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Recent Advances in Understanding Apicomplexan Parasites [Version 1; Peer Review: 2 Approved] Frank Seeber1, Svenja Steinfelder2

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Recent Advances in Understanding Apicomplexan Parasites [Version 1; Peer Review: 2 Approved] Frank Seeber1, Svenja Steinfelder2 F1000Research 2016, 5(F1000 Faculty Rev):1369 Last updated: 17 JUL 2019 REVIEW Recent advances in understanding apicomplexan parasites [version 1; peer review: 2 approved] Frank Seeber1, Svenja Steinfelder2 1FG16: Mycotic and parasitic agents and mycobacteria, Robert Koch-Institute, Berlin, Germany 2Institute of Immunology, Center of Infection Medicine, Free University Berlin, Berlin, Germany First published: 14 Jun 2016, 5(F1000 Faculty Rev):1369 ( Open Peer Review v1 https://doi.org/10.12688/f1000research.7924.1) Latest published: 14 Jun 2016, 5(F1000 Faculty Rev):1369 ( https://doi.org/10.12688/f1000research.7924.1) Reviewer Status Abstract Invited Reviewers Intracellular single-celled parasites belonging to the large phylum 1 2 Apicomplexa are amongst the most prevalent and morbidity-causing pathogens worldwide. In this review, we highlight a few of the many recent version 1 advances in the field that helped to clarify some important aspects of their published fascinating biology and interaction with their hosts. Plasmodium falciparum 14 Jun 2016 causes malaria, and thus the recent emergence of resistance against the currently used drug combinations based on artemisinin has been of major interest for the scientific community. It resulted in great advances in F1000 Faculty Reviews are written by members of understanding the resistance mechanisms that can hopefully be translated the prestigious F1000 Faculty. They are into altered future drug regimens. Apicomplexa are also experts in host cell commissioned and are peer reviewed before manipulation and immune evasion. Toxoplasma gondii and Theileria sp., publication to ensure that the final, published version besides Plasmodium sp., are species that secrete effector molecules into the host cell to reach this aim. The underlying molecular mechanisms for is comprehensive and accessible. The reviewers how these proteins are trafficked to the host cytosol (T. gondii and who approved the final version are listed with their Plasmodium) and how a secreted protein can immortalize the host cell ( names and affiliations. Theileria sp.) have been illuminated recently. Moreover, how such secreted proteins affect the host innate immune responses against T. gondii and the Jeroen Saeij, University of California, Davis, liver stages of Plasmodium has also been unraveled at the genetic and 1 molecular level, leading to unexpected insights. USA Methodological advances in metabolomics and molecular biology have Daniel Gold, University of California, Davis, been instrumental to solving some fundamental puzzles of mitochondrial USA carbon metabolism in Apicomplexa. Also, for the first time, the generation of stably transfected Cryptosporidium parasites was achieved, which opens 2 Julius Lukes, Czech Academy of Sciences and up a wide variety of experimental possibilities for this understudied, Faculty of Science, České Budějovice, Czech important apicomplexan pathogen. Republic Keywords Any comments on the article can be found at the Apicomplexa , parasites , Plasmodium , T. gondii , CRISPR/Cas9 end of the article. Page 1 of 14 F1000Research 2016, 5(F1000 Faculty Rev):1369 Last updated: 17 JUL 2019 Corresponding author: Frank Seeber ([email protected]) Competing interests: The authors declare that they have no competing interests. Grant information: The authors are senior members of the Research Training Group 2046 (GRK 2046) "Parasite Infections: From Experimental Models to Natural Systems" funded by the Deutsche Forschungsgemeinschaft (DFG). Copyright: © 2016 Seeber F and Steinfelder S. This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. How to cite this article: Seeber F and Steinfelder S. Recent advances in understanding apicomplexan parasites [version 1; peer review: 2 approved] F1000Research 2016, 5(F1000 Faculty Rev):1369 (https://doi.org/10.12688/f1000research.7924.1) First published: 14 Jun 2016, 5(F1000 Faculty Rev):1369 (https://doi.org/10.12688/f1000research.7924.1) Page 2 of 14 F1000Research 2016, 5(F1000 Faculty Rev):1369 Last updated: 17 JUL 2019 Introduction An estimated one-third of the human population is chronically Apicomplexa comprise a large phylum of single-celled, obligate infected with Toxoplasma gondii leading to toxoplasmosis. It can intracellular protozoan organisms that all have a parasitic lifestyle. cause severe symptoms in newborns (e.g. encephalitis and ocular Among the more than 6000 named and probably more than one disease) when a previously non-infected mother contracts the million unnamed species1 are some