Structure and Function of the Parasitophorous Vacuole in Eimeria Species R[ Entzeroth \ F[R[ Mattig\ R[ Werner!Meier
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Essential Function of the Alveolin Network in the Subpellicular
RESEARCH ARTICLE Essential function of the alveolin network in the subpellicular microtubules and conoid assembly in Toxoplasma gondii Nicolo` Tosetti1, Nicolas Dos Santos Pacheco1, Eloı¨se Bertiaux2, Bohumil Maco1, Lore` ne Bournonville2, Virginie Hamel2, Paul Guichard2, Dominique Soldati-Favre1* 1Department of Microbiology and Molecular Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland; 2Department of Cell Biology, Sciences III, University of Geneva, Geneva, Switzerland Abstract The coccidian subgroup of Apicomplexa possesses an apical complex harboring a conoid, made of unique tubulin polymer fibers. This enigmatic organelle extrudes in extracellular invasive parasites and is associated to the apical polar ring (APR). The APR serves as microtubule- organizing center for the 22 subpellicular microtubules (SPMTs) that are linked to a patchwork of flattened vesicles, via an intricate network composed of alveolins. Here, we capitalize on ultrastructure expansion microscopy (U-ExM) to localize the Toxoplasma gondii Apical Cap protein 9 (AC9) and its partner AC10, identified by BioID, to the alveolin network and intercalated between the SPMTs. Parasites conditionally depleted in AC9 or AC10 replicate normally but are defective in microneme secretion and fail to invade and egress from infected cells. Electron microscopy revealed that the mature parasite mutants are conoidless, while U-ExM highlighted the disorganization of the SPMTs which likely results in the catastrophic loss of APR and conoid. Introduction *For correspondence: Toxoplasma gondii belongs to the phylum of Apicomplexa that groups numerous parasitic protozo- Dominique.Soldati-Favre@unige. ans causing severe diseases in humans and animals. As part of the superphylum of Alveolata, the ch Apicomplexa are characterized by the presence of the alveoli, which consist in small flattened single- membrane sacs, underlying the plasma membrane (PM) to form the inner membrane complex (IMC) Competing interest: See of the parasite. -
(Alveolata) As Inferred from Hsp90 and Actin Phylogenies1
J. Phycol. 40, 341–350 (2004) r 2004 Phycological Society of America DOI: 10.1111/j.1529-8817.2004.03129.x EARLY EVOLUTIONARY HISTORY OF DINOFLAGELLATES AND APICOMPLEXANS (ALVEOLATA) AS INFERRED FROM HSP90 AND ACTIN PHYLOGENIES1 Brian S. Leander2 and Patrick J. Keeling Canadian Institute for Advanced Research, Program in Evolutionary Biology, Departments of Botany and Zoology, University of British Columbia, Vancouver, British Columbia, Canada Three extremely diverse groups of unicellular The Alveolata is one of the most biologically diverse eukaryotes comprise the Alveolata: ciliates, dino- supergroups of eukaryotic microorganisms, consisting flagellates, and apicomplexans. The vast phenotypic of ciliates, dinoflagellates, apicomplexans, and several distances between the three groups along with the minor lineages. Although molecular phylogenies un- enigmatic distribution of plastids and the economic equivocally support the monophyly of alveolates, and medical importance of several representative members of the group share only a few derived species (e.g. Plasmodium, Toxoplasma, Perkinsus, and morphological features, such as distinctive patterns of Pfiesteria) have stimulated a great deal of specula- cortical vesicles (syn. alveoli or amphiesmal vesicles) tion on the early evolutionary history of alveolates. subtending the plasma membrane and presumptive A robust phylogenetic framework for alveolate pinocytotic structures, called ‘‘micropores’’ (Cavalier- diversity will provide the context necessary for Smith 1993, Siddall et al. 1997, Patterson -
Predatory Flagellates – the New Recently Discovered Deep Branches of the Eukaryotic Tree and Their Evolutionary and Ecological Significance
