high-throughput mass spectrometry-based proteomic technologies. Here, we (i) review current mass-spectrometry-based proteomic methods, with an emphasis on a high-throughput ‘bottom-up’ approach; (ii) summarise recent progress in the proteomics of parasitic nematodes of animals, with a focus on molecules inferred to be involved in host–parasite interactions; and (iii) discuss future research directions that could enhance our knowledge and understanding of the molecular interplay between nematodes and host animals, in order to work toward new, improved methods for the treatment, diagnosis and control of nematodiases. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
17 pages, 1230 KiB  
Review
Trematode Proteomics: Recent Advances and Future Directions
by Adam P. S. Bennett and Mark W. Robinson
Pathogens 2021, 10(3), 348; https://doi.org/10.3390/pathogens10030348 - 16 Mar 2021
Cited by 18 | Viewed by 4348
Abstract
Trematodes cause disease in millions of people worldwide, but the absence of commercial vaccines has led to an over-reliance on a handful of monotherapies to control infections. Since drug-resistant fluke populations are emerging, a deeper understanding of parasite biology and host interactions is [...] Read more.
Trematodes cause disease in millions of people worldwide, but the absence of commercial vaccines has led to an over-reliance on a handful of monotherapies to control infections. Since drug-resistant fluke populations are emerging, a deeper understanding of parasite biology and host interactions is required to identify new drug targets and immunogenic vaccine candidates. Mass spectrometry-based proteomics represents a key tool to that end. Recent studies have capitalised on the wider availability of annotated helminth genomes to achieve greater coverage of trematode proteomes and discover new aspects of the host–parasite relationship. This review focusses on these latest advances. These include how the protein components of fluke extracellular vesicles have given insight into their biogenesis and cellular interactions. In addition, how the integration of transcriptome/proteome datasets has revealed that the expression and secretion of selected families of liver fluke virulence factors and immunomodulators are regulated in accordance with parasite development and migration within the mammalian host. Furthermore, we discuss the use of immunoproteomics as a tool to identify vaccine candidates associated with protective antibody responses. Finally, we highlight how established and emerging technologies, such as laser microdissection and single-cell proteomics, could be exploited to resolve the protein profiles of discrete trematode tissues or cell types which, in combination with functional tools, could pinpoint optimal targets for fluke control. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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16 pages, 1232 KiB  
Review
Spirocerca lupi Proteomics and Its Role in Cancer Development: An Overview of Spirocercosis-Induced Sarcomas and Revision of Helminth-Induced Carcinomas
by Catalina Porras-Silesky, María José Mejías-Alpízar, Javier Mora, Gad Baneth and Alicia Rojas
Pathogens 2021, 10(2), 124; https://doi.org/10.3390/pathogens10020124 - 26 Jan 2021
Cited by 9 | Viewed by 4677
Abstract
Spirocerca lupi is a parasitic nematode of canids that induces a myriad of clinical manifestations in its host and, in 25% of infections, leads to the formation of sarcomas. The description of the protein composition of the excretory and secretory products (Sl [...] Read more.
Spirocerca lupi is a parasitic nematode of canids that induces a myriad of clinical manifestations in its host and, in 25% of infections, leads to the formation of sarcomas. The description of the protein composition of the excretory and secretory products (Sl-ESP) of S. lupi has shed light on its possible interactions with the host environment, including migration within the host and mechanisms of immunomodulation. Despite this, the process by which S. lupi induces cancer in the dog remains poorly understood, and some hypotheses have arisen regarding these possible mechanisms. In this review, we discuss the role of specific ESP from the carcinogenic helminths Clonorchis sinensis, Opisthorchis viverrini and Schistosoma haematobium in inducing chronic inflammation and cancer in their host’s tissues. The parasitic worms Taenia solium, Echinococcus granulosus, Heterakis gallinarum, Trichuris muris and Strongyloides stercoralis, which have less-characterized mechanisms of cancer induction, are also analyzed. Based on the pathological findings in spirocercosis and the mechanisms by which other parasitic helminths induce cancer, we propose that the sustained inflammatory response in the dog´s tissues produced in response to the release of Sl-ESP homologous to those of other carcinogenic worms may lead to the malignant process in infected dogs. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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Other

11 pages, 1056 KiB  
Brief Report
Recognition Pattern of the Fasciola hepatica Excretome/Secretome during the Course of an Experimental Infection in Sheep by 2D Immunoproteomics
by David Becerro-Recio, Javier González-Miguel, Alberto Ucero, Javier Sotillo, Álvaro Martínez-Moreno, José Pérez-Arévalo, Krystyna Cwiklinski, John P. Dalton and Mar Siles-Lucas
Pathogens 2021, 10(6), 725; https://doi.org/10.3390/pathogens10060725 - 9 Jun 2021
Cited by 10 | Viewed by 3197
Abstract
Excretory/secretory products released by helminth parasites have been widely studied for their diagnostic utility, immunomodulatory properties, as well as for their use as vaccines. Due to their location at the host/parasite interface, the characterization of parasite secretions is important to unravel the molecular [...] Read more.
Excretory/secretory products released by helminth parasites have been widely studied for their diagnostic utility, immunomodulatory properties, as well as for their use as vaccines. Due to their location at the host/parasite interface, the characterization of parasite secretions is important to unravel the molecular interactions governing the relationships between helminth parasites and their hosts. In this study, the excretory/secretory products from adult worms of the trematode Fasciola hepatica (FhES) were employed in a combination of two-dimensional electrophoresis, immunoblot and mass spectrometry, to analyze the immune response elicited in sheep during the course of an experimental infection. Ten different immunogenic proteins from FhES recognized by serum samples from infected sheep at 4, 8, and/or 12 weeks post-infection were identified. Among these, different isoforms of cathepsin L and B, peroxiredoxin, calmodulin, or glutathione S-transferase were recognized from the beginning to the end of the experimental infection, suggesting their potential role as immunomodulatory antigens. Furthermore, four FhES proteins (C2H2-type domain-containing protein, ferritin, superoxide dismutase, and globin-3) were identified for the first time as non-immunogenic proteins. These results may help to further understand host/parasite relationships in fasciolosis, and to identify potential diagnostic molecules and drug target candidates of F. hepatica. Full article
(This article belongs to the Special Issue Proteomics of Host-Helminth Interactions)
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