Inverted recruitment of autophagy proteins to the Plasmodium berghei parasitophorous vacuole membrane

Schmuckli‐Maurer, Jacqueline; Reber, Vera Blinn; Wacker, Rahel; Bindschedler, Annina; Zakher, A.; Heussler, Volker

doi:10.1371/journal.pone.0183797

Cited by 19 publications

(30 citation statements)

References 51 publications

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“…Another similarity between plant-pathogen and mammalianparasite interfaces is the induction of autophagy responses that are directed towards the pathogens, which are contained in modified phagosomal compartments, similar to recent observations with P. infestans (Dagdas et al, 2016(Dagdas et al, , 2018. For instance, components of mammalian autophagy machinery such as ATG8 (the LC3/ GABRAP family in mammalian cells) as well as the autophagy cargo receptors p62 (also known as SQSTM) and NBR1 target the peri-microbial membrane interface engulfing the Plasmodium parasite (Schmuckli-Maurer et al, 2017;Wacker et al, 2017;Real et al, 2018) (see poster). Interestingly, similar to the P. infestans RXLR effector PexRD54, one of the PVM-embedded plasmodium effector proteins, called UIS3, binds to the mammalian ATG8 isoform LC3 to avoid being degraded by autophagy (Real et al, 2018).…”

Section: Similarities Between Plant-pathogen and Animal-parasite Intesupporting

confidence: 70%

“…Autophagy is a conserved eukaryotic trafficking process, in which cellular components and microbes are removed or relocated after engulfment in vesicular double-membrane-enclosed structures called autophagosomes (Lamb et al, 2013;Dagdas et al, 2018). Interestingly, selective forms of autophagy are induced at the perimicrobial interfaces in both plant and metazoan cells to counteract pathogen invasion (Thurston et al, 2012;Choi et al, 2014;Haldar et al, 2014;Schmuckli-Maurer et al, 2017;Wacker et al, 2017;Dagdas et al, 2018;Real et al, 2018). In plants, a defense-related autophagy machinery comprising the autophagy cargo receptor NBR1 (also known as Joka2) and the core autophagy adaptor ATG8 (ATG8CL isoform) target the EHM during P. infestans infection (see poster) (Dagdas et al, 2016).…”

Section: Diversion Of Autophagy Machinery To the Pathogen Interfacementioning

confidence: 99%

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The plant–pathogen haustorial interface at a glance

Bozkurt

Kamoun

2020

Journal of Cell Science

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Many filamentous pathogens invade plant cells through specialized hyphae called haustoria. These infection structures are enveloped by a newly synthesized plant-derived membrane called the extrahaustorial membrane (EHM). This specialized membrane is the ultimate interface between the plant and pathogen, and is key to the success or failure of infection. Strikingly, the EHM is reminiscent of host-derived membrane interfaces that engulf intracellular metazoan parasites. These perimicrobial interfaces are critical sites where pathogens facilitate nutrient uptake and deploy virulence factors to disarm cellular defenses mounted by their hosts. Although the mechanisms underlying the biogenesis and functions of these host-microbe interfaces are poorly understood, recent studies have provided new insights into the cellular and molecular mechanisms involved. In this Cell Science at a Glance and the accompanying poster, we summarize these recent advances with a specific focus on the haustorial interfaces associated with filamentous plant pathogens. We highlight the progress in the field that fundamentally underpin this research topic. Furthermore, we relate our knowledge of plant-filamentous pathogen interfaces to those generated by other plant-associated organisms. Finally, we compare the similarities between host-pathogen interfaces in plants and animals, and emphasize the key questions in this research area.

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Section: Similarities Between Plant-pathogen and Animal-parasite Intesupporting

confidence: 70%

Section: Diversion Of Autophagy Machinery To the Pathogen Interfacementioning

confidence: 99%

The plant–pathogen haustorial interface at a glance

Bozkurt

Kamoun

2020

Journal of Cell Science

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“…After sporozoites enter the hepatocyte cytoplasm, they form a parasite vacuolar membrane that interfaces with the host autophagy system [35][36][37]. Parasites have designed a system to escape this endogenous cytoplasmic immunity that involves disrupting autophagy and lysosome interactions with the parasitophorous vacuole membrane (PVM) [38].…”

Section: Discussionmentioning

confidence: 99%

Identification of Plasmodium falciparum proteoforms from liver stage models

Winer

Edgel

Zou

et al. 2020

Malar J

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Background: Immunization with attenuated malaria sporozoites protects humans from experimental malaria challenge by mosquito bite. Protection in humans is strongly correlated with the production of T cells targeting a heterogeneous population of pre-erythrocyte antigen proteoforms, including liver stage antigens. Currently, few T cell epitopes derived from Plasmodium falciparum, the major aetiologic agent of malaria in humans are known. Methods:In this study both in vitro and in vivo malaria liver stage models were used to sequence host and pathogen proteoforms. Proteoforms from these diverse models were subjected to mild acid elution (of soluble forms), multi-dimensional fractionation, tandem mass spectrometry, and top-down bioinformatics analysis to identify proteoforms in their intact state. Results:These results identify a group of host and malaria liver stage proteoforms that meet a 5% false discovery rate threshold. Conclusions:This work provides proof-of-concept for the validity of this mass spectrometry/bioinformatic approach for future studies seeking to reveal malaria liver stage antigens towards vaccine development.

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“…The autophagy‐mediated clearance of P. berghei by hepatocytes, is one of the few mechanisms studied by IVM. Components of the host autophagy machinery, such as microtubule‐associated protein 1 light chain 3 (LC3), the autophagy receptors p62, NBR1 and NDP52 as well as ubiquitin decorate the parasitophorous vacuolar membrane (PVM), in which Plasmodium develops into hepatic merozoites (Figure d(ii)) (Prado et al, ; Schmuckli‐Maurer et al, ; Wacker et al, ). Parasites that escape the so‐called Plasmodium ‐associated autophagy‐related (PAAR)‐response shield LC3 from downstream effector proteins (Real et al, ) and control the amount of PVM‐associated LC3 in the propagating schizont (Agop‐Nersesian et al, ).…”

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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Inverted recruitment of autophagy proteins to the Plasmodium berghei parasitophorous vacuole membrane

Cited by 19 publications

References 51 publications

The plant–pathogen haustorial interface at a glance

The plant–pathogen haustorial interface at a glance

Identification of Plasmodium falciparum proteoforms from liver stage models

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

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