Protistology 14 (1), 15–22 (2020) Protistology Predatory flagellates – the new recently discovered deep branches of the eukaryotic tree and their evolutionary and ecological significance Denis V. Tikhonenkov Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, 152742, Russia | Submitted March 20, 2020 | Accepted April 6, 2020 | Summary Predatory protists are poorly studied, although they are often representing important deep-branching evolutionary lineages and new eukaryotic supergroups. This short review/opinion paper is inspired by the recent discoveries of various predatory flagellates, which form sister groups of the giant eukaryotic clusters on phylogenetic trees, and illustrate an ancestral state of one or another supergroup of eukaryotes. Here we discuss their evolutionary and ecological relevance and show that the study of such protists may be essential in addressing previously puzzling evolutionary problems, such as the origin of multicellular animals, the plastid spread trajectory, origins of photosynthesis and parasitism, evolution of mitochondrial genomes. Key words: evolution of eukaryotes, heterotrophic flagellates, mitochondrial genome, origin of animals, photosynthesis, predatory protists, tree of life Predatory flagellates and diversity of eu- of the hidden diversity of protists (Moon-van der karyotes Staay et al., 2000; López-García et al., 2001; Edg- comb et al., 2002; Massana et al., 2004; Richards The well-studied multicellular animals, plants and Bass, 2005; Tarbe et al., 2011; de Vargas et al., and fungi immediately come to mind when we hear 2015). In particular, several prevailing and very abun- the term “eukaryotes”. However, these groups of dant ribogroups such as MALV, MAST, MAOP, organisms represent a minority in the real diversity MAFO (marine alveolates, stramenopiles, opistho- of evolutionary lineages of eukaryotes. -
Vaccination with Recombinant Microneme Proteins Confers Protection Against Experimental Toxoplasmosis in Mice
RESEARCH ARTICLE Vaccination with Recombinant Microneme Proteins Confers Protection against Experimental Toxoplasmosis in Mice Camila Figueiredo Pinzan1, Aline Sardinha-Silva1, Fausto Almeida1, Livia Lai2, Carla Duque Lopes1, Elaine Vicente Lourenço3, Ademilson Panunto-Castelo4, Stephen Matthews2, Maria Cristina Roque-Barreira1* 1 Department of Cell and Molecular Biology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil, 2 Division of Molecular Biosciences, Imperial College London, South Kensington Campus, London, SW7 2AZ, United Kingdom, 3 Department of Medicine, Division of Rheumatology, University of California Los Angeles, Los Angeles, California, 90095–1670, United States of America, 4 Department of Biology, School of Philosophy, Sciences and Literature of Ribeirão Preto, University of Sao Paulo, Ribeirão Preto, São Paulo, Brazil * [email protected] OPEN ACCESS Abstract Citation: Pinzan CF, Sardinha-Silva A, Almeida F, Lai L, Lopes CD, Lourenço EV, et al. (2015) Vaccination Toxoplasmosis, a zoonotic disease caused by Toxoplasma gondii, is an important public with Recombinant Microneme Proteins Confers health problem and veterinary concern. Although there is no vaccine for human toxoplas- Protection against Experimental Toxoplasmosis in mosis, many attempts have been made to develop one. Promising vaccine candidates uti- Mice. PLoS ONE 10(11): e0143087. doi:10.1371/ journal.pone.0143087 lize proteins, or their genes, from microneme organelle of T. gondii that are involved in the initial stages of host cell invasion by the parasite. In the present study, we used different Editor: Takafumi Tsuboi, Ehime University, JAPAN recombinant microneme proteins (TgMIC1, TgMIC4, or TgMIC6) or combinations of these Received: June 17, 2015 proteins (TgMIC1-4 and TgMIC1-4-6) to evaluate the immune response and protection Accepted: October 4, 2015 against experimental toxoplasmosis in C57BL/6 mice. -
Sexual Development in Plasmodium Parasites: Knowing When It’S Time to Commit
REVIEWS VECTOR-BORNE DISEASES Sexual development in Plasmodium parasites: knowing when it’s time to commit Gabrielle A. Josling1 and Manuel Llinás1–4 Abstract | Malaria is a devastating infectious disease that is caused by blood-borne apicomplexan parasites of the genus Plasmodium. These pathogens have a complex lifecycle, which includes development in the anopheline mosquito vector and in the liver and red blood cells of mammalian hosts, a process which takes days to weeks, depending on the Plasmodium species. Productive transmission between the mammalian host and the mosquito requires transitioning between asexual and sexual forms of the parasite. Blood- stage parasites replicate cyclically and are mostly asexual, although a small fraction of these convert into male and female sexual forms (gametocytes) in each reproductive cycle. Despite many years of investigation, the molecular processes that elicit sexual differentiation have remained largely unknown. In this Review, we highlight several important recent discoveries that have identified epigenetic factors and specific transcriptional regulators of gametocyte commitment