Cellular Biology of Protozoan Parasites of Mammals

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Parasitology".

Deadline for manuscript submissions: closed (31 December 2023) | Viewed by 14205

Special Issue Editors


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Guest Editor
Centro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboadisabled, Lisbon, Portugal
Interests: centrosome; microtubule cytoskeleton; cilia; tubulin; the role of cytoskeleton in host-parasite interaction

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Guest Editor
CIISA - Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisbon, Portugal
Interests: microtubule cytoskeleton; apicomplexa protozoa; host-parasite interaction

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Guest Editor
CIISA - Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisbon, Portugal
Interests: neosporosis; toxoplasmosis; besnoitiosis; African swine fever; host-parasite interactions; immunity
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Special Issue Information

Dear Colleagues,

Protozoan parasites that affect mammals are a large and diverse group of unicellular eukaryotic microorganisms responsible for a vast number of different diseases. Geographically, these diseases can be restricted to certain areas, especially in the tropical and subtropical areas, but others have a worldwide distribution. The diseases caused by protozoa parasites are diverse and range from very mild forms to life-threatening infections, depending on the parasite and on the host. Some examples are leishmaniasis, malaria, trypanosomiasis, toxoplasmosis, besnoitiosis, babesiosis, trichomoniasis, amebiasis, cryptosporidiosis, giardiasis, and primary amoebic meningoencephalitis. At the cellular level, as a strategy to adapt to their hosts, many of the protozoan parasites developed several cellular specialized structures and mechanisms that are not observed in other organisms. The study of these features is of key importance to understand Biology and open the possibility to identify specific molecular targets and mechanisms that can be exploited for the development of new therapeutic approaches that would not compromise the host. These parasites invade a range of cells of different tissues in their hosts and can be transmitted by fecal-oral transmission (contaminated food or water or person-to-person contact), predator-prey, and vector transmission (hematophogous arthropod). Facing the rapid climatic changes and the high mobility of the populations, a better understanding on how they can disseminate outside of the host may be important to prevent the diseases. Compared to other pathogens, such as viruses and bacteria, protozoan parasites have more complex genomes, cell structures and life cycles; and have an immense repertoire of strategies to circumvent the host defense mechanisms. In this context, for this topic, we welcome Original Research articles, Reviews, and Brief Research Reports that cover, but are not limited to, the following topics:

  • Host/parasite interactions
  • Host cell invasion strategies
  • Parasite replication and differentiation
  • Host pathways exploited by parasites
  • Cell biology of organelles involved in host/parasite interactions
  • Survival strategies to reside outside the hosts (e.g. Cyst and encystment).
  • Omics resources for investigating the cell biology of host/parasite interactions
  • How parasites evolved - phylogenetic studies
  • New strategies for diagnosis and therapeutics of protozoan diseases
  • In vitro models to study protozoan parasites (e.g. 3D organoid and spheroid systems)

Dr. Helena Soares
Dr. Sofia Nolasco
Dr. Alexandre Leitão
Guest Editors

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Keywords

  • protozoa
  • parasites
  • protozoan parasite
  • infection, host invasion
  • host/parasite interactions
  • parasite replication
  • protozoan diseases
  • parasitic diseases

Published Papers (7 papers)

