Autophagy in protists and their hosts: When, how and why?

Romano, Patricia Silvia; Akematsu, Takahiko; Besteiro, Sébastien; Bindschedler, Annina; Carruthers, Vern B.; Chahine, Zeinab; Coppens, Isabelle; Descoteaux, Albert; Duque, Thabata Lopes Alberto; He, Cynthia Y.; Heussler, Volker T.; Roch, Karine G. Le; Li, Fengjun; Menezes, Juliana Perrone Bezerra de; Menna-Barreto, Rubem Figueiredo Sadok; Mottram, Jeremy C.; Schmuckli‐Maurer, Jacqueline; Turk, Boris; Veras, Patrícia Sampaio Tavares; Salassa, Betiana Nebaí; Vanrell, María Cristina

doi:10.1080/27694127.2022.2149211

Cited by 6 publications

(9 citation statements)

References 433 publications

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“…In Plasmodium , over 80% of all liver stage parasites are labeled with LC3B but many of them persist and successfully develop (Prado et al., 2015; Wacker et al., 2017). This suggests that Plasmodium has evolved different strategies to evade clearance by the autophagic machinery and potentially even benefits from it (Agop‐Nersesian et al., 2018; Aguilera et al., 2024; Romano et al., 2023). Here, we even provide evidence that LC3B localization at the PVM supports parasite survival in infected HeLa cells.…”

Section: Discussionmentioning

confidence: 99%

“…Host cells are equipped with a variety of mechanisms to eliminate intracellular pathogens. These cell defense mechanisms include autophagy and related responses (Agop‐Nersesian et al., 2018; Levine et al., 2011; Romano et al., 2023). Autophagy is a catabolic process in the cell that allows the delivery of cytosolic material to lysosomal degradation (Morishita & Mizushima, 2019).…”

Section: Introductionmentioning

confidence: 99%

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LC3B labeling of the parasitophorous vacuole membrane of Plasmodium berghei liver stage parasites depends on the V‐ATPase and ATG16L1

Bindschedler,

Schmuckli‐Maurer,

Buchser

et al. 2024

Molecular Microbiology

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The protozoan parasite Plasmodium, the causative agent of malaria, undergoes an obligatory stage of intra‐hepatic development before initiating a blood‐stage infection. Productive invasion of hepatocytes involves the formation of a parasitophorous vacuole (PV) generated by the invagination of the host cell plasma membrane. Surrounded by the PV membrane (PVM), the parasite undergoes extensive replication. During intracellular development in the hepatocyte, the parasites provoke the Plasmodium‐associated autophagy‐related (PAAR) response. This is characterized by a long‐lasting association of the autophagy marker protein, and ATG8 family member, LC3B with the PVM. LC3B localization at the PVM does not follow the canonical autophagy pathway since upstream events specific to canonical autophagy are dispensable. Here, we describe that LC3B localization at the PVM of Plasmodium parasites requires the V‐ATPase and its interaction with ATG16L1. The WD40 domain of ATG16L1 is crucial for its recruitment to the PVM. Thus, we provide new mechanistic insight into the previously described PAAR response targeting Plasmodium liver stage parasites.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

LC3B labeling of the parasitophorous vacuole membrane of Plasmodium berghei liver stage parasites depends on the V‐ATPase and ATG16L1

Bindschedler,

Schmuckli‐Maurer,

Buchser

et al. 2024

Molecular Microbiology

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“…and Trypanosoma cruzi , respectively, and are severe, life‐threatening illnesses with limited treatments, which is why they are considered orphan or neglected diseases. In contrast to bacteria, protists are eukaryotic cells that possess many processes like mammalian cells, including autophagy in some cases (parasite autophagy will not be covered in this review; see [124]). Nevertheless, mammalian cells represent an excellent niche for the nutrition, replication, and immune system evasion of these parasites.…”

Section: Parasites and Autophagymentioning

confidence: 99%

Autophagy as an innate immunity response against pathogens: a Tango dance

Aguilera,

Delgui,

Reggiori

et al. 2023

FEBS Letters

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Intracellular infections as well as changes in the cell nutritional environment are main events that trigger cellular stress responses. One crucial cell response to stress conditions is autophagy. During the last 30 years, several scenarios involving autophagy induction or inhibition over the course of an intracellular invasion by pathogens have been uncovered. In this review, we will present how this knowledge was gained by studying different microorganisms. We intend to discuss how the cell, via autophagy, tries to repel these attacks with the objective of destroying the intruder, but also how some pathogens have developed strategies to subvert this. These two fates can be compared with a Tango, a dance originated in Buenos Aires, Argentina, in which the partner dancers are in close connection. One of them is the leader, embracing and involving the partner, but the follower may respond escaping from the leader. This joint dance is indeed highly synchronized and controlled, perfectly reflecting the interaction between autophagy and microorganism.

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“…In contrast, enzymes required for autophagic body breakdown in yeasts have been known since the early 1990s [ 8 ], showing how neglected this aspect of plant autophagy is. Two of the important uncertainties are the existence of a functional plant analog of the yeast vacuolar putative lipase Atg15/Aut5/Cvt17 and its involvement in the final steps of autophagy, in particular, the degradation of autophagic bodies [ 9 , 10 ]. Atg15 is the best-known and best-described protein involved in autophagic body breakdown in yeast [ 11 , 12 , 13 , 14 ].…”

Section: Introductionmentioning

confidence: 99%

Identification and Potential Participation of Lipases in Autophagic Body Degradation in Embryonic Axes of Lupin (Lupinus spp.) Germinating Seeds

Wleklik,

Stefaniak,

Nuc

et al. 2023

IJMS

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Autophagy is a fundamental process for plants that plays a crucial role in maintaining cellular homeostasis and promoting survival in response to various environmental stresses. One of the lesser-known stages of plant autophagy is the degradation of autophagic bodies in vacuoles. To this day, no plant vacuolar enzyme has been confirmed to be involved in this process. On the other hand, several enzymes have been described in yeast (Saccharomyces cerevisiae), including Atg15, that possess lipolytic activity. In this preliminary study, which was conducted on isolated embryonic axes of the white lupin (Lupinus albus L.) and Andean lupin (Lupinus mutabilis Sweet), the potential involvement of plant vacuolar lipases in the degradation of autophagic bodies was investigated. We identified in transcriptomes (using next-generation sequencing (NGS)) of white and Andean lupin embryonic axes 38 lipases with predicted vacuolar localization, and for three of them, similarities in amino acid sequences with yeast Atg15 were found. A comparative transcriptome analysis of lupin isolated embryonic axes cultured in vitro under different sucrose and asparagine nutrition, evaluating the relations in the levels of the transcripts of lipase genes, was also carried out. A clear decrease in lipase gene transcript levels caused by asparagine, a key amino acid in lupin seed metabolism which retards the degradation of autophagic bodies during sugar-starvation-induced autophagy in lupin embryonic axes, was detected. Although the question of whether lipases are involved in the degradation of autophagic bodies during plant autophagy is still open, our findings strongly support such a hypothesis.

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Autophagy in protists and their hosts: When, how and why?

Cited by 6 publications

References 433 publications

LC3B labeling of the parasitophorous vacuole membrane of Plasmodium berghei liver stage parasites depends on the V‐ATPase and ATG16L1

LC3B labeling of the parasitophorous vacuole membrane of Plasmodium berghei liver stage parasites depends on the V‐ATPase and ATG16L1

Autophagy as an innate immunity response against pathogens: a Tango dance

Identification and Potential Participation of Lipases in Autophagic Body Degradation in Embryonic Axes of Lupin (Lupinus spp.) Germinating Seeds

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