and development, providing crucial insights into this obligate cellular differentiation process. Trophozoite Malaria affects almost 200 million people worldwide and viewed under the microscope, it resembles a flat disc. 1 A highly metabolically active and causes 584,000 deaths annually ; thus, developing a After the ring stage, the parasite rounds up as it enters the asexual form of the malaria better understanding of the mechanisms that drive the trophozoite stage, in which it is far more metabolically parasite that forms during development of the transmissible form of the malaria active and expresses surface antigens for cytoadhesion. the intra‑erythrocytic developmental cycle following parasite is a matter of urgency. -
Comparative Transcriptome Analysis of Second- and Third-Generation Merozoites of Eimeria Necatrix
Su et al. Parasites & Vectors (2017) 10:388 DOI 10.1186/s13071-017-2325-z RESEARCH Open Access Comparative transcriptome analysis of second- and third-generation merozoites of Eimeria necatrix Shijie Su1,2,3, Zhaofeng Hou1,2,3, Dandan Liu1,2,3, Chuanli Jia1,2,3, Lele Wang1,2,3, Jinjun Xu1,2,3 and Jianping Tao1,2,3* Abstract Background: Eimeria is a common genus of apicomplexan parasites that infect diverse vertebrates, most notably poultry, causing serious disease and economic losses. Eimeria species have complex life-cycles consisting of three developmental stages. However, the molecular basis of the Eimeria reproductive mode switch remains an enigma. Methods: Total RNA extracted from second- (MZ-2) and third-generation merozoites (MZ-3) of Eimeria necatrix was subjected to transcriptome analysis using RNA sequencing (RNA-seq) followed by qRT-PCR validation. Results: A total of 6977 and 6901 unigenes were obtained from MZ-2 and MZ-3, respectively. Approximately 2053 genes were differentially expressed genes (DEGs) between MZ-2 and MZ-3. Compared with MZ-2, 837 genes were upregulated and 1216 genes were downregulated in MZ-3. Approximately 95 genes in MZ-2 and 48 genes in MZ-3 were further identified to have stage-specific expression. Gene ontology category and KEGG analysis suggested that 216 upregulated genes in MZ-2 were annotated by 70 GO assignments, 242 upregulated genes were associated with 188 signal pathways, while 321 upregulated genes in MZ-3 were annotated by 56 GO assignments, 322 upregulated genes were associated with 168 signal pathways. The molecular functions of upregulated genes in MZ-2 were mainly enriched for protein degradation and amino acid metabolism. -
Intriguing Parasites and Intramembrane Proteases
Downloaded from genesdev.cshlp.org on September 29, 2021 - Published by Cold Spring Harbor Laboratory Press PERSPECTIVE Intriguing parasites and intramembrane proteases Robert B. Rawson1 Department of Molecular Genetics, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA Rhomboid intramembrane proteases occur throughout The parasitic lifestyle the kingdoms of life. In this issue of Genes & Develop- Parasitism poses common challenges to the diverse or- ment, Baxt and colleagues (pp. 1636–1646) report that ganisms that practice it. Parasites must first locate and the single proteolytic rhomboid (EhROM1) from Ent- enter a host. Next, in many cases, host tissues or cells amoeba histolytica cleaves cell surface galactose-bind- must be invaded, requiring some means of attachment ing or N-acetylgalactosamine-binding (Gal/Gal-NAc) and introgression. The successful parasite usually estab- lectins. EhROM1 and lectins colocalize during phagocy- lishes a long-term infection, and this potentially affords tosis and receptor capping. EhROM1 is found at the base the host ample time to mount a vigorous immune re- of the cap rather than in the cap proper, suggesting a role sponse to the invader. In order to survive and reproduce in receptor shedding and implying that EhROM1 is cru- while “dining at another’s table,” the parasite must cial for amoebal infection. somehow manage to evade host immune defenses that may act at several stages of the infection cycle. Broadly, Parasitic protists are fascinating organisms in their own extracellular parasites are subject to the humoral re- right, with their typically complex life cycles, distinctive sponse, while intracellular stages are the target of cellu- physiologies, and uncertain relationships. -
A Novel Rhoptry Protein As Candidate Vaccine Against Eimeria Tenella Infection