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Research

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13 pages, 6969 KiB  
Article
Killing of Plasmodium Sporozoites by Basic Amphipathic α-Helical Fusion Peptides
by Manuela C. Aguirre-Botero, Eduardo Aliprandini, Anisha Gladston, Olga Pacios, Rafael Miyazawa Martins, Jean-Luc Poyet and Rogerio Amino
Microorganisms 2024, 12(3), 480; https://doi.org/10.3390/microorganisms12030480 - 27 Feb 2024
Viewed by 972
Abstract
Membranolytic molecules constitute the first line of innate immune defense against pathogenic microorganisms. Plasmodium sporozoites are potentially exposed to these cytotoxic molecules in the hemolymph and salivary glands of mosquitoes, as well as in the skin, blood, and liver of the mammalian host. [...] Read more.
Membranolytic molecules constitute the first line of innate immune defense against pathogenic microorganisms. Plasmodium sporozoites are potentially exposed to these cytotoxic molecules in the hemolymph and salivary glands of mosquitoes, as well as in the skin, blood, and liver of the mammalian host. Here, we show that sporozoites are resistant to bacteriolytic concentration of cecropin B, a cationic amphipathic antimicrobial insect peptide. Intriguingly, anti-tumoral cell-penetrating peptides derived from the anti-apoptotic protein AAC11 killed P. berghei and P. falciparum sporozoites. Using dynamic imaging, we demonstrated that the most cytotoxic peptide, called RT39, did not significantly inhibit the sporozoite motility until the occurrence of a fast permeabilization of the parasite membrane by the peptide. Concomitantly, the cytosolic fluorescent protein constitutively expressed by sporozoites leaked from the treated parasite body while To-Pro 3 and FITC-labeled RT39 internalized, respectively, binding to the nucleic acids and membranes of sporozoites. This led to an increase in the parasite granularity as assessed by flow cytometry. Most permeabilization events started at the parasite’s posterior end, resulting in the appearance of a fluorescent dot in the anterior part of sporozoites. Understanding and exploiting the susceptibility of sporozoites and other plasmodial stages to membranolytic molecules might foster strategies to eliminate the parasite and block its transmission. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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12 pages, 7326 KiB  
Article
Insights into the Cell Division of Neospora caninum
by Ramiro Tomasina, Fabiana C. González, Soledad Echeverría, Andrés Cabrera and Carlos Robello
Microorganisms 2024, 12(1), 61; https://doi.org/10.3390/microorganisms12010061 - 28 Dec 2023
Cited by 1 | Viewed by 985
Abstract
Neospora caninum is an apicomplexan protozoan parasite responsible for causing neosporosis in a range of animal species. It results in substantial economic losses in the livestock industry and poses significant health risks to companion and wild animals. Central to its survival and pathogenicity [...] Read more.
Neospora caninum is an apicomplexan protozoan parasite responsible for causing neosporosis in a range of animal species. It results in substantial economic losses in the livestock industry and poses significant health risks to companion and wild animals. Central to its survival and pathogenicity is the process of cell division, which remains poorly understood in this parasite. In this study, we explored the cell division of Neospora caninum using a combination of modern and classic imaging tools, emphasizing its pivotal role in perpetuating the parasite’s life cycle and contributing to its ability to persist within host organisms. We described the intricacies of endodyogeny in Neospora caninum, detailing the dynamics of the cell assembly and the nuclear division by ultrastructure expansion microscopy and regular confocal microscopy. Furthermore, we explored the centrosome dynamics, the centrioles and the apicoplast through the advancement of the cell cycle. Our analysis described with unprecedented detail, the endodyogeny in this parasite. By advancing our understanding of these molecular mechanisms, we aimed to inspire innovative strategies for disease management and control, with the ultimate goal of mitigating the devastating impact of neosporosis on animal health and welfare. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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9 pages, 562 KiB  
Communication
Zoonotic Parasites in Playgrounds in Southern Spain: A One Health Approach
by Laura Lorenzo-Rebenaque, Sandra López-Fernández, Francisco Marco-Jiménez, Laura Montoro-Dasi, Clara Marin, Santiago Vega, Eduardo Martínez-Manzanares and Fernando Fariñas
Microorganisms 2023, 11(3), 721; https://doi.org/10.3390/microorganisms11030721 - 10 Mar 2023
Cited by 4 | Viewed by 3038
Abstract
Zoonotic parasitic diseases are considered a global threat to public health. In this sense, canines and felines may be infected by different cosmopolitan parasites, with playgrounds serving as an important focus of infection for humans, as well as domestic or wild animals. Knowledge [...] Read more.
Zoonotic parasitic diseases are considered a global threat to public health. In this sense, canines and felines may be infected by different cosmopolitan parasites, with playgrounds serving as an important focus of infection for humans, as well as domestic or wild animals. Knowledge of the epidemiological situation of parasites in animal reservoirs integrated into the environment, identifying the spread pathways, is a key element for an effective response to this threat. Thus, the aim of this study was to assess the frequency of intestinal parasites with zoonotic potential in 120 playgrounds in the Malaga province (Spain). Samples were processed and analysed following standard parasitological procedures. Some 36.7% of playgrounds were parasite-positive with one or more zoonotic parasites. The most common parasites recovered were nematodes (60.0%), followed by protozoan species (33.3%) and cestodes (6.7%). In the parasite-positive playgrounds, Toxocara spp. (17.0 ± 3.5%) and Giardia duodenalis (17.0 ± 3.4%) were the most predominant parasites. In addition, 34.1% of playgrounds were infected with multiple parasites. Our results show a high presence of parasitic forms with zoonotic potential in playgrounds in Malaga, Spain. Due to the close contact between pets and humans in playgrounds, the potential zoonotic risk may increase if prevention and control measures are not designed. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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20 pages, 4828 KiB  
Article
The Tubulin Superfamily in Apicomplexan Parasites
by Naomi Morrissette, Izra Abbaali, Chandra Ramakrishnan and Adrian B. Hehl
Microorganisms 2023, 11(3), 706; https://doi.org/10.3390/microorganisms11030706 - 9 Mar 2023
Cited by 6 | Viewed by 2148
Abstract
Microtubules and specialized microtubule-containing structures are assembled from tubulins, an ancient superfamily of essential eukaryotic proteins. Here, we use bioinformatic approaches to analyze features of tubulins in organisms from the phylum Apicomplexa. Apicomplexans are protozoan parasites that cause a variety of human and [...] Read more.
Microtubules and specialized microtubule-containing structures are assembled from tubulins, an ancient superfamily of essential eukaryotic proteins. Here, we use bioinformatic approaches to analyze features of tubulins in organisms from the phylum Apicomplexa. Apicomplexans are protozoan parasites that cause a variety of human and animal infectious diseases. Individual species harbor one to four genes each for α- and β-tubulin isotypes. These may specify highly similar proteins, suggesting functional redundancy, or exhibit key differences, consistent with specialized roles. Some, but not all apicomplexans harbor genes for δ- and ε-tubulins, which are found in organisms that construct appendage-containing basal bodies. Critical roles for apicomplexan δ- and ε-tubulin are likely to be limited to microgametes, consistent with a restricted requirement for flagella in a single developmental stage. Sequence divergence or the loss of δ- and ε-tubulin genes in other apicomplexans appears to be associated with diminished requirements for centrioles, basal bodies, and axonemes. Finally, because spindle microtubules and flagellar structures have been proposed as targets for anti-parasitic therapies and transmission-blocking strategies, we discuss these ideas in the context of tubulin-based structures and tubulin superfamily properties. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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Review