of great public health and infection during pregnancy by ingesting infectious stages economic relevance, since they cause severe diseases in humans of T. gondii via contaminated food, water, or dust7. The latest and livestock, affecting millions each year2–6. Therefore, increased numbers from WHO rank toxoplasmosis highest with respect knowledge about their biology in general, e.g. to exploit vulner- to the overall lifelong disease burden among those foodborne abilities, and their interaction with the host organism, e.g. to diseases caused by protozoan parasites8. stimulate the immune system, is of great importance and prom- ises major benefits in understanding and combating the diseases The same study identified cryptosporidiosis (caused by two they cause. In addition, they possess a fascinating biology as Cryptosporidium species, Cryptosporidium hominis and Crypt- intracellular eukaryotes thriving within another eukaryotic cell osporidium parvum) as the second most important disease in (Figure 1), which clearly sets them apart from other pathogens like this class. Worldwide, each of these species infects 8–10 million bacteria and viruses. Taken together, these are all good reasons to people per year, but in addition they also cause considerable pay attention to these fascinating organisms. This review will focus disease in livestock. on four important genera. Lastly, Theileria parva, a tick-transmitted apicomplexan of rumi- Plasmodium falciparum and four other Plasmodium species that nants, leads to the death of more than 1 million cattle per year affect humans cause malaria, a mosquito-transmitted, poten- in sub-Saharan Africa, causing costs of >300 million US$. This tially deadly disease. According to the latest data from the World has severe socio-economic consequences for those regions4. Health Organization (WHO), the number of deaths due to malaria has declined by 48% between 2000 and 2015 but the disease still T. gondii, and to a lesser extent Plasmodium sp., has also gained causes the loss of ca. 438,000 lives each year of the 218 million increased attention from cell biologists owing to a number of people infected, mostly children under 5 years of age5. unique mechanisms of host cell entry, division, motility, etc., Figure 1. Morphology of intracellular Toxoplasma gondii tachyzoites. Transmission electron micrograph of the intracellular Toxoplasma gondii tachyzoite stage as one example of Apicomplexa. Shown are parasites inside an infected fibroblast host cell, residing within a parasitophorous vacuole (PV), which is surrounded by a membrane (parasitophorous vacuolar membrane, PVM, in blue) (left). On the right, some host and parasite organelles are outlined. The apicoplast is a plastid-derived organelle harboring some essential metabolic pathways. Micronemes are specialized secretory organelles at the apical end that store proteins important for gliding motility and host cell invasion130. The role of dense granules and rhoptries are detailed in the text. This basic organellar setup is shared with Plasmodium sp. Page 3 of 14 F1000Research 2016, 5(F1000 Faculty Rev):1369 Last updated: 17 JUL 2019 thereby becoming model organisms for such aspects9. Both medi- to the discovery of artemisinin in the 1970s28,29. It is the ingredi- cal importance and model character are reflected by the overall ent of a traditional Chinese herbal anti-malarial treatment that, citations in PubMed (several thousands from January 2013– when metabolized in situ to dihydroartemisinin, very efficiently December 2015 for the four taxa), making it impossible to cover kills Plasmodium sp.. Artemisinin combination therapies (ACTs) even the most interesting discoveries of the last 2–3 years in all are currently the drugs of choice and recommended by WHO for areas of apicomplexan research in reasonable depth. Consequently, treating P. falciparum infections worldwide, largely because drug only a few, admittedly subjective highlights in the fields of cell resistance against other available compounds precludes their and molecular biology, biochemistry, and immunology as well further use in many areas of Africa and South-East Asia (SEA)30. as aspects concerning drugs will be mentioned here. These were ACTs consist of fast-acting artemisinin (or its derivatives) and selected because they are expected to make a major impact in the less-potent, long-acting partner drugs. Artemisinin’s mode of action following years or offer explanations for puzzling unexplained is unique in the sense that not a single protein or cell component observations in apicomplexan biology. but a multitude of parasite molecules are targeted by the com- pound via the generation of highly reactive endoperoxide-derived Methodological advances as game-changers radicals31. These affect at least 124 parasites but few, if any, host pro- Many new
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