Article A Novel Rhoptry Protein as Candidate Vaccine against Eimeria tenella Infection Xingju Song 1,2, Xu Yang 1,2, Taotao Zhang 1,2, Jing Liu 1,2 and Qun Liu 1,2,* 1 National Animal Protozoa Laboratory, College of Veterinary Medicine, China Agricultural University, Beijing 100083, China; [email protected] (X.S.); [email protected] (X.Y.); [email protected] (T.Z.); [email protected] (J.L.) 2 Key Laboratory of Animal Epidemiology of the Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100083, China * Correspondence: [email protected] Received: 25 July 2020; Accepted: 10 August 2020; Published: 12 August 2020 Abstract: Eimeria tenella (E. tenella) is a highly pathogenic and prevalent species of Eimeria that infects chickens, and it causes a considerable disease burden worldwide. The secreted proteins and surface antigens of E. tenella at the sporozoite stage play an essential role in the host–parasite interaction, which involves attachment and invasion, and these interactions are considered vaccine candidates based on the strategy of cutting off the invasion pathway to interrupt infection. We selected two highly expressed surface antigens (SAGs; Et-SAG13 and Et-SAG) and two highly expressed secreted antigens (rhoptry kinases Eten5-A, Et-ROPK-Eten5-A and dense granule 12, Et-GRA12) at the sporozoite stage. Et-ROPK-Eten5-A and Et-GRA12 were two unexplored proteins. Et-ROPK-Eten5-A was an E. tenella-specific rhoptry (ROP) protein and distributed in the apical pole of sporozoites and merozoites. Et-GRA12 was scattered in granular form at the sporozoite stage. -
Plasmodium Falciparum Full Life Cycle and Plasmodium Ovale Liver Stages in Humanized Mice
ARTICLE Received 12 Nov 2014 | Accepted 29 May 2015 | Published 24 Jul 2015 DOI: 10.1038/ncomms8690 OPEN Plasmodium falciparum full life cycle and Plasmodium ovale liver stages in humanized mice Vale´rie Soulard1,2,3, Henriette Bosson-Vanga1,2,3,4,*, Audrey Lorthiois1,2,3,*,w, Cle´mentine Roucher1,2,3, Jean- Franc¸ois Franetich1,2,3, Gigliola Zanghi1,2,3, Mallaury Bordessoulles1,2,3, Maurel Tefit1,2,3, Marc Thellier5, Serban Morosan6, Gilles Le Naour7,Fre´de´rique Capron7, Hiroshi Suemizu8, Georges Snounou1,2,3, Alicia Moreno-Sabater1,2,3,* & Dominique Mazier1,2,3,5,* Experimental studies of Plasmodium parasites that infect humans are restricted by their host specificity. Humanized mice offer a means to overcome this and further provide the opportunity to observe the parasites in vivo. Here we improve on previous protocols to achieve efficient double engraftment of TK-NOG mice by human primary hepatocytes and red blood cells. Thus, we obtain the complete hepatic development of P. falciparum, the transition to the erythrocytic stages, their subsequent multiplication, and the appearance of mature gametocytes over an extended period of observation. Furthermore, using sporozoites derived from two P. ovale-infected patients, we show that human hepatocytes engrafted in TK-NOG mice sustain maturation of the liver stages, and the presence of late-developing schizonts indicate the eventual activation of quiescent parasites. Thus, TK-NOG mice are highly suited for in vivo observations on the Plasmodium species of humans. 1 Sorbonne Universite´s, UPMC Univ Paris 06, CR7, Centre d’Immunologie et des Maladies Infectieuses (CIMI-Paris), 91 Bd de l’hoˆpital, F-75013 Paris, France. -
The Parasitophorous Vacuole Membrane Surrounding Plasmodium and Toxoplasma: an Unusual Compartment in Infected Cells
Journal of Cell Science 111, 1467-1475 (1998) 1467 Printed in Great Britain © The Company of Biologists Limited 1998 JCS5005 COMMENTARY The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells Klaus Lingelbach1 and Keith A. Joiner2 1FB Biology/Zoology, Philipps-University Marburg, 35032 Marburg, Germany 2Department of Internal Medicine, Section of Infectious Diseases, Yale School of Medicine, New Haven, Connecticut 06520-8022, USA Published on WWW 14 May 1998 SUMMARY Plasmodium and Toxoplasma belong to a group of are unique phenomena in cell biology. Here we compare unicellular parasites which actively penetrate their biological similarities and differences between the two respective mammalian host cells. During the process of parasites, with respect to: (i) the formation, (ii) the invasion, they initiate the formation of a membrane, the so- maintenance, and (iii) the biological role of the vacuolar called parasitophorous vacuolar membrane, which membrane. We conclude that most differences between the surrounds the intracellular parasite and which differs organisms primarily reflect the different biosynthetic substantially from endosomal membranes or the capacities of the host cells they invade. membrane of phagolysosomes. The