High resolution microscopy reveals an unusual architecture of the <i>Plasmodium berghei</i> endoplasmic reticulum

Kaiser, Gesine; Niz, Mariana De; Zuber, Benoît; Burda, Paul‐Christian; Kornmann, Benoı̂t; Heussler, Volker; Stanway, Rebecca R.

doi:10.1111/mmi.13490

Cited by 29 publications

(41 citation statements)

References 66 publications

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“…Each exo-erythrocytic stage parasite (EEF: exo-erythrocytic form) generates tens of thousands of nuclei by the process of exo-erythrocytic schizogony. This rapid nuclear division is accompanied by growth and replication of organelles including the Golgi apparatus, endoplasmic reticulum, mitochondrion and apicoplast and by the vast expansion of the plasma membrane (4–6). Nuclei and organelles are eventually segregated into individual merozoites.…”

Section: Introductionmentioning

confidence: 99%

Transcriptome analysis ofPlasmodium bergheiduring exo-erythrocytic development

Caldelari

Dogga

Schmid³

et al. 2019

Preprint

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SummaryThe complex life cycle of malaria parasites requires well-orchestrated stage specific gene expression. In the vertebrate host the parasites grow and multiply by schizogony in two different environments: within erythrocytes and within hepatocytes. Whereas erythrocytic parasites are rather well-studied in this respect, relatively little is known about the exo-erythrocytic stages. In an attempt to fill this gap, we performed genome wide RNA-seq analyses of various exo-erythrocytic stages of Plasmodium berghei including sporozoites, samples from a time-course of liver stage development and detached cells, which contain infectious merozoites and represent the final step in exo-erythrocytic development. The analysis represents the completion of the transcriptome of the entire life cycle of P. berghei parasites with temporal detailed analysis of the liver stage allowing segmentation of the transcriptome across the progression of the life cycle. We have used these RNA-seq data from different developmental stages to cluster genes with similar expression profiles, in order to infer their functions. A comparison with published data of other parasite stages confirmed stage-specific gene expression and revealed numerous genes that are expressed differentially in blood and exo-erythrocytic stages. One of the most exo-erythrocytic stage-specific genes was PBANKA_1003900, which has previously been annotated as a “gametocyte specific protein”. The promoter of this gene drove high GFP expression in exo-erythrocytic stages, confirming its expression profile seen by RNA-seq. The comparative analysis of the genome wide mRNA expression profiles of erythrocytic and different exo-erythrocytic stages improves our understanding of gene regulation of Plasmodium parasites and can be used to model exo-erythrocytic stage metabolic networks and identify differences in metabolic processes during schizogony in erythrocytes and hepatocytes.

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Section: Introductionmentioning

confidence: 99%

Transcriptome analysis ofPlasmodium bergheiduring exo-erythrocytic development

Caldelari

Dogga

Schmid³

et al. 2019

Preprint

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“…HeLa cells (gift from Robert Menard, Pasteur Institute, Paris, France) were authenticated by short tandem repeat DNA profiling (Microsynth) and cultured as described before (30). We transfected 2 × 10 6 HeLa cells with 4 µg of plasmid DNA of the following fluorescent reporter constructs with program T-28 in an Amaxa Nucleofector (Lonza): mCherry-utrophin (7) (Addgene plasmid 26740), GFP-utrophin (7) (Addgene plasmid 26737), GFP-C1-PLCdelta-PH (12) (Addgene plasmid 21179), AKT-PH-GFP (13) (Addgene plasmid 18836), Lact-C2-GFP (14) (Addgene plasmid 22853), ezrin-GFP (15), ezrin(T567D)-GFP (16) (Addgene plasmid 20681), E-cadherin–GFP (17) (Addgene plasmid 28009), A2BR-YFP (18) (Addgene plasmid 37202), GFP-DRD2 (19) (Addgene plasmid 24099), PM-GFP (20) (Addgene plasmid 21213), and GFP-GPI (TRAIL and DAF) (21).…”