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14 pages, 2067 KiB  
Review
Balancing Act: Tubulin Glutamylation and Microtubule Dynamics in Toxoplasma gondii
by Inês L. S. Delgado, João Gonçalves, Rita Fernandes, Sara Zúquete, Afonso P. Basto, Alexandre Leitão, Helena Soares and Sofia Nolasco
Microorganisms 2024, 12(3), 488; https://doi.org/10.3390/microorganisms12030488 - 28 Feb 2024
Viewed by 975
Abstract
The success of the intracellular parasite Toxoplasma gondii in invading host cells relies on the apical complex, a specialized microtubule cytoskeleton structure associated with secretory organelles. The T. gondii genome encodes three isoforms of both α- and β-tubulin, which undergo specific post-translational modifications (PTMs), [...] Read more.
The success of the intracellular parasite Toxoplasma gondii in invading host cells relies on the apical complex, a specialized microtubule cytoskeleton structure associated with secretory organelles. The T. gondii genome encodes three isoforms of both α- and β-tubulin, which undergo specific post-translational modifications (PTMs), altering the biochemical and biophysical proprieties of microtubules and modulating their interaction with associated proteins. Tubulin PTMs represent a powerful and evolutionarily conserved mechanism for generating tubulin diversity, forming a biochemical ‘tubulin code’ interpretable by microtubule-interacting factors. T. gondii exhibits various tubulin PTMs, including α-tubulin acetylation, α-tubulin detyrosination, Δ5α-tubulin, Δ2α-tubulin, α- and β-tubulin polyglutamylation, and α- and β-tubulin methylation. Tubulin glutamylation emerges as a key player in microtubule remodeling in Toxoplasma, regulating stability, dynamics, interaction with motor proteins, and severing enzymes. The balance of tubulin glutamylation is maintained through the coordinated action of polyglutamylases and deglutamylating enzymes. This work reviews and discusses current knowledge on T. gondii tubulin glutamylation. Through in silico identification of protein orthologs, we update the recognition of putative proteins related to glutamylation, contributing to a deeper understanding of its role in T. gondii biology. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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20 pages, 1567 KiB  
Review
Molecular Mechanisms of Persistence in Protozoan Parasites
by Asfiha Tarannum, Cristian Camilo Rodríguez-Almonacid, Jorge Salazar-Bravo and Zemfira N. Karamysheva
Microorganisms 2023, 11(9), 2248; https://doi.org/10.3390/microorganisms11092248 - 7 Sep 2023
Viewed by 2391
Abstract
Protozoan parasites are known for their remarkable capacity to persist within the bodies of vertebrate hosts, which frequently results in prolonged infections and the recurrence of diseases. Understanding the molecular mechanisms that underlie the event of persistence is of paramount significance to develop [...] Read more.
Protozoan parasites are known for their remarkable capacity to persist within the bodies of vertebrate hosts, which frequently results in prolonged infections and the recurrence of diseases. Understanding the molecular mechanisms that underlie the event of persistence is of paramount significance to develop innovative therapeutic approaches, given that these pathways still need to be thoroughly elucidated. The present article provides a comprehensive overview of the latest developments in the investigation of protozoan persistence in vertebrate hosts. The focus is primarily on the function of persisters, their formation within the host, and the specific molecular interactions between host and parasite while they persist. Additionally, we examine the metabolomic, transcriptional, and translational changes that protozoan parasites undergo during persistence within vertebrate hosts, focusing on major parasites such as Plasmodium spp., Trypanosoma spp., Leishmania spp., and Toxoplasma spp. Key findings of our study suggest that protozoan parasites deploy several molecular and physiological strategies to evade the host immune surveillance and sustain their persistence. Furthermore, some parasites undergo stage differentiation, enabling them to acclimate to varying host environments and immune challenges. More often, stressors such as drug exposure were demonstrated to impact the formation of protozoan persisters significantly. Understanding the molecular mechanisms regulating the persistence of protozoan parasites in vertebrate hosts can reinvigorate our current insights into host–parasite interactions and facilitate the development of more efficacious disease therapeutics. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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27 pages, 1469 KiB  
Review
Plasmodium falciparum Development from Gametocyte to Oocyst: Insight from Functional Studies
by Dinkorma T. Ouologuem, Antoine Dara, Aminatou Kone, Amed Ouattara and Abdoulaye A. Djimde
Microorganisms 2023, 11(8), 1966; https://doi.org/10.3390/microorganisms11081966 - 31 Jul 2023
Cited by 2 | Viewed by 2222
Abstract
Malaria elimination may never succeed without the implementation of transmission-blocking strategies. The transmission of Plasmodium spp. parasites from the human host to the mosquito vector depends on circulating gametocytes in the peripheral blood of the vertebrate host. Once ingested by the mosquito during [...] Read more.
Malaria elimination may never succeed without the implementation of transmission-blocking strategies. The transmission of Plasmodium spp. parasites from the human host to the mosquito vector depends on circulating gametocytes in the peripheral blood of the vertebrate host. Once ingested by the mosquito during blood meals, these sexual forms undergo a series of radical morphological and metabolic changes to survive and progress from the gut to the salivary glands, where they will be waiting to be injected into the vertebrate host. The design of effective transmission-blocking strategies requires a thorough understanding of all the mechanisms that drive the development of gametocytes, gametes, sexual reproduction, and subsequent differentiation within the mosquito. The drastic changes in Plasmodium falciparum shape and function throughout its life cycle rely on the tight regulation of stage-specific gene expression. This review outlines the mechanisms involved in Plasmodium falciparum sexual stage development in both the human and mosquito vector, and zygote to oocyst differentiation. Functional studies unravel mechanisms employed by P. falciparum to orchestrate the expression of stage-specific functional products required to succeed in its complex life cycle, thus providing us with potential targets for developing new therapeutics. These mechanisms are based on studies conducted with various Plasmodium species, including predominantly P. falciparum and the rodent malaria parasites P. berghei. However, the great potential of epigenetics, genomics, transcriptomics, proteomics, and functional genetic studies to improve the understanding of malaria as a disease remains partly untapped because of limitations in studies using human malaria parasites and field isolates. Full article
(This article belongs to the Special Issue Cellular Biology of Protozoan Parasites of Mammals)
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