biogenesis and the maintenance of the vacuolar membrane are closely related Key words: Host cell invasion, Membrane biogenesis, to the peculiar cellular organization of these parasites and Parasitophorous vacuole, Plasmodium, Toxoplasma INTRODUCTION several species of the genus Plasmodium as model systems. T. gondii and P. falciparum infect mammalian cells causing Apicomplexa are unicellular eukaryotes which are obligatory toxoplasmosis and human malaria, respectively. Both parasites intracellular parasites with short-lived extracellular stages. have complex life cycles. Our discussion will centre primarily Unlike many other microbial organisms which utilize on the erythrocytic stages (merozoitertrophozoiterschizont) phagocytic properties of their host cells for invasion, of P. -
Phosphorylation of Rhoptry Protein Rhoph3 Is Critical for Host Cell Invasion by the Malaria Parasite
RESEARCH ARTICLE Molecular Biology and Physiology crossm Downloaded from Phosphorylation of Rhoptry Protein RhopH3 Is Critical for Host Cell Invasion by the Malaria Parasite Roseleen Ekka,a Ankit Gupta,a* Sonika Bhatnagar,a Pawan Malhotra,b Pushkar Sharmaa http://mbio.asm.org/ aEukaryotic Gene Expression Laboratory, National Institute of Immunology, New Delhi, India bInternational Center for Genetic Engineering and Biotechnology, New Delhi, India Roseleen Ekka and Ankit Gupta contributed equally to this work; the order of authors was decided on the basis of the alphabetical order of the surnames and the time spent in the laboratory. ABSTRACT Merozoites formed after asexual division of the malaria parasite invade the host red blood cells (RBCs), which is critical for initiating malaria infection. The process of invasion involves specialized organelles like micronemes and rhoptries on October 21, 2020 at NATIONAL INSTITUTE OF IMMUNOLOGY (NII) that discharge key proteins involved in interaction with host RBC receptors. RhopH complex comprises at least three proteins, which include RhopH3. RhopH3 is critical for the process of red blood cell (RBC) invasion as well as intraerythrocytic develop- ment of human malaria parasite Plasmodium falciparum. It is phosphorylated at ser- ine 804 (S804) in the parasite; however, it is unclear if phosphorylation regulates its function. To address this, a CRISPR-CAS9-based approach was used to mutate S804 to alanine (A) in P. falciparum. Using this phosphomutant (R3_S804A) of RhopH3, we demonstrate that the phosphorylation of S804 is critical for host RBC invasion by the parasite but not for its intraerythrocytic development. Importantly, the phosphoryla- tion of RhopH3 regulates its localization to the rhoptries and discharge from the parasite, which is critical for RBC invasion. -
Independent Roles of Apical Membrane Antigen 1 and Rhoptry Neck Proteins During Host Cell Invasion by Apicomplexa
CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Cell Host & Microbe Article Independent Roles of Apical Membrane Antigen 1 and Rhoptry Neck Proteins during Host Cell Invasion by Apicomplexa Donatella Giovannini,1,5 Stephan Spa¨ th,1,5 Ce´ line Lacroix,1 Audrey Perazzi,2,3,4 Daniel Bargieri,1 Vanessa Lagal,2,3,4 Camille Lebugle,2,3,4 Audrey Combe,1 Sabine Thiberge,1 Patricia Baldacci,1 Isabelle Tardieux,2,3,4,6 and Robert Me´ nard1,6,* 1Institut Pasteur, Unite´ de Biologie et Ge´ ne´ tique du Paludisme, 75724 Paris, France 2INSERM, U1016, Institut Cochin, 75014 Paris, France 3CNRS, UMR8104, 75014 Paris, France 4Universite´ Paris Descartes, 75014 Paris, France 5These authors contributed equally to this work 6These authors contributed equally to this work *Correspondence: [email protected] DOI 10.1016/j.chom.2011.10.012 SUMMARY parasite motor to host cell actin (Gonzalez et al., 2009), thereby serving as an anchor through which the motile zoite glides into During invasion, apicomplexan parasites form an a parasitophorous vacuole (PV). Zoite internalization is a rapid intimate circumferential contact with the host cell, process, typically lasting a few tens of seconds. the tight junction (TJ), through which they actively The proteins that compose the TJ have long remained elusive. glide. The TJ, which links the parasite motor to the In 2005, two groups independently proposed the model of a TJ host cell cytoskeleton, is thought to be composed composed of interacting apical membrane antigen 1 (AMA1) of interacting apical membrane antigen 1 (AMA1) and rhoptry neck (RON) proteins (Alexander et al., 2005; Lebrun et al., 2005), which are unique to and conserved in apicomplex- and rhoptry neck (RON) proteins.