Section: Methodsmentioning

confidence: 99%

Manipulation of the Host Cell Membrane during Plasmodium Liver Stage Egress

Burda

Caldelari

Heussler

2017

mBio

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A crucial step in the life cycle of Plasmodium parasites is the transition from the liver stage to the blood stage. Hepatocyte-derived merozoites reach the blood vessels of the liver inside host cell-derived vesicles called merosomes. The molecular basis of merosome formation is only partially understood. Here we show that Plasmodium berghei liver stage merozoites, upon rupture of the parasitophorous vacuole membrane, destabilize the host cell membrane (HCM) and induce separation of the host cell actin cytoskeleton from the HCM. At the same time, the phospholipid and protein composition of the HCM appears to be substantially altered. This includes the loss of a phosphatidylinositol 4,5-bisphosphate (PIP2) reporter and the PIP2-dependent actin-plasma membrane linker ezrin from the HCM. Furthermore, transmembrane domain-containing proteins and palmitoylated and myristoylated proteins, as well as glycosylphosphatidylinositol-anchored proteins, lose their HCM localization. Collectively, these findings provide an explanation of HCM destabilization during Plasmodium liver stage egress and thereby contribute to our understanding of the molecular mechanisms that lead to merosome formation.

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“…(iii) Parasites that escape the autophagy‐associated response control the amount of PVM‐associated LC3 during development (Scale bar, 10 μm) (Image adapted from Agop‐Nersesian et al, ). (iv) IVM has allowed visualisation of organelle fission during schizogony, such as the endoplasmic reticulum (Pb Sec61b shown in white) at sub‐cellular resolution (Scale bar, 10 μm) (Image adapted from Kaiser et al, ). (v) A key IVM‐based discovery was the mechanism of egress of parasites from the liver.…”

Section: Organs In the Abdominopelvic Cavitiesmentioning

confidence: 99%

Intravital imaging of host‐parasite interactions in organs of the thoracic and abdominopelvic cavities

Niz

Carvalho

Penha‐Gonçalves

et al. 2020

Cellular Microbiology

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Infections with protozoan and helminthic parasites affect multiple organs in the mammalian host. Imaging pathogens in their natural environment takes a more holistic view on biomedical aspects of parasitic infections. Here, we focus on selected organs of the thoracic and abdominopelvic cavities most commonly affected by parasites. Parasitic infections of these organs are often associated with severe medical complications or have health implications beyond the infected individual. Intravital imaging has provided a more dynamic picture of the host-parasite interplay and contributed not only to our understanding of the various disease pathologies, but has also provided fundamental insight into the biology of the parasites. K E Y W O R D S diseases, imaging, infection, intravital, microscopy, parasitology 1 | INTRODUCTION Most parasitic infections in mammals involve organs of the thoracic, abdominal and pelvic cavities, and may cause severe complications as a result of damage to these organs. Organs in the thoracic cavity include the heart, the lungs, the thymus, the thyroid and parathyroid.The heart is an important target of Trypanosoma cruzi; and the lungs, are key targets of multiple parasites causing a broad spectrum of pathology ranging from focal lesions to diffuse lung damage. In the abdominal cavity, organs include the stomach, the intestine, the liver, the gallbladder, the pancreas, the spleen, the kidneys, the adrenal glands and regional lymph nodes. In the pelvic cavity, the reproductive organs and the urinary bladder are harboured. All the above organs can be compromised by vector-borne and soil/water/food-borne parasites alike. Intravital microscopy (IVM) allows studying cellular and sub-cellular events within living animals, including host-pathogen interactions. In this review, we focus on key IVM-based findings on parasite biology in different organs of the thoracic and abdominopelvic cavities. Importantly, some of these organs pose specific challenges for visualisation. Here, we discuss the advances on surgical procedures, imaging platforms and image processing tools that have made visualisation of parasites within these organs possible. | ORGANS IN THE THORACIC CAVITYThe organs in the thoracic cavity most frequently affected by parasites are the lungs and heart (Figure 1a). The heart as the central organ of the circulatory system carries out vital functions by distributing blood, oxygen and nutrients to tissues and removing metabolic waste

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High resolution microscopy reveals an unusual architecture of the Plasmodium berghei endoplasmic reticulum

Cited by 29 publications

References 66 publications

Transcriptome analysis ofPlasmodium bergheiduring exo-erythrocytic development

Transcriptome analysis ofPlasmodium bergheiduring exo-erythrocytic development

Manipulation of the Host Cell Membrane during Plasmodium Liver Stage Egress

Intravital imaging of host‐parasite interactions in organs of the thoracic and abdominopelvic